Sustainable Management of Environmental Contaminants: Eco-friendly Remediation Approaches (Environmental Contamination Remediation and Management) 3031084454, 9783031084454

Citation preview

Environmental Contamination Remediation and Management

Tariq Aftab   Editor

Sustainable Management of Environmental Contaminants Eco-friendly Remediation Approaches

Environmental Contamination Remediation and Management Series Editors Erin R. Bennett, School of the Environment, Trent University, Peterborough, Canada Iraklis Panagiotakis, Environmental Engineer & Scientist, ENYDRON – Environmental Protection Services, Athens, Greece Advisory Editors Maria Chrysochoou, Department of Civil & Environmental Engineering, University of Connecticut, Storrs, CT, USA Dimitris Dermatas, School of Civil Engineering, National Technical University of Athens, Zografou, Greece Luca di Palma, Chemical Engineering Materials Environment, Sapienza University of Rome, Rome, Italy Demetris Francis Lekkas, Environmental Engineering and Science, University of the Aegean, Mytilene, Greece Mirta Menone, National University of Mar del Plata, Mar del Plata, Argentina Chris Metcalfe, School of the Environment, Trent University, Peterborough, Canada Matthew Moore, United States Department of Agriculture, National Sedimentation Laboratory, Oxford, MS, USA

There are many global environmental issues that are directly related to varying levels of contamination from both inorganic and organic contaminants. These affect the quality of drinking water, food, soil, aquatic ecosystems, urban systems, agricultural systems and natural habitats. This has led to the development of assessment methods and remediation strategies to identify, reduce, remove or contain contaminant loadings from these systems using various natural or engineered technologies. In most cases, these strategies utilize interdisciplinary approaches that rely on chemistry, ecology, toxicology, hydrology, modeling and engineering. This book series provides an outlet to summarize environmental contamination related topics that provide a path forward in understanding the current state and mitigation, both regionally and globally. Topic areas may include, but are not limited to, Environmental Fate and Effects, Environmental Effects Monitoring, Water Re-use, Waste Management, Food Safety, Ecological Restoration, Remediation of Contaminated Sites, Analytical Methodology, and Climate Change.

Tariq Aftab Editor

Sustainable Management of Environmental Contaminants Eco-friendly Remediation Approaches

Editor Tariq Aftab Department of Botany Aligarh Muslim University Aligarh, Uttar Pradesh, India

ISSN 2522-5847 ISSN 2522-5855 (electronic) Environmental Contamination Remediation and Management ISBN 978-3-031-08445-4 ISBN 978-3-031-08446-1 (eBook) https://doi.org/10.1007/978-3-031-08446-1 © The Editor(s) (if applicable) and The Author(s), under exclusive license to Springer Nature Switzerland AG 2022 This work is subject to copyright. All rights are solely and exclusively licensed by the Publisher, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilms or in any other physical way, and transmission or information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed. The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. The publisher, the authors, and the editors are safe to assume that the advice and information in this book are believed to be true and accurate at the date of publication. Neither the publisher nor the authors or the editors give a warranty, expressed or implied, with respect to the material contained herein or for any errors or omissions that may have been made. The publisher remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. This Springer imprint is published by the registered company Springer Nature Switzerland AG The registered company address is: Gewerbestrasse 11, 6330 Cham, Switzerland

Preface

Environmental contaminants are chemicals that accidentally or deliberately enter the environment, often, but not always, as a result of human activities. Some of these contaminants may have been manufactured for industrial use, and because they are very stable, they do not break down easily. If released to the environment, these contaminants may enter the food chain. Other environmental contaminants are naturally-occurring chemicals, but industrial activity may increase their mobility or increase the amount available to circulate in the environment, allowing them to enter the food chain at higher levels than would otherwise occur. Environmental contaminants influence the physiological cell reactions at different and heterogeneous basics and lead to altering in normal cell function primarily at the molecular and biochemical level. Molecular responses to such common environmental stresses have been studied intensively over the last few years, in which there is an intricate network of signaling pathways controlling perception of these environmental stress signals, the generation of second messengers and signal transduction. Recent advances in many areas of plant and microbial research, including genotyping, make scientists optimistic that valuable solutions will be found to allow deployment/commercialization of strategies better able to tolerate these environmental stresses. Environmental remediation was historically viewed as an inherently sustainable activity, as it restores contamination; however, researchers and practitioners are increasingly recognizing that there can be substantial environmental footprints and socioeconomic costs associated with remediation. Sustainability is an imperative in the emerging green and sustainable remediation movement, which is reshaping the entire remediation industry. Understanding the significant roles of sustainable or eco-friendly approaches in mitigating environmental contaminants, the current subject has recently attracted the attention of scientists from across the globe. Therefore, I bring forth a comprehensive volume Sustainable Management of Environmental Contaminants: Eco-friendly Remediation Approaches highlighting the various prospects. I am hopeful that this volume will furnish the requisite of all those who are working or have interest in the proposed topic.

v

vi

Preface

I am highly grateful to all our contributors for accepting our invitation for not only sharing their knowledge and research, but for venerably integrating their expertise in dispersed information from diverse fields in composing the chapters and enduring editorial suggestions to finally produce this venture. I also thank Springer Nature team for their generous cooperation at every stage of the book production. Lastly, thanks are also due to well-wishers, research students and editor’s family members for their moral support, blessings and inspiration in the compilation of this book. Aligarh, India

Tariq Aftab

Contents

1

2

3

4

Sustainable Management of Environmental Contaminants: Factors, Control, and Phytoremediation . . . . . . . . . . . . . . . . . . . . . . . . . Misbah Naz, Muhammad Ammar Raza, Muhammad Tariq, Sania Zaib, Sohail Ahmed Rajper, Muhammad Jafar Jaskani, Muhammad Ahsan, Zhicong Dai, and Daolin Du

1

Environmental Sustainability with Polyhydroxyalkanoates (PHA) as Plastic Alternatives . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Lucas Vinicius Santini Ceneviva and Takeharu Tsuge

17

Advanced Sewage Disinfection Technologies Eco-Friendly with the Environment and Public Health . . . . . . . . . . . . . . . . . . . . . . . . Yenifer González, Pablo Salgado, Gloria Gómez, and Gladys Vidal

51

Application of Fungi and Bacteria in the Management of Azo Dyes in the Industrial Effluents . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Mayola García-Rivero, María Aurora Martínez-Trujillo, and María Isabel Neria-González

71

5

Bioremediation: An Effective, Significant and Eco-friendly Approach for Sustainable Management . . . . . . . . . . . . . . . . . . . . . . . . . 119 Ankita Mallick, Subhajoy Dey, Soustav Datta, and Mainak Barman

6

Exploitation of Arbuscular Mycorrhizal (AM) Fungi as a Sustainable Management Strategy for Remediation of Cadmium-Contaminated Soils . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 139 Harmanjit Kaur, Tashima, and Bhawna Sunkaria

7

Medicinal and Aromatic Plant Species with Potential for Remediation of Metal(loid)-Contaminated Soils . . . . . . . . . . . . . . . 173 Katarína Král’ová and Josef Jampílek

vii

viii

Contents

8

Heavy Metal Toxicity and Phytoremediation by the Plants of Brassicaceae Family: A Sustainable Management . . . . . . . . . . . . . . 237 Kakan Ball, Zerald Tiru, Arka Pratim Chakraborty, Parimal Mandal, and Sanjoy Sadhukhan

9

Combating Nanotoxicity in Plants: Green Nanotechnology Perspective for a Sustainable Future . . . . . . . . . . . . . . . . . . . . . . . . . . . . 265 Pooja Singh and Krishna Kumar Choudhary

10 Strategies and Recent Advances in the Management of Waste Present in Soil and Water by Microbes . . . . . . . . . . . . . . . . . . . . . . . . . . 289 Samar Mortazavi, Sara Abdollahi, and Behnam Asgari Lajayer 11 Green Remediation for Sustainable Environment . . . . . . . . . . . . . . . . 313 Krati Singh, Swati Agarwal, Sonu Kumari, and Suphiya Khan 12 Application of Nanotechnology in Remediation of Environmental Pollutants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 343 Amra Bratovcic, Majid Darroudi, Arumugam Sundaramanickam, and Jasmina Ibrahimpasic 13 Seed Priming as a Sustainable Solution to Mitigate Salinity and Drought Stress in Plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 357 Swarnavo Chakraborty and Aryadeep Roychoudhury 14 Microbial Biosurfactants: Characterization, Properties, and Environmental Applications . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 371 Fatima Zahoor, Nazia Jamil, and Rida Batool 15 Gene–Environment Interaction During Bioremediation . . . . . . . . . . . 391 Kingsley Erhons Enerijiofi, Efeota Bright Odozi, Saheed Ibrahim Musa, Nnachor Emmanuel Chuka, and Beckley Ikhajiagbe 16 Myco-Remediation: A Sustainable Biodegradation of Environmental Pollutants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 425 Mohee Shukla, Rohit Shukla, Saket Jha, Ravikant Singh, and Anupam Dikshit 17 Achieving Eco-friendly Environment Through Sustainable Management of Solid Wastes in Soil Ecosystem . . . . . . . . . . . . . . . . . . 451 Kingsley Erhons Enerijiofi and Frederick Osaro Ekhaise 18 Mycoremediation of Agricultural Waste for the Cultivation of Edible Mushroom . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 471 Vivek Kumar Dhiman, Devendra Singh, Himanshu Pandey, Divya Chauhan, Vinay Kumar Dhiman, and Devendra Pandey

Contents

ix

19 Removal of Organic Dyes from Wastewaters Using Metal Oxide Nanoparticles . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 483 Majid Darroudi, Amra Bratovcic, Zahra Sabouri, and Samaneh Sadat Tabrizi Hafez Moghaddas 20 Thiourea can Mitigate the Adverse Effect of Ozone on Crop Productivity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 509 M. P. Sahu 21 Challenges and Solutions for Sustainable Urban Water Management . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 533 Yusra Mahfooz, Abdullah Yasar, Rameesha Tanveer, and Amt-ul-Bari Tabinda

Editor and Contributors

About the Editor Dr. Tariq Aftab received his Ph.D. in the Department of Botany at Aligarh Muslim University, India, and is currently Assistant Professor there. He is the recipient of a prestigious Leibniz-DAAD fellowship from Germany, Raman Fellowship from the Government of India and Young Scientist Awards from the State Government of Uttar Pradesh (India) and the Government of India. After completing his doctorate, he has worked as Research Fellow at National Bureau of Plant Genetic Resources, New Delhi, and as Post-doctorate Fellow at Jamia Hamdard, New Delhi, India. He also worked as Visiting Scientist at Leibniz Institute of Plant Genetics and Crop Plant Research (IPK), Gatersleben, Germany, and in the Department of Plant Biology, Michigan State University, USA. He is a member of various scientific associations from India and abroad. He has edited 15 books with international publishers, including Elsevier Inc., Springer Nature and CRC Press (Taylor & Francis Group), co-authored several book chapters and published over 80 research papers in peerreviewed international journals. His research interests include physiological, proteomic and molecular studies on medicinal and crop plants.

xi

xii

Editor and Contributors

Contributors Abdollahi Sara Department of Environment, Faculty of Natural Resources and Environment, Malayer University, Malayer, Iran Agarwal Swati Department of Bioscience and Biotechnology, Banasthali Vidyapith, Banasthali Tonk, Rajasthan, India Ahsan Muhammad Department of Horticultural Sciences, The Islamia University of Bahawalpur, Bahawalpur, Pakistan Asgari Lajayer Behnam Department of Soil Science, Faculty of Agriculture, University of Tabriz, Tabriz, Iran Ball Kakan Plant Molecular Biology Laboratory, Department of Botany, Raiganj University, Raiganj, Uttar Dinajpur, West Bengal, India Barman Mainak Department of Genetics and Plant Breeding, Bidhan Chandra Krishi Viswavidyalaya, Mohanpur, Nadia, West Bengal, India Batool Rida Institute of Microbiology and Molecular Genetics, Faculty of Life Sciences, University of the Punjab, Lahore, Pakistan Bratovcic Amra Faculty of Technology, University of Tuzla, Tuzla, Bosnia and Herzegovina Ceneviva Lucas Vinicius Santini Department of Materials Science and Engineering, Tokyo Institute of Technology, Yokohama, Japan Chakraborty Arka Pratim Mycology and Plant Pathology Laboratory, Department of Botany, Raiganj University, Raiganj, Uttar Dinajpur, West Bengal, India Chakraborty Swarnavo Post Graduate Department of Biotechnology, St. Xavier’s College (Autonomous), Kolkata, West Bengal, India Chauhan Divya Department of Biotechnology Banasthali Vidyapeeth, Jaipur, Rajasthan, India Choudhary Krishna Kumar Botany Section, MMV, Banaras Hindu University, Varanasi, India Chuka Nnachor Emmanuel Department of Plant Biology and Biotechnology, University of Benin, Benin, Nigeria Dai Zhicong Institute of Environment and Ecology, School of The Environment and Safety Engineering, Jiangsu University, Zhenjiang, Jiangsu Province, P. R. China; Jiangsu Collaborative Innovation Center of Technology and Material of Water Treatment, Suzhou University of Science and Technology, Suzhou, Jiangsu Province, P. R. China Darroudi Majid Nuclear Medicine Research Center, Mashhad University of Medical Sciences, Mashhad, Iran;

Editor and Contributors

xiii

Department of Medical Biotechnology and Nanotechnology, Faculty of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran Datta Soustav Department of Fruit Science, Bidhan Viswavidyalaya, Mohanpur, Nadia, West Bengal, India

Chandra

Krishi

Dey Subhajoy Department of Agricultural Meteorology and Physics, Bidhan Chandra Krishi Viswavidyalaya, Mohanpur, Nadia, West Bengal, India Dhiman Vinay Kumar Department of Microbiology, Dr. Yashwant Singh Parmar University of Horticulture and Forestry, Nauni, Solan, India; Department of Biotechnology, Himachal Pradesh University, Shimla, Himachal Pradesh, India Dhiman Vivek Kumar Department of Biotechnology, Himachal Pradesh University, Shimla, Himachal Pradesh, India Dikshit Anupam Biological Product Laboratory, Department of Botany, University of Allahabad, Prayagraj, Uttar Pradesh, India Du Daolin Institute of Environment and Ecology, School of The Environment and Safety Engineering, Jiangsu University, Zhenjiang, Jiangsu Province, P. R. China Ekhaise Frederick Osaro Applied Environmental Bioscience and Public Health Research Group, Department of Microbiology, University of Benin, Benin, Nigeria Enerijiofi Kingsley Erhons Department of Biological Sciences, Glorious Vision University (formerly Samuel Adegboyega University), Ogwa, Edo State, Nigeria; Applied Environmental Bioscience and Public Health Research Group, Department of Microbiology, University of Benin, Benin, Nigeria García-Rivero Mayola Laboratory of Enzymatic Catalysis, Division of Chemical and Biochemical Engineering, Tecnológico de Estudios Superiores de Ecatepec, Ecatepec de Morelos, Edo. México, Mexico González Yenifer Engineering and Biotechnology Environmental Group, Environmental Science Faculty and Center EULA–, Chile, Universidad de Concepción, Concepción, Chile Gómez Gloria Engineering and Biotechnology Environmental Group, Environmental Science Faculty and Center EULA–, Chile, Universidad de Concepción, Concepción, Chile Ibrahimpasic Jasmina Biotechnical Faculty, University of Bihac, Bihac, Bosnia and Herzegovina Ikhajiagbe Beckley Department of Plant Biology and Biotechnology, University of Benin, Benin, Nigeria Jamil Nazia Institute of Microbiology and Molecular Genetics, Faculty of Life Sciences, University of the Punjab, Lahore, Pakistan

xiv

Editor and Contributors

Jampílek Josef Department of Analytical Chemistry, Faculty of Natural Sciences, Comenius University, Bratislava, Slovakia Jaskani Muhammad Jafar Faculty of Agriculture, Institute of Horticultural Sciences, University of Agriculture Faisalabad, Faisalabad, Pakistan Jha Saket Biological Product Laboratory, Department of Botany, University of Allahabad, Prayagraj, Uttar Pradesh, India Kaur Harmanjit Post Graduate, Department of Botany, Government College for Girls, Ludhiana, Punjab, India Khan Suphiya Department of Bioscience and Biotechnology, Banasthali Vidyapith, Banasthali Tonk, Rajasthan, India Král’ová Katarína Institute of Chemistry, Faculty of Natural Sciences, Comenius University, Bratislava, Slovakia Kumari Sonu Department of Bioscience and Biotechnology, Banasthali Vidyapith, Banasthali Tonk, Rajasthan, India Mahfooz Yusra Sustainable Development Study Center, GC University, Lahore, Pakistan Mallick Ankita Department of Agricultural Meteorology and Physics, Bidhan Chandra Krishi Viswavidyalaya, Mohanpur, Nadia, West Bengal, India Mandal Parimal Mycology and Plant Pathology Laboratory, Department of Botany, Raiganj University, Raiganj, Uttar Dinajpur, West Bengal, India Martínez-Trujillo María Aurora Laboratory of Enzymatic Catalysis, Division of Chemical and Biochemical Engineering, Tecnológico de Estudios Superiores de Ecatepec, Ecatepec de Morelos, Edo. México, Mexico Moghaddas Samaneh Sadat Tabrizi Hafez Department of Medical Biotechnology and Nanotechnology, Faculty of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran Mortazavi Samar Department of Environment, Faculty of Natural Resources and Environment, Malayer University, Malayer, Iran Musa Saheed Ibrahim Department of Biology and Forensic Science, Admiralty University of Nigeria, Delta State, Nigeria Naz Misbah Institute of Environment and Ecology, School of The Environment and Safety Engineering, Jiangsu University, Zhenjiang, Jiangsu Province, P. R. China Neria-González María Isabel Laboratory of Integrative Microbiology and Molecular Biology, Division of Chemical and Biochemical Engineering, Tecnológico de Estudios Superiores de Ecatepec, Ecatepec de Morelos, Edo. México, Mexico Odozi Efeota Bright Department of Medical Laboratory Science, School of Basic Medical Science, University of Benin, Benin, Nigeria

Editor and Contributors

xv

Pandey Devendra Division of Crop Improvement and Biotechnology, Central Institute for Subtropical Horticulture, Lucknow, Uttar Pradesh, India Pandey Himanshu Department of Biotechnology, Dr. Yashwant Singh Parmar University of Horticulture and Forestry, Nauni, Solan, India Rajper Sohail Ahmed Department of Biotechnology, Sindh Agricultural University Tandojam, Tandojam, Pakistan Raza Muhammad Ammar School of Food Science and Biotechnology, Key Laboratory of Fruits and Vegetables Postharvest and Processing Technology Research of Zhejiang Province, Zhejiang Gongshang University, Hangzhou, China Roychoudhury Aryadeep Post Graduate Department of Biotechnology, St. Xavier’s College (Autonomous), Kolkata, West Bengal, India Sabouri Zahra Applied Biomedical Research Center, Mashhad University of Medical Sciences, Mashhad, Iran Sadhukhan Sanjoy Plant Molecular Biology Laboratory, Department of Botany, Raiganj University, Raiganj, Uttar Dinajpur, West Bengal, India Sahu M. P. Swami Keshwanand Rajasthan Agricultural University, Bikaner, India Salgado Pablo Department of Civil Engineering, Faculty of Engineering, Universidad Católica de La Santísima Concepción, Concepción, Chile Shukla Mohee Biological Product Laboratory, Department of Botany, University of Allahabad, Prayagraj, Uttar Pradesh, India Shukla Rohit Biological Product Laboratory, Department of Botany, University of Allahabad, Prayagraj, Uttar Pradesh, India Singh Devendra Department of Biotechnology, B. N. College of Engineering And Technology, Lucknow, Uttar Pradesh, India Singh Krati Department of Bioscience and Biotechnology, Banasthali Vidyapith, Banasthali Tonk, Rajasthan, India Singh Pooja Botany Section, MMV, Banaras Hindu University, Varanasi, India Singh Ravikant Department of Biotechnology, Swami Vivekanand University, Sagar, Madhya Pradesh, India Sundaramanickam Arumugam CAS in Marine Biology, Faculty of Marine Sciences, Annamalai University, Parangipettai, India Sunkaria Bhawna Department of Botany, Akal University, Bathinda, Punjab, India Tabinda Amt-ul-Bari Sustainable Development Study Center, GC University, Lahore, Pakistan Tanveer Rameesha Sustainable Development Study Center, GC University, Lahore, Pakistan

xvi

Editor and Contributors

Tariq Muhammad Department of Pharmacology, Lahore Pharmacy Collage, Lahore, Pakistan Tashima Department of Botany, Akal University, Bathinda, Punjab, India Tiru Zerald Plant Physiology Laboratory, Department of Botany, Raiganj University, Raiganj, Uttar Dinajpur, West Bengal, India Tsuge Takeharu Department of Materials Science and Engineering, Tokyo Institute of Technology, Yokohama, Japan Vidal Gladys Engineering and Biotechnology Environmental Group, Environmental Science Faculty and Center EULA–, Chile, Universidad de Concepción, Concepción, Chile Yasar Abdullah Sustainable Development Study Center, GC University, Lahore, Pakistan Zahoor Fatima Institute of Microbiology and Molecular Genetics, Faculty of Life Sciences, University of the Punjab, Lahore, Pakistan Zaib Sania Department of Biochemistry, Biological Sciences, Quaid-i-Azam University, Islamabad, Pakistan

Chapter 1

Sustainable Management of Environmental Contaminants: Factors, Control, and Phytoremediation Misbah Naz, Muhammad Ammar Raza, Muhammad Tariq, Sania Zaib, Sohail Ahmed Rajper, Muhammad Jafar Jaskani, Muhammad Ahsan, Zhicong Dai, and Daolin Du Abstract Despite the fact that it is not a new phenomenon, environmental pollution remains the world’s most pressing problem and the leading cause of disease and death among humans. Through urbanization, industrialization, mining, and exploratory operations, humans are in the forefront of polluting the world ecosystem. Both developing and developed countries suffer this burden, while developed countries have done a better job of maintaining their environment due to their increased knowledge and rigorous legislation. Even though the world is upset about pollution, its damage persists due to the catastrophic long-term implications. This chapter M. Naz · Z. Dai (B) · D. Du Institute of Environment and Ecology, School of The Environment and Safety Engineering, Jiangsu University, 301 Xuefu Road, Zhenjiang 21201, Jiangsu Province, P. R. China e-mail: [email protected]; [email protected] M. A. Raza School of Food Science and Biotechnology, Key Laboratory of Fruits and Vegetables Postharvest and Processing Technology Research of Zhejiang Province, Zhejiang Gongshang University, Hangzhou 310018, China M. Tariq Department of Pharmacology, Lahore Pharmacy Collage, Lahore, Pakistan S. Zaib Department of Biochemistry, Biological Sciences, Quaid-i-Azam University, Islamabad, Pakistan S. A. Rajper Department of Biotechnology, Sindh Agricultural University Tandojam, Tandojam, Pakistan M. J. Jaskani Faculty of Agriculture, Institute of Horticultural Sciences, University of Agriculture Faisalabad, Faisalabad, Pakistan M. Ahsan Department of Horticultural Sciences, The Islamia University of Bahawalpur, Bahawalpur, Pakistan Z. Dai Jiangsu Collaborative Innovation Center of Technology and Material of Water Treatment, Suzhou University of Science and Technology, Suzhou 215009, Jiangsu Province, P. R. China © The Author(s), under exclusive license to Springer Nature Switzerland AG 2022 T. Aftab (ed.), Sustainable Management of Environmental Contaminants, Environmental Contamination Remediation and Management, https://doi.org/10.1007/978-3-031-08446-1_1

1

2

M. Naz et al.

covers the various types of pollution, as well as the causes and effects of pollution, and offers potential strategies for dealing with pollution in order to build a healthy and sustainable ecosystem. Pollution is impeding the economic development of coal reserves. The standards for environmental protection in developed countries are comparatively stricter than in developing countries. As a result, getting a mining license entails time-consuming procedures that cause delays. Indian authorities have also begun to impose tough environmental pollution regulations. Therefore, environmental issues can be fully avoided, although such solutions are costly. Keywords Phytoremediation · Environmental contaminants · Sustainable management

1.1 Introduction Various actions are required to monitor and control environmental hazards to health, each of which is directed at a specific hazard or form of public health concern (Charlesworth et al. 2011). Monitoring means the use of routine measurements for the detection of changes in the environment or health, or the data from different resources could also be used for this purpose. The control of environmental hazards depends on defining acceptable exposure levels, thereby determining health risks and level of control required to keep exposure below specified thresholds (Cohrssen and Covello 1999). Specific control issues related to food and water safety, air pollution, noise, and ionization and electromagnetic radiation are discussed. A specific issue of the health associated with environmental hazards is the “disease group”. However, cluster surveys are very controversial and are generally not helpful because they do not help in clear understanding of the origin of cluster (Vautz et al. 2006). Today environmental pollution is a hot topic; water, soil, and air all subjected to the same pollution. As a “universal sink”, the greatest burden of pollution is being born by the soil. It is being contaminated in many ways. In order to maintain fertility of soil and to enhance the productivity, it is urgent to control soil pollution (Havugimana et al. 2015). Pollution is actually unwanted changes in the chemical, physical, and biological traits of water, soil, and air, and these changes ultimately affect the lives of human, plants, and animals as well as the industrial progress. Pollutants are things that adversely affect people’s health, comfort, property, or the environment (Ajibade et al. 2021). Generally speaking, by-products or residues produced by waste, sewage, and by accidental discharge are the main sources for the introduction of pollutants in the air, water, and soil, and hence, our environment is being polluted (Gasi´nski et al. 2022). The basis of agriculture is soil, and all crops either rely on it or use it to provide food for humans or animals. Somewhat accelerated erosion is causing us to lose this valuable natural resource (Ashraf et al. 2014). In addition, the large amount of man-made waste, sludge, and other products produced by the new garbage treatment plant and even sewage are polluting the soil. For the maintenance of soil fertility and

1 Sustainable Management of Environmental Contaminants: Factors …

3

productivity, implementation of strict control is necessary, and this will ultimately be helpful for the health of all organisms (Baligar et al. 2001). Terrestrial ecological risk assessment of contaminated soil, sewage sludge improvement, pesticides application, and other activities of human that cause terrestrial environments to be exposed to harmful substances is a complex task, accompanied by many related issues (Ashraf et al. 2014). This assessment is not only a relatively new scientific field that has developed rapidly since the mid-1980s, but compared with most aquatic environments, soil is often traded on private land, which also complicates the situation as real estate (Charlesworth et al. 2011). Therefore, professional and economic disagreements between the interests of scientists, stakeholders, authorities, engineers, managers, lawyers, non-governmental organizations (NGOs), and regulators are not uncommon. Despite ignoring these aspects, there are still several unresolved issues in the way; at present, risk assessments are done, and the effects of man-made substances on the terrestrial environment are managed (Steger 2000).

1.2 Phytoremediation in Heavy Metal Toxicity Heavy metal is a harmful pollutant that exists in soil and water. Phytoremediation is a plant-based method which is cost effective and eco-friendly and is used to remove heavy metals from different media using hyper-accumulating plant species (Kiran et al. 2017) (Fig. 1.1). Heavy metals are very harmful to all biological components of the environment. Heavy metal pollution comes either directly from water sources or by biological amplification. Occasionally in mining areas, high concentrations of air also become a source of heavy metal pollution (Liu et al. 2018). For example, the tragedy of the Love Canal at Niagara Falls in the USA explains the catastrophic effect of heavy metals on human and animal populations. Several traditional technologies are used to eradicate heavy metals, but these technologies require huge capital costs and also have other drawbacks. For instance, chemical method used for this purpose not only removes heavy metals but also degrades valuable components of the soil. In addition, this method produces a large amount of mud, and the per capita cost has also increased (Eskander and Saleh 2017).

1.2.1 Phytoremediation as a Sustainable Way: To Restore Heavy Metal-Contaminated Land The pollution of heavy metals on the land leads to the decline of soil function. Chemical pollution of agricultural land can cause negative effects, especially human health (Ali et al. 2019). The factor that causes heavy metals to be included in the pollutant group is the non-degradable nature of heavy metals. Several physical and

4

M. Naz et al.

Fig. 1.1 Beneficial role of phytoremediation in lowering metal toxicity from the environment

chemical techniques have been used to remove pollutants from polluted environments (Mudhoo et al. 2012). However, these technologies require high costs, intensive labor, irreversible changes in soil properties that cannot be restored and other contributions to pollution. Phytoremediation is one of the methods to reduce toxicity or applicable heavy metal migration and environmentally friendly in situ or ex situ (Padhan et al. 2021). Phytoremediation techniques include plant stabilization, plant stimulation, plant transformation, plant filtration, and plant extraction. This article aims to study phytoremediation from sustainable indicators, namely environmental, social, and economic aspects (Upcraft and Guo 2020). Phytoremediation is one of the sustainable methods for restoring contaminated land, which has the lowest cost compared with other methods. Healthy and fertile agricultural land is the key to food security, so through the use of phytoremediation, it can restore low-fertility contaminated land through sustainability (Evangelou et al. 2015). The greatest environmental threat is toxic metal contamination in the soil. Chemical treatments for removing heavy metals (HMs) from the environment, including as heat treatment, electrical remediation, soil replacement, precipitation, and chemical leaching, are frequently expensive and ineffective on agriculture (Selvi et al. 2019). To rehabilitate the contaminated environment, however, a variety of measures are

1 Sustainable Management of Environmental Contaminants: Factors …

5

employed. Phytoremediation is one of them, and it is based on the use of hyperaccumulating plant species that can survive high levels of hazardous heavy metals in the environment/soil. Green plants are used to remove, decompose, or detoxify hazardous metals in this technique. Plant stabilization, plant degradation, rhizosphere filtration, plant extraction, and plant volatilization are the most common phytoremediation procedures used in soil purification (Li et al. 2019). In large-scale applications, traditional phytoremediation technologies have some drawbacks. To improve the efficacy of plants, genetic engineering approaches such as transgene, nanoparticle addition, phytohormone-assisted phytoremediation, plant growth-promoting bacteria, and AMF inoculation are applied (Nedjimi 2021). As a purifying candidate for HMs, different elements of HM toxicity and decontamination processes are reviewed in this paper, with a focus on phytoremediation. Finally, it discusses some recent advancements in phytoremediation (Kumar et al. 2021).

1.2.2 Water Phytoremediation has become a sustainable technology for the removal of Cd from wastewater and contaminated soil. Compared with other traditional Cd metal removal technologies, phytoremediation has high performance results (Cristaldi et al. 2017). In the past two decades, plant species of various families have been considered as Cd hyper-accumulators. Different hyper-accumulative plants have different abilities to accumulate, isolate, and detoxify Cd. Research is making progress to clarify the various mechanisms by which different plants resist Cd toxicity at the physiological and molecular levels (Gomes 2012). However, the genetic control for the detoxification of cadmium in plants has not been determined yet. Although a great deal of progress has been made in the field of cadmium phytoremediation, under field condition limited research has been conducted. Therefore, there is an urgent need to study and improve the design of phytoremediation experiments related to the cadmium concentration in water and soil. Besides, the treatment method of cadmium-rich biomass needs to be further explored (Pandey and Bajpai 2019). Furthermore, to provide unique solutions for the removal of Cd from wastewater and polluted soil, current approaches must be combined with phytoremediation techniques. Phytoremediation is a strategy for cleaning contaminated media that is both environmentally friendly and helpful (Table 1.1). This approach is for contaminants to be absorbed by the roots, accumulated in bodily tissues, decomposed, and transformed into less hazardous forms (Ibrahim et al. 2016).

1.2.3 Soil Phytoremediation is a type of bioremediation that aids in the removal, transfer, stabilization, and/or destruction of contaminants from contaminated water and soil. Plants

6

M. Naz et al.

Table 1.1 Phytoremediation is a recently developed technology The mechanisms of phytoremediation

Phytoextraction, phytostabilization, phytovolatilization, phytodegradation, phytodesalination, rhizofiltration, rhizodegradation, and phytoevaporation

Mechanisms were affected by Species of plants, medium qualities, metal bioavailability, and several factors the addition of chelating agent Plant utilized

Plants used for phytoremediation (metallophytes) are usually categorized as metal indicators, metal excluders, and metal hyper-accumulators

Plant

Various types of plants to remove, transfer, stabilize, and/or destroy contaminants in the soil and groundwater

Water

Rhizofiltration, a water remediation technique whereby contaminants are taken by the plant roots

Soil

Traditional soil decontamination procedures have a number of drawbacks (including environmental and financial costs). As a result, this fact necessitates the exploration of certain alternate ways for the remediation of polluted sites

Food

Heavy metals are unable to be degraded physiologically. They could get into the food chain by contaminating soil and crop plants

Health

It is necessary to understand the effects of heavy metals on human health, as well as phytoremediation approaches and heavy metal removal mechanisms

typically emit chemicals through their roots that serve as nutrition for soil microbes (Kumar et al. 2018). Plants fix pollutants by combining pollutants with soil particles, making them difficult to absorb by plants or humans. Unlike plant extraction, plant stabilization mainly focuses on isolating pollutants in the soil around the roots, rather than pollutants in plant tissues (Cunningham et al. 1996).

1.2.4 Plant (1) Rhizosphere biodegradation: In this process, plants release compounds through their roots in the soil to provide nutrients for microbes. Microbes promote biodegradation (Cesco et al. 2012). (2) The plant is stable: In this process, the compounds produced by plants fix pollutants instead of degrading them (Pilon-Smits 2005). (3) Plant accumulation or extraction: Plant roots in this process absorb pollutants as well as other nutrients and water. This does not destroy the quality of nutrients but ends up in the leaves and buds of plant. This method is mainly used for wastes containing metals (Jain et al. 2019). Water-soluble metals are usually absorbed by plants and stored in the aerial twigs of plants, which are plucked and smelted for possible metal recovery or disposal as hazardous waste (Masaroviˇcová and Kráˇlová 2018). Cd, Ni, Zn, As, Se, and Cu are

1 Sustainable Management of Environmental Contaminants: Factors …

7

among the easily accessible metals absorbed by plants. Co, Mn, and Fe are metals with a moderate bioavailability, and Cr and U have a low bioavailability. The use of chelating chemicals in the soil boosts lead bioavailability. Likewise, citric acid and ammonium nitrate can be employed to boost uranium and radioactive cesium 137 availability, respectively (Abdel-Sabour and Al-Salama 2007).

1.2.5 Food Because the majority of soil heavy metals concentrate in crops, these metals could be transmitted to other media via the food chain. The bio-concentration factors (BCF) of several heavy metals at the crop–soil interface, particularly for key global crops such as wheat and corn, have been measured (Joseph et al. 2021). Ingestion of metalcontaminated food crops poses a significant risk to human health. Ingestion of heavy metal polluted vegetables can cause a variety of major health problems, including malnutrition, weakened immunity, gastrointestinal cancer, and mental impairment (Ali and Malik 2021). Such heavy metals might accumulate in human bones and adipose tissue, consuming critical nutrients and weakening immune defense capacities. Heavy metals like as Cd, Pb, Al, and Mn have also been linked to intrauterine development retardation (Mehri 2020).

1.2.6 Health Heavy metal contamination pollutes the environment and puts people’s health at risk. As a result, food security and diversity have become worldwide challenges. Restoration requires a deeper knowledge of the soil-to-food crop transmission pathway (Rai et al. 2019). The above chapter describes the global geographic pattern of heavy metal sources and analyzes the most advanced soil metal contamination cleanup approaches. Pollutants in the environment are a global threat to human health and wildlife. Phytoremediation is a new approach that uses plants and related soil bacteria to reduce the content or toxic effects of environmental pollutants in a cost-effective manner (Sadhu et al. 2018). Plants that have the ability to reduce contaminants in the air are utilized for air phytoremediation, which improves air quality and helps to reduce greenhouse gas emissions by fixing CO2 through photosynthesis. Geographic trends, on the other hand, may help us understand how their impact on human health issues varies by country, as well as the source of metal pollutants, which has seldom been investigated (Weyens et al. 2015).

8

M. Naz et al.

1.3 Phytoremediation Mechanism and Plants Adaptation As a result of many natural processes and industrial operations, heavy metal deposition in soil has increased rapidly. As these metals are non-biodegradable, they remain in the environment and can enter the food chain via crop plants, eventually accumulating in the human body via bio-magnification (Wuana and Okieimen 2011). Because of its dangerous composition, heavy metal contamination poses a major threat to human health and ecosystems. As a consequence, land contamination treatment is crucial. Phytoremediation is a non-hazardous approach that can be a cost-effective mitigation measure for heavy metal-contaminated soil. A detailed understanding of the mechanisms of heavy metal accumulation and tolerance in plants is essential to improve the efficacy of phytoremediation (Ashraf et al. 2019). In this chapter, we look at how heavy metals are taken up, transported, and detoxified in plants. The uses of genetic engineering, microbial aid, and chelation assistance approaches are among the ways we use to improve plant stability and extraction efficiency (Tekere 2020). Heavy metal detoxification is a necessary step before implementing phytoremediation. To deal with the toxicity of heavy metals, plants employ two defense strategies: avoidance and tolerance. Plants use these two methods to keep heavy metal concentrations in their cells below the toxicity threshold level (Ali and Malik 2021). Toxic contaminants can be extracted and removed from the soil via phytoremediation, which uses plants to limit their bioavailability in the soil (Padmavathiamma and Li 2007). Even at low quantities, plants can absorb ionic substances from the soil through their roots. Heavy metals are accumulated by plants in their rhizosphere ecosystem, which regulates their bioavailability, allowing contaminated soil to be recovered and soil fertility to be stabilized (Hooda 2007). The following are some of the advantages of employing phytoremediation: (i) cost-effective and practical phytoremediation is an autotrophic system fueled by solar energy, making it simple to run and maintain, and (ii) environmentally and ecologically friendly reducing pollutants environmental and ecosystem exposure, (iii) applicability can be used across a vast region and is simple to dispose of, (iv) minimizing the danger of pollution transmission by stabilizing heavy metals, preventing corrosion and metal leaching, and stabilizing heavy metals, and (v) it has the ability to release a variety of organic chemicals into the soil in order to boost soil fertility (Yan et al. 2020). In recent decades, a lot of research has been done to figure out how heavy metal tolerance works and how to improve phytoremediation performance (Devi and Kumar 2020). The detoxifying mechanisms (avoidance and tolerance) employed by plants to deal with heavy metals are detailed in this article, as well as the mechanism of heavy metal absorption and transfer in plants. The main goal is to give an overview of recent breakthroughs in phytoremediation technology development, such as approaches for increasing heavy metal bioavailability, tolerance, and accumulation (Padmavathiamma and Li 2007). This chapter also discussed the application of genetic engineering to improve plant performance during phytoremediation.

1 Sustainable Management of Environmental Contaminants: Factors …

9

1.3.1 Phytoremediation Harvesting Heavy Metals At hazardous waste sites, physical and chemical processes include excavating and burying the soil, fixing/inactivating (chemically treating the soil to fix the metal), desorbing and leaching the metal from the soil with acid solutions or proprietary leaching agents, and then leaching the metal (Sarwar et al. 2017). The soil, hydrosphere, atmosphere, lithosphere, and biosphere are all damaged by pollution. Over the last two decades, significant efforts have been made to reduce pollution sources and restore damaged water and soil resources. Phytoremediation is gaining popularity in academia and practice since it is less expensive and has less side effects than physical and chemical approaches (Artiola et al. 2019). Plants with the ability to improve soil and water quality have been identified in over 400 species. Among the most studied plants are Thlaspi, Brassica, Sedum alfredii H., and Arabidopsis. By transferring metal hyper-enriched genes from low-biomass wild species to highbiomass output farmed species, current technological breakthroughs are expected to play a promising role in the formation of new super-enriched plants in the future (Giri et al. 2015). This article’s goal is to provide a rapid summary of recent developments in the subject of water and soil resource phytoremediation.

1.4 Phytoremediation and Policies Management Phytoremediation is a promising approach for clearing up organic and inorganic harmful chemicals in polluted soil. Heavy metals are among these contaminants because of the harm it causes to human health and terrestrial ecosystems (Pandey et al. 2021). A global audience has been drawn to it; numerous studies have attempted to understand the mechanisms involved in this process. This study used a variety of plant species for phytoremediation and the acquisition of final biological products such as biofuels and biogas for combustion and heating (Adriano et al. 2004). In recent years, plant technology has become increasingly popular around the world. Because of its diversity, economic profitability, and environmental consequences, such as erosion management and soil quality and function enhancement, the process of valuing biomass is described in the phytoremediation process; also, related tests on polluted biomass utilized as a raw material or bioenergy are created through thermal and biochemical conversion. Pretreatment of biomass to boost yield, as well as treatment to control metal transfer in the environment, is also highlighted. Finally, the feasibility, benefits, and hazards of hazardous metal-contaminated biomass conversion were reviewed, as well as the gap in the conversion process (Meena et al. 2017).

10

M. Naz et al.

1.4.1 Post-Remediation Biomass Management Phytoremediation is a potential approach of pollution treatment, but there is need to manage the biomass produce during this process because it may cause secondary contamination after returning to the environment (Saxena et al. 2019). As a result, research and policy formation for post-biomass restoration management are required. The legislation on “post-phytoremediation management” addresses biomass management after phytoremediation, stimulates the recycling of biomass with known environmental dangers, and includes specific policies for managers (Muthusaravanan et al. 2020). To support and enlighten such policies and laws, more study is required. To analyses the several biomass management strategies, a detailed research proposes using plant biomass as a biofuel after phytoremediation (compression, incineration, ashing, pyrolysis, direct disposal, and liquid extraction, for example) incineration (Song and Park 2017). Despite this, there has been little research done in this area of management, and there is little local or international policy information on these issues (Table 1.2). As phytoremediation is widely employed in Korea and many other countries, it is vital to analyze the biomass management methods used after phytoremediation as well as the policies used to support these systems. No articles have been published, as far as the author is aware, that recommend policies based on direct evidence from scientific investigations (Agarwal et al. 2019). As an outcome, in this work, we reviewed existing phytoremediation technologies and policies while also testing our own postremediation biomass management techniques. We presented the requirements for effective biomass management systems and underlined the necessity to establish policies to handle waste concerns generated by the phytoremediation process by integrating these findings (Padoan et al. 2018). Biomass that has been reconditioned must be handled, because they may cause secondary contamination after returning to the environment. As a result, research into post-remediation biomass management is essential. Biomass could be one of the most cost-effective and ecologically friendly solutions as a co-composting material. We have demonstrated through actual tests that biomass post-remediation management is beneficial in this study (Song and Park 2017). We are more confident in the requirements of such policies now that we have a scientific foundation. Nonetheless, despite its potential, there is a dearth of research and policy development to encourage this type of management. Postphytoremediation management laws must be enacted to regulate the management of biomass after phytoremediation, as well as to promote the recycling of biomass that is recognized to pose environmental hazards (using environmentally friendly methods). Specific policies for managers must be devised, as well as more research to support and enlighten such policies and legislation (Khan et al. 2021). These laws, on the other hand, solely apply to biomass utilization after restoration and are not meant to encourage post-restoration management (Holl 2017). As a consequence, in order to achieve sustainable development, the government must enact the post-phytoremediation or even post-bioremediation management law, which requires the government to (a) manage post-phytoremediation biomass in order to prevent

1 Sustainable Management of Environmental Contaminants: Factors …

11

Table 1.2 Policy relating to post-remediation controlling Objective

Radiation safety requirements relevant to remediation

Scope

The restoration of terrestrial and freshwater ecosystems is discussed in this report

Structure

To the topic, providing information on the remedial requirements for radiation safety and the regulatory framework that governs them

Evaluating factors governing the need for remediation

The significance of the environment as a source of population exposure is determined by the contamination’s site-specific characteristics, emphasizing the requirement of thorough pathway study

In situ soil measurements

The quantity of variation in deposition density, the complexity of the landscape, and the purpose for which the data are needed should all influence the amount of soil and other sampling done

secondary contamination and (b) ensure the prevention of toxic waste recycling (Sheoran et al. 2010).

1.5 Research Policy and Post-remediation Management Despite the fact that phytoremediation is a promising approach of pollution prevention, the biomass created during the remediation process must be controlled, because it causes secondary contamination after returning to the environment (Song and Park 2017). As a consequence, post-biomass restoration management research and policy formation are required. Despite the fact that many phytoremediation studies have been published, research on post-remediation management is quite scarce (Fletcher et al. 2020). Therefore, a new study was undertaken that used biomass as a mixed composting material and found that it improved soil properties and performance of plant. In spite of its worth, however, there is currently a scarcity of research and regulations to support this management style (Song and Park 2017). Finally, we advise the public to support legislation that explains how to treat biomass after phytoremediation, stimulates the recycling of biomass with known environmental dangers, and includes specific policies for managers. To support and enlighten such policies and laws, more study is required (Khan et al. 2021). The following conditions may provide a radiation danger; nevertheless, there are regulatory controls in place in conforming facilities and activities. The formulation of specific remedial goals should ensure that the repair process, the site, and the human health and environmental values are all adequately protected for each project; remediation goals usually include defined and measurable end points. When encountered, elements of remediation activities serve as genuine goals to be attained by remedial

12

M. Naz et al.

efforts and serve to signify the end of these actions (Hadley et al. 2014). It is also crucial to be aware of any existing legal papers (such as notices, permits, leases, or commercial obligations) that could have a substantial impact on the restoration goal. It is not always practicable or cost effective to have all of the essential information. Prior to beginning remediation, establish remediation standards (Bardos et al. 2011). Determining the final repair objective can be a staged or iterative process in this case, with the need to revisit the cleanup aim (and the post-repair goal). Endpoints may need to consider crises if the goal is not achieved, or include more uncertainty/responsive actions if the goal is not met obtaining information. One of the restrictions that influences the repair plan selection is the time period to attain the restoration goal. Based on the current state of the site data and information submitted, the regulatory agency will examine whether the site can be closed once the repair goals have been met, and there are no active repair requirements (Kaim et al. 2018). To alleviate significant pollution problems, post-harvest treatment of polluted phytoremediation by-products is needed. In recent years, metal contamination became a particularly problematic problem. Traditional approaches have a significant impact on soil fertility. Remedial technology has a harmful impact on the ecosystem (Zhang et al. 2020). Phytoremediation has been shown to be a cost-effective, environmentally benign, and aesthetically pleasing approach that is best suited to developing countries. But despite the advantages of phytoremediation technique, it still generates a huge volume of polluted material. Pollution is exacerbated by the environment. Advanced technologies such as composting and compaction, combustion and gasification, plant decomposition, and pyrolysis are required for post-harvest treatment of these by-products (Ghosh and Singh 2005). A phytoremediation approach that uses high-biomass weeds produces a lot of the polluted biomass. As a result, proper disposal and management are required to keep pollutants out of the food chain. The plants chosen for phytoremediation should be inedible, disease resistant, and tolerant, and they should be able to give renewed vitality. Phytoremediation technology’s post-harvest management provides an alternative to biomass conversion to biofuels (Purakayastha and Chhonkar 2010). Phytoremediation technique becomes more practical as a result of this. Pre-harvest approaches of creating sustainable phytoremediation technologies rely heavily on post-harvest procedures.

1.6 Conclusion and Remarks • To decrease and absorb runoff, prevent erosion, and increase habitat, plant grass, trees, and plants in bare areas, pet waste, vehicle oil, and household chemicals should all be properly disposed of. • In lawns and gardens, fertilizers and pesticides should be used sparingly, and environmental control should include natural and mechanical ventilation, filtration, ultraviolet sterilization exposure, and other air purification measures. Environmental controls may not be able to remove all dangers if administrative controls (policies and work practices) are insufficient. Environmental Monitoring and

1 Sustainable Management of Environmental Contaminants: Factors …

13

Control (EMC) refers to a manned spacecraft’s internal environment, which includes the atmosphere, water supply, and all surfaces. • The term “monitoring” refers to the process of continuously and vigilantly monitoring the state of these areas over time in order to guarantee that conditions remain within acceptable bounds. • Scientists and engineers who must regulate the crew’s air and water quality will face particular hurdles in the enclosed environment of a spacecraft with a closed loop or near to a closed loop life support system. • The composition, feed rate, pressure, and temperature of solid, gas, and liquid components must be maintained to ensure mechanical health, i.e., system maintainability and dependability, as well as human health.

References Abdel-Sabour M, Al-Salama Y (2007) Zinc and cobalt phytoextraction by different plant species. Rem J: J Environ Cleanup Costs Technol Tech 18(1):109–119 Adriano DC, Wenzel W, Vangronsveld J, Bolan N (2004) Role of assisted natural remediation in environmental cleanup. Geoderma 122(2–4):121–142 Agarwal P, Sarkar M, Chakraborty B, Banerjee T (2019) Phytoremediation of air pollutants: prospects and challenges. In: Phytomanagement of polluted sites. Elsevier, pp 221–241 Ajibade FO, Adelodun B, Lasisi KH, Fadare OO, Ajibade TF, Nwogwu NA, Sulaymon ID, Ugya AY, Wang HC, Wang A (2021) Environmental pollution and their socioeconomic impacts. In: Microbe mediated remediation of environmental contaminants. Elsevier, pp 321–354 Ali H, Khan E, Ilahi I (2019) Environmental chemistry and ecotoxicology of hazardous heavy metals: environmental persistence, toxicity, and bioaccumulation. J Chem. https://doi.org/10. 1155/2019/6730305 Ali Q, Malik A (2021) Genetic response of growth phases for abiotic environmental stress tolerance in cereal crop plants. Genetika 53(1):419–456 Artiola J, Walworth J, Musil S, Crimmins M (2019) Soil and land pollution. In: Environmental and pollution science. Elsevier, pp 219–235 Ashraf MA, Maah MJ, Yusoff I (2014) Soil contamination, risk assessment and remediation. Environ Risk Assess Soil Contam 1:3–56 Ashraf S, Ali Q, Zahir ZA, Ashraf S, Asghar HN (2019) Phytoremediation: environmentally sustainable way for reclamation of heavy metal polluted soils. Ecotoxicol Environ Saf 174:714–727 Baligar V, Fageria N, He Z (2001) Nutrient use efficiency in plants. Commun Soil Sci Plant Anal 32(7–8):921–950 Bardos RP, Bakker LM, Slenders HL, Nathanail CP (2011) Sustainability and remediation. In: Dealing with contaminated sites. Springer, pp 889–948 Cesco S, Mimmo T, Tonon G, Tomasi N, Pinton R, Terzano R, Neumann G, Weisskopf L, Renella G, Landi L (2012) Plant-borne flavonoids released into the rhizosphere: impact on soil bio-activities related to plant nutrition. A review. Biol Fertil Soils 48(2):123–149 Charlesworth S, De Miguel E, Ordóñez A (2011) A review of the distribution of particulate trace elements in urban terrestrial environments and its application to considerations of risk. Environ Geochem Health 33(2):103–123 Cohrssen JJ, Covello VT (1999) Risk analysis: a guide to principles and methods for analyzing health and environmental risks. DIANE Publishing

14

M. Naz et al.

Cristaldi A, Conti GO, Jho EH, Zuccarello P, Grasso A, Copat C, Ferrante M (2017) Phytoremediation of contaminated soils by heavy metals and PAHs. A brief review. Environ Technol Innov 8:309–326 Cunningham SD, Anderson TA, Schwab AP, Hsu F (1996) Phytoremediation of soils contaminated with organic pollutants. Adv Agron 56(1):55–114 Devi P, Kumar P (2020) Concept and application of phytoremediation in the fight of heavy metal toxicity. J Pharm Sci Res 12(6):795–804 Eskander S, Saleh H (2017) Phytoremediation: an overview. Environ Sci Eng, Soil Pollut Phytorem 11:124–161 Evangelou MW, Papazoglou EG, Robinson BH, Schulin R (2015) Phytomanagement: phytoremediation and the production of biomass for economic revenue on contaminated land. In: Phytoremediation. Springer, pp 115–132 Fletcher J, Willby N, Oliver DM, Quilliam RS (2020) Phytoremediation using aquatic plants. In: Phytoremediation concepts and strategies in plant sciences. Springer International Publishing, pp 205–260 Gasi´nski A, Kawa-Rygielska J, Mikulski D, Kłosowski G, Głowacki A (2022) Application of white grape pomace in the brewing technology and its impact on the concentration of esters and alcohols, physicochemical parameteres and antioxidative properties of the beer. Food Chem 367:130646 Ghosh M, Singh S (2005) A review on phytoremediation of heavy metals and utilization of it’s by products. Asian J Energy Environ 6(4):18 Giri K, Paliwal R, Suyal DC, Mishra G, Pandey S, Rai J, Verma P (2015) Potential application of plant-microbe interaction for restoration of degraded ecosystems. In: Handbook of research on uncovering new methods for ecosystem management through bioremediation. IGI Global, pp 255–285 Gomes HI (2012) Phytoremediation for bioenergy: challenges and opportunities. Environ Technol Rev 1(1):59–66 Hadley PW, Gathungu P, Koponen JT, Myers P, Sotelo JI (2014) Improving objectives for cleanup sites. Remediat J 24(4):7–26 Havugimana E, Bhople BS, Kumar A, Byiringiro E, Mugabo JP, Kumar A (2015) Soil pollution– major sources and types of soil pollutants. Environ Sci Eng 11:53–86 Holl KD (2017) Research directions in tropical forest restoration. Ann Mo Bot Gard 102(2):237–250 Hooda V (2007) Phytoremediation of toxic metals from soil and waste water. J Environ Biol 28(2):367 Ibrahim RK, Hayyan M, AlSaadi MA, Hayyan A, Ibrahim S (2016) Environmental application of nanotechnology: air, soil, and water. Environ Sci Pollut Res 23(14):13754–13788 Jain P, Andotra A, Aziz A, Kaur P, Mahajan A, Kumar A (2019) Phytoremediation-a miracle technique for waste water treatment. Res J Pharm Technol 12(4):2009–2016 Joseph S, Cowie AL, Van Zwieten L, Bolan N, Budai A, Buss W, Cayuela ML, Graber ER, Ippolito J, Kuzyakov Y (2021) How biochar works, and when it doesn’t: a review of mechanisms controlling soil and plant responses to biochar. GCB Bioenergy 13:1731–1764 Kaim A, Cord AF, Volk M (2018) A review of multi-criteria optimization techniques for agricultural land use allocation. Environ Model Softw 105:79–93 Khan AHA, Kiyani A, Mirza CR, Butt TA, Barros R, Ali B, Iqbal M, Yousaf S (2021) Ornamental plants for the phytoremediation of heavy metals: present knowledge and future perspectives. Environ Res 110780 Kiran B, Pathak K, Kumar R, Deshmukh D (2017) Phycoremediation: an eco-friendly approach to solve water pollution problems. In: Microbial applications vol 1. Springer, pp 3–28 Kumar V, Shahi S, Singh S (2018) Bioremediation: an eco-sustainable approach for restoration of contaminated sites. In: Microbial bioprospecting for sustainable development. Springer, pp 115–136 Kumar V, Kaushal A, Shah MP, Singh K (2021) Phytoaugmentation technology for phytoremediation of environmental pollutants: current scenario and future prospects. In: Bioremediation for environmental sustainability. Elsevier, pp 329–381

1 Sustainable Management of Environmental Contaminants: Factors …

15

Li C, Zhou K, Qin W, Tian C, Qi M, Yan X, Han W (2019) A review on heavy metals contamination in soil: effects, sources, and remediation techniques. Soil Sediment Contam: Int J 28(4):380–394 Liu J, Xin X, Zhou Q (2018) Phytoremediation of contaminated soils using ornamental plants. Environ Rev 26(1):43–54 Masaroviˇcová E, Kráˇlová K (2018) Woody species in phytoremediation applications for contaminated soils. In: Ansari, A., Gill, S., Gill, R., R. Lanza, G., Newman, L. (eds) phytoremediation. Springer, Cham. https://doi.org/10.1007/978-3-319-99651-6_14 Meena VS, Meena SK, Verma JP, Kumar A, Aeron A, Mishra PK, Bisht JK, Pattanayak A, Naveed M, Dotaniya M (2017) Plant beneficial rhizospheric microorganism (PBRM) strategies to improve nutrients use efficiency: a review. Ecol Eng 107:8–32 Mehri A (2020) Trace elements in human nutrition (ii)–an update. Int J Prev Med 11. https://doi. org/10.4103/ijpvm.IJPVM_48_19 Mudhoo A, Garg VK, Wang S (2012) Removal of heavy metals by biosorption. Environ Chem Lett 10(2):109–117 Muthusaravanan S, Sivarajasekar N, Vivek J, Priyadharshini SV, Paramasivan T, Dhakal N, Naushad M (2020) Research updates on heavy metal phytoremediation: enhancements, efficient postharvesting strategies and economic opportunities. In: Green materials for wastewater treatment, pp 191–222 Nedjimi B (2021) Phytoremediation: a sustainable environmental technology for heavy metals decontamination. SN Appl Sci 3(3):1–19 Padhan D, Rout PP, Kundu R, Adhikary S, Padhi PP (2021) Bioremediation of heavy metals and other toxic substances by microorganisms. In: Soil bioremediation: an approach towards sustainable technology, pp 285–329 Padmavathiamma PK, Li LY (2007) Phytoremediation technology: hyper-accumulation metals in plants. Water Air Soil Pollut 184(1):105–126 Padoan E, Passarella I, Dino G, Prati M, Bergante S, Facciotto G, Ajmone-Marsan F (2018) The suitability of short rotation forestry for phytoremediation of urban soil, development of a protocol for urban areas. In: REMEDIATE conference, remediation and land management: research meets practice, pp 37–37 Pandey VC, Bajpai O (2019) Phytoremediation: from theory toward practice. In: Phytomanagement of polluted sites. Elsevier, pp 1–49 Pandey N, Chandra J, Xalxo R, Sahu K (2021) Concept and types of phytoremediation. In: Approaches to the remediation of inorganic pollutants, pp 281–302 Pilon-Smits E (2005) Phytoremediation. Annu Rev Plant Biol 56:15–39 Purakayastha T, Chhonkar P (2010) Phytoremediation of heavy metal contaminated soils. In: Soil heavy metals. Springer, pp 389–429 Rai PK, Lee SS, Zhang M, Tsang YF, Kim K-H (2019) Heavy metals in food crops: health risks, fate, mechanisms, and management. Environ Int 125:365–385 Sadhu SD, Garg M, Kumar A (2018) Major environmental issues and new materials. In: New polymer nanocomposites for environmental remediation. Elsevier, pp 77–97 Sarwar N, Imran M, Shaheen MR, Ishaque W, Kamran MA, Matloob A, Rehim A, Hussain S (2017) Phytoremediation strategies for soils contaminated with heavy metals: modifications and future perspectives. Chemosphere 171:710–721 Saxena G, Purchase D, Mulla SI, Saratale GD, Bharagava RN (2019) Phytoremediation of heavy metal-contaminated sites: eco-environmental concerns, field studies, sustainability issues, and future prospects. Rev Environ Contam Toxicol 249:71–131 Selvi A, Rajasekar A, Theerthagiri J, Ananthaselvam A, Sathishkumar K, Madhavan J, Rahman PK (2019) Integrated remediation processes toward heavy metal removal/recovery from various environments-a review. Front Environ Sci 7:66 Sheoran V, Sheoran A, Poonia P (2010) Soil reclamation of abandoned mine land by revegetation: a review. Int J Soil, Sed Water 3(2):13 Song U, Park H (2017) Importance of biomass management acts and policies after phytoremediation. J Ecol Environ 41(1):1–6

16

M. Naz et al.

Steger U (2000) Environmental management systems: empirical evidence and further perspectives. Eur Manag J 18(1):23–37 Tekere M (2020) Biological strategies for heavy metal remediation. In: Methods for bioremediation of water and wastewater pollution. Springer, pp 393–413 Upcraft T, Guo M (2020) Phytoremediation value chains and modeling. In: Sustainable remediation of contaminated soil and groundwater, pp 325–366 Vautz W, Zimmermann D, Hartmann M, Baumbach JI, Nolte J, Jung J (2006) Ion mobility spectrometry for food quality and safety. Food Addit Contam 23(11):1064–1073 Weyens N, Thijs S, Popek R, Witters N, Przybysz A, Espenshade J, Gawronska H, Vangronsveld J, Gawronski SW (2015) The role of plant–microbe interactions and their exploitation for phytoremediation of air pollutants. Int J Mol Sci 16(10):25576–25604 Wuana RA, Okieimen FE (2011) Heavy metals in contaminated soils: a review of sources, chemistry, risks and best available strategies for remediation. Int Sch Res Net. https://doi.org/10.5402/2011/ 402647 Yan A, Wang Y, Tan SN, Mohd Yusof ML, Ghosh S, Chen Z (2020) Phytoremediation: a promising approach for revegetation of heavy metal-polluted land. Front Plant Sci 11:359 Zhang H, Yuan X, Xiong T, Wang H, Jiang L (2020) Bioremediation of co-contaminated soil with heavy metals and pesticides: influence factors, mechanisms and evaluation methods. Chem Eng J 398:125657

Chapter 2

Environmental Sustainability with Polyhydroxyalkanoates (PHA) as Plastic Alternatives Lucas Vinicius Santini Ceneviva and Takeharu Tsuge

Abstract The plastic pollution in the environment has reached alarming levels. Plastics can also negatively affect living beings through the food web physically and chemically by its breakage to microplastics and release of its additives in the environment. The main culprits for plastic pollution are single-use petrol-based nondegradable plastics, that might take centuries to be completely absorbed by the environment and use non-renewable raw materials. Consequently, many bioplastics have been developed as alternatives for those conventional plastics, but most are either only bio-based, not completely biodegradable in all environments, or have insufficient properties for the desired applications. Polyhydroxyalkanoates are natural polymers produced by many bacteria as energy storage, and in the last decades, they have been developed onto an extensive family of polymers, that can be designed to any application, can be biosynthesized from agricultural, industrial, or food waste, and are inherently biodegradable in all environments, making them a perfect and truly sustainable alternative for current fossil-based plastics. Keywords Plastic pollution · Bioplastics · Polyhydroxyalkanoates · Biosynthesis · Biodegradation

2.1 Introduction Plastic materials have been widely used across innumerable applications due to their unique and versatile properties, low cost, light weight, and simple manufacture (Andrady and Neal 2009). However, due to their high longevity in nature and degradation to small particles, termed “microplastics,” they tend to accumulate and cause numerous negative impacts to the environment (Ya et al. 2021; Qi et al. 2020). In 2019, the world production of plastic products reached 369 million tons (Plastics Europe 2020). For their manufacture, an average of 4% of the extracted fossil fuels are L. V. S. Ceneviva · T. Tsuge (B) Department of Materials Science and Engineering, Tokyo Institute of Technology, Yokohama, Japan e-mail: [email protected] © The Author(s), under exclusive license to Springer Nature Switzerland AG 2022 T. Aftab (ed.), Sustainable Management of Environmental Contaminants, Environmental Contamination Remediation and Management, https://doi.org/10.1007/978-3-031-08446-1_2

17

18

L. V. S. Ceneviva and T. Tsuge

used, but if their consumption continues to grow as expected, this number could reach 20% by 2050 (Rujni´c-Sokele and Pilipovi´c 2017). In addition, overall, from 1950 to 2015, only 9% of plastic waste was recycled, 12% was incinerated, and 79% are accumulating in landfills and in the environment (Geyer et al. 2017). Moreover, due to the COVID-19 pandemic, there was a significant increase in the use of plastic-based medical equipment (e.g., masks, gloves, and hand-sanitizer packages) and single-use packaging plastics, due to the health and safety concerns (Benson et al. 2021), as well as interruptions (i.e., suspensions, cancelations, and postponements) in plastic pollution reduction policies in many countries (da Costa 2021). About 80% of the plastics in the oceans has land origin, either by mismanagement of dumps and landfills, discharge of rainwater, sewage, industrial facilities, or coastal tourism (Kaza et al. 2018), and estimations say that by 2050 there might be more plastics than fish in the oceans (Kaza et al. 2018). Of the litter in the oceans, 62% are food and beverage packaging (Kaza et al. 2018), since 42% of the non-fibrous plastics produced are used as packaging, which generally have a very short life cycle (Geyer et al. 2017). Additionally, although the scientific, political, and public concern of plastic pollution in the oceans, there are few studies regarding microplastic pollution in soil, which is supposed to have a much greater accumulation than in the oceans (Ya et al. 2021; Qi et al. 2020). Similar to the harm faced by aquatic organisms, terrestrial organisms can also suffer from physical and chemical damage (e.g., on their immune systems, feeding behavior, and development) of the bioaccumulation of plastics and their additives, which is also spread through the food web (Ya et al. 2021; Qi et al. 2020). Moreover, microplastics can also affect the soil organic carbon and nitrogen cycling, its microbial activity, and nutrient transfer (Qi et al. 2020). Consequently, there is great interest in the production of bio-based and/or biodegradable plastics. Generically known as “bioplastics,” they can be classified into three types (Ross et al. 2017): • Non-biodegradable from renewable sources, e.g., polyethylene (PE), polypropylene (PP), and polyethylene terephthalate (PET) • Biodegradable from petroleum origin, e.g., polycaprolactone (PCL) and polybutylene adipate terephthalate (PBAT) • Biodegradable from renewable sources, e.g., polylactic acid (PLA), polyhydroxyalkanoate (PHA), polybutylene succinate (PBS), and starch and cellulose derivatives used in blends. One type of bio-based and biodegradable bioplastic that has stood out is the polymer family of polyhydroxyalkanoates (PHAs), because of its versatility, biocompatibility, and being completely biodegradable in any medium (Chen et al. 2015). PHAs are aliphatic polyesters naturally produced by more than 300 species of grampositive and gram-negative bacteria, as intracellular energy reserve under conditions of excess carbon sources and nutrients limitation (Anjum et al. 2016). Through three major metabolic routes, more than 160 types of PHA monomers of small and mediumlength chains are biosynthesized by amino acids, sugars, and fatty acids (Chen et al. 2015; Anjum et al. 2016; Choi et al. 2020b), generating various homopolymers and

2 Environmental Sustainability with Polyhydroxyalkanoates (PHA) …

19

copolymers with different side groups and main chain lengths and, consequently, with a wide variety of properties (Chen et al. 2015; Anjum et al. 2016).

2.2 Structure and Properties of Polyhydroxyalkanoates The general chemical structure of the PHA polymer family is depicted in Fig. 2.1. Basically, by increasing the number of methylene groups in its backbone chain, “x,” and the pure (R)-enantiomeric side-chain functional group, “R,” innumerable monomer types are possible as homopolymers or constituents of copolymers PHAs (Taguchi et al. 2012). The first PHA to be identified was the poly(3-hydroxybutyrate) (in which x = 1 and R = methyl group), P(3HB), in Bacillus megaterium by Lemoigne (1926), in the Pasteur Institute. In the following years, P(3HB) was also identified in many other microorganisms, suggesting its role as an intracellular carbon and energy reserve, similar to starch and glycogen, in many types of bacteria (Williamson and Wilkinson 1958; Macrae and Wilkinson 1958; Doudoroff and Stanier 1959; Forsyth et al. 1958; Dawes and Senior 1973). Intracellularly, PHAs are stored inside proteinic granules, with 0.2–0.5 μm in size (Dawes and Senior 1973) and able to accumulate up to 90% of PHA related to the total dry cell weight (Wang and Lee 1997). It has been reported that these PHA granules are also responsible to increase the bacterial resistance to many physical and chemical stresses (Obruca et al. 2018). Moreover, although isolated PHAs, like P(3HB), are known for having high crystallinity (between 60 and 80%) (Choi et al. 2020a), in vivo (i.e., inside the granules of the cell), they tend to present amorphous structures (Sedlacek et al. 2019). After the discovery of PHAs in 1926, there were only few developments in the field in the next decades as it failed to attract research and commercial interests. This is mainly due to the initial belief that 3-hydroxybutyrate (3HB) monomer was the only constituent of this new class of natural polymers (Sudesh et al. 2000). Although P(3HB) presents mechanical properties similar to commodity plastics, like polypropylene (PP), and having good barrier properties, it also has low thermal stability (due to its melting temperature being near to its degradation temperature) Fig. 2.1 General chemical structure of polyhydroxyalkanoate

20

L. V. S. Ceneviva and T. Tsuge

(McAdam et al. 2020) and is stiff and brittle (due to the phenomenon of secondary crystallization, that deteriorates its mechanical properties) (Taguchi et al. 2012), limiting its applications. The identification of other hydroxyalkanoate (HA) monomers than 3HB by Wallen and Rohwedder (1974) led to a revolution in the field, as the incorporation of other monomer unit into P(3HB) could improve its properties significantly (Sudesh et al. 2000). Consequently, only 20 years later, by the use of different bacteria, structurally related carbon sources, and metabolic engineering, 91 types of HA were already biosynthesized (Steinbüchel and Valentin 1995). By 2013, more 64 monomers were computed, summing to 155 different HA monomers (Agnew and Pfleger 2013), and as new monomers are discovered or developed every year, it is considered that there are now over 160 different HA monomers (Choi et al. 2020b). As a result of the identification of new HA, it became a common practice to categorize them as short-chain-length PHA (scl-PHA), medium-chain-length PHA (mcl-PHA), and long-chain-length PHA (lcl-PHA) (Luengo et al. 2003). scl-PHAs are composed of HA monomers with 3–5 carbons (C3-C5) (Luengo et al. 2003), have properties similar to thermoplastics, have high crystallinity, are hard and brittle, and have low elongation at break (Lu et al. 2009; Muthuraj et al. 2021). They are mainly represented by the monomers 3HB, 4-hydroxybutyrate (4HB), and 3hydroxyvalerate (3HV) (Muthuraj et al. 2021). In opposition, mcl-PHAs, that have 6–14 carbon units (C6-C14) (Luengo et al. 2003), are elastomeric polymers with low crystallinity, having low degrees of polymerization ( 1200

5

14

44

n.a.2 n.a.

591

1320

1000

230

7

35

400

620

12

Elongation at break (%)

30

45

149

9350

3500

1–3

1700

200

1420

Young’s modulus (MPa)

(continued)

Rai et al. (2011)

Tanadchangsaeng et al. (2009)

Tanadchangsaeng et al. (2009)

Tanadchangsaeng et al. (2009)

Doi et al. (1995)

Doi et al. (1995)

Doi et al. (1995)

Sudesh et al. (2000)

Doi (1990)

Doi (1990)

Yamana et al. (1996)

Doi et al. (1990)

Saito and Doi (1994)

Saito and Doi (1994)

Saito and Doi (1994)

Horvath et al. (2018)

Farah et al. (2016)

Brydson (1999)

Sudesh et al. (2000)

Sudesh et al. (2000)

Furutate et al. (2021b)

References

2 Environmental Sustainability with Polyhydroxyalkanoates (PHA) … 23

197

191

171

140, 150

149, 167

141, 158

140, 157

18

15

11

11

−1

−9, 19

−8, 25

−9, 34

29.7

P(3H2MB)

P(3H2MB-co-8% 3HB)

P(3H2MB-co-20% 3HB)

P(3H2MB-co-75% 3HB)

P(3HB-co-15% LA)

P(3HB-co-29% LA)

P(3HB-co-47% LA)

P(2HB)

98.7

8.5

7

7

10

n.a.

n.a.

n.a.

583

n.a.

n.a.

n.a.

11

8

Tensile strength (MPa)

75

153

154

194

n.a.

n.a.

n.a.

37

n.a.

n.a.

n.a.

180

118

Young’s modulus (MPa)

173

86

154

75

n.a.

n.a.

n.a.

520

n.a.

n.a.

n.a.

270

226

Elongation at break (%)

Matsumoto et al. (2013)

Yamada et al. (2011)

Yamada et al. (2011)

Yamada et al. (2011)

Watanabe et al. (2015)

Furutate et al. (2021a)

Furutate et al. (2021a)

Furutate et al. (2021b)

Curley et al. (1996)

Honma et al. (2004)

Mizuno et al. (2014)

Hiroe et al. (2016)

Hiroe et al. (2016)

References

low density polyethylene; PS: polystyrene; PET: polyethylene terephthalate; P(3H5PhV): poly(3-hydroxy-5-phenylvalerate); P(3H5PxV): poly(3hydroxy-5-phenoxyvalerate); P(3H5pMPhV): poly(3-hydroxy-5-(p-methylphenyl)valerate) 2 n.a.: data not available 3 n.d.: not detected

1 LDPE:

88

23

P(3H5PxV)

P(3H5pMPhV) 95

82

n.d.

15.7

P(3HDD)

P(3H5PhV)

T m (°C)

n.d.3

T g (°C) 70

P(3HD)

−46

Polymer1

Table 2.1 (continued)

24 L. V. S. Ceneviva and T. Tsuge

2 Environmental Sustainability with Polyhydroxyalkanoates (PHA) …

25

2.3 Enzymes and Metabolic Pathways Involved in PHA Biosynthesis 2.3.1 PHA-Producing Bacteria From the discovery of P(3HB) in Bacillus megaterium in 1926 (Lemoigne), more than 300 species of gram-positive and gram-negative bacteria have already been identified as PHA producers (Anjum et al. 2016), with most of them being gram-negative bacteria (Lu et al. 2009; Valappil et al. 2007). Gram-positive PHA-producing bacteria have the advantages of not having the lipopolysaccharide (LPS) outer membrane, which favors its use in biomedical applications as LPS releases endotoxins that leads to strong immunogenic reactions, and of having the metabolic ability to biosynthesize 3HV and 4HB monomers from unrelated, and thus unexpensive carbon sources (Valappil et al. 2007). However, they have been reported to present much lower PHA contents than gram-negative PHA-producing bacteria, as well as most strains can only produce scl-PHAs, thus hindering its industrial use (Valappil et al. 2007; Tan et al. 2014). The main representative is the Bacillus genus, which have many interesting characteristics: (1) They are relatively more thermostable than most bacteria, (2) they are able to utilize a wide range of carbon sources for PHA production, (3) their PHA synthesizing enzymes, i.e., PHA synthases, have alcoholysis activity that can be useful to control the molecular weight of PHAs and introduce block structures into the copolymers, but (i) their production of endospores for survival in stressful environments can downturn the energy resources from PHA production, and (ii) their natural production of PHA degrading enzymes, i.e., PHA depolymerases, can lead to lower molecular weight PHAs (Valappil et al. 2007; Tsuge et al. 2015). Some examples of other relevant gram-positive PHA-producing bacteria are in genera Streptomyces, Rhodococcus, Clostridium, and Nocardia (Lu et al. 2009). Between gram-negative PHA-producing bacteria, Ralstonia eutropha H16, also known as Cupriavidus necator H16, is a typical scl-PHA producer and is considered the model PHA-producing strain due to many attractive characteristics (Reinecke and Steinbüchel 2009): (1) It is able to use a broad range of carbon sources for its metabolism, as sugars, organic acids, and C1 gases, due to it being both heterotrophic and autotrophic (Tan et al. 2014); (2) knowledge of its genome sequence and PHA synthase crystal structure is available, and thus, precise bioengineering of its genome and synthase is possible (Pohlmann et al. 2006; Kim et al. 2017a); and (3) it is able to accumulate high amounts of PHA in certain culture conditions, e.g., from 67 to 89% (Tan et al. 2014). Other gram-negative bacteria of interest are many species of the Pseudomonas genus, e.g., P. putida, P. mendocina, P. fluorescens, and P. oleovorans, as they are the main mcl-PHA producers by using unrelated and related carbon sources (Sharma et al. 2020). Some of them are even able to synthesize scl-co-mcl-PHAs, as Pseudomonas sp. 61-3 and Pseudomonas stutzeri 1317 (Matsusaki et al. 1998; Chen et al. 2004). There has also been a great interest in the use of extremophiles bacteria, as they can survive in extreme habitat conditions,

26

L. V. S. Ceneviva and T. Tsuge

e.g., high or low temperature, high or low pH, high salinity, high osmotic pressure, under radiation, under desiccation, and in man-made toxic environments, as that means they can be used to produce PHA in unsterile and continuous way in stressful conditions for most other bacteria (Obulisamy and Mehariya 2021; Chen and Jiang 2018). One of them is the Halomonas bluephagenesis strain, which is a halophilic and alkaliphilic bacteria isolated from a salt lake in China, that have high grow (Tan et al. 2011), its genome was completely sequenced in 2011 (Cai et al. 2011), it has been continually engineered to improve its PHA synthesis (Zhao et al. 2017) and diversity (Ye et al. 2018) and easier downstream separation (Shen et al. 2019), and recently, by modifications in its LPS outer membrane, it was finally possible to incorporate plasmids by electroporation transformation (before, only techniques like CRISPR/Cas9, conjugation, and suicide plasmid-mediated two-step homologous recombination were possible for genetic manipulation) (Wang et al. 2021; Zheng et al. 2020). Although Escherichia coli is not a native PHA producer, since Slater et al. (1988) and Schubert et al. (1988) successfully expressed PHB synthase genes through plasmids and cosmids and produced PHB, it has become one of the most used bacteria for production of various PHAs in research laboratories and industry by construction of metabolic pathways (Chen 2009; Li et al. 2007) due to its simple culture conditions, rapid growth, biochemical and physiological comprehension, metabolic versatility, and easy genetic and genomic engineering manipulation (Pontrelli et al. 2018). Other gram-negative PHA-producing bacteria genera and species worth mentioning are Allochromatium vinosum, Aeromonas caviae, Aeromonas hydrophila, Rhodospirillum rubrum, Methylocystis parvus, Azotobacter spp., Nocardia spp., and Alcaligenes spp. (Choi et al. 2020b; Chen 2009; McAdam et al. 2020). In an effort to reduce costs, mixed microbial consortia (MMC) have been studied as alternatives to pure culture of PHA-producing bacteria. As there is no need to keep an axenic culture, there will be lower operational cost in sterilization, equipment, and process control (Bhalerao et al. 2020). Moreover, as the MMC can naturally adapt to various waste substrates, substantial reductions in PHA production costs are possible, as it is estimated that 40–50% of the cost comes from the raw materials, with 70–80% of it coming from the carbon sources (Reis et al. 2003). Generally, MMC production is based in a three-stage process: (1) fermentation stage to convert waste substrate to volatile fatty acids (VFA, precursors for PHA biosynthesis), (2) feast-famine cycle condition of substrates to enrich the MMC with bacteria that can produce large quantities of PHA (as they need this ability to survive the famine stage), and finally (3) production in which the MMC enriched with PHA-producing bacteria will convert the VFA to PHAs (Guho et al. 2020).

2.3.2 Enzymes and Other Proteins Although this great diversity in PHA-producing bacteria, they all have in common the ability to synthesize enzymes that can convert the carbon sources transported to

2 Environmental Sustainability with Polyhydroxyalkanoates (PHA) …

27

its intracellular region to direct PHA-precursors and then polymerize them by ester bonds between the carboxyl group of one monomer with the hydroxyl group of the next monomer (Steinbüchel and Valentin 1995). Between the numerous enzymes involved in the biosynthesis of PHAs and formation of their granules, the PHA synthases are the most important as they are responsible for PHA polymerization; thus, they also affect the monomer composition, molecular weight, polydispersity, and productivity (Kim et al. 2017a). Moreover, their substrate specificity determines which substrates can be used for PHA polymerization and thus which types of monomers can be formed (Kim et al. 2017a). By 2003, more than 59 different PHA synthase genes were reported to be cloned and characterized (Rehm 2003), and in the last years, a great number of putative PhaCs have been identified (Yang et al. 2013; Foong et al. 2014). They are commonly abbreviated as “PhaC” and can be classified according to their substrate specificity and subunit composition into four classes. Class I synthases are represented by Ralstonia eutropha, have substrate specificity preference for scl-HAs, and are composed of one type of subunit, PhaC, with 61–73 kDa of molecular weight, and form a homodimer. Class II synthases are represented by Pseudomonas oleovorans, have substrate specificity preference for mcl-HAs, and are composed of one type of subunit, PhaC, with 60–65 kDa, encoded in two synthase genes, phaC1 and phaC2, and form a homodimer. Class III synthases are represented by Allochromatium vinosum, have substrate specificity preference for scl-HAs, are composed of two subunits, PhaC and PhaE, both with ≈40 kDa each, and form heterodimers. Finally, Class IV synthases are represented by Bacillus megaterium, have substrate specificity preference for scl-HAs, are composed of two subunits, PhaC with ≈40 kDa and PhaR with ≈22 kDa, and form heterodimers (Rehm 2003; Mierzati and Tsuge 2020). It should be noted that although not completely understood, both subunits PhaE and PhaR are necessary for PHA polymerization in classes III and IV, respectively (Tsuge et al. 2015). Table 2.2 summarizes the differences between the PHA synthase classes. However, there are also some exceptions of strains that could biosynthesize sclco-mcl-PHA, as Aeromonas caviae (Fukui and Doi 1997) from Class I, Pseudomonas sp. 61–3 (Matsusaki et al. 1998) and Pseudomonas stutzeri 1317 (Chen et al. 2004) from Class II, Thiocapsa pfennigii (Liebergesell et al. 2000) from Class III, and Bacillus cereus from Class IV (Caballero et al. 1995). The structure of the PhaCs is composed of a N-terminal domain, that can affect the PHA polymerization by localization of the enzyme to the PHA granules and its stabilization, and a C-terminal catalytic domain (Kim et al. 2017b). The C-terminal domain is composed of a CAP-subdomain, which by its conformation can inhibit the enzyme activity by blocking the entrance of substrates, and a α/β core subdomain, in which is localized the Cys-His-Asp catalytic triad. In it, Cys might act as a covalent nucleophile, His as an electron donor, and Asp as a general base (Kim et al. 2017a; Chek et al. 2017). Next to the Cys of the catalytic triad, there is a conserved region present in all PhaCs composed of a lipase box with generic amino acid sequence of (GX-C-X-GG), in which X is a non-specific amino acid, making PhaCs into the lipase superfamily of enzymes, which generally have Ser instead of Cys in the catalytic

PhaC1 and PhaC2 (60–65 kDa)

PhaC and PhaE (≈40 kDa each)

PhaC and PhaR (≈40 kDa) and (≈20 kDa)

IV

PhaC (61–73 kDa)

II

I

Subunits

III

Class

Table 2.2 Classification of PHA synthases

scl-HA-CoA

scl-HA-CoA

mcl-HA-CoA

scl-HA-CoA

Substrate specificity

scl-PHA

scl-PHA

mainly mcl-PHA

mainly scl-PHA

Type of PHA

Bacillus megaterium

Allochromatium vinosum

Pseudomonas oleovorans

Ralstonia eutropha

Representative microorganism

28 L. V. S. Ceneviva and T. Tsuge

2 Environmental Sustainability with Polyhydroxyalkanoates (PHA) …

29

center (Jia et al. 2000; Nambu et al. 2020). However, many PhaCs do not follow this lipase-box sequence, with changes mainly in the Gly, which is substituted by other amino acids, like Ala and Ser. Therefore, Nambu et al. (2020) studied substitution of Gly to other amino acids by point mutagenesis and concluded that PhaCs’ box sequence could be expanded to [GAST]-X-C-X-[GASV]-[GA] without significant impairment to PHA accumulation and/or catalytic activity. There is great interest in engineering those synthases to increase its substrate specificity or have more precise control over the structure and molecular weight of the biosynthesized PHA, but due to lack of available crystal structure of PHA synthases, most studies used random mutagenesis and semi-rational approaches, e.g., error-prone PCR and formation of chimeras between two different PHA synthases, respectively (Choi et al. 2020a). For instance, by introducing single substitution mutations in the amino acids N149S (Ans149 → Ser) and D171G (Asp171 → Gly), called double mutation NSDG, the PhaC of Aeromonas caviae presented the ability to biosynthesize P(3HB-co-3HHx) with higher 3HHx content than the wild type (Tsuge et al. 2007). Recently, the crystal structure of catalytic subunit PhaC of PHA synthases from Ralstonia eutropha (Kim et al. 2017a) and Chromobacterium sp. USM2 (Chek et al. 2017) was solved, which will aid onto higher understanding of the catalytic mechanism of PHA polymerization and could also allow for rational design of PHA synthases (Taguchi et al. 2012). Indeed, Harada et al. (2021) was able to increase the 3HHx content in P(3HB-co-3HHx) even further with PhaCAc NSDG by creating a homology model of the PhaCAc ’s crystal structure based on the crystal structure of the catalytic subunit of Ralstonia eutropha (Kim et al. 2017a) to predict the contents of its substrate pocket and introduce a third mutation in it. Moreover, PHA depolymerase, known as PhaZ, is responsible for PHA biodegradation and also influences PHA production and properties as the synthesis and depolymerization through PhaCs and PhaZs are dynamic biochemical reactions, occurring simultaneously to supply bacteria with energy resources, and the lack of PHA depolymerase genes in the host strain could result in higher production and/or higher molecular weight (Cai et al. 2009; Arikawa et al. 2016). PHA depolymerases will be discussed in detail in Sect. 2.5. Phasins are the proteins of highest quantity on the surface of the granules (Wieczorek et al. 1995), they are amphiphilic molecules with the hydrophobic part turned to the polymer inside the granule and the hydrophilic part to the cytoplasm, they have low molecular weight (11–25 kDa) (Pieper-Furst et al. 1994; Wieczorek et al. 1995), and they have several functions. Their primary function is to act as a barrier between the polymers in the granules and the cytoplasm, thus stabilizing them and preventing their coalescence (Wieczorek et al. 1995), but in recent years, many other functions were discovered. Phasins are reported to regulate the formation, size, number, localization, and distribution of PHAs’ granules, thus affecting the PHA accumulation in the cell (Mezzina et al. 2021; Zhou et al. 2012; de Almeida et al. 2007), as well as promoting the microorganism growth and increasing its resistance to stress (de Almeida et al. 2007; de Almeida et al. 2011). More interesting, several studies found that phasins also interact with PhaCs and PhaZs through several mechanisms, promoting PHAs’ synthesis and degradation (Mezzina et al. 2020; Ushimaru et al.

30

L. V. S. Ceneviva and T. Tsuge

2014). Some examples of phasins and their microorganism of origin are PhaPs (C. necator and B. cereus), phaI (P. putida), and PhaFs (P. oleovorans and P. putida KT2442) (Sznajder et al. 2015; Ushimaru et al. 2014; Kihara et al. 2017; Dinjaski and Pietro 2013; Galán et al. 2011; Prieto et al. 1999). There are also other granule-associated proteins which are not considered phasins, as PhaR, PhaQ, and PhaM. PhaR negatively regulates phasin expression, by binding to them when cultivation conditions are not favorable for PHA biosynthesis or in final stages of PHA accumulation, but on the beginning of PHA production, they bind to the granules, allowing phasin production (Pötter et al. 2002). Although PhaQ does not have significant amino acid sequence similarity with PhaRs, it has similar function by also negatively regulating phasin expression (Lee et al. 2004). PhaM have similar functions to phasins, as it also regulates the formation, size, number, and distribution of PHAs’ granules (Pfeiffer et al. 2011; Ushimaru and Tsuge 2016). Moreover, PhaM are also considered primers for PHA biosynthesis, as they activate it by forming complexes with PhaCs (Pfeiffer and Jendrossek 2014), although this might not be the case of every bacterium (Ushimaru and Tsuge 2016). Besides PHA synthases and depolymerases, phasins, and regulator proteins, other enzymes of importance are the numerous other enzymes that participate in intermediate steps of their metabolic pathways.

2.3.3 Metabolic Pathways So far, 14 natural or designed metabolic pathways were reported, with three pathways being the most common and studied (Meng et al. 2014). Pathway I, represented by Ralstonia eutropha, uses sugar, fatty acids, and amino acids as unrelated carbon sources to produce scl-PHAs. First, the carbon source, e.g., glucose, is converted to acetyl-CoA through inherent metabolic pathways of the bacteria, e.g., glycolysis; then, two acetyl-CoA molecules are condensed to acetoacetyl-CoA by the enzyme 3-ketothiolase (PhaA). Next, NADPH-dependent acetoacetyl-CoA is reduced to (R)-3HB-CoA by acetoacetyl-CoA reductase (PhaB), using NADPH as a cofactor. Finally, PhaC polymerizes (R)-3HB-CoA to P(3HB) by esterification (Sagong et al. 2018; Mierzati and Tsuge 2020). Pathway II, known as β-oxidation pathway, is represented by Pseudomonas spp. and uses fatty acids as related carbon sources to produce mcl-PHAs. First, by acyl-CoA synthetase (FadD), fatty acids are oxidated to their CoA thioester, acyl-CoA, which as it enters the β-oxidation cycle will be catabolized in two carbons by each step of the cycle, being oxidated to enoyl-CoA by acyl-CoA dehydrogenase (FadE). EnoylCoA can then either be converted to (R)-3-hydroxyacyl-CoA, a direct precursor for mcl-PHAs, by (R)-3-hydroxyacyl-CoA hydratase (PhaJ), or oxidated to (S)-3hydroxyacyl-CoA by acyl-CoA dehydrogenase (FadB). Next, (S)-3-hydroxyacylCoA is oxidated to 3-ketoacyl-CoA, by acyl-CoA dehydrogenase (FadB), which can either be converted to (R)-3-hydroxyacyl-CoA by 3-ketoacyl-ACP reductase (FabG)

2 Environmental Sustainability with Polyhydroxyalkanoates (PHA) …

31

or oxidated to an acyl-CoA with two carbons less by 3-ketoacyl-ACP dehydrase (FabA), reinitiating the cycle, and releasing acetyl-CoA, which can also be converted to (R)-3HB-CoA by the Pathway I. Finally, (R)-3-hydroxyacyl-CoA and (R)-3HBCoA can be polymerized by PhaCs to mcl- or scl-PHAs, respectively (Lu et al. 2009; Choi et al. 2020a; Mezzina et al. 2021). Pathway III, known as fatty acid de novo biosynthesis pathway, is also common in Pseudomonas spp. and uses sugar, fatty acids, and amino acids as unrelated carbon sources to produce mcl-PHAs. While in β-oxidation, the number of carbons is reduced by two in each cycle, in the fatty acid de novo biosynthesis, the number of carbons is increased by two in each cycle. First, as in Pathway I, the carbon source is converted to acetyl-CoA, which is carboxylated to malonyl-CoA by acetylCoA carboxylase (Acc) and then to malonyl-acyl carrier protein (ACP) by malonylCoA:ACP transacylase (FabD). Next, malonyl-ACP can either be condensed with acetyl-CoA to acetoacetyl-ACP by 3-ketoacyl-ACP synthase III (FabH) or condensed with acyl-ACP to 3-ketoacyl-ACP by 3-ketoacyl-ACP synthase I (FabB) and 3ketoacyl-ACP synthase II (FabF). Acetoacetyl-ACP can be further converted to acetoacetyl-CoA by FabH and then to (R)-3HB-CoA by 3-ketoacyl-ACP reductase (FabG). On the other hand, 3-ketoacyl-ACP can either be converted to 3-ketoacylCoA by FabH or to (R)-3-hydroxyacyl-ACP by FabG. In sequence, 3-ketoacylCoA is converted to (R)-3-hydroxyacyl-CoA by FabG, and (R)-3-hydroxyacyl-ACP can either be converted to (R)-3-hydroxyacyl-CoA by 3-hydroxyacyl-CoA:ACP transacylase (PhaG) or to enoyl-ACP by 3-hydroxyacyl-ACP dehydrase (FabA). Enoyl-ACP is then converted to acyl-ACP by enoyl-ACP reductase (FabI), starting a new step in the cycle. Finally, (R)-3-hydroxyacyl-CoA and (R)-3HB-CoA can be polymerized by PhaCs to mcl- or scl-PHAs, respectively (Lu et al. 2009; Choi et al. 2020a; Mezzina et al. 2021). Figure 2.2 summarizes the three main metabolic pathways described above.

2.4 Carbon Sources As demonstrated by Fig. 2.2, PHA-producing bacteria are able to metabolize mainly sugars and fatty acid molecules as carbon sources for PHA production. Consequently, natural or industrially processed raw materials composed of complex mixtures of them, as vegetable oils or wastes (of agricultural, industrial, or municipal origin), could also be used as cheaper alternatives to single molecules as carbon sources for PHA production as long as the bacteria have metabolic pathways to process them into direct precursors, either naturally or engineered. Sugars are monosaccharides and disaccharides, like sucrose, glucose, fructose, xylose, galactose, lactose, and arabinose. Many bacteria have inherent metabolism to convert them to unrelated precursors for PHA biosynthesis. Due to their easy metabolic assimilation, low cost, compared to other pure raw materials for PHA production, and relatively high cell productivity and polymer accumulation, they

Fig. 2.2 Metabolic pathways for PHA biosynthesis

32 L. V. S. Ceneviva and T. Tsuge

2 Environmental Sustainability with Polyhydroxyalkanoates (PHA) …

33

have been used by many companies as the main carbon source for P(3HB) and its copolymers industrial production (Jiang et al. 2016; Agnew and Pfleger 2013; Leong et al. 2014; Chen 2009; Choi et al. 1998; Wang and Lee 1997). Moreover, polysaccharides, like starch and cellulose, present in plants as energy storage and structural function, can also be used as carbon sources, either directly or after some form of pre-treatment to break them into smaller molecules (Govil et al. 2020; Castilho et al. 2009). Therefore, there is great interest in the efficient and productive use of selected polysaccharides-based crops and wastes as carbon sources for PHA production. Some agricultural products of interest are plants and fruits juice (e.g., sugarcane, sugar beet, pineapple), corn syrup, corn starch, potato starch, and cassava starch, while wastes as molasses (e.g., sugarcane, sugar beet), cheese whey, wheat and rice bran, sugarcane bagasse, oil palm frond, wheat and rice straw, sugarcane vinasse, etc., are also being evaluated for use with wild (pure or MMC) or recombinant PHA-producing bacteria (Anjum et al. 2016; Rodriguez-Perez et al. 2018; Nielsen et al. 2017; Pakalapati et al. 2018; Castilho et al. 2009; Aslan et al. 2016; Raza et al. 2018; Jiang et al. 2016). Fatty acids and fatty acids-based substrates, are of even greater interest, as they can be used as related carbon sources to obtain specific monomeric components through the β-oxidation pathway, and theoretically, they also have double yield of g of PHA/g of substrate than sugars (0.3–0.4 g P(3HB)/g of glucose versus 0.6– 0.8 g PHA/g of fatty acids in oils) (Akiyama et al. 2003). However, due to their high cost, toxicity for the cells, and immiscibility with water, pure fatty acids are generally limited to low concentrations or production in smaller scales (Zhuang et al. 2014; Jaramillo-Sánchez and Alcaraz-Zapata 2020). Moreover, as for sugars, many agricultural products can be used as sources of fatty acids, with vegetable oils standing out due to their high concentration and variety of fatty acids (Orsavova et al. 2015). Some examples of agricultural products and wastes being studied as fatty acid sources for PHA production are soybean oil, palm oil, coconut oil, corn oil, palm kernel oil, jatropha oil, canola oil, sunflower oil, olive oil, waste frying oil, tallow, animal fat, waste fish oil, oil from spent coffee ground, wastewater (from several industries), plant oil mills waste, manure, etc. (Surendran et al. 2020; Anjum et al. 2016; Ciesielski et al. 2015; Talan et al. 2020; Du et al. 2012; Magdouli et al. 2015; Sohn et al. 2021). However, it should be highlighted that the use of crops that are also used for food production can also lead to higher environmental and humanitarian costs, with their effects on soil, and possible decrease of availability and higher inflation of food products that share the same origin in undeveloped countries (Bishop et al. 2021). On the other hand, the use of wastes would have the opposite effect, giving practical and economical use to materials that would originally be discarded, and thus giving PHA an even better environmental impact as a sustainable biodegradable material. Furthermore, other carbon sources of interest are amino acids and C1 substrates. Amino acids can act either as unrelated or related precursors for PHA. For instance, (1) Yu et al. (2009) was able to synthesize a terpolyester containing 3HB, 3HV, and 4-hydroxyvalerate (4HV) using levulinic acid as the sole carbon source or in conjunction with glucose; (2) in Saika et al. (2014), leucine was able to be converted to 3-hydroxy-4-methylvalerate (3H4MV) by recombinant E. coli expressing the

34

L. V. S. Ceneviva and T. Tsuge

required metabolism; and (3) Mizuno et al. (2018) was able to biosynthesize PHAs containing 2HA units 2H4MV, 2H3PhP, 2H3MB, and 2H3MV from leucine, phenylalanine, valine, and isoleucine, respectively. Moreover, there are many studies on capturing carbon from C1 gases CO, CO2 , or CH4 by either autotrophic PHAproducing bacteria or recombinant strains, thus being a solution for reduction of these pollutants in the air as well as being a cheap carbon source for PHA production (Dürre and Eikmanns 2015; Khosravi-Darani et al. 2013). One bacterium that has being greatly researched for that is Ralstonia eutropha, as it is considered the model PHA-producing bacteria and can use the Calvin-Benson-Bassham (CBB) cycle for carbon fixation of CO2 (Reinecke and Steinbüchel 2009; Bowien and Kusian 2002; Tanaka et al. 1995; Miyahara et al. 2020; Thorbecke et al. 2021).

2.5 PHA Biodegradation and Life Cycle Analysis The main advantage of PHAs as biodegradable materials is that as they are naturally produced, many bacteria and fungi in various environments have the ability to biodegrade them through PHA depolymerases and other enzymes like esterases and lipases, by hydrolyzing their ester bonds (Sudesh et al. 2000; Jaeger et al. 1995). The PHA is initially converted to water-soluble oligomers and monomers and eventually to CO2 and H2 O, in aerobic conditions, or CO2 and CH4 , in anaerobic conditions (Sudesh et al. 2000; Meereboer et al. 2020).

2.5.1 PHA Depolymerases Near 600 PHA depolymerases have been reported hitherto, which are classified as extracellular (with scl-PHA or mcl-PHA substrate specificity) or intracellular (with scl-PHA or mcl-PHA substrate specificity) (Knoll et al. 2009). Both types of depolymerase act on different substrates; while intracellular depolymerase is present into the cell cytoplasm and degrades the amorphous PHA in protein-coated granules inside the bacteria cells for carbon and energy acquisition, the extracellular depolymerase secreted outer the cell acts on semi-crystalline PHA from lysed PHA-producing bacteria or PHA materials on the environment (Choi et al. 2020a). The structure of PHA depolymerases is composed of a C-terminal substrate binding domain, an N-terminal catalytic domain, and a linker region attaching both domains, which is common between many other depolymerizing enzymes (Sudesh et al. 2000). The catalytic domain contains a Ser-His-Asp catalytic triad, with Ser as the active center, and with it a lipase box (G-X-S-X-G), which can be positioned either at the middle of the catalytic domain or next to the N-terminal, although some intracellular PhaZs do not possess lipase box (Sudesh et al. 2000; Knoll et al. 2009; Suzuki et al. 2021). In the case of marine PhaZs, they have significant differences against terrestrial PhaZs: (1) The lipase box is only found at the center of the catalytic

2 Environmental Sustainability with Polyhydroxyalkanoates (PHA) …

35

domain; (2) they have two substrate binding domains, making their molecular masses higher than terrestrial PhaZs (60–70 kDa against 40–50 kDa of terrestrial PhaZs); (3) they also have lower average substrate binding constant, which means they have lower binding to substrates; and (4) the linker domain is composed of fibronectin type III and cadherin, while in terrestrial PhaZs is composed of fibronectin type III and threonine (Suzuki et al. 2021). Moreover, similar to PhaCs, that tend to produce enantiomeric pure (R)-PHAs, PhaZs also have preference for (R)-HA units for enzyme activity, with (S)-HA units showing low hydrolysis degradation or not inducing the production of PhaZs (Sudesh et al. 2000; Suzuki et al. 2021). However, besides PhaZ’s activity and substrate specificity, the rate of biodegradation on PHAs also depends in material properties and environmental factors (Choi et al. 2020a). The biodegradation is affected either by the crystallinity, crystal size, lamellar thickness, molecular weight, thermal properties, monomer type and composition, surface area and shape, additives, and physical form of the material, as well as by the location, sunlight, UV light, salinity, temperature, moisture, pH, nutrient supply, presence or absence of oxygen, and composition and abundance of microorganisms of the environment (Choi et al. 2020a; Sudesh et al. 2000; Ong et al. 2017; Suzuki et al. 2021). The crystallinity is considered of great importance in extracellular depolymerization, as PHA polymerases selectively bind to crystalline regions, but the catalytic domain primarily hydrolyzes the amorphous phase; thus, the biodegradation rate decreases with higher crystallinity, but crystalline regions are essential for starting the biodegradation process (Sudesh et al. 2000).

2.5.2 Biodegradation Evaluation About the polymer biodegradation evaluation itself, there are many different conditions and methods that could be used: (1) The sample condition could be either in its final product shape, as a film, or as powder (Harrison et al. 2018); (2) the environmental conditions could either be natural, simulated (mimicking natural environment), or in industrially controlled degradation (e.g., industrial composting and anaerobic digestion) (Kjeldsen et al. 2021; SAPEA 2020); (3) then, the biodegradation itself could be directly assessed by measuring the concentration of degradation products (e.g., 3-hydroxyalkanoic acids, carbon dioxide, or methane release) or the weight loss of the sample, as well as by oxygen consumption, and changes in the optical density at 600 nm of a biodegradation solution and in the material properties (e.g., molecular weight, crystallinity, mechanical properties, thermal properties, changes in monomeric composition, or surface aspect by microscopy techniques) (Harrison et al. 2018; Müller 2005; Sudesh et al. 2000). Due to great variation of conditions and methods, many local and international standard methodologies were created with the intent of standardizing the biodegradation evaluation in each environment of interest. Table 2.3 presents some of those methods, in which the American Society of Testing Materials (ASTM), the International Organization for Standardization (ISO), and the European Committee for

36

L. V. S. Ceneviva and T. Tsuge

Standardization (CEN) methods are more commonly used (Harrison et al. 2018; SAPEA 2020; Koller and Mukherjeec 2020). In most of the cases, a polymer material is considered as biodegradable if over 60–90% of it is biodegraded in a maximum specific amount of time, which varies by each method in each environment (Harrison et al. 2018; Filiciotto and Rothenberg 2021). According to Renewable Carbon (2021), part of the Nova Institute, P(3HB), P(4HB), and some PHA copolymers (P(3HB-co-4HB), P(3HB-co-3HV), P(3HBco-3HV-co-4HV), P(3HB-co-3HHx), P(3HB-co-3HO), and P(3HB-co-3HD)) are considered of proven biodegradability in marine environment (TÜV Austria OK biodegradable MARINE), fresh water (TÜV Austria OK biodegradable WATER), soil (TÜV Austria OK biodegradable SOIL and DIN CERTCO DIN-Geprüft Biodegradable in Soil), home composting (TÜV Austria OK compost HOME and DIN CERTCO DIN-Geprüft Home Compostable), landfill (not available standard method), anaerobic digestion (EN 13432 and EN 14995), and industrial composting (TÜV Austria OK compost INDUSTRIAL and DIN CERTCO DIN-Geprüft Industrial Compostable). Parallelly, PLA and PBS, which are bio-based biodegradable polymers of higher global commercial production than PHAs (European Bioplastics 2021), only have proven biodegradability in anaerobic digestion (PLA) and industrial composting (PLA and PBS) (Renewable Carbon 2021). Indeed, Narancic et al. (2018) had similar results by evaluating PHA and other commercial bioplastic biodegradation in controlled industrial composting conditions (ISO 14855), home composting (ISO 14855 at 28 °C), anaerobic digestion (ISO 15985), soil biodegradation test (ISO 17556), marine biodegradation (ASTM D6691), fresh water (ISO 14851), and aqueous anaerobic biodegradation test (ISO 14853). P(3HB) (from Titan), although its high crystallinity, achieved ≥90% of biodegradation in all tests within 43–136 days, on the other hand, PLA (from Nature Works) and PBS (from NaturePlast) were only biodegradable in Industrial Composting (PLA and PBS) and Anaerobic Digestion (PLA). Table 2.4 summarizes some of their results.

2.5.3 Life Cycle Assessment Besides its inherent biodegradability, for PHAs to be truly more sustainable options than petrol-based plastics, they also should have a smaller environmental impact than them. For that, a technique called “Life Cycle Assessment” (LCA) is used to evaluate the environmental impact of its life cycle, that could be from the raw materials to production (“cradle-to-gate”), use, reuse/recycling, or final disposal (“cradle-tograve”). Its methodology is standardized by ISO 14040:2006 and ISO 14044:2006 in four steps: (1) goal and scope definition, (2) inventory analysis, (3) impact assessment, and (4) interpretation. However, different considerations on the design of the LCA scope can have great impact on the results, leading to difficulties on comparing between different LCAs or different conclusion for the same product. For instance, besides which categories will be assessed and their weight, considerations on the raw materials used, scale of production, system boundary (e.g., is only raw material

ASTM D5511-18

ASTM D7081-05

ISO 14855-2:2018

ASTM D6400-19

ASTM D5338-15

ISO 15985:2014

Anaerobic digestion

ISO 14855-1:2005

Industrial composting

ISO 14855 at 28ºC

Home composting

ASTM D5988-18

ISO 17556:2019

Soil

Table 2.3 Standard method for polymer biodegradation evaluation

ISO 22403:2020

ISO 22404:2019

ISO/FDIS 23977-2

ISO/FDIS 23977-1

ISO 19679:2016

ISO 18830:2016

ASTM D7991-15

ASTM D6691-17

Marine environment

ASTM D5271-02

ISO 14853:2016

ISO 14852:2018

ISO 14851:2019

Fresh water

ASTM D6340-98

ASTM D5271-02

ASTM D5209-92

ISO 14852:2018

ISO 14851:2019

ASTM D5210-92

ISO 14853:2016

ISO 13975:2012

Aerobic wastewater Anaerobic and/or sewage sludge aqueous environment

2 Environmental Sustainability with Polyhydroxyalkanoates (PHA) … 37

≈15% (≈90 days)

≥90% (127 days)

≥90% (127 days)

≥90% (207 days)

≥90% (45 days)

≥90% (45 days)

PBS

P(3HB)

PCL1

2 The

≥90% (88 days)

Not evaluated2

0% (max. 1 year)

0% (max. 1 year)

Home composting

≥90% (136 days)

≥90% (136 days)

0% (max. 2 years)

0% (max. 2 years)

Soil

≈80% (56 days)

≈90% (43 days)

≈20% (56 days)

≈10% (56 days)

Marine environment

1 mg/L), lead to an ecological impact on the aquatic world. Even if the water may appear crystalline, the pollution may reside for long periods in sediments and fish, affecting the food chain (Slama et al. 2021). The specific characteristics of textile effluents depend on the textiles manufactured and chemicals used in the dyeing of the fibers. Generally, these effluents have an odor, color, high BOD, COD, reduction in TOC values, total solids, chemical compounds, and trace metals like Cr, As, Cu, and Zn (Mani and Hameed 2019). These effluents are produced at relatively high temperatures (50–60 °C) and high pH (Chengalroyen and Dabbs 2013; Shetty and Krishnakumar 2020). The discharge of such dyes into the environment generates the conversion of the azo group to aromatic amines, released after the action of bacteria during the degradation of azo dyes. These aromatic amines are associated with mutagenic and/or carcinogenic properties. Their toxicity will depend on the metabolic activation of the amino group as the reactive intermediate hydroxylamine, which can cause significant damage to DNA and proteins. Therefore, the bioaccumulation of such products could result in a toxic impact on aquatic life forms and even have carcinogenic and mutagenic effects on humans (Brüschweiler and Merlot 2017). On the other hand, the azo dyes inhibit the tyrosinase enzyme, which may provoke the inhibition of melanin synthesis, producing hypopigmentation (Dubey et al. 2007). For this reason, azo dyes that release carcinogenic aromatic amines have been prohibited in clothing textiles in the European Union (http://ec.europa.eu/health/scientific_c ommittees/consumer_safety/index_en.htm). Also, they were considered by several regulatory organizations as the German Commission, whose mission is the investigation of health risks of chemical compounds in the work area (Bardi et al. 2018); and the Australian Competition & Consumer Commission (ACCC), who has the responsibility of the product safety regulation in Australia between the Consumer Commission and the States and Territories (https://www.productsafety.gov.au/pro ducts/chemicals/azo-dyes). In the United States, no accurate or specific regulation explicitly restricts the use of azo dyes. In its place, diverse aromatic amines released

78

M. García-Rivero et al.

from azo dyes are restricted or prohibited. Therefore, we can still conclude that certain types of azo dyes are prohibited or restricted in the United States due aromatic amines are restricted. However, only some states follow such restrictions (https://www.com pliancegate.com/azo-dye-regulations-united-states/).

4.4 Physical, Chemical, and Biological Treatments for Dye Removal Industrial effluents are harmful to the environment and human health, and any form of life. Environmental legislation is forcing the industry to treat its effluents. In addition, the need for lower water consumption and the increasing cost for the industrial sector are leading the industrial sector to treat and reuse colorful effluents and reduce environmental pollution. To this end, various typical physical–chemical strategies, such as coagulation, flocculation, activated carbon adsorption, and reverse osmosis techniques, are used to remove the color from textile effluents. Moreover, various techniques and methods that degrade this effluent use Fenton’s Reagent, ozonation, photochemical oxidation, and electrochemical oxidation. These methods are known as Advanced Oxidation Processes, which are unconventional processes designed to remove persistent organic compounds that resist conventional treatments, such as azo dyes. All they are effective for color removal, but these also have some disadvantages and limitations such as elevated costs, a high energetic demand, the use of large quantities of chemical products, low efficiency, and secondary pollution problems. However, some of these methods are inapplicable to many dyes, limiting their application on a large scale (Chen et al. 2018; Kabra et al. 2013; Omeje et al. 2020; Shah 2019; Sosa-Martínez et al. 2020). Besides, these methods generate a large amount of sludge, resulting in higher pollution than the effluents (Jin and Ning 2013). From the advantages and disadvantages of the physicochemical processes for dye removal from textile effluents, the research has focused on studying efficient methods without stressing the natural environment and endangering the life forms (Tahir et al. 2016). For this, different biological treatments have been implemented to remove, decolorize, and degrade azo dyes, using a wide variety of organisms such as bacteria, fungi, yeasts, and algae. Although, bacteria and fungi are the main actors in wastewater treatment due to their ability to produce degradative enzymes oxidoreductases, responsible for decomposing of recalcitrant pollutants. For this reason, both microbial groups are of great interest in the treatment of dyes of textile effluents, mainly treatments that allow the elimination or mineralization of the dye molecules are desirable since these treatments are respectful with the environment, safe, clean (no sludge), and economical. It could be combined with other types of treatments. Dye decolorization by biological methods occurs through biosorption, enzymatic degradation (known as biodegradation), or a combination of both through microbial cultures (Almeida and Corso 2019), and these are commonly applied for the treatment

4 Application of Fungi and Bacteria in the Management of Azo …

79

of colored wastewaters. Microbial degradation, adsorption by microbial biomass (living or dead), and bioaccumulation by growing cells are applied frequently for the treatment of industrial wastewaters since many microorganisms such as bacteria, yeast, algae, and fungi, as much as certain plants, can absorb, accumulate, and degrade different organic pollutants (Parmar and Shukla 2018). The biosorption/adsorption process occurs by physicochemical interactions and ion exchange mechanisms among bio adsorbent functional groups (mainly hydroxyl and carboxyl of cellulose molecules found in the microbial cell wall) and dyes without the formation of metabolites. Biological materials such as chitin, chitosan, peat, yeast, and fungi biomass can be used as chelating and complexing sorbents to concentrate and remove dyes from a solution. However, biosorption is not a practical approach for treating large volumes of dye-contaminated industrial effluents due to this generating large volumes of biomass for final disposal (Almeida and Corso 2019; Khan et al. 2013). Agricultural wastes are also used as materials to absorb dyes and can be treated by solid-state fermentation in the presence of white-rot fungi for both dye removal and laccase production. The result can be used as soil fertilizer (Chengalroyen and Dabbs 2013), but also lignocellulosic substrates after solid-state fermentation (SSF) can be dried and stored for use later as suitable catalysts and adsorbents for dye decolorization, as this would contain part of the produced laccase immobilized (Wang et al. 2019). On the other hand, biological processes catalyze the biodegradation of azo dyes by using enzymes such as hydrolases, oxygenases, ligninases, peroxidases and laccases, reductive enzymes azoreductase, and non-specific reductases (MG reductase and DCIP reductase). Also, they catalyze other reactions with enzymatically reduced electron carriers. All these enzymes are responsible for decomposing recalcitrant pollutants as azo dyes.

4.5 Enzymes The fungal and bacterial enzymes have gained attention for decolorizing and/or degradation of azo dyes in wastewater as alternative strategies for physical–chemical treatments. The oxidoreductases enzymes are beneficial because they generate highly reactive free radicals that cause a series of complex spontaneous cleavage reactions and transform recalcitrant compounds (Martínez et al. 2017; Telke et al. 2008). Therefore, it is crucial to describe the characteristics of the main enzymes related to dye decolorization/degradation and identify or understand their catalytic activity.

80

M. García-Rivero et al.

4.5.1 Laccases Laccases (EC 1.10.3.2, benzenediol: oxygen oxidoreductases) are arranged primarily as monomers, dimers, or tetramers with a typical molecular weight range of 60– 80 kDa for the monomer and carbohydrate content of 15–20% (Chakroun et al. 2010). Laccases are generally produced as isoenzymes; their synthesis and secretion are induced for environmental factors differently among the fungal species. Usually, the fungal growth under carbon and/or nitrogen-limited conditions (Casas et al. 2013) and adding yeast extract and copper have a positive effect on laccase production by white-rot fungi (WRF) (Zhu et al. 2016), by the ascomycete Paraconiothyrium variable (Forootanfar et al. 2012) and the deuteromycete Pestalotiopsis sp. (Hao et al. 2007). The addition of inducers to culture media (Piscitelli et al. 2011), such as phenolic compounds and lignocellulosic substrates (Hadibarata et al. 2013), also promotes enzymatic production. The catalytic activity of laccases requires four copper atoms distributed in three different copper centers (Types 1, 2, and 3). The Type 1 copper (T1 Cu) is where the oxidation of the reducing substrate occurs, while Type 2 copper (T2 Cu) and two Type 3 coppers (T3 Cu) conform a trinuclear cluster in which molecular oxygen reduces to two molecules of water (Jones and Solomon 2015). The catalytic efficiency of laccases depends on the redox potential of the T1 copper. Therefore, the fungal laccases with a high redox potential of the T1 site are of particular interest in biotechnology for bioremediation processes (Shleev et al. 2005). Compared to heme peroxidases, laccases have low redox potential that allows direct oxidation of phenolic compounds such as catechol, hydroquinone, 2,6-dimethoxyphenol, syringaldazine, and even aromatic amines (Kahraman and Gurdal 2002). The oxidation efficiency of the laccase of high-redox-potential substrates increases by adding synthetic mediators (Cañas and Camarero 2010). The information on bacterial laccases is poor, with scarce examples. Bacteria such as Micrococcus glutamic, Pseudomonas desmolyticum NCIM 2112 can produce laccases in the degradation of diazo Direct Blue-6 dye. Also, P. desmolyticum shows phenol-oxidase activity concerning the oxidation of azo dyes (Kalme et al. 2007). However, the specificity of the substrate during the decolorization of the dye of bacterial laccases is not yet clear.

4.5.2 Lignin Peroxidase Lignin peroxidase (LiP, EC 1.11.1.14, diarylpropane peroxidase or ligninase I) is a monomeric hemoprotein glycosylated with a molecular size of 38−43 kDa (Yang et al. 2005). The family of extracellular LiP consists of a few isoenzymes in some species and up to 16 isoenzymes identified in Trametes versicolor culture (Johansson and Nyman 1993). In native producers such as Phanerochaete chrysosporium, LiP is produced in response to nitrogen and/or carbon depletion and may be inhibited

4 Application of Fungi and Bacteria in the Management of Azo …

81

by high nitrogen concentrations (Huang et al. 2020). Compounds such as Tween 80, Mn+2 , and veratryl alcohol (VA) have shown a positive effect on the production of LiP (Wang et al. 2008). In the presence of endogenously produced peroxide, LiP catalyzes the oxidation of aromatic non-phenolic structures. The oxidative reaction requires the presence of VA, which is the substrate for LiP and is a secreted fungal metabolite. The LiP has two oxidation sites, the typical heme-cavity of peroxidases and the tryptophan residue (Trp171) on the enzyme surface. The first binding site for substrates is the hemecavity, where the initial reaction with H2 O2 occurs, and the reducing substrates, such as VA and non-phenolic lignin compounds, are oxidized at the surface tryptophan residue (Recabarren et al. 2016). The VA cation radical produced has been proposed as a radical mediator to oxidize polymeric substrates with which LiP presumably cannot interact directly (Recabarren et al. 2016) and phenolic substrates (Koduri and Tien 1995). The catalytic cycle of LiP occurs in three steps: (1) The first reaction step is the oxidation of the resting ferric enzyme [Fe (III)] by hydrogen peroxide (H2 O2 ) as an electron acceptor resulting in the formation of compound I oxo-ferryl intermediate. (2) Compound I is reduced by a substrate molecule such as a non-phenolic substrate and receives one electron to form compound II. (3) In this step involves the subsequent donation of a second electron to compound II by the reduced substrate, returning the LiP to the resting ferric oxidation state to complete the oxidation cycle (Falade et al. 2017).

4.5.3 Manganese Peroxidase Manganese peroxidase (MnP, EC 1.11.1.13 Mn2+ : hydrogen peroxide oxidoreductase) is a monomeric hemoprotein with molecular mass of 40–50 kDa (Rekik et al. 2018). The MnP catalyzes a H2 O2 -dependent oxidation of Mn2+ to form highly reactive Mn3+ , which subsequently oxidizes phenolic substrates to produce free radicals. The Mn3+ produced is released from the active site, and it is stabilized by physiological chelator which can be oxalate, malonate, or maleate that are secreted by many WRF (Mäkelä et al. 2002). MnP whose synthesis and secretion are influenced by carbon and nitrogen-limited conditions, fungal developmental state, and the addition of inducing agents to the culture medium like Mn2+ (Hakala et al. 2005; Järvinen et al. 2012). The catalytic cycle of MnP initiates by the reaction of the native ferric enzyme and H2 O2 to form MnP compound I, a Fe4+ -oxo-porphyrin-radical complex. A monochelated Mn2+ ion donates one electron to the porphyrin intermediate to form Compound II and is oxidized to Mn3+ . The native enzyme similarly generated from Compound II by donating one electron from Mn2+ to form Mn3+ (Hofrichter 2002). Mn3+ chelators, in turn, mediate the oxidation of organic substrates such as phenolic substrates, including simple phenols, amines, and dyes; however, Mn3+ chelator is a

82

M. García-Rivero et al.

mild oxidant under physiological conditions and, by itself, is not capable of oxidizing non-phenolic compounds (Wong 2009). Although the lignin modifier enzymes (LME) produced by different microorganisms have similar characteristics, the redox potential of each enzyme differs by the enzyme itself and the microorganism that produces them. LiPs have the highest redox potential, followed by MnP, which in turn is a more potent oxidant than laccase; therefore, LiPs can oxidize non-phenolic substrates with a high redox potential (Wong et al. 2019). The LME produced by white-rot basidiomycetes has higher oxidative capacities than those produced by other fungi. For instance, laccases from WRF belong to the high-redox-potential group, and many laccases from ascomycete are attached to the middle-redox-potential group (Wang et al. 2015). For this, WRF is considered the better option for azo dye decolorization. However, some researchers have reported that deuteromycetes and ascomycetes are potential laccase producers offering advantages such as short growth period, simple life cycle, and ease of genetic modification (Li et al. 2014) Therefore, azo dye treatment with ascomycota fungi has been promising in cutting costs and providing an environmentally friendly procedure. On the other side, bacterial oxidases were characterized in Streptomyces chromofuscus, intra- and extracellular lignin-peroxidases, laccases, tyrosinase, riboflavin reductase, NADHDCIP reductase, and aminopyrine N-demethylase which were reported too. These enzymes catalyze the bacterial decolorization and degradation of azo dyes (Saranraj and Manigandan 2018). Lignin peroxidase from Bacillus adusta has a low degradation capacity toward azo dyes and phthalocyanine dyes, but the decomposition rate of veratryl alcohol is most high. So far, the enzymes described are of fungal origin, but the bacterial oxidoreductase involved in the degradation processes of azo dyes are not different from the enzymes produced by fungi, except for the azoreductases that are more of bacterial origin.

4.5.4 Azoreductases Azoreductases were firstly discovered in the intestinal microbiota, but they are present in many organisms and are oxygen-sensitive. These enzymes are constitutively produced into the cell and then released extracellularly, registering higher enzymatic activity than the intracellular enzymes (Sandhya 2010). The enzymatic activity of the azoreductases requires cofactors such as NADH, NADPH, FAD, or riboflavin. Bacterial azoreductases are classified as flavin-independent and flavindependent azoreductases. However, the flavin-dependent azoreductases are reclassified based on their cofactor since they can only use NADH or NADPH or both, acting as electron donors. These enzymes catalyze the breakdown of the azo bond (N=N) in the dye, producing aromatic amines (decolorization process), as showing the following reaction:

4 Application of Fungi and Bacteria in the Management of Azo …

83

The azoreducers of strictly aerobic bacteria are intracellular and are enzymes highly specific to the structure of the azo dye. Studies of the azoreductases indicate that they are independent of flavoproteins, have a conserved putative binding site for NADPH in the amino-terminal region, and have a weight of 20.557 Da. The enzymes catalyze the reductive cleavage of azo bonds after the amine aromatics are oxidized by mono and dioxygenase enzymes, capable of incorporating oxygen into the aromatic ring from O2 , continuing its degradation (Perei et al. 2001; Razo-Flores et al. 1997; Seo et al. 2009). The reduction of the azo dye under anaerobic conditions is catalyzed by extracellular-specific azo enzymes and non-specific enzymes. Non-specific enzymes are present in many anaerobic, facultative, and aerobic bacteria. However, the specificity of azoreductases for the anaerobic bacteria is still in doubt. Research on the azoreductases shows that they are flavoproteins capable of reducing azo and nitroaromatic dyes. These enzymes require cofactors such as FMN or FDN but cannot cross cell walls except flavins so that they can act as a redox mediator. Furthermore, since the azoreductases of anaerobic bacteria are extracellular and require electron carriers, and in its absence, the dye could act as the acceptor of electrons, taking them from the electrons transport chain. Other enzymes, as tyrosinases, can also participate in the dye decolorization process by participating in the degradation of Direct Blue-6 by P. desmolyticum and the dispersed brown dye 3REL by a microbial consortium formed by Galactomyces geotrichum and Bacillus sp. (Jadhav et al. 2008; Kalme et al. 2007; Saranraj and Manigandan 2018).

4.6 Fungal Degradation of Azo Dyes The capacity of several fungi to transform azo dyes using LME has been extensively reported. The potential use of these enzymes for the treatment of dye-containing industrial effluents has been proposed. The details about the oxidation mechanisms of azo dyes have been described both using purified preparations of laccases, LiP and MnP and also by using fungal cultures in which these enzymes are produced and

84

M. García-Rivero et al.

act in a sequential and/or coordinated way to degrade the corresponding dye. In this regard, laccases and peroxidases use a similar mechanism for azo-dye oxidation in basidiomycetes (Pricelius et al. 2007), deuteromycetes (Chivukula and Renganathan 1995), and ascomycetes (Adnan et al. 2015). However, due to their higher oxidative capacities, laccases from basidiomycetes decolorized dyes more efficiently than ascomycetes (Claus et al. 2002). The initial step of azo dye degradation is the cleavage of the azo bond, which can be carried out by two routes (López et al. 2004). 1. Symmetrical cleavage

2. Asymmetrical cleavage

Both can take place simultaneously (Ali et al. 2013). It has been suggested that peroxidases can catalyze both reactions (López et al. 2004; Zhao et al. 2006) or laccases (Adnan et al. 2014; Zille et al. 2005). Those oxidation products can be transformed following different reactions and identify the likely pathway of azo dye degradation.

4.6.1 Degradation of Azo Dye by Laccases Laccases decolorize azo dyes through a highly non-specific free radical mechanism forming phenolic compounds, thereby avoiding the formation of toxic aromatic amines. Differences in dye degradation by laccases are attributed to the specific catalytic properties of the enzyme and the structure of the dye. It has been shown that the presence of electron-donating methyl and methoxy substituents seemed to enhance laccase activity, while electron-withdrawing chloro, fluoro, and nitro substituents inhibited oxidation of azophenols (Abadulla et al. 2000; Legerská et al. 2018). The dye removal efficiency and the removal rate decreased are inversely

4 Application of Fungi and Bacteria in the Management of Azo …

85

proportional to azo group number of dyes (Forootanfar et al. 2016); even the substituents of the phenolic rings of the azo dyes determine the type of the initial reaction of dye degradation and the final products obtained (Zille et al. 2005). With methyl azo dyes (methyl orange), the initial step of dye degradation is a oneelectron extraction from the amino substituent; the resulting radical cation undergoes oxidation, which leads to the formation of an iminium ion, and then, a secondary amine can be formed through solvolysis processes (Zille et al. 2005). On the other hand, the dye degradation pathway develops in three steps with phenolic azo dyes. In the first step, laccases oxidize the phenolic group using one electron, generating a phenoxy radical oxidated later to a carbonium ion in the second step. In the third step, a nucleophilic attack by water on the phenolic ring carbon bearing the azo linkage to produce 3-diazenyl-benzenesulfonic acid and 1,2-naphthoquinone then takes place (Zille et al. 2005). This pathway was also described for the degradation of Acid Red 97 with the laccases produced by the ascomycete Peroneutypa scoparia (Pandi et al. 2019); in the same way, acid orange 7 can be degraded in a very similar way through laccase producing 1-amino-2-naphthol and sulfanilic acid (Lai et al. 2017).

4.6.2 Degradation of Azo Dye by Peroxidases The proposed degradation pathway of Orange II by MnP can be carried out by both symmetrical and asymmetrical azo bond cleavage (López et al. 2004). The first detected that the 4-nitrosobenzenesulfonate and sulfanilate could be transformed by an enzymatic or spontaneous reaction to yield 3, 4-aminobenzensulfonato. In the second pathway, it was formed 1, 2-naphthoquinone and 4diazoniumbenzenesulfonate. The latter undergo hydrolysis reactions, reduction, and scavenged by oxygen to yield the corresponding 4-sulfophenylhidroperoxide.

4.6.3 Degradation of Azo Dye by Fungal Cultures The biodegradation pathway of dyes by fungal cultures is not easy to elucidate because of the participation of non-ligninolytic enzymes, which can contribute to the transformation of the dye structure, and the formation of intermediate metabolites, which can be challenging to detect, because in some cases these products are absorbed on fungal biomass (Adnan et al. 2015). Despite these limitations, partial degradation pathways have been proposed in which the relative contributions of LiP, MnP, and laccase to the decolorization of azo dyes may be different for each fungus. These proposals coincide in that the initial step is the cleavage of the azo bond by oxidation or reduction reactions in which different enzymes could be involved (Gomi et al. 2011).

86

M. García-Rivero et al.

The degradation pathway of Disperse Orange 3 by Pleurotus ostreatus proposed by Zhao et al. (2006) presume that LiP and laccase were involved in the dye degradation; however, one of the first products generated (4-nitroaniline) by the symmetric azo bond cleavage does not seem to be generated by a ligninolytic enzyme. On the other hand, it is proposed that the LiP involvement in an initial collateral reaction that produces nitrobenzene due to the veratryl alcohol was detected in the culture medium before the product formation. In the subsequent reaction, LiP and laccase involve in producing 4-nitroanisole. The results obtained in the degradation of amaranth by Bjerkandera adusta Dec 1 (Gomi et al. 2011) suggested that the initial attack on the azo bond must proceed mainly by reduction and hydrolysis, via the action of several enzymes, and peroxidases do not promote it. In the subsequent dye structure modification, the MnP could produce naphthalene rings transformed into butadiene derivatives and several aromatic compounds. Adnan et al. (2014) suggested that reactive black 5 (RB5) biodegradation by Trametes gibbosa initiates by oxidative cleavage of the azo bond, probably mediated by laccase, leading to the formation of the sodium salt of 8-amino-naphthalene1,2-diol and 4-sulfooxyethylsulfonyl-1-phenol. Then, the naphthalene compound is further oxidized to 2-amino-6-(2-carboxy-ethyl)-benzoic acid through intradiol cleavage mediated by a dioxygenase enzyme. In the subsequent reaction, the laccase catalyzed the decarboxylation of this compound into phenylamine. Finally, the ring cleavage of phenylamine to sec-butylamine could be mediated by MnP. However, some intermediate products are hypothesized, as they were not detected. Moreover, the ligninolytic enzymes involved in the RB5 biodegradation were not quantified. Later, the same group of researchers studied the degradation of RB5 by the ascomycete Trichoderma atroviride F03 in more detail (Adnan et al. 2015). Laccase was the only MLE produced by this fungus, and therefore, the biodegradation of RB5 was attributed to that enzyme. The bis-azo bond’s cleavage initiated the RB5 biodegradation and then deamination and hydroxylation reactions mediated by laccase to produce naphthalene-1,2 8-triol and sulfuric acid mono-[2-(toluene-4sulfonyl)-ethyl] ester. Then, the desulfonation of sulfuric acid mono-[2-(toluene4-sulfonyl)-ethyl] ester led to the formation of 1,2,4-trimethylbenzene. On the other hand, the naphthalene-1,2,8-triol oxidizes to produce 2-(2-carboxy-ethyl)-6hydroxy-benzoic acid that could be further degraded via two possible pathways: (i) It undergone decarboxylation and methylation to form 2,4-ditertbutylphenol and (ii) it transformed to benzoic acid by decarboxylation mechanism. Figure 4.3 illustrates the combination of the possible reactions that some authors have suggested to RB5 degradation by different microorganisms using LME. Regardless of the enzyme that could participate, the end product can be an aromatic compound which in the best of cases can split to form an alkane that could be metabolized, thus achieving the mineralization of the dye. Many of the intermediaries were not detected in the medium, but instead, they were absorbed in the biomass.

4 Application of Fungi and Bacteria in the Management of Azo …

87

Fig. 4.3 Reactions that can lead to biodegradation of RB5 by (→) Trichoderma atroviride (Adnan et al. 2015), (→) Trametes gibbosa (Adnan et al. 2014), and (→) Trichosporon akiyoshidainum (Martorell et al. 2017). Compounds in parentheses were not determined in the liquid medium

4.7 Bacterial Degradation of Azo Dyes Bacterial degradation of azo dyes begins with reducing the azo bond by azoreductases. The azoreductases of strictly aerobic bacteria are intracellular and dependent on the coenzymes NADH and NADPH; they are highly specific but cannot reduce large and complex dyes since they cannot cross the cell membrane. On the other hand, anaerobic or facultative bacteria’s azoreductases are extracellular and are more efficient. This suggests that the degradation of the azo dyes begins under anaerobic conditions to generate the cleavage of the azo bond, forming the respective aromatic amines. Furthermore, under anaerobic conditions, more azo and complex dyes can degrade. However, the aromatic amines produced are not always easy to degrade under anaerobic conditions; studies suggest that the degradation of amines is more effective in the presence of oxygen. Therefore, in pure cultures, facultative

88

M. García-Rivero et al.

or microaerophilic aerobic bacteria can be more efficient than cultures with strict aerobic bacteria, in addition to alternating atmospheres. Also, mixed cultures are another alternative for greater efficiency in the degradation of azo dyes. Bacterial degradation of azo dyes until their mineralization by aerobic bacteria only is possible for simple azo dyes; since they can assimilate them as carbon and energy source to grow. Xenophilus azovorans KF 46 (previously Pseudomonas sp. KF46) and Pigmentiphaga kullae K24 (previously Pseudomonas sp. K24) can grow aerobically with carboxy-orange I and carboxy-orange II as carbon sources, respectively (Pandey et al. 2007). Pseudomonas sp. BN9 grown with 2,4-dihydroxybenzoate by NADH, NADH-dependent enzyme, dioxygenase, and monooxygenase tests the degradation of aromatic compounds that can result from the azo dye reduction. Caulobacter subvibrioides strain C7-D produces a semiconstitutive azoreductase capable of reducing the azo bond, is not sensitive to oxygen and weights 30 kDa. The enzyme can reduce Acid Orange (AO) 6, AO7, AO8, AO12, Acid Red (AR) 88, AR151, and Methyl Red (MR) dyes. However, the AO7 day was the best inducer and is the substrate with the highest reduction rate. Whereas, the azoreductase of Rhodopseudomonas palustris requires anaerobic conditions, pH 8 and a temperature between 30 - 35 °C to treat up to a concentration of 1250 mg/L of azo dye (Saranraj and Manigandan 2018). However, not all colorants can be degraded in the presence of oxygen. Thus, the decoloration should make in the absence of oxygen and continue the degradation of the corresponding amines under aerobic conditions. For example, Pseudomonas paucimobilis is capable of degrading sulfanilic acid (4-aminobenzenesulfonic acid), which is generated from reduction of acid orange dye 7 under anaerobic conditions (García-Martínez et al. 2015). The reduction of sulfanilic acid is carried out in the absence of nitrogen and under aerobic conditions (Perei et al. 2001). Figure 4.4 illustrates the resumed azo dye degradation process by bacteria.

4.8 Applying of Fungi and Bacteria in the Management of Azo Dyes As mentioned before, the treatment of azo dyes is of great interest for its ecological and health implications. Considering that physical, chemical, and physical–chemical treatments may not be very efficient or expensive, the use of the genetic and metabolic diversity of bacteria and fungi becomes an option for the treatment of textile effluents. Both microbial groups can degrade different dyes due to their vast production of enzymes and detoxify the generated products (Slama et al. 2021). Although these microorganisms are used to treat azo dyes, microbial processes are slow compared with physical and chemical treatments, and sometimes these are not reproducible due to the high dye concentrations and the generation of toxic products that can stop biodegradation. In addition, the presence of a small amount of dye in the water (10– 50 mg L−1 ) is noticeable. For this reason, different strategies are being developed

4 Application of Fungi and Bacteria in the Management of Azo …

89

Fig. 4.4 Possible mechanism of decolorization and degradation of the acid orange 7 azo dye. 1. Route of degradation of aromatic amines proposed from previous reports for Pseudomonas sp. 2. Metabolic pathway described for the degradation of sulfated aromatic amines by Pseudomonas paucimobilis. 3. Auto-oxygenation route of aromatic amines generated from an electrochemical process, where Shewanella oneidensis is at the anode under anaerobic conditions, the cathode is covered by laccases in the presence of oxygen. The mechanism bases on previously reported data (Mani and Hameed 2019; Perei et al. 2001; Seo et al. 2009)

for treating the textile effluent through the use of axenic cultures, mixed culture, consortiums, or immobilized cells or enzymes.

4.8.1 Bacterial Process for Azo Dye Degradation Degradation of azo dyes by bacteria is of particular interest due to their short life cycle; they are easy to cultivate, show rapid growth under aerobic and anaerobic conditions, and can be facultative, producing fewer secondary wastes. In addition, bacteria can use different substrates as a carbon source and have an inherent capacity to survive in stressful conditions of salinity and temperature. Aerobic azo dye decolorization processes directed by bacteria reduce the level of dye by adsorption at the sludge biomass in a nonenzymatic process, although to degrade the azo dyes, these bacteria must be in the presence of additional carbon and energy sources; this favors the amount of biomass and the release of metabolites that act as reducing agents for dyes by non-specific reactions between them. Therefore, bacterial conventional wastewater treatment in aerobic conditions is not helpful for decolorizing dissolved azo dyes and other colorants since this is economically not viable commercially (Shah 2019). However, if aerobic bacteria are subjected to

90

M. García-Rivero et al.

microaerophilic conditions, the rate of decolorization increases due to the production of azoreductases, which are sensitive to oxygen and are more active in low oxygen concentrations or absence of its (Padmavathy et al. 2003; Zee 2002). Then, the bacterial processes under microaerophilic conditions are more efficient than the conventional aerobic treatments of colored wastewaters (Kuhad et al. 2004). The reactions are developed in the dye degradation process by anaerobic bacteria such as Pseudomonas luteola, Aeromonas hydrophila, Bacillus subtilis, Pseudomonas sp., and Proteus mirabilis at neutral pH and become extremely non-specific when low molecular weight redox mediators are in the reaction. On the other hand, anaerobic bacteria decolorize the azo dye faster under anaerobic conditions, reducing the azo bond’s cleavage from the dye molecule by specific and non-specific enzymatic action. Activated sludge is another strategy for decolorizing azo dyes, as they often provide additional carbon sources for the microorganisms present; it increases the rate of dye reduction and facilitates the formation and regeneration of reducing equivalents of the enzyme systems mediator’s non-specific reducers. In addition, the sludge represents an environment that facilitates anaerobic and aerobic atmospheres that help decolorize dyes and degrade the aromatic amines generated. All this allows achieving a high degree of biodegradation and mineralization of a wide variety of azo dyes, making this process more suitable for application on a commercial scale. Another way to degrade azo dyes is by using pure cultures, but carbon and nitrogen sources alternate to the dye are used. Such is the case of the Reactive Red 141 dye degradation by Rhizobium radiobacter MTCC 816. The azo dye degradation was under anoxic conditions using different nitrogen and carbon sources at neutral pH and 30 °C. Enzyme analysis showed the presence of various oxidative and reducing enzymes indicating their participation in the removal of color. Some degradation products were less phytotoxic than the dye itself (Telke et al. 2008). Anaerobic cultures can be developed in static conditions, as this favors the oxygen depletion needed to reduce azo dyes. In most cases, anaerobic bacterial decolorization processes are inexpensive and environmentally friendly, and degradation metabolites formed because of dye decolorization were less toxic than untreated wastewaters (Chen et al. 2018; Parmar and Shukla 2018; Shah 2019; Srinivasan and Sadasivam 2018). However, in some cases, the bacterial anaerobic azo dye degradation processes produce aromatic amines that cannot be further mineralized and are more challenging to biodegrade than the parent dye. Also, some bacterial are often specific to a type of dye, which limits their use in treating wastewater from the textile industry that is complex chemically. So, there is a need for an approach where complete degradation of dyes can be achieved, and this may become possible by the synergistic interaction of bacterial consortium, in which different strains can attack the color molecule at different positions or can use the metabolites produced by another bacterial strain for further decomposition (Chen et al. 2018; Parmar and Shukla 2018). As aerobic bacteria can mineralize the aromatic amines and sulfonated amino aromatics, it has suggested a combination of the anaerobic cleavage of azo dyes with aerobic treatment; this can be done sequentially or simultaneously.

4 Application of Fungi and Bacteria in the Management of Azo …

91

Different studies show that the decolorization by pure or mixed bacterial cultures and combining an aerobic/anaerobic atmosphere increases the reaction is not specific of dyes concerning organisms. These decolorization treatments have included low molecular weight and enzymatic redox mediators for non-specific reductive cleavage of the azo dye. Decolorization by specific or non-specific reactions of azo dyes generates aromatic amines, most toxic, and resistant to degradation, particularly in anaerobic conditions. For this reason, the sequential bacterial processes microaerophilic/aerobic or aerobic/microaerophilic or aerobic/anaerobic are most effective for treating the azo dye (Chengalroyen and Dabbs 2013; Shah 2019; Ikram et al. 2020). Other experiments indicate that when using cell extracts, there is cell lysis in situ or the cells are in starvation, cofactors are released into the medium and favor the reduction of azo dye concerning intact or static cells. However, in intact cells, the dye transport system at the membrane level, the dye reduction is affected for complex and highly polar dyes, as those with sulfate groups. For this reason, the reduction of the dye is carried out in an extracellular way by non-specific reactions that occur between reduced compounds generated by the anaerobic biomass. Such is the case of reducing sulfate bacteria capable of reducing sulfate to hydrogen sulfide, which could act as a reducing agent on the azo dye. Another similar strategy is using methanogenic cultures under anoxic conditions, which leads to a non-specific decolorization of azo dyes. However, it has its limitations since it requires a yeast extract or peptone, making the process not very viable on an industrial scale (Pandey et al. 2007). In addition, a large number of aromatic amines are produced, and only some are mineralized by methanogenic bacteria; most amines are toxic, and sulfonated aromatic amines are more resistant that require aerobic microorganisms capable of degrading them in aerobic conditions.

4.8.2 Fungal Process for Azo Dye Degradation The strategies of dye remotion by fungal treatment are effective in the case of certain dyes and have their drawbacks and limitations (Tahir et al. 2016). Fungi have a robust oxidative system and high level of enzyme secretion, which eliminates the problem of substrate diffusion into the cells. However, the action of these enzymes favors in acidic conditions (pH 4.0–5.0), but textile dyes carry a high pH, which means a limitation (Chengalroyen and Dabbs 2013). Besides, fungi have an adequate growth rate in relatively cheap medium, which makes them good industrial candidates (Omeje et al. 2020). The oxidative metabolism decolorization of dye can also happen through biosorption onto either live or dead mycelium (Kumari and Naraian 2016). Besides, fungi have shown strong adaptability and efficiency in removing decolorization intermediates as aromatic amines and phenolics, compounds with high toxicity and low biodegradability (Sen et al. 2016).

92

M. García-Rivero et al.

WRF have been extensively studied to develop bioprocesses for the mineralization of azo dyes; P. chrysosporium, T. versicolor, B. adusta, and Coriolus versicolor are the WRF most used for decolorization processes (Dwivedi and Singh Tomar 2018). WRF decomposes dyes efficiently under aerobic conditions (Kumari and Naraian 2016), an advantage over the aerobic bacterial process. The disadvantages of using WRF culture include the slow fungal growth, which would take a long time for them to degrade azo dyes; the susceptibility to contamination by bacteria and other fungi during wastewater treatment, leading to instability of the system; and the harsh fermentation conditions, as carbon and nitrogen concentrations in the medium have a significant effect on the expression of laccase and peroxidases by these fungi (Khan et al. 2013). Besides, WRF is not naturally found in wastewater, and therefore, enzyme production may be unreliable. So, using fungal cultures in textile dye decolorization processes may cause further problems such as the accumulation of biomass, long adaptation time of the microorganisms, or difficulties in establishing the optimum conditions for degradation. All these disadvantages must be overcome before the practical application of fungal cultures in wastewater treatment. Therefore, it is necessary to screen other fungi with strong adaptability and high efficiency in degrading azo dyes in wastewater (He et al. 2018; Parmar and Shukla 2018). Filamentous fungi other than white-rot basidiomycetes have also been found to be able to degrade several azo dyes (He et al. 2018). In this respect, several Aspergillus species could mean a reliable option, as they have a broad-spectrum substrate and easier achievement of high stability, flexibility, and adaptability on a wide pH range; as much as tolerance to high dye concentrations and the ability to degrade a broad spectrum of dyes (Ning et al. 2018). Besides, decolorization processes developed by different Aspergillus species tend to take less time to perform than those from WRF (Kanmani et al. 2011; Laraib et al. 2020). Recently, dye biodegradation research has focused on simulating real wastewaters and semisynthetic media conditions, for example, the ability of fungal cultures to tolerate bacterial contamination that happens during the treatment of real non-sterile wastewaters; in this case, competition between biodegradative fungi and invading microorganisms for available nutrients may diminish the efficiency of the decolorization process (Svobodová and Novotný 2018). Axenic cultures can attack dye molecules at different positions depending on their nature and action mode on a specific dye. However, this attack could yield metabolic end products that may be toxic. The use of mixed cultures would enhance the synergistic metabolic activities of the microbial community, allowing that the toxic metabolic products of one strain be further metabolized as nutrient sources to carbon dioxide, ammonia, and water by another strain in the culture (Jadhav et al. 2016). Therefore, mixed cultures could be a good strategy for decolorizing wastewater and semisynthetic media. Table 4.2 resumes some dye decolorization processes that use bacteria, fungi, or mixed culture.

4 Application of Fungi and Bacteria in the Management of Azo …

93

Table 4.2 Dye decolorization bioprocesses developed with bacteria, fungi, or mixed cultures Microorganism

Dye

Comments

Aeromonas hydrophila

Cristal violet

Bacteria decolorized 99% Bharagava et al. of dye in the presence of (2018) sucrose and yeast extract. It also produced laccase and lignin peroxidase and reduced the toxicity of the decolorized effluent

References

Providencia sp. SRS82

Acid black 210 Bacteria degraded (AB210) 100 mg L−1 dye within 90 min under static conditions and tolerated concentrations as high as 2000 mg L−1 of dye

Agrawal et al. (2014)

Coriolus versicolour (NBRC Acid orange 7 9791)

Spongy pellets showed an Hai et al. (2013) excellent decolorization (>99%) of the dye in the synthetic wastewater. Fungus attached to plastic supports showed high enzymatic activity and decolorization/degradation for an extended period. High decolorization (95%) was obtained after one day. The process developed in a membrane bioreactor under non-sterile conditions

Penicillium oxalicum SAR-3

Acid red 183, Direct blue 15 and Direct red 75

The strain had high degradation levels (95–100%) of almost all dyes within 120 h. In these cultures, MnP activity seemed to be the most important for dye decolorization

Ceriporia lacerata ZJSY

Congo red

Fungus reached a Wang et al. decolorization of 90% after (2017) 48-h culture, caused by absorption mycelia and enzymatic degradation, although dye decolorization products resulted in more toxicity than the original dye

Saroj et al. (2014)

(continued)

94

M. García-Rivero et al.

Table 4.2 (continued) Microorganism

Dye

Comments

Novel indigenous bacteria consortium

Direct blue 2B

System reached Cao et al. (2019) decolorization values from 60 to 90% (with 50–200 mgdye L−1 ) and 35–65% (with 400–1500 mgdye L−1 ) after 36-h culture

References

Morganella sp. HK-1

Reactive black-B (RB-B)

The isolate completely degraded RB-B (20 g L−1 ) within 24 h under static conditions

Pathak et al. (2014)

Bacterial consortium

Reactive green-19

More than 97% of removal efficiency achieved within 24 h

Das and Mishra (2017)

Mixed culture composed of Bacillus sp. V1DMK, V5DMK, V7DMK and V12DMK, Lysinibacillus sp. V3DMK and Ochrobacterium sp. V10DMK

Reactive violet The culture developed in Jain et al. (2012) 5R was minimal medium with a low amount of glucose, yeast extract and 20 g L−1 NaCl, and decolorized RV5 with 200 mg L−1 within 18 h, under static condition

A bacterial consortium of Enterobacter dissolvens AGYP1 and Pseudomonas aeruginosa AGYP2

Acid maroon V Culture degraded 93% decolorization of 100 mg L−1 dye after 20 h under static incubation. This consortium also could decolorize 16 other textile dyes

Consortium Aspergillus ochraceus-Pseudomonas sp. SUK

Rubine GFL and textile effluent

Patel et al. (2012)

The process developed Lade et al. decolorization (higher than (2012) 95% in 30–35 h without forming amines under microaerophilic conditions) and detoxification of the dyes. There was a synergetic reaction of the fungal and bacteria process

4.8.3 Bioprocesses that Use Enzymes for Azo Dye Decolorization Different reactor configurations employing bacteria and fungi have developed effective textile dye decolorization. These processes have been developed in liquid cultures, using several decolorization and biodegradation methods. These decolorization processes have been carried out in batch, fed-batch or semi-continuous, draw-fill,

4 Application of Fungi and Bacteria in the Management of Azo …

95

and continuous cultures with a range of reactor configurations that include activated sludge, trickling filters, aerobic granular sludge, lagoons, oxidizing beds, constructed wetlands, aerobic filters, membrane bioreactors, packed bed, fluidized beds, stirred tank, and air-lift reactors (Khan et al. 2019; Kuhad et al. 2004; Lemus-Gómez et al. 2018). In some cases, decolorization by microbial cultures is not easily applicable on a large scale, and the studies of decolorization of synthetic dyes by crude or purified enzymes become critical. Therefore, the application of isolated enzymes or enzyme crude extracts could represent a better alternative for eco-friendly and efficient removal of color from contaminated wastewater, and several bioprocesses have been developed using only these enzymes for degrading textile dyes (Chacko and Subramaniam 2011; Singh et al. 2015; Wong et al. 2019). Dye decolorization and biotransformation catalyzed by enzymes have shown that the process is efficient, and a high color remotion can be achieved in short times, compared to those reported for microbial cultures (Mishra and Maiti 2019). For developing enzymatic processes, enzymes must be obtained from microbial cultures. Submerged cultures are used for laccase production by most fungal species, while SSF tends to be economical for producing bacterial laccases, although enzyme efficiency varies with the enzyme class and its production source (Mishra and Maiti 2019). The potential advantages of enzymatic treatments are their application to ample amounts of dyes over wide pH and temperature ranges and moderate ionic strength or salinity and to some extent in the presence of organic solvents; and the perspective of saving energy and materials (Mishra and Maiti 2019; Sosa-Martínez et al. 2020). The use of enzymes in dye decolorization processes has been studied in a tank, and tubular reactors developed batch-wise, semi-continuously or continuously. However, most of the processes using ligninolytic enzymes have been done in small assays, at assay conditions different from those prevailing in a natural waste stream; only a few of the enzymatic processes developed at lab scale have been studied at pilot or full-scale operation, as optimization and scaling-up of all these processes at the same time is difficult (Méndez-Hernández and Loera 2019). Promising studies include the use of purified enzymes to mineralize dyes. For operating an enzymatic process with high productivity, the system requires enzyme stability with ease of operation and low cost. More studies that employ pure or combined enzymes considered the recovery and reuse of enzymes, which is an essential requirement for a full-scale application (Chengalroyen and Dabbs 2013; Méndez-Hernández and Loera 2019). However, the industrial application of enzymes in dye wastewater treatment is often restricted because they are susceptible to inhibition, lack long-term operational stability and reusability, and their use increases production costs (Kabra et al. 2013; Wong et al. 2019). The physicochemical nature of the effluents, including pH, high concentrations of different ions, temperature, and the presence of toxicants can provoke the inactivation of enzymes and microbial cells. Therefore, recent studies have focused on having more active and versatile enzymes and microbial cultures with high stability and low cost to fulfill the treatment criteria of colored effluents.

96

M. García-Rivero et al.

4.8.4 Immobilization as an Alternative Bioprocess for Dye Decolorization of Wastewater Overall, the rate of dye degradation by microbial cells depends on operational parameters, and the degradation rate would not be persistent all through the process. Eventually, reacting microbial biomass would be lost, resulting in an inconsistent degradation rate. On the other hand, highly colored effluent can reduce enzymes’ catalytic activity and stability, and their utilization is practically impossible if enzymes are in the solution. Immobilization can overcome some of the limitations of biodegradation processes by improving the resistance of enzymes against heavy metal inhibition and diminishing the susceptibility to denaturing chemicals (Mishra and Maiti 2019; Teerapatsakul et al. 2017). Also, immobilization allows the long-term utilization of microbial or enzymatic systems. Besides, the immobilized matrices can withstand the toxicity of the dyes, and immobilized microorganisms and enzymes provide a high level of degradation capability and are more robust to environmental alarms such as temperature, pH, or toxic compounds exposure as compared to the conventional microbial cultures or enzyme extracts (Kurade et al. 2019). Thus, the immobilization of microbial biomass or enzymes, pure or in a crude extract, would be recommended to maintain active degradation biomass in the system (Shetty and Krishnakumar 2020). Immobilization of microorganisms or enzymes for decolorizing effluents from the textile industry has used matrices as polyvinyl alcohol, calcium alginate, stainless steel sponge, polyurethane foam, chitosan, chitin, cellulose derivatives, charcoal activated carbon, loofah sponge, sugarcane bagasse, nylon net, steel wood, orange peels, scouring pad, sand, coconut bagasse, and corn cobs, among others. These matrices are selected based on high porosity, inert nature, easy availability, and low cost (Hamad and Saied 2021; Kurade et al. 2019; Laraib et al. 2020). Immobilization of azoreductases, laccases, oxidoreductases as tyrosinase, MnP, and LiP obtained pure or in a crude extract from multiple sources has helped in the degradation of numerous synthetic dyes. The immobilization of dye-degrading enzymes on specific support material enhances the decolorization efficiency, supports reusable enzymes with improved enzyme stabilization, and allows extensive use. Also, immobilization improves the resistance capability of enzymes against heavy metal inhibition, and the immobilized enzymes are remarkably less susceptible to denaturing chemicals (Mishra and Maiti 2019; Teerapatsakul et al. 2017). Adsorption is the most scalable immobilization technique in the current industry due to its more straightforward mechanism, high efficiency, and affordability (Wong et al. 2019). Entrapment has been a widely used strategy for immobilization of laccases on an industrial scale and has been extensively used to remove dyes as it is easier to operate, provides no structural changes to the enzymes, and minimizes the leakage of the enzyme into the solution. Enzyme entrapment in alginate beads using air-lift reactors can serve as better bioprocessing for enzyme-mediated dye degradation for implementation industries.

4 Application of Fungi and Bacteria in the Management of Azo …

97

Table 4.3 summarizes several bioprocesses that use immobilized enzymes using different immobilization techniques.

4.8.5 Bioprocesses Developed with Bacteria and Fungi Immobilized Systems Microbial cell immobilization evolved as an alternative to enzyme immobilization as it eliminates the laborious and expensive process of enzyme isolation and purification. Additionally, immobilized microbial cells can be operated in the continuous or semi-continuous production process; it means an efficient recovery of the biocatalyst, provides a more extended period of enzyme activity and storage, and eliminates strain genetic instability problems for recombinant strains. The advantages of immobilized cell systems have led to their increasing application in wastewater treatment (Purbasha and Bhaskara 2021). Bioprocesses developed with immobilized bacteria have shown that these biocatalysts are more efficient than free suspended cells. Besides, commonly bacterial processes are developed first under anaerobic conditions and a subsequent aerobic operation to degrade and mineralize the synthetic dye or an industrial effluent; however, this strategy in immobilization is scarce. There are few studies about the treatment of real textile effluents by immobilized fungi, and most of them have been performed with white-rot fungus (Arikan et al. 2019). Irrespective of the microbial system used, it is crucial to consider that individual microbial strains are only effective against a particular type of dye, but industrial wastewaters have a complex chemical composition that needs the action of several different enzymes. These facts highlight the need to develop bioprocesses with microbial consortia, and the corresponding immobilized systems are also critical (Purbasha and Bhaskara 2021). In this respect, Table 4.4 summarizes several bioprocesses that use microorganisms, bacteria, fungi, or a consortium immobilized in different supports. Only a few studies have tested the potential of immobilized microorganisms for effluent color removal in bioreactors; immobilized microbial consortia showed more potential for industrial applications. Most of the studies performed by researchers have utilized anaerobic/microaerophilic reactors, and a few reports use aerobic reactors as rotating biological contractors, air-lift reactors, and packed bed reactors for effluent treatment with immobilized systems (Purbasha and Bhaskara 2021). Developing dye decolorization and/or degradation processes using immobilized microorganisms in a continuous mode bioreactor or a sequential batch reactor could be an adequate strategy for textile industry wastewater. It allows the long-term utilization of biological systems and high degradation rate and makes them more resistant to environmental changes. In this respect, immobilized T. versicolor in polyurethane cubes in using a highly reproducible technique. Immobilized fungi operated for 93 days with a decolorization higher than 50%; although the ability to degrade by immobilized fungi decreased as dye concentration increased, the final mycelium

Synthetic dye effluent (SDE) contained 1-hydroxybenzotriazole, Remazol Black 5, Remazol Brilliant Blue R, Remazol Brilliant Violet 5, Reactive Orange 16, Reactive Red 120, sodium chloride, sodium carbonate, sodium hydroxide, and acetic acid

Remazol brilliant blue R

Dye degraded

Chitosan beads with genipin Congo red as a cross-linker

Cellulose nanofiber

Laccase from Pleurotus florida NCIM 1243

Purified laccase from T. pubescens

Silica zirconium hybrid dropped with copper ions

Laccase

Adsorption

Entrapment

Immobilization support

Enzyme

Immobilization technique

Table 4.3 Use of enzymes immobilized by different techniques in dye decolorization processes References

Sathishkumar et al. (2014)

(continued)

The immobilized Datta et al. (2021), enzyme had 60% of Ma et al. (2018) residual activity after 11 cycles, high pH, and operational stability and dye decolorization of 60.81%

The immobilized enzyme had a simulated dye effluent decolorization or around 85% for up to five cycles and may be used as a good candidate for textile effluent decolorization

After ten consecutive Datta et al. (2021), reuses, the immobilized Li et al. (2020) laccase maintained more than 61% of its original activity and showed excellent degradation (>65%) of various synthetic dyes

Observations

98 M. García-Rivero et al.

Immobilization technique

Chitosan beads

Laccases from Pleurotus ostreatus

Sandalfix golden yellow CRL

Acid black 172

Chitosan beads crosslinked with glutaraldehyde

Purified laccase from Trametes pubescens

Dye degraded Indigo carmine and other commercial aromatic dyes

Immobilization support

Laccases from Copper alginate beads Ganoderma sp. KU-Alk4

Enzyme

Table 4.3 (continued) References

The immobilized enzyme had better catalytic activity and stability to harsh conditions and had a great potential to decolorize dyes with removals of 90%

Immobilized enzyme retained 60% of its activity after six cycles of continuous use, reaching 68.84% of decolorization

(continued)

Datta et al. (2021), Jamil et al. (2018)

Datta et al. (2021), Zheng et al. (2016)

Immobilized enzymes Datta et al. (2021), had enhanced Teerapatsakul et al. temperature stability at (2017) 55 °C, were stable at pH up to 10, and completed 14 runs of complete dye degradation. This system could be feasible for operation in the industry

Observations

4 Application of Fungi and Bacteria in the Management of Azo … 99

Immobilization technique Immobilization support Alginate-gelatin gel

Calcium alginate bead

Calcium alginate beads crosslinked with glutaraldehyde

Enzyme

Laccase from Brevibacterium halotolerans

Laccase from Trametes versicolor

Lignin peroxidase from Ganoderma lucidum IBL-05

Table 4.3 (continued)

Sandal reactive dyes

Remazol T

Congo red

Dye degraded

References

The immobilized enzyme reached decolorization efficiencies of 66% after four decolorization cycles and retained 41% decolorization activity after seven repeated cycles

Dye degradation of 92% within 72 h. Immobilized enzymes retained up to 60% of their original activity after three use cycles

(continued)

Shaheen et al. (2017)

Datta et al. (2021), Noreen et al. (2016)

Higher thermal and pH Datta et al. (2021), stability of the enzyme. Reda et al. (2018) Immobilized enzymes retained up to 65% of their activity after seven continuous cycles

Observations

100 M. García-Rivero et al.

Encapsulation

Immobilization technique

Agarose gel matrix

Purified MnP from Ganoderma lucidum IBL-05

Five different textile effluents

Drimarene blue K2RL

Dye degraded

Core–shell system of copper Remazole brilliant blue R alginate incorporated with Fe2 O3

Sol–gel matrix of trimethoxysilane and propyltetramethoxysilane

Crude MnP from Pleurotus ostreatus IBL-02

Laccase

Immobilization support

Enzyme

Table 4.3 (continued)

Asgher et al. (2013), Purbasha and Bhaskara (2021)

References

Beads with the immobilized enzyme decolorized 54.2% to 75.8% of dye after 4 h. The immobilized system showed a decolorization of 37.6–54.8% of real wastewater

(continued)

Le et al. (2016), Purbasha and Bhaskara (2021)

Immobilized enzyme Bilal et al. (2017), was applied in a packed Purbasha and bed reactor, showing Bhaskara (2021) maximum decolorization for all the effluents in the range of 78.9–98.4% after six consecutive cycles

The immobilized enzyme showed complete decolorization of dye and decolorization rates higher than 97% for different textile effluents within 5 h reaction time

Observations

4 Application of Fungi and Bacteria in the Management of Azo … 101

Nanomaterials

Immobilization technique

Crosslinked polyacrylonitrile/chitosan composite membrane

Chitosan beads

Commercial Tyrosinase from mushroom

Purified LiP from Schizophyllum commune IBL-06

EDTA-Cu(II) chelating magnetic nanoparticles

Chitosan grafted polyacrylamide hydrogel

Laccase from T. versicolor

Commercial laccase

Immobilization support

Enzyme

Table 4.3 (continued)

Indigo carmine

Sandal fix foron blue E2 BLN, Red C4 BLN, Turq blue GWWF 165%, Golden yellow CRL, Black CKF and Blue GWF

Acid blue 113 and Direct black 22

Malachite green

Dye degraded

Purbasha and Bhaskara (2021), Veismoradi et al. (2019)

Purbasha and Bhaskara (2021), Sun et al. (2015)

References

(continued)

Enzyme retained 70% Datta et al. (2021), of their original activity Fernandes et al. after five consecutive (2017) cycles

The immobilized Purbasha and enzyme showed Bhaskara (2021), efficient decolorization Sofia et al. (2016) (70–95%) and exhibited thermostability and reusability

The immobilized enzyme used in an enzyme membrane reactor accounted for 95% dye removal with remarkable efficiency (80%) even after ten cycles of dye degradation

After six cycles, the immobilized enzyme showed high chemical and thermal stability and better durability

Observations

102 M. García-Rivero et al.

Immobilization technique

Magnetic poly(p-phenylenediamine) iron oxide nanocomposite

Reactive blue 19

Immobilized enzymes retained 43% of their initial dye removal capacity after eight continuous cycles

Dye was removed within 12 h with degradation of 96.76%

Commercial laccases

Reactive violet 1

Observations

Maximum decolorization rate of 77%

Amino-functionalized silica

Laccase from Ganoderma cupreum AG-1

Dye degraded

Commercial laccase from Magnetic iron nanoparticles Acid fuchsine Trametes versicolor

Immobilization support

Enzyme

Table 4.3 (continued)

Datta et al. (2021), Liu et al. (2016)

Datta et al. (2021), Gao et al. (2018)

Datta et al. (2021), Gahlout et al. (2017)

References

4 Application of Fungi and Bacteria in the Management of Azo … 103

104

M. García-Rivero et al.

Table 4.4 Dye decolorization processes with bacteria, fungi, or mixed cultures immobilized in different supports Immobilization matrix

Microorganism

Dye

Comments

Sol–gel

Pseudomonas sp.

Remazol black, methyl orange, and benzyl orange

Immobilization Tuttolomondo protected bacteria et al. (2014) from the aggressive external surroundings; it produced seven times more extracellular dye-degrading enzymes and maintained a dye decolorization percentage around 80% after four reuse cycles

Calcium alginate matrix

Enterobacter agglomerans

Methyl red

The immobilized Moutaouakkil system maintained its et al. (2004) dye decolorization rate over 95% after seven cycles of repeated batch decolorization

Coconut shell biochar

Brevibacillus parabrevis

Congo red

After six days, the immobilized system removed 95.71% of the dye sample in continuous mode

Calcium alginate

Rhodococcus strain Methyl UCC 0004 orange

Immobilized beads Maniyam et al. had 66% more dye (2018) removal activity than free cells and reduced decolorization time by 67% in up to nine batches

Luffa cylindrica (Loofa)

Lysinibacillus sp. RGS

Reductive and oxidative enzymatic activities degraded 200 mg L−1 dye and 50% real textile effluent

Blue HERD and 50% real textile effluent

References

Abu Talha et al. (2018), Purbasha and Bhaskara (2021)

Bedekar et al. (2014)

(continued)

4 Application of Fungi and Bacteria in the Management of Azo …

105

Table 4.4 (continued) Immobilization matrix

Microorganism

Dye

Comments

References

Polyurethane foam

Bacterial consortium obtained from soil samples

Congo red (CR)

Batch studies with the immobilized system removed CR dye (100 mg L−1 ) entirely after 12 h under microaerophilic conditions. Also, 92% removal of a real textile effluent within 20-h culture. The process developed in an up-flow column reactor reached similar decolorization yields and mineralization

Lade et al. (2015), Purbasha and Bhaskara (2021)

Calcium alginate

T. hirsuta

Indigo carmine

Dye decolorization Domínguez was performed in et al. (2005) batch mode in the air-lift bioreactor and continued for 40 days without disrupting the bioparticles. High dye decolorization was attained at short duration, indicating the stability of this process

Macro porous Aspergillus polymeric support carbonarius M333 and Penicillium glabrum pG1

Real textile Batch and continuous Arikan et al. industry up-flow packed bed (2019) wastewater bioreactor. 78.8% decolorization after three cycles in the bioreactor

Polyurethane foam

Congo red

A microbial consortium from the wastewater disposal site of textile effluent

Immobilized Lade et al. consortium showed (2015) complete degradation of the dye and 92% of real textile wastewater and 99% for congo red (continued)

106

M. García-Rivero et al.

Table 4.4 (continued) Immobilization matrix

Microorganism

Dye

Comments

References

Calcium alginate, polyvinyl alcohol, stainless steel sponge (SSS) and polyurethane foam (PUF)

Microbial consortium with Brevibacillus laterosporus and Galactomyces geotrichum

Textile effluent and Remazol red

Microbial consortia Kurade et al. immobilized in SSS (2019) and PUF exhibited 110% decolorization along 11–15-h culture. Consortium immobilized in polyvinyl alcohol and calcium alginate also decolorized 110% of the dye, but after 20–24 h. All the immobilized systems showed >95% textile effluent decolorization within 48 h. Consortia immobilized in polyvinyl alcohol and calcium alginate were stable for five cycles of decolorization

retained 37% of its ability for consuming glucose (Santos Viveros 2019). This immobilization system was used lately to decolorize and degrade Reactive Black 5 in a 1L stirred tank reactor, showing an efficiency of around 84% (Martínez-Sánchez et al. 2018). On the other hand, this immobilized fungi was used to operate a sequential batch reactor, known as draw fill, that operated for 27 days with nine cycles of 72 h each that reached a dye decolorization of 96 ± 1.39% (Fig. 4.5), irrespective of initial dye concentration and the number of cycles (Lemus-Gómez et al. 2018). There is a need to develop easy to operate and cost-effective methods for removing azo dyes from wastewater. Although many techniques are available for dye removal, several factors determine their technical and economic feasibility. These factors are grouped into two categories: those related to microbial growth or enzyme action conditions and those related to dye solution or wastewater characteristics. The operational parameters of the first group that affect decolorization of textile dyes include the following: (i) oxygen, that is a high-redox-potential electron acceptor and exerts inhibitory effect on dye reduction process; (ii) pH, that exerts a significant effect on the efficiency of dye decolorization as it determines the growth response and the extent of dye decolorization, although the optimum pH of color removal is around neutral or slightly alkaline; (iii) temperature, that affects the metabolism, microbial growth rate, and the physiological state of dyes, as much as gas solubility; (iv) inoculum size, that varies with the microbial species used; (v) carbon an nitrogen supplements, that depend on the nature of pollutants and can enhance

4 Application of Fungi and Bacteria in the Management of Azo …

107

Fig. 4.5 Results of Reactive Black 5 decolorization by T. versicolor immobilized in PUF. a Absorption spectra of the samples obtained in the last cycle of operation between 538 and 635 h. b Samples obtained from immobilized fungus culture

microbial growth and metabolic activity; (vi) chemical nature of dye, composition, and volume of the dye-containing wastewater, that can influence the efficiency of its removal due to the toxicity of dye at higher concentrations and the ability of enzymes to binding the substrate efficiently at very low concentrations (Garg and Tripathi 2017; Teerapatsakul et al. 2017). Factors related to the characteristics of dye solution or wastewaters include dose and cost of required chemicals to be added for dye decolorization, equipment necessary, operational and maintenance costs, environmental fate, and handling costs of generated waste. Each dye removal technique has its limitations, and one single process may not be enough to achieve complete decolorization as desired for reuse. So, developing an integrated approach wherein consortia of diverse types of microbial strains, i.e., algae, bacteria, and fungus, could be used such that each of the strains would eliminate a particular contaminant from the effluent simultaneously is also essential to achieve complete bleaching (Garg and Tripathi 2017; Parmar

108

M. García-Rivero et al.

and Shukla 2018; Shetty and Krishnakumar 2020). Furthermore, using microorganisms or microbial enzymes or combining this with a physicochemical method offers another alternative to obtain a better result with economic viability (Jamee and Siddique 2019).

4.9 Conclusions There is a need to develop easy to operate and cost-effective methods for removing azo dyes from wastewater. Adsorption and degradation of azo dyes to mineralization are adequate methodologies to remove them from the environment and can be developed by using bacterial and fungal culture and enzymatic treatments, either free or immobilized. The use of microbial sources proved to be a promising approach compared to conventional physicochemical approaches. Although WRF is more efficient for dye biodegradation, it is challenging to keep fungal cultures active in activated sludge systems due to their nutritional requirements and environmental conditions. However, fungal decolorization systems can be developed from the characteristics of these biological systems. Bacterial decolorization of azo dyes in textile effluents is faster under microaerophilic or anaerobic conditions. However, the aerobic degradation of the aromatic amines produced is not effective under anaerobic conditions, limiting the treatment of azo dyes by aerobic bacteria, suggesting the development of processes that alternate an aerobic/anaerobic or microaerophilic/aerobic atmosphere and using with pure or mixed cultures. Likewise, these bacterial processes can be alternated with chemical methods to increase their efficiency, limiting their use on a large scale. Although several bioprocesses have been developed to achieve a high decolorization of azo dyes, most of them are still at the laboratory level to obtain basic information that allows reaching industrial level management of textile effluents for the removal of present dyes, which represents a significant challenge for biotechnology and process engineering. On the other hand, enzyme treatments are promising since they considerably reduce the processing time required to develop the related technologies.

References Abadulla E, Tzanov T, Costa S, Robra KH, Cavaco-Paulo A, Gubitz GM (2000) Decolorization and detoxification of textile dyes with a laccase from Trametes hirsuta. Appl Environ Microbiol 66(8):3357–3362. https://doi.org/10.1128/AEM.66.8.3357-3362.2000 Abu Talha M, Goswami M, Giri BS, Sharma A, Rai BN, Singh RS (2018) Bioremediation of Congo red dye in immobilized batch and continuous packed bed bioreactor by Brevibacillus parabrevis using coconut shell bio-char. Bioresour Technol 252(Nov 2017):37–43. https://doi.org/10.1016/ j.biortech.2017.12.081

4 Application of Fungi and Bacteria in the Management of Azo …

109

Adeel S, Zuber M, Fazal-ur-Rehman, Zia KM (2018) Microwave-assisted extraction and dyeing of chemical and bio-mordanted cotton fabric using harmal seeds as a source of natural dye. Environ Sci Pollut Res 25(11):11100–11110. https://doi.org/10.1007/s11356-018-1301-2 Adnan LA, Mohd Yusoff AR, Hadibarata T, Khudhair AB (2014) Biodegradation of bis-azo dye reactive black 5 by white-rot fungus Trametes gibbosa sp. WRF 3 and its metabolite characterization. Water Air Soil Pollut 225(10). https://doi.org/10.1007/s11270-014-2119-2 Adnan LA, Sathishkumar P, Mohd Yusoff AR, Hadibarata T (2015) Metabolites characterisation of laccase mediated Reactive Black 5 biodegradation by fast growing ascomycete fungus Trichoderma atroviride F03. Int Biodeterior Biodegradation 104:274–282. https://doi.org/10.1016/j. ibiod.2015.05.019 Agrawal S, Tipre D, Patel B, Dave S (2014) Optimization of triazo Acid Black 210 dye degradation by Providencia sp. SRS82 and elucidation of degradation pathway. Process Biochem 49(1):110– 119. https://doi.org/10.1016/j.procbio.2013.10.006 Ali L, Algaithi R, Habib HM, Souka U, Rauf MA, Ashraf SS (2013) Soybean peroxidase-mediated degradation of an azo dye—a detailed mechanistic study. BMC Biochem 14(1). https://doi.org/ 10.1186/1471-2091-14-35 Almeida EJR, Corso CR (2019) Decolorization and removal of toxicity of textile azo dyes using fungal biomass pelletized. Int J Environ Sci Technol 16(3):1319–1328. https://doi.org/10.1007/ s13762-018-1728-5 Ardila-Leal LD, Poutou-Piñales RA, Pedroza-Rodríguez AM, Quevedo-Hidalgo BE (2021) A brief history of colour, the environmental impact of synthetic dyes and removal by using laccases. Molecules 26(13). https://doi.org/10.3390/molecules26133813 Arikan EB, Isik Z, Bouras HD, Dizge N (2019) Investigation of immobilized filamentous fungi for treatment of real textile industry wastewater using up flow packed bed bioreactor. Bioresour Technol Rep 7(Mar):100197. https://doi.org/10.1016/j.biteb.2019.100197 Asgher M, Aslam B, Iqbal HMN (2013) Novel catalytic and effluent decolorization functionalities of sol-gel immobilized Pleurotus ostreatus IBL-02 manganese peroxidase produced from bioprocessing of wheat straw. Cuihua Xuebao/Chin J Catal 34(9):1756–1761. https://doi.org/10. 1016/s1872-2067(12)60647-0 Babu BR, Parande AK, Raghu S, Prem Kumar T (2007) Cotton textile processing: waste generation and effluent treatment. J Cotton Sci 11(3):141–153 Bardi L, Marzona M, Arabaci G, Usluoglu A, Oils E, Ordinance CG, German T, Goods C, Sen SK, Raut SS, Bandyopadhyay P, Raut SS, Involved E, Bacterial IN, Of D, Azo T, Karim ME, Dhar K, Hossain MT et al (2018) Fungal decolouration and degradation of azo dyes: a review. Fungal Biol Rev30(3):112–133. https://doi.org/10.1016/j.fbr.2016.06.003 Bedekar PA, Saratale RG, Saratale GD, Govindwar SP (2014) Development of low cost upflow column bioreactor for degradation and detoxification of Blue HERD and textile effluent by Lysinibacillus sp. RGS immobilized on Loofa. Int Biodeterior Biodegradation 96:112–120. https://doi. org/10.1016/j.ibiod.2014.09.007 Benkhaya S, El Harfi S, AEl Harfi A (2017) Classifications, porperties and applications of textile dyes: a review. Appl J Environ Eng Sci3(3):311–320 Bharagava RN, Mani S, Mulla SI, Saratale GD (2018) Degradation and decolourization potential of an ligninolytic enzyme producing Aeromonas hydrophila for crystal violet dye and its phytotoxicity evaluation. Ecotoxicol Environ Saf 156(Nov 2017):166–175. https://doi.org/10.1016/j. ecoenv.2018.03.012 Bilal M, Asgher M, Iqbal HMN, Hu H, Wang W, Zhang X (2017) Bio-catalytic performance and dye-based industrial pollutants degradation potential of agarose-immobilized MnP using a packed bed reactor system. Int J Biol Macromol 102:582–590. https://doi.org/10.1016/j.ijbiomac.2017. 04.065 Brüschweiler BJ, Merlot C (2017) Azo dyes in clothing textiles can be cleaved into a series of mutagenic aromatic amines which are not regulated yet. Regul Toxicol Pharmacol 88:214–226. https://doi.org/10.1016/j.yrtph.2017.06.012

110

M. García-Rivero et al.

Calà E, Gosetti F, Gulmini M, Serafini I, Ciccola A, Curini R, Salis A, Damonte G, Kininger K, Just T, Aceto M (2019) It’s only a part of the story: analytical investigation of the inks and dyes used in the privilegium maius. Molecules 24(12). https://doi.org/10.3390/molecules24122197 Cañas AI, Camarero S (2010) Laccases and their natural mediators: biotechnological tools for sustainable eco-friendly processes. Biotechnol Adv 28(6):694–705. https://doi.org/10.1016/j.bio techadv.2010.05.002 Cao J, Sanganyado E, Liu W, Zhang W, Liu Y (2019) Decolorization and detoxification of Direct Blue 2B by indigenous bacterial consortium. J Environ Manage 242(May):229–237. https://doi. org/10.1016/j.jenvman.2019.04.067 Casas N, Blánquez P, Vicent T, Sarrà M (2013) Laccase production by Trametes versicolor under limited-growth conditions using dyes as inducers. Environ Technol (United Kingdom) 34(1):113– 119. https://doi.org/10.1080/09593330.2012.683820 Cerrón-Infantes DA, Unterlass MM (2018) Síntesis ecoamigables de colorantes. Rev Quím 32(1):18–31. https://revistas.pucp.edu.pe/index.php/quimica/article/view/20342 Chacko JT, Subramaniam K (2011) Enzymatic degradation of azo dyes—a review. Int J Environ Sci 1(6):1250–1260. https://doi.org/10.6088/ijes.00106020018 Chakroun H, Mechichi T, Martinez MJ, Dhouib A, Sayadi S (2010) Purification and characterization of a novel laccase from the ascomycete Trichoderma atroviride: application on bioremediation of phenolic compounds. Process Biochem 45(4):507–513. https://doi.org/10.1016/j.procbio.2009. 11.009 Chen Y, Feng L, Li H, Wang Y, Chen G, Zhang Q (2018) Biodegradation and detoxification of Direct Black G textile dye by a newly isolated thermophilic microflora. Bioresour Technol 250(Oct 2017):650–657. https://doi.org/10.1016/j.biortech.2017.11.092 Chengalroyen MD, Dabbs ER (2013) The microbial degradation of azo dyes: minireview. World J Microbiol Biotechnol 29(3):389–399. https://doi.org/10.1007/s11274-012-1198-8 Chivukula M, Renganathan V (1995) Phenolic azo dye oxidation by laccase from Pyricularia oryzae. Appl Environ Microbiol 61(12):4374–4377. https://doi.org/10.1128/aem.61.12.4374-4377.1995 Claus H, Faber G, König H (2002) Redox-mediated decolorization of synthetic dyes by fungal laccases. Appl Microbiol Biotechnol 59(6):672–678. https://doi.org/10.1007/s00253-002-1047-z Das A, Mishra S (2017) Removal of textile dye reactive green-19 using bacterial consortium: process optimization using response surface methodology and kinetics study. J Environ Chem Eng 5(1):612–627. https://doi.org/10.1016/j.jece.2016.10.005 Datta S, Veena R, Samuel MS, Selvarajan E (2021) Immobilization of laccases and applications for the detection and remediation of pollutants: a review. Environ Chem Lett 19(1):521–538. https:// doi.org/10.1007/s10311-020-01081-y Domínguez A, Couto SR, Sanromán MÁ (2005) Dye decolorization by Trametes hirsuta immobilized into alginate beads. World J Microbiol Biotechnol 21(4):405–409. https://doi.org/10.1007/ s11274-004-1763-x Dubey SK, Pandey A, Bajaj AK, Misra K (2007) Some commercial azo dyes as inhibitors of mushroom tyrosinase DOPA oxidase activity. J Pharmacol Toxicol 2(8):718–724 Dwivedi P, Singh Tomar R (2018) Bioremediation of textile effluent for degradation and decolourization of synthetic dyes: a review. Int J Curr Res Life Sci 7(04):1948–1951. http://ijcrls.com/ sites/default/files/issues-pdf/01223.pdf Falade AO, Nwodo UU, Iweriebor BC, Green E, Mabinya LV, Okoh AI (2017) Lignin peroxidase functionalities and prospective applications. Microbiol Open 6(1):1–14. https://doi.org/10.1002/ mbo3.394 Fernandes RA, Daniel-da-Silva AL, Tavares APM, Xavier AMRB (2017) EDTA-Cu (II) chelating magnetic nanoparticles as a support for laccase immobilization. Chem Eng Sci 158(May 2016):599–605. https://doi.org/10.1016/j.ces.2016.11.011 Flores EB, Roque CP, Ochoa RL (1995) Discusión Sobre Varias Teorías Del Color. Rev Quím IX:99–109 Franciscon E, Piubeli F, Fantinatti-Garboggini F, Ragagnin de Menezes C, Serrano Silva I, CavacoPaulo A, James Grossman M, Regina Durrant L (2010) Polymerization study of the aromatic

4 Application of Fungi and Bacteria in the Management of Azo …

111

amines generated by the biodegradation of azo dyes using the laccase enzyme. Enzyme Microbiol Technol 46:360–365. https://doi.org/10.1016/j.enzmictec.2009.12.014 Forootanfar H, Moezzi A, Aghaie-Khozani M, Mahmoudjanlou Y, Ameri A, Niknejad F, Faramarzi MA (2012) Synthetic dye decolorization by three sources of fungal laccase. J Environ Health Sci Eng 9(1):1–10 Forootanfar H, Rezaei S, Zeinvand-Lorestani H, Tahmasbi H, Mogharabi M, Ameri A, Faramarzi MA (2016) Studies on the laccase-mediated decolorization, kinetic, and microtoxicity of some synthetic azo dyes. J Environ Health Sci Eng 14(1):1–9. https://doi.org/10.1186/s40201-0160248-9 Gahlout M, Rudakiya DM, Gupte S, Gupte A (2017) Laccase-conjugated amino-functionalized nanosilica for efficient degradation of Reactive Violet 1 dye. Int Nano Lett 7(3):195–208. https:// doi.org/10.1007/s40089-017-0215-1 Gao Z, Yi Y, Zhao J, Xia Y, Jiang M, Cao F, Zhou H, Wei P, Jia H, Yong X (2018) Co-immobilization of laccase and TEMPO onto amino-functionalized magnetic Fe3 O4 nanoparticles and its application in acid fuchsin decolorization. Bioresour Bioprocess 5(1). https://doi.org/10.1186/s40643018-0215-7 García-Martínez Y, Bengoa C, Stüber F, Fortuny A, Font J, Fabregat A (2015) Biodegradation of acid orange 7 in an anaerobic-aerobic sequential treatment system. Chem Eng Process 94:99–104. https://doi.org/10.1016/j.cep.2014.12.011 Garg SK, Tripathi M (2017) Microbial strategies for discoloration and detoxification of azo dyes from textile effluents. Res J Microbiol 12(1):1–19. https://doi.org/10.3923/jm.2017.1.19 Gomi N, Yoshida S, Matsumoto K, Okudomi M, Konno H, Hisabori T, Sugano Y (2011) Degradation of the synthetic dye amaranth by the fungus Bjerkandera adusta Dec 1: inference of the degradation pathway from an analysis of decolorized products. Biodegradation 22(6):1239–1245. https://doi.org/10.1007/s10532-011-9478-9 Gregory P (1990) Classification of dyes by chemical structure. In: The chemistry and application of dyes, pp 17–47. https://doi.org/10.1007/978-1-4684-7715-3_2 Hadibarata T, Adnan LA, Yusoff ARM, Yuniarto A, Rubiyatno, Zubir MMFA, Khudhair AB, Teh ZC, Naser MA (2013) Microbial decolorization of an azo dye reactive black 5 using white-rot fungus Pleurotus eryngii F032. Water Air Soil Pollut 224(6):1–9. https://doi.org/10.1007/s11 270-013-1595-0 Hai FI, Yamamoto K, Nakajima F, Fukushi K, Nghiem LD, Price WE, Jin B (2013) Degradation of azo dye acid orange 7 in a membrane bioreactor by pellets and attached growth of Coriolus versicolour. Bioresour Technol 141:29–34. https://doi.org/10.1016/j.biortech.2013.02.020 Hakala TK, Lundell T, Galkin S, Maijala P, Kalkkinen N, Hatakka A (2005) Manganese peroxidases, laccases and oxalic acid from the selective white-rot fungus Physisporinus rivulosus grown on spruce wood chips. Enzyme Microb Technol 36:461–468. https://doi.org/10.1016/j.enzmictec. 2004.10.004 Hamad MTMH, Saied MSS (2021) Kinetic studies of Congo red dye adsorption by immobilized Aspergillus niger on alginate. Appl Water Sci 11(2):1–12. https://doi.org/10.1007/s13201-02101362-z Hao J, Song F, Huang F, Yang C, Zhang Z, Zheng Y (2007) Production of laccase by a newly isolated deuteromycete fungus Pestalotiopsis sp. and its decolorization of azo dye. J Ind Microbiol Biotechnol 34:233–240. https://doi.org/10.1007/s10295-006-0191-3 He X, Song C, Li Y, Wang N, Xu L, Han X, Wei D (2018) Efficient degradation of azo dyes by a newly isolated fungus Trichoderma tomentosum under non-sterile conditions. Ecotoxicol Environ Saf 150(Jan):232–239. https://doi.org/10.1016/j.ecoenv.2017.12.043 Hofrichter M (2002) Review: lignin conversion by manganese peroxidase (MnP). Enzyme Microb Technol 30(4):454–466. https://doi.org/10.1016/S0141-0229(01)00528-2 Huang S, Huang D, Wu Q, Hou M, Tang X, Zhou J (2020) The effects of environmental C/N on the activities of lignin-degrading enzymes produced by Phanerochaete chrysosporium. Pedosphere 30(2):285–292. https://doi.org/10.1016/S1002-0160(17)60391-6

112

M. García-Rivero et al.

Ikram M, Zahoor M, El-Saber Batiha G (2020) Biodegradation and decolorization of textile dyes by bacterial strains: a biological approach for wastewater treatment. Z Phys Chem 0(0). https:// doi.org/10.1515/zpch-2020-1708 Jadhav SU, Jadhav MU, Kagalkar AN, Govindwar SP (2008) Decolorization of brilliant blue G dye mediated by degradation of the microbial consortium of Galactomyces geotrichum and Bacillus sp. J Chin Inst Chem Eng 39(6):563–570. https://doi.org/10.1016/j.jcice.2008.06.003 Jadhav I, Vasniwal R, Shrivastava D, Jadhav K (2016) Microorganism-based treatment of azo dyes. J Environ Sci Technol 9(2):188–197. https://doi.org/10.3923/jest.2016.188.197 Jain K, Shah V, Chapla D, Madamwar D (2012) Decolorization and degradation of azo dye— Reactive Violet 5R by an acclimatized indigenous bacterial mixed cultures-SB4 isolated from anthropogenic dye contaminated soil. J Hazard Mater 213–214:378–386. https://doi.org/10.1016/ j.jhazmat.2012.02.010 Jamee R, Siddique R (2019) Biodegradation of synthetic dyes of textile effluent by microorganisms: an environmentally and economically sustainable approach. Eur J Microbiol Immunol 9(4):114– 118. https://doi.org/10.1556/1886.2019.00018 Jamil F, Asgher M, Hussain F, Bhatti HN (2018) Biodegradation of synthetic textile dyes by chitosan beads cross-linked laccase from Pleurotus ostreatus IBL-02. J Anim Plant Sci 28(1):231–243 Järvinen J, Taskila S, Isomäki R, Ojamo H (2012) Screening of white-rot fungi manganese peroxidases: a comparison between the specific activities of the enzyme from different native producers. AMB Express 2:1–9 Jin X, Ning Y (2013) Laccase production optimization by response surface methodology with Aspergillus fumigatus AF1 in unique inexpensive medium and decolorization of different dyes with the crude enzyme or fungal pellets. J Hazard Mater 262:870–877. https://doi.org/10.1016/j. jhazmat.2013.09.024 Jin XC, Liu GQ, Xu ZH, Tao WY (2007) Decolorization of a dye industry effluent by Aspergillus fumigatus XC6. Appl Microbiol Biotechnol 74(1):239–243. https://doi.org/10.1007/s00253-0060658-1 Johansson T, Nyman PO (1993) Isozymes of lignin peroxidase and manganese (II) peroxidase from the white-rot basidiomycete Trametes versicolor. Arch Biochem Biophys 300(1):49–56 Jones SM, Solomon EI (2015) Electron transfer and reaction mechanism of laccases. NIH Public Access 72(5):869–883. https://doi.org/10.1007/s00018-014-1826-6.Electron Juan-Tresserras J (2000) El uso de las plantas para el lavado y teñido de tejidos en época romana: Análisis de residuos de la fullonica y la tinctoria de Barcino. El Uso de Las Plantas Para El Lavado y Teñido de Tejidos En Época Romana: Análisis de Residuos de La Fullonica y La Tinctoria de Barcino 11(11):45–62. https://doi.org/10.5209/CMPL.30870 Kabra AN, Khandare RV, Govindwar SP (2013) Development of a bioreactor for remediation of textile effluent and dye mixture: a plant-bacterial synergistic strategy. Water Res 47(3):1035– 1048. https://doi.org/10.1016/j.watres.2012.11.007 Kahraman SS, Gurdal IH (2002) Effect of synthetic and natural culture media on laccase production by white rot fungi. Biores Technol 82(3):215–217. https://doi.org/10.1016/S0960-8524(01)001 93-6 Kalme SD, Parshetti GK, Jadhav SU, Govindwar SP (2007) Biodegradation of benzidine based dye Direct Blue-6 by Pseudomonas desmolyticum NCIM 2112. Biores Technol 98(7):1405–1410. https://doi.org/10.1016/j.biortech.2006.05.023 Kanmani P, Kumar RS, Yuvaraj N, Paari KA, Pattukumar V, Arul V (2011) Microbial decolorization of synthetic dyes and reactive dyes of industrial effluents by using a novel fungus Aspergillus proliferans. Water Environ Res 83(11):2099–2106. https://doi.org/10.2175/106143011x12928 814444655 Khan R, Bhawana P, Fulekar MH (2013) Microbial decolorization and degradation of synthetic dyes: a review. Rev Environ Sci Biotechnol 12(1):75–97. https://doi.org/10.1007/s11157-0129287-6

4 Application of Fungi and Bacteria in the Management of Azo …

113

Khan R, Patel V, Khan Z (2019) Bioremediation of dyes from textile and dye manufacturing industry effluent. In: Abatement of environmental pollutants: trends and strategies. Elsevier Inc. https:// doi.org/10.1016/B978-0-12-818095-2.00005-9 Koduri RS, Tien M (1995) Oxidation of guaiacol by lignin peroxidase. J Biol Chem 270(38):22254– 22258. https://doi.org/10.1074/jbc.270.38.22254 Kojima N, Komatsu Y (2010) Hydroxylamine, oxime and hydroxamic acid derivatives of nucleic acids. In: PATAI’S chemistry of functional groups. https://doi.org/10.1002/9780470682531.pat 0514 Kuhad RC, Sood N, Tripathi KK, Singh A, Ward OP (2004) Developments in microbial methods for the treatment of dye effluents. Adv Appl Microbiol 56:185–213. https://doi.org/10.1016/S00652164(04)56006-9 Kumari S, Naraian R (2016) Decolorization of synthetic brilliant green carpet industry dye through fungal co-culture technology. J Environ Manage 180:172–179. https://doi.org/10.1016/j.jenvman. 2016.04.060 Kurade MB, Waghmode TR, Xiong JQ, Govindwar SP, Jeon BH (2019) Decolorization of textile industry effluent using immobilized consortium cells in upflow fixed bed reactor. J Clean Prod 213:884–891. https://doi.org/10.1016/j.jclepro.2018.12.218 Lade HS, Waghmode TR, Kadam AA, Govindwar SP (2012) Enhanced biodegradation and detoxification of disperse azo dye Rubine GFL and textile industry effluent by defined fungalbacterial consortium. Int Biodeterior Biodegradation 72:94–107. https://doi.org/10.1016/j.ibiod. 2012.06.001 Lade H, Govindwar S, Paul D (2015) Mineralization and detoxification of the carcinogenic azo dye Congo red and real textile effluent by a polyurethane foam immobilized microbial consortium in an upflow column bioreactor. Int J Environ Res Public Health 12(6):6894–6918. https://doi.org/ 10.3390/ijerph120606894 Lai C, Liu S, Wu G, Lin C (2017) Enhanced bio-decolorization of acid orange 7 and electricity generation in microbial fuel cells with superabsorbent-containing membrane and laccase-based bio-cathode. J Clean Prod. https://doi.org/10.1016/j.jclepro.2017.08.047 Laraib Q, Shafique M, Jabeen N, Naz SA, Nawaz HR, Solangi B, Zubair A, Sohail M (2020) Luffa cylindrica immobilized with aspergillus terreus QMS-1: an efficient and cost-effective strategy for the removal of congo red using stirred tank reactor. Pol J Microbiol 69(2):193–203. https:// doi.org/10.33073/PJM-2020-022 Le TT, Murugesan K, Lee CS, Vu CH, Chang YS, Jeon JR (2016) Degradation of synthetic pollutants in real wastewater using laccase encapsulated in core-shell magnetic copper alginate beads. Bioresour Technol 216:203–210. https://doi.org/10.1016/j.biortech.2016.05.077 Le Coz CJ (2011) Clothing. In: Johansen JD, Frosch P, Lepoittevin JP (eds) Contact dermatitis, 5th edn. Springer, Berlin, pp 793–817. https://doi.org/10.1007/978-3-642-03827-3_40 Legerská B, Chmelová D, Ondrejoviˇc M (2018) Decolourization and detoxification of monoazo dyes by laccase from the white-rot fungus Trametes versicolor. J Biotechnol 285(Aug):84–90. https://doi.org/10.1016/j.jbiotec.2018.08.011 Lemus-Gómez LE, Martínez-Trujillo MA, Membrillo-Venegas I, García-Rivero M (2018) Performance analysis of azo dye decolorization by immobilized Trametes versicolor in a sequencing batch reactor. Environ Eng Sci 35(12). https://doi.org/10.1089/ees.2018.0033 Li Q, Ge L, Cai J, Pei J, Xie J, Zhao L (2014) Comparison of two laccases from Trametes versicolor for application in the decolorization of dyes. J Microbiol Biotechnol 24(4):545–555. https://doi. org/10.4014/jmb.1310.10079 Li Z, Chen Z, Zhu Q, Song J, Li S, Liu X (2020) Improved performance of immobilized laccase on Fe3 O4 @C-Cu2+ nanoparticles and its application for biodegradation of dyes. J Hazard Mater 399(June):123088. https://doi.org/10.1016/j.jhazmat.2020.123088 Liu Y, Yan M, Geng Y, Huang J (2016) Laccase immobilization on poly(p-phenylenediamine)/Fe3 O4 nanocomposite for reactive blue 19 dye removal. Appl Sci (Switzerland) 6(8). https://doi.org/10. 3390/app6080232

114

M. García-Rivero et al.

López C, Valade AG, Combourieu B, Mielgo I, Bouchon B, Lema JM (2004) Mechanism of enzymatic degradation of the azo dye Orange II determined by ex situ 1H nuclear magnetic resonance and electrospray ionization-ion trap mass spectrometry. Anal Biochem 335(1):135– 149. https://doi.org/10.1016/j.ab.2004.08.037 Ma HF, Meng G, Cui BK, Si J, Dai YC (2018) Chitosan crosslinked with genipin as supporting matrix for biodegradation of synthetic dyes: laccase immobilization and characterization. Chem Eng Res Des 132:664–676. https://doi.org/10.1016/j.cherd.2018.02.008 Mäkelä M, Galkin S, Hatakka A, Lundell T (2002) Production of organic acids and oxalate decarboxylase in lignin-degrading white rot fungi. Enzyme Microb Technol 30(4):542–549. https:// doi.org/10.1016/S0141-0229(02)00012-1 Mani A, Hameed SAS (2019) Improved bacterial-fungal consortium as an alternative approach for enhanced decolourisation and degradation of azo dyes: a review. Nat Environ Pollut Technol 18(1):49–64 Maniyam MN, Yaacob NS, Azman HH, Ab Ghaffar NA, Abdullah H (2018) Immobilized cells of Rhodococcus strain UCC 0004 as source of green biocatalyst for decolourization and biodegradation of methyl orange. Biocatal Agric Biotechnol 16(Aug):569–578. https://doi.org/10.1016/j. bcab.2018.10.008 Martínez AT, Ruiz-Dueñas FJ, Camarero S, Serrano A, Linde D, Lund H, Vind J, Tovborg M, Herold-Majumdar OM, Hofrichter M, Liers C, Ullrich R, Scheibner K, Sannia G, Piscitelli A, Pezzella C, Sener ME, Kılıç S, van Berkel WJH et al (2017) Oxidoreductases on their way to industrial biotransformations. Biotechnol Adv 35(6):815–831. https://doi.org/10.1016/j.biotec hadv.2017.06.003 Martínez-Sánchez J, Membrillo-Venegas I, Martínez-Trujillo A, García-Rivero AM (2018) Decolorization of reactive black 5 by immobilized Trametes versicolor. Rev Mex Ing Quim 17(1). https://doi.org/10.24275/uam/izt/dcbi/revmexingquim/2018v17n1/Martinez Martorell MM, Pajot HF, De Figuero LIC (2017) Biological degradation of Reactive Black 5 dye by yeast Trichosporon akiyoshidainum. Biochem Pharmacol 5(6):5987–5993. https://doi.org/10. 1016/j.jece.2017.11.012 Méndez-Hernández JE, Loera O (2019) Biotechnological potential of ligninolytic enzymes for pollutant biodegradation in water: from test-tbes to full-scale enzymatic reactors. Rev Mex Ing Quím 18(1):397–417. https://doi.org/10.24275/uam/izt/dcbi/revmexingquim/2019v1 8n2/Mendez Mishra S, Maiti A (2019) Applicability of enzymes produced from different biotic species for biodegradation of textile dyes. Clean Technol Environ Policy 21(4):763–781. https://doi.org/10. 1007/s10098-019-01681-5 Moutaouakkil A, Zeroual Y, Dzayri FZ, Talbi M, Lee K, Blaghen M (2004) Decolorization of azo dyes with Enterobacter agglomerans immobilized in different supports by using fluidized bed bioreactor. Curr Microbiol 48(2):124–129. https://doi.org/10.1007/s00284-003-4143-0 Ning C, Qingyun L, Aixing T, Wei S, Youyan L (2018) Decolorization of a variety of dyes by Aspergillus flavus A5p1. Bioprocess Biosyst Eng 41(4):511–518. https://doi.org/10.1007/s00 449-017-1885-9 Noreen S, Asgher M, Hussain F, Iqbal A (2016) Performance improvement of Ca-alginate bead cross-linked laccase from Trametes versicolor IBL-04. BioResources 11(1):558–572. https://doi. org/10.15376/biores.11.1.558-572 Omeje KO, Nnolim NE, Ezema BO, Ozioko JN, Eze SOO (2020) Synthetic dyes decolorization potential of agroindustrial waste-derived thermo-active laccase from Aspergillus species. Biocatal Agric Biotechnol 29(July):101800. https://doi.org/10.1016/j.bcab.2020.101800 Padmavathy S, Sandhya S, Swaminathan K, Subrahmanyam YV, Chakrabarti T, Kaul SN (2003) Aerobic decolorization of reactive azo dyes in presence of various cosubstrates. Chem Biochem Eng Q 17(2):147–151 Pandey A, Singh P, Iyengar L (2007) Bacterial decolorization and degradation of azo dyes. Int Biodeterior Biodegradation 59(2):73–84. https://doi.org/10.1016/j.ibiod.2006.08.006

4 Application of Fungi and Bacteria in the Management of Azo …

115

Pandi A, Kamini NR, Saravanan P, Gowthaman MK (2019) A sustainable approach for degradation of leather dyes by a new fungal laccase. J Cleaner Prod 211:590–597. https://doi.org/10.1016/j. jclepro.2018.11.048 Parmar ND, Shukla SR (2018) Decolourization of dye wastewater by microbial methods—a review. Indian J Chem Technol 25(4):315–323 Patel Y, Mehta C, Gupte A (2012) Assessment of biological decolorization and degradation of sulfonated di-azo dye Acid Maroon V by isolated bacterial consortium EDPA. Int Biodeterior Biodegradation 75:187–193. https://doi.org/10.1016/j.ibiod.2012.10.004 Pathak H, Soni D, Chauhan K (2014) Evaluation of in vitro efficacy for decolorization and degradation of commercial azo dye RB-B by Morganella sp. HK-1 isolated from dye contaminated industrial landfill. Chemosphere 105:126–132. https://doi.org/10.1016/j.chemosphere. 2014.01.004 Perei K, Rákhely G, Kiss I, Polyák B, Kovács KL (2001) Biodegradation of sulfanilic acid by Pseudomonas paucimobilis. Appl Microbiol Biotechnol 55(1):101–107. https://doi.org/10.1007/ s002530000474 Pervaiz S, Mughal TA, Khan FZ, Hayat S, Aslam A, Shah SF (2017) Environmental friendly leather dyeing using Tagetes erecta L. (Marigold) waste flowers. Int J of Biosci (IJB) 10(2):382–390. https://doi.org/10.12692/ijb/10.1.382-390 Piscitelli A, Giardina P, Lettera V, Pezzella C, Sannia G, Faraco V (2011) Induction and transcriptional regulation of laccases in fungi. Curr Genomics 12(2):104–112. https://doi.org/10.2174/138 920211795564331 Platzek T (2010) Risk from exposure to arylamines from consumer products and hair dyes. Front Biosci (Elite edn) 1169–1183 Pricelius S, Held C, Sollner S, Deller S, Murkovic M, Ullrich R, Hofrichter M, Cavaco-paulo A, Macheroux P, Guebitz GM (2007) Enzymatic reduction and oxidation of fibre-bound azo-dyes. Enzyme Microb Technol 40:1732–1738. https://doi.org/10.1016/j.enzmictec.2006.11.004 Purbasha S, Bhaskara R (2021) Immobilization as a powerful bioremediation tool for abatement of dye pollution: a review. Environ Rev 29(999):1–23 Razo-Flores E, Donlon B, Lettinga G, Field JA (1997) Biotransformation and biodegradation of Nsubstituted aromatics in methanogenic granular sludge. FEMS Microbiol Rev 20(3–4):525–538. https://doi.org/10.1016/S0168-6445(97)00031-4 Recabarren R, Fuenzalida I, Jans V, Morales A (2016) Studying the binding mechanisms of veratryl alcohol to P. chrysosporium lignin peroxidase: insights from theoretical approaches. Theor Chem Acc 135(3):1–12. https://doi.org/10.1007/s00214-016-1828-6 Reda FM, Hassan NS, El-Moghazy AN (2018) Decolorization of synthetic dyes by free and immobilized laccases from newly isolated strain Brevibacterium halotolerans N11 (KY883983). Biocatal Agric Biotechnol 15(May):138–145. https://doi.org/10.1016/j.bcab.2018.05.020 Rekik H, Jaouadi NZ, Bouacem K, Zenati B, Kourdali S, Badis A, Annane R, Bouanane-Darenfed A, Bejar S, Jaouadi B (2018) Physical and enzymatic properties of a new manganese peroxidase from the white-rot fungus Trametes pubescens strain i8 for lignin biodegradation and textile-dyes biodecolorization. Int J Biol Macromol 125:514–525. https://doi.org/10.1016/j.ijbiomac.2018. 12.053 Said B, Souad MR, Ahmed EH (2020) A review on classifications, recent synthesis and applications of textile dyes. Inorg Chem Commun (Mar):107891 Samanta AK, Agarwal P (2009) Application of natural dyes on textiles. Indian J Fibre Text Res 34:384–399 Sandhya S (2010) Biodegradation of azo dyes under anaerobic condition: role of azoreductase. In: Biodegradation of azo dyes, pp 39–57 Santos Viveros P (2019) Remoción del colorante negro básico OM en un reactor de lecho fluidizado con Trametes versicolor. In: Memorias de residencia. Tecnológico de Estudios Superiores de Ectepec

116

M. García-Rivero et al.

Saranraj P, Manigandan M (2018) Enzymes involved in bacterial decolourization and degradation of textile azo dyes. Indo-Asian J Multidisc Res (IAJMR) 4(1):1369–1376. https://doi.org/10.22192/ iajmr.2018.4.1.5 Saroj S, Kumar K, Pareek N, Prasad R, Singh RP (2014) Biodegradation of azo dyes Acid Red 183, Direct Blue 15 and Direct Red 75 by the isolate Penicillium oxalicum SAR-3. Chemosphere 107:240–248. https://doi.org/10.1016/j.chemosphere.2013.12.049 Sathishkumar P, Kamala-Kannan S, Cho M, Kim JS, Hadibarata T, Salim MR, Oh BT (2014) Laccase immobilization on cellulose nanofiber: the catalytic efficiency and recyclic application for simulated dye effluent treatment. J Mol Catal B Enzym 100:111–120. https://doi.org/10.1016/ j.molcatb.2013.12.008 SCCS (2011) Scientific committee on consumer safety Basic Red 51. https://doi.org/10.2772/99115 Sen SK, Raut S, Bandyopadhyay P, Raut S (2016) Fungal decolouration and degradation of azo dyes: a review. Fungal Biol Rev 30(3):112–133. https://doi.org/10.1016/j.fbr.2016.06.003 Seo JS, Keum YS, Li QX (2009) Bacterial degradation of aromatic compounds. Int J Environ Res Public Health 6(1). https://doi.org/10.3390/ijerph6010278 Shah MP (2019) Bioremediation of azo dye. In: Microbial wastewater treatment. Elsevier Inc. https://doi.org/10.1016/B978-0-12-816809-7.00006-3 Shaheen R, Asgher M, Hussain F, Bhatti HN (2017) Immobilized lignin peroxidase from Ganoderma lucidum IBL-05 with improved dye decolorization and cytotoxicity reduction properties. Int J Biol Macromol 103:57–64. https://doi.org/10.1016/j.ijbiomac.2017.04.040 Shetty K, Krishnakumar G (2020) Algal and cyanobacterial biomass as potential dye biodecolorizing material: a review. Biotech Lett 42(12):2467–2488. https://doi.org/10.1007/s10529-020-03005-w Shleev S, Christenson A, Serezhenkov V, Burbaev D, Yaropolov A (2005) Electrochemical redox transformations of T1 and T2 copper sites in native Trametes hirsuta laccase at gold electrode. Biochem J 385:745–754 Singh RL, Singh PK, Singh RP (2015) Enzymatic decolorization and degradation of azo dyes—a review. Int Biodeterior Biodegradation 104:21–31. https://doi.org/10.1016/j.ibiod.2015.04.027 Slama HB, Bouket AC, Pourhassan Z, Alenezi FN, Silini A, Cherif-Silini H, Oszako T, Luptakova L, Goli´nska P, Belbahri L (2021) Diversity of synthetic dyes from textile industries, discharge impacts and treatment methods. Appl Sci (Switzerland) 11(14):1–21. https://doi.org/10.3390/app 11146255 Sofia P, Asgher M, Shahid M, Randhawa MA (2016) Chitosan beads immobilized Schizophyllum commune IBL-06 lignin peroxidase with novel thermo stability, catalytic and dye removal properties. J Anim Plant Sci 26(5):1451–1463 Sosa-Martínez JD, Balagurusamy N, Montañez J, Peralta RA, Moreira R de FPM, Bracht A, Peralta RM, Morales-Oyervides L (2020) Synthetic dyes biodegradation by fungal ligninolytic enzymes: process optimization, metabolites evaluation and toxicity assessment. J Hazard Mater400(June):123254. https://doi.org/10.1016/j.jhazmat.2020.123254 Srinivasan S, Sadasivam SK (2018) Exploring docking and aerobic-microaerophilic biodegradation of textile azo dye by bacterial systems. J Water Process Eng 22(Jan):180–191. https://doi.org/10. 1016/j.jwpe.2018.02.004 Sun H, Yang H, Huang W, Zhang S (2015) Immobilization of laccase in a sponge-like hydrogel for enhanced durability in enzymatic degradation of dye pollutants. J Colloid Interface Sci 450:353– 360. https://doi.org/10.1016/j.jcis.2015.03.037 Svobodová K, Novotný Cˇ (2018) Bioreactors based on immobilized fungi: bioremediation under non-sterile conditions. Appl Microbiol Biotechnol 102(1):39–46. https://doi.org/10.1007/s00 253-017-8575-z Tahir U, Yasmin A, Khan UH (2016) Phytoremediation: potential flora for synthetic dyestuff metabolism. J King Saud Univ Sci 28(2):119–130. https://doi.org/10.1016/j.jksus.2015.05.009 Teerapatsakul C, Parra R, Keshavarz T, Chitradon L (2017) Repeated batch for dye degradation in an airlift bioreactor by laccase entrapped in copper alginate. Int Biodeterior Biodegradation 120:52–57. https://doi.org/10.1016/j.ibiod.2017.02.001

4 Application of Fungi and Bacteria in the Management of Azo …

117

Telke A, Kalyani D, Jadhav J, Govindwar S (2008) Kinetics and mechanism of reactive red 141 degradation by a bacterial isolate Rhizobium radiobacter MTCC 8161. Acta Chim Slov 55(2):320–329 Tuttolomondo MV, Alvarez GS, Desimone MF, Diaz LE (2014) Removal of azo dyes from water by sol-gel immobilized Pseudomonas sp. J Environ Chem Eng 2(1):131–136. https://doi.org/10. 1016/j.jece.2013.12.003 Veismoradi A, Mousavi SM, Taherian M (2019) Decolorization of dye solutions by tyrosinase in enzymatic membrane reactors. J Chem Technol Biotechnol 94(11):3559–3568. https://doi.org/ 10.1002/jctb.6158 Wang P, Hu X, Cook S, Begonia M, Lee KS, Hwang HM (2008) Effect of culture conditions on the production of ligninolytic enzymes by white rot fungi Phanerochaete chrysosporium (ATCC 20696) and separation of its lignin peroxidase. World J Microbiol Biotechnol 24(10):2205–2212. https://doi.org/10.1007/s11274-008-9731-5 Wang J, Feng J, Jia W, Chang S, Li S, Li Y (2015) Lignin engineering through laccase modification: a promising field for energy plant improvement. Biotechnol Biofuels 8(1):1–11. https://doi.org/ 10.1186/s13068-015-0331-y Wang N, Chu Y, Wu F, Zhao Z, Xu X (2017) Decolorization and degradation of Congo red by a newly isolated white rot fungus, Ceriporia lacerata, from decayed mulberry branches. Int Biodeterior Biodegradation 117:236–244. https://doi.org/10.1016/j.ibiod.2016.12.015 Wang F, Terry N, Xu L, Zhao L, Ding Z, Ma H (2019) Fungal laccase production from lignocellulosic agricultural wastes by solid-state fermentation: a review. Microorganisms 7(12). https://doi.org/ 10.3390/microorganisms7120665 Wong DWS (2009) Structure and action mechanism of ligninolytic enzymes. Appl Biochem Biotechnol 157(2). https://doi.org/10.1007/s12010-008-8279-z Wong JKH, Tan HK, Lau SY, Yap PS, Danquah MK (2019) Potential and challenges of enzyme incorporated nanotechnology in dye wastewater treatment: a review. J Environ Chem Eng 7(4):103261. https://doi.org/10.1016/j.jece.2019.103261 Yang JS, Yuan HL, Wang HX, Chen WX (2005) Purification and characterization of lignin peroxidases from Penicillium decumbens P6. World J Microbiol Biotechnol 21:435–440 van der Zee FP (2002) Anaerobic azo dye reduction. Wageningen University Zhao X, Hardin IR, Hwang HM (2006) Biodegradation of a model azo disperse dye by the white rot fungus Pleurotus ostreatus. Int Biodeterior Biodegradation 57(1):1–6. https://doi.org/10.1016/j. ibiod.2005.10.008 Zheng F, Cui BK, Wu XJ, Meng G, Liu HX, Si J (2016) Immobilization of laccase onto chitosan beads to enhance its capability to degrade synthetic dyes. Int Biodeterior Biodegradation 110(4):69–78. https://doi.org/10.1016/j.ibiod.2016.03.004 Zhu C, Bao G, Huang S (2016) Optimization of laccase production in the white-rot fungus Pleurotus ostreatus (ACCC 52857) induced through yeast extract and copper. Biotechnol Biotechnol Equip 30(2):270–276. https://doi.org/10.1080/13102818.2015.1135081 Zille A, Gornacka B, Rehorek A, Cavaco-Paulo A (2005) Degradation of azo dyes by Trametes villosa laccase over long periods of oxidative conditions. Appl Environ Microbiol 71(11):6711– 6718. https://doi.org/10.1128/AEM.71.11.6711-6718.2005

Chapter 5

Bioremediation: An Effective, Significant and Eco-friendly Approach for Sustainable Management Ankita Mallick, Subhajoy Dey, Soustav Datta, and Mainak Barman

Abstract As civilisation has advanced, human desires have increased and diversified. Consequently, natural resources have been drastically exhausted. Many environmental issues have been intensified as a result of the excessive consumption of resources. Soil and water contamination has become a matter of great concern as a result of industrialisation and the usage of natural resources. Toxicity occurs in environment as a result of pollution, such as poisoning of soil or water, or as a result of occupational exposure. In low amounts, some of these metals are beneficial to us, but in higher concentrations, they are highly toxic. Metal contamination has a high rate of morbidity and mortality. In the recent time of environmental protection, the utilisation of microbes to recover heavy metals from soil, sediments and water has aroused a lot of interest. Metal biotransformation is the basic mechanism of microbial remediation for environmental decontamination. Microbial remediation is a cutting-edge technique for reclaiming damaged areas that employs metal immobilisation. If this method is implemented, heavy metals will be less accessible to living systems. Bacillus, Enterobacter, Escherichia, Pseudomonas, as well as some yeasts and fungi, aid in the bioremediation of contaminated soil and water through heavy metal bio-absorption and bioaccumulation. We have provided an overview of bioremediation as an effective and eco-friendly sustainable approach to the critical illness of contaminated soil and water in this article. Keywords Contamination · Bioremediation · Soil · Water · Sustainable management · Microorganisms A. Mallick · S. Dey Department of Agricultural Meteorology and Physics, Bidhan Chandra Krishi Viswavidyalaya, Mohanpur, Nadia, West Bengal, India S. Datta (B) Department of Fruit Science, Bidhan Chandra Krishi Viswavidyalaya, Mohanpur, Nadia, West Bengal, India e-mail: [email protected] M. Barman Department of Genetics and Plant Breeding, Bidhan Chandra Krishi Viswavidyalaya, Mohanpur, Nadia, West Bengal, India © The Author(s), under exclusive license to Springer Nature Switzerland AG 2022 T. Aftab (ed.), Sustainable Management of Environmental Contaminants, Environmental Contamination Remediation and Management, https://doi.org/10.1007/978-3-031-08446-1_5

119

120

A. Mallick et al.

5.1 Introduction Contamination of soils, groundwater, sediments, surface water and air with toxic and poisonous compounds is among the most pressing matters confronting the industrialised world today (Baker and Herson 1994). The concentration of different metals deposited in soil and water has increased as a result of the industrial advancement, posing a significant threat to human life and aquatic biota. Extracting cadmium, lead, mercury and chromium from diverse environmental and human activities has an enormous influence on 66 million people around the world, according to current research (Earth 2015). Additionally, tainted drinking water has impacted around 150 million individuals around the world (Ravenscroft et al. 2011). They are not always hazardous to human health, but they also affect wildlife and flora and they are not biodegradable in nature. When metals are present in our bodies, they have the potential to cause major health issues by interfering with our regular physiological functions. Arsenic, copper, iron and nickel, for example, are beneficial to the body in low concentrations but detrimental in elevated concentration. Aluminium, beryllium, cadmium, lead and mercury, for example, have no biological purpose and are highly poisonous, disrupting bodily functions to a great extent. They led to serious activities to be disrupted by accumulating in key organs and glands such as the heart, brain, kidney, bone and liver. They also displace critical nutritious elements from their normal locations in the system, causing biological tasks to be disrupted to a large level, such as when lead or cadmium displaces calcium in an enzyme reaction, leading the enzymatic process to be greatly disrupted number of health disorders. Metals cause genotoxicity because they annoy the body and alter the DNA. These metals cause cancer by causing genetic instability (Leonard et al. 2004). When we consider the massive influence that these metals have on our bodies, we have to wonder how they get into our bodies. We get exposed to these metals through our environment, whether it is our personal environment or our workplace. These pollutants can be found in meals and beverages, as well as in the air we breathe and through our skin. Wearing gloves, utilising safe breathing apparatus and eating organically cultivated food are all ways to protect ourselves. However, all of the aforementioned safeguards do not completely protect us against heavy metal exposure (Ray and Ray 2009). Water pollution is proportionate to the level of contamination in our environment. Surface run-off, sewage and industrial effluents gather contaminants in streams and rivers, which are then transmitted to the waterways, ponds, lakes and reservoirs that provide our drinking water (Skeat 1969). Due to the obvious necessity of cleaning up these sites, new methods have been developed that concentrate on the eradication of pollutants rather than the traditional disposal system. Physico-chemical techniques to metal pollution reclamation are expensive, environmentally dangerous and generate secondary products, prompting the usage of biological agents judiciously. Over the course of evolution, microorganisms living in metal-contaminated soil and water have evolved a complicated system of metal oxidation through cellular mechanisms. Among these new technologies,

5 Bioremediation: An Effective, Significant and Eco-friendly …

121

bioremediation, which entails the use of microbes or biological processes to destroy pollutants, is a considerable one (Boothapy 2000). Bioremediation is referred to as the use of biological processes to remove, reduce or convert polluting or contaminating chemicals. Microbial bioremediation is a practice in which microorganisms break down hazardous organic contaminants to levels below the permissible limit in a wide range of environments (Gareth and Furlong 2003). Most of the previous research has concentrated on the techniques and processes that enable microorganism metal resistance (Ezzouhri et al. 2009). Both active and passive adsorptions of heavy metals have previously been observed (Das et al. 2008). The capacity of microorganisms to oxidise metals is also very useful for heavy metals removal (Wu et al. 2020), developing the foundation for contaminant removal (Aziz et al. 2020). In the aquatic environment, microorganisms play a prominent part in metal removal. Bioremediation appears to be quite economical and creates less site inconvenience; it eliminates waste permanently, reduces long-term liability and has a better level of public acceptance as well as regulatory backing; and it can be integrated with other physical and chemical therapeutic approaches (Boothapy 2000). The application of bio-remediating agents can reduce both the environmental and financial costs of waste disposal (Pillay 1992), whereas natural resources are valuable assets to human, bioremediation of polluted sites and habitats will be the most environmentally responsible way to protect the rare resources while also ensuring effective waste recycling (Divya et al. 2015). In recent decades, heavy metals have received considerable attention in the aspect of environmental research (Salem et al. 2000). This chapter discusses the principles, strategies and application of bioremediation in various fields which dictates the significance and effectiveness of this holistic approach for eco-friendly and sustainable management of pollutants in this generation.

5.2 Principles of Bioremediation The total condition of the environment is intrinsically tied to the quality of life on Earth. We used to think we could never run out of land or resources; today, however, the world’s resources reflect our carelessness and ignorance in using them to varying degrees. Contamination with detectable amounts of inorganic and organic substances as a result of industrial (and transportation) pollution, on the other hand, is perhaps the most significant issue facing society today. Recent advances in molecular biology as well as in ecology have opened the door to more efficient biological processes in polluted water and land. Bioremediation is a subject of study that is rapidly gaining importance in terms of humanity’s long-term sustainability and existence. Bioremediation is the process of biological degradation of organic wastes to a benign state or concentrations below regulatory concentration limits under controlled settings (Mueller et al. 1996). It uses naturally existing bacteria, fungus, or plants to degrade or detoxify chemicals that are detrimental to human health and/or the environment. Contaminants are used by microorganisms as a food supply as well as

122

A. Mallick et al.

a source of energy (Azubuike et al. 2016). The microorganisms may be native to the polluted location or separated from elsewhere as well as transported to the polluted site, a process termed as bio-augmentation. Microorganisms successfully degrade or change a complex and harmful contamination into a simpler or less harmful one (Ayangbenro and Babalola 2017). Environmental conditions that allow for microbial growth and activity are required for bioremediation to be successful. Its use typically entails manipulating environmental factors in order to speed up microbial development and breakdown (Sharma 2012). The basic purpose of bioremediation is to encourage the local micro-flora in a polluted site to develop to their maximum potential as well as to produce a greater number of enzymes as secondary metabolites by supplying more food and appropriate growing circumstances. These metabolites are significantly more effective at breaking down the complicated pollutant into smaller components (Chen and Wang 2017). Bioremediation is the process of degrading environmental pollutants into less hazardous forms using living creatures, typically bacteria. Bioremediation, like other approaches, has inherent limits. Microbial assault is resistant to some pollutants, e.g. chlorinated organic and high aromatic hydrocarbon. They degrade slowly or not at all, making it difficult to anticipate the rate of bioremediation clean-up; standards do not exist for predicting whether a pollutant can be destroyed. Bioremediation procedures are often less expensive than traditional methods like cremation as well as on-site treatment is possible for some pollutants, reducing the risk of exposure for clean-up workers and the possibility of wider exposure owing to transportation mishaps. The majority of bioremediation systems are operated under aerobic circumstances, but anaerobic environments (Colberg and Young 1995) may allow microbes to break down substances that are otherwise resistant to degradation. Aerobic bacteria are utilised more frequently in bioremediation approaches than anaerobic bacteria (Azubuike et al. 2016). Controlling as well as optimising bioremediation processes is a complicated system involving numerous variables. The presence of a microbial population capable of degrading contaminants and the availability of contaminants to the microbial population as well as environmental circumstances are among these considerations (type of soil, pH, temperature, the presence of oxygen or other electron acceptors and nutrients). Metal-transforming microbes include bacteria (Arthrobacter sp. and Streptomyces sp.), archaea (Phylum sp.), fungus (Aspergillus sp. and Penicillium sp.) and yeast (Saccharomyces cerevisiae) (Gupta and Singh 2017) (Table 5.1). Most bioremediation systems are run under aerobic conditions, but running a system under anaerobic conditions may permit microbial organisms to degrade otherwise recalcitrant molecules.

5 Bioremediation: An Effective, Significant and Eco-friendly …

123

Table 5.1 Several contaminants suitable for bioremediation Class of contaminants

Specific example

More potential source

Chlorinated solvents

Tricholroetheylene Perchloroetylene

Dry cleaners

Polychlorinated biphenyls

4-Chlorobiphenyl 4,4-Dichlorobiphenyl

Electrical manufacturing power station

Chlorinated phenol

Pentacholrophenol

Timber treatment, landfills

“BTEX”

Toluenen, benzene, ethylbenzene

Chemical manufacture, airports, paint manufacture, port facilities, railway wards

Polyaromatic hydrocarbons (PAHs)

Fluorene, naphthalene, pyrene, Oil production and storage, gas benzo (a) pyrene work sites, engine works, landfills

Pesticides

Atrazine, carbaryl, diazinon, 2,4-D, parathion, glycophosphate

Agriculture, timber treatment plants, pesticide manufacture

Adapted and modified from Vidali (2001)

5.3 Factors Influencing Bioremediation Various biotic and abiotic variables influence microbial cell activity and growth, affecting a variety of biological activities in a microbial community. Microbes have a first-rate ability to adapt the new environments, yet they do have some limitations. To improve microbial action and forecast the effective bioremediation process, a thorough understanding of microbial ecology is essential (Watanabe 2001). There are three sorts of variables which influence microbial processes, viz. (1) environmental physico-chemical properties or abiotic factors, (2) biological factors or biotic factors and (3) environmental factors whereby physico-chemical and climatic circumstances are among the key factors impacting the metabolic rates of microorganisms.

5.3.1 Physico-chemical Factors Affecting Bioremediation Redox potential (Eh), pH, ionic strength, temperature, solubility, presence or absence of electron acceptors and donors and age of organometalic ions are examples of physico-chemical factors. Biosorption is a pH-dependent phenomenon in which the isoelectric point in a solution influences the net negative charge on the microbial cell surface, which is a basic stage in hazardous metal removal by bacteria. Additionally, the ionic state of ligands, such as carboxyl residues, phosphoryl residues, S–H groups as well as amino acid groups, alters as a result of this alteration (Sa˘g et al. 1995). Because soluble metal ions may only undergo enzymatic reduction, bioremediation procedures entail reducing metal ions to insoluble form by microbes from higher to lower oxidation states (pH dependent). Metals with higher oxidation

124

A. Mallick et al.

states are usually soluble (Garbisu and Alkorta 2003). The solubility of metal ions is affected by pH values, which increases as the pH of the medium decreases, impacting microbial cell adsorption (Blázquez et al. 2009). Moreover, metal ions must attach to the microbial cell surface at lower pH levels (Rajendran et al. 2002; Han and Gu 2010), considering that metal ions prefer to precipitate in an alkaline media. Pseudomonas sp. and Burkholderia cepacia produce gluconic acid, while Rhizobium sp. and Bacillus firmus make ketogluconic acid (Robles-González et al. 2008). The pH of the fluid is lowered by these bacteria, which increases the solubility of metal ions. Metal ion mobilisation is increased by organometalic compounds (Puzon et al. 2005). The biodegradation processes are further influenced by the presence of electron acceptors, such as oxygen in aerobic microorganisms and NO3 1− , SO4 2− and Fe (III) oxides in anaerobic microorganisms (Lovely 2003).

5.3.2 Biological Factors Influencing Bioremediation Biological factors are not always visible, but their importance is frequently revealed with the implementation of bioremediation techniques. Microbes have several inherent characteristics that influence substrate degradation, such as plasmidencoded genes that supply substrate specificity as well as encode specific enzymes (proteins); it has, however, been seen in nature that microbes, particularly bacterial cells, have diverse specificity for various substrates (Mars et al. 1997). Bacterial chemotaxis is a beneficial bacterial activity for degrading refractory organic substances (Pandey and Jain 2002). Bioremediation microbial communities frequently rely on complicated multispecies interaction networks as represented in Fig. 5.1. Organohalide-respiratory bacteria can only survive in consortia, and their isolation as well as culture is very tough. It was defined by Maphosa et al. (2010) as a function of metagenomics or community genomics in which data from member species of consortia that enable substrate degradation is provided by metagenomics sequencing. Furthermore, bacteria’ optimal growing circumstances are unpredictably variable (Ingham et al. 2007). Microbes and microbial communities are essential for the efficient functioning of Earth’s ecosystems, and variables altering their composition, metabolism and abundance may disrupt ecosystems (Nweke et al. 2007). Allelopathic effects of terrestrial plants on the microbial population may have a deleterious impact on soil microorganisms’ ability to degrade (Chakraborty et al. 2012). Because of the solubility of OCs and the lack of oxygen, aerobic microbial activity is reduced. A few microorganisms, on the other hand, use other sources of organic carbon, electron acceptor as well as energy as co-metabolic substrate to degrade the recalcitrant, such as Mycobacterium gilvum, which, according to reports, degrades pyrene aerobically in the rhizosphericzone of Phragmites australis at the same time as benzo(a)pyrene degradation (Toyama et al. 2011). The toxic pressure placed by the pollutants on the bacteria which cause enzymatic modifications determines when microbial breakdown of xenobiotics begins (Pandey and Jain 2002).

5 Bioremediation: An Effective, Significant and Eco-friendly …

125

Fig. 5.1 Layout showing factors affecting the microbial ecology, thereby affecting bioremediation processes of microbes Adapted and modified from Srivastava et al. (2014)

5.3.3 Environmental Factors Influencing Bioremediation Process 5.3.3.1

Nutrients

Although microorganisms may be found in polluted soil, they may not be present in sufficient numbers to allow for the site’s bioremediation. Their development as well as activity must be encouraged. To aid indigenous microorganisms, biostimulation usually entails the provision of nutrients and oxygen. These nutrients are the fundamental components of life, allowing bacteria to produce the enzymes required to break down pollutants. In living creatures, carbon is the most basic element, and it is required in higher amounts compared to other components. It makes up around 95% of the weight of cells, together with hydrogen, oxygen, and nitrogen. Phosphorous and sulphur account for 70% of the remaining materials. Carbon to nitrogen is a 10:1 nutritional requirement, whereas carbon to phosphorous is a 30:1 nutritional requirement (Vidali 2001).

126

5.3.3.2

A. Mallick et al.

Environmental Requirements for Bioremediation

Temperature, pH and moisture all have an impact on microbial growth and activity. Despite the fact that microorganisms have been isolated in severe environments, the majority of them thrive in a narrow temperature range, making it critical to obtain optimal conditions. If the pH of the soil is highly acidic, lime can be used to neutralise it. The rate of many biological reactions is affected by temperature, and for every 10 °C increase in temperature, the rate of many of them doubles. The cells, however, die at a particular temperature (Pritchard et al. 1992). During late spring, summer and autumn, a plastic covering can be utilised to increase solar heating. All living species require water to survive; therefore, irrigation is required to reach the ideal moisture amount. The level of oxygen accessible in the system determines whether it is aerobic or anaerobic. Under aerobic conditions, hydrocarbons are easily destroyed, but chlorinated compounds are only decomposed under anaerobic conditions. It is necessary to till the land in order to enhance the amount of oxygen in the soil. Magnesium peroxide or hydrogen peroxide can be released into the environment in rare instances. The proper supply of air, nutrients and water is controlled by the soil structure. To improve soil structure, materials like gypsum or organic matter can be employed. Low soil permeability can obstruct water, nutrient as well as oxygen transport. As a result, in situ clean-up may not be possible in soils with low permeability.

5.4 Climate Change and Bioremediation Factors such as increased CO2 levels and rising air temperatures characterise global climate change. Microbes have greater capability to break down soil organic matter at increasing CO2 (Nie et al. 2013) and nutrients in ecosystems that are predominantly affected by biotic as well as abiotic variables play a major role in carbon (C) cycling. However, research on soil bacteria and climate change (Castro et al. 2010; Nie et al. 2013) suggests alterations in the microbial niche’s physico-chemical properties that may modify microbial metabolic activities and hence the bioremediation process. Microbial extracellular enzyme synthesis is influenced by climatic circumstances, as well as microbial activity and soil physico-chemical parameters (Sowerby et al. 2005). Frey et al. (2013) observed enhanced utilisation efficacy of refractory substrate in soils by microorganisms at greater temperatures as an effective feedback to climate, despite the fact that the microbial populations are thought to be limiting climatic feedbacks from ecosystems (Bardgett et al. 2008). Increased ambient CO2 levels have been linked to increased bacterial abundance and decreased fungal abundance (Castro et al. 2010). The fungal/bacterial biomass ratio in soil decreases as fungal biomass decreases in warm and dry conditions (Sowerby et al. 2005), showing that the volume of carbon cycling in an ecosystem has been lowered, further disrupting the natural breakdown process by using naturally occurring microbes capable of degrading hazardous compounds through co-metabolism aided by naturally available

5 Bioremediation: An Effective, Significant and Eco-friendly …

127

carbon. Microbial enzymatic activity is expected to increase significantly if soil temperature rises as a result of global climate change (Baldrian et al. 2013).

5.5 Bioremediation Strategies Bioremediation is a novel and promising strategy to remove metals from contaminated water as well as soils and recovering those metals. Bioremediation, as defined by Adhikari et al. (2004), is the process of using microbes or plants to clean up hazardous waste, as well as it is the safest way to get rid of toxins from soil and water. To deteriorate and transform contaminants in the environment into safer or less dangerous forms, bioremediation relies mostly on microbes or microbial processes (Garbisu and Alkorta 2003). Because of the activities of human being, the amount of toxins which are discharged into the atmosphere has skyrocketed in recent decades. Microbes living in soil and water contaminated with metals have evolved complex metal oxidation mechanism based on cellular processes. Microorganisms’ ability to oxidise metals can be used as well to get rid of metal contamination (Wu et al. 2020). The ability of toxic metals together with metalloids to oxidise varies depending on whether the microbial population is found in an aquatic or terrestrial setting. The creation of various metal minerals by metal-oxidising microorganisms has the potential to reduce dangerous metals and metalloids to levels that are acceptable to regulatory bodies. Therefore, it is critical to utilise bioremediation techniques to lessen the harmful impacts of pollutants in the water as well as soil. Recently, the application of bioremediation has risen dramatically for several forms of contaminants, from radionuclides to rare metals. The Environmental Protection Agency (EPA) (2001, 2002) claims that there are primarily two techniques for the removal and transportation of trash such as ex situ and in situ type of bioremediation.

5.5.1 Ex Situ Bioremediation To encourage microbial decomposition, this method necessitates the excavation of polluted soil or groundwater pumping. Land farming is a basic practice whose purpose is to encourage the growth of native biodegradative microorganisms as well as make it easier for them to break down contaminants aerobically. In the case of composting, organic components encourage the growth of a diversified microbial community. Biopiles combine land farming with composting where native aerobic along with anaerobic microbes can thrive in an ideal environment. Slurry phase bioremediation is a faster procedure where water and other additives are added to polluted soil inside a huge tank known as bioreactor in order to maintain microbes already existing in the soil in touch with soil toxins. Nutrients as well as oxygen are introduced, along with the bioreactor’s parameters are carefully monitored to supply the microorganisms the best circumstances to break down the pollutants.

128

A. Mallick et al.

5.5.2 In Situ Bioremediation In situ bioremediation entails direct removal of toxins at their origin or contamination sites, resulting in less dust and allowing for the treatment of huge volume of soil with lower pollution release. This includes flowing aqueous solution through contaminated soil to supply oxygen as well as nutrients to naturally occurring microbes that degrade organic pollutants. In situ bioremediation is most commonly used to break down pollutants in saturated soils as well as groundwater and uses non-hazardous microbes to digest the pollutants in a less expensive way. There are two categories under in situ type of bioremediation, engineered in situ bioremediation entails introducing various microorganisms to the polluted site, whereas in situ bioremediation strategy entails giving nutrients and oxygen to indigenous or naturally occurring microbial communities to improve their metabolic activity. Engineered systems should be introduced to a specific site when the circumstances are not adequate. Engineered in situ bioremediation enhances the decomposition by making the physico-chemical circumstances better to promote microorganism development.

5.6 Significance of Bioremediation The public considers bioremediation as a suitable waste treatment option for polluted materials because it is a natural process. When the pollutant is present, the number of microorganisms capable of decomposing it increases; when the contaminant is destroyed, the population of biodegradable organisms’ declines. Carbon dioxide, water and cell biomass are examples of treatment leftovers that are usually innocuous. Bioremediation strategies rely on the correct bacteria in the right place at the right time, as well as the suitable environmental variables for degradation to happen for bioremediation to be successful. Bacteria and fungi, which have the physiological and metabolic ability to break down contaminants, are the right microorganisms. Bioremediation is frequently less expensive and causes minimum site interruption; it permanently eliminates waste, reduces long-term liability and can be combined with other physical or chemical treatment methods. This is a critical procedure because it allows target pollutants to be completely destroyed rather than being transferred from one medium to another in the environment, such as from land to water or air. Bioremediation is typically carried out on-site, causing little or no disruption to normal activities. This also eliminates the need to transport huge amounts of waste off-site, as well as the health and environmental problems that may arise during transportation.

5 Bioremediation: An Effective, Significant and Eco-friendly …

129

5.7 Application of Bioremediation for Sustainable Management 5.7.1 Bioremediation of Polluted Soil Fossil fuels are the principal energy source for global industry. There is a substantial risk of environmental pollution as a result of fossil fuel imports/exports and industry. It is now known, however, that hydrocarbons are the greatest source of carbon in the planetary system. Petroleum and coal both contain a class of chemicals known as hopanoids, which are widely found in bacterial cell walls (Gold 1985), implying that all of these fuels came from microorganisms at some point. On this basis, it is reasonable to assume that biodegradation of these fuels has always occurred to some level. Members of the genera Corynebacterium, Micrococcus, Bacillus, Flavobacterium and Pseudomonas have been discovered to bioenhance petrol and diesel, as well as crude oil spills in soils around gas stations (Rahman et al. 2002). Pentachlorophenol was remediated using Flavobacterium and Arthrobacter, but 2,4,5-trichlorophenooxyacetic acid elimination was expedited with Pseudomonas cepacia and Rhodococcus chlorophenolicus (Halden et al. 1999). Petroleum PAHs are reported to be biodegraded by bacteria of the species Cycloclasticus in a marine environment (Kasai et al. 2002). Due to their ability to degrade numerous PAHs, Da Silva et al. (2003) determined a number of Paenibacillus species to be agriculturally important. In recent study, the use of microorganisms for bioremediation has received a lot of attention. Fungi, on the other hand, may play a significant part in the rehabilitation process. Fungi, in general, can withstand more environmental stress than bacteria, and they may play a role in the breakdown of petroleum hydrocarbons in soil (Prenafeta-Boldú et al. 2002). Da Silva et al. (2003) separated filamentous fungus from estuary sediments in Brazil and tested their capability to break down PAHs in culture, specifically pyrene. The most efficient was a Cyclothyrium sp., which degraded 70, 74, 38 and 59% of phenanthrene, pyrene, benzo[a]pyrene and anthracene, respectively. A Cladophialophora sp. has also been found to digest toluene, ethylbenzene and xylene (Prenafeta-Boldú et al. 2002).

5.7.2 Microbial Remediation of Metals in Soils Because of the physical, structural, chemical and biological heterogeneities found in soils, metal-polluted soils pose the highest barrier to remediation efforts of all metalcontaminated systems. Because metal contamination is so common in both developing and developed areas of the world, soil remediation through metal removal, containment and/or detoxification is a top priority. Mercury levels in fish (Jewett and Duffy 2007), arsenic in drinking water (Wang and Wai 2004) and metal uptake by agricultural crops are also recent examples of metal contamination’s health and environmental implications (Howe et al. 2005). The activities of indigenous microbial

130

A. Mallick et al.

communities will be directly influenced by changes in soil chemical and physical factors. The proliferation of sulphate-reducing bacteria and the generation of metal sulphides will be aided by saturating a soil with reducing conditions. Such accelerated intrinsic metal bioremediation in soils by soil condition adjustment is possible, but given the transient nature of the environmental change, it may be short lived. Several microbes can make inorganic nanoparticles from soluble metals in the environment (Rajendran and Gunasekaran 2007). Bacteria and fungi have been reported to create silver nanoparticles (Nair and Pradeep 2002), gold nanoparticles (Ahmad et al. 2003a, b) and cadmium nanoparticles (Ahmad et al. 2003a, b). Rhodococcus sp., an actinomycete, accumulated gold particles along the cytoplasmic membrane and cell wall, but no harmful consequences were identified (Ahmad et al. 2003a). Lactobacillus strains developed intracellular gold and silver granules without causing any harm to the cells (Nair and Pradeep 2002). Fungi and actinomycetes have been found to synthesise nanoparticles outside of their cells (Ahmad et al. 2002, 2003a, b). The recovery of these nanoparticles is of interest, because metals can be stabilised in situ for use in bioremediation. Washing soils with microbial products is an ex situ procedure that depends on an increase in metal solubility to improve removal of metals. After five washings, Pseudomonas azotoformans separated from oil sludge produced a siderophore that was capable of removing 92.8% of the arsenic from soil contaminated with arsenic (Nair et al. 2007). According to Nair et al. (2007), siderophores can desorb metals from soil surfaces, assisting in their removal. Juwarkar et al. (2007) found that using a microbially generated di-rhamnolipid surfactant to remove 92% Cd and 88% Pb from cadmium- and lead-contaminated soils alleviated metal stress and increased soil microbiological diversity. The technique of obtaining improved biological activity after gene transfer from an introduced donor organism into a member of the native soil population is known as gene bio-augmentation (Maier and Gentry 2015). If metal-resistant/detoxifying genes were transmitted to trans-conjugant bacterial communities inside a metalpolluted soil, greater metal detoxification activity may be attained (Pepper et al. 2002). While gene bio-augmentation has mostly been investigated for the reduction of organic pollutants (Jussila et al. 2007), it has the potential to develop huge, diversified metal-resistant populations within a soil. In a lead-polluted soil, Vivas et al. (2003) demonstrated that the bacteria Brevibacillus sp. increased nitrogen and phosphorus intake, nodule formation, plant development and mycorrhizal infection of Trifolium pratense L. (red clover). Plant uptake of heavy metals is also aided by microbially generated siderophores, which make the metal more accessible to the plant and improve phyto-extraction of the metal from the surrounding soil (Neubauer et al. 2000).

5 Bioremediation: An Effective, Significant and Eco-friendly …

131

5.7.3 Bioremediation of Contaminated Underground Aquifers Groundwater contamination with gasoline is a severe environmental issue since it can contaminate drinking water supplies. When subterranean aquifers are contaminated with gasoline, anaerobic zones form, when compared to toluene and xylenes, benzene is significantly more persistent (Lovely 1997). Although studies have shown that benzene biodegradation happens under perchlorate-reducing (Chakraborty et al. 2005), nitrate-reducing (Ulrich and Edwards 2003), iron-reducing (Lovely et al. 1994), sulphate-reducing (Lovely et al. 1995) and methanogenic conditions (Kasai et al. 2005), in situ activities of anaerobic benzene degradation are typically very low, showing that bio-augmentation, rather than biostimulation, may be more effective to accelerate it. The isolated strain of an anaerobic benzene-degrading bacteria (Azoarcus sp. strain DN11) was tested in a laboratory bio-augmentation experiment utilising benzene-polluted groundwater from the former coal distillation plant site, indicating that DN11 could be useful to degrade benzene in underground aquifers at low concentrations and subsequent pathogenicity of strain DN11 utilising model organisms such as mice (Singh et al. 2009).

5.7.4 Anaerobic Metabolism and Bioremediation of Explosives-Contaminated Soil Nitro-substituted aromatics make up a large percentage of xenobiotic compounds released into the environment for agricultural as well as industrial purposes. Plastics, pesticides, pharmaceuticals, landfill dumping of industrial wastes and military usage of explosives are all ways for nitroaromatic chemicals to enter soil, water and food. Military operations such as the fabrication, loading and disposal of explosives and propellants primarily inject the nitroaromatic chemical trinitrotoluene (TNT) into soil and water habitats. TNT and other nitroaromatics have been biotransformed by aerobic bacteria in the laboratory on numerous occasions (Boopathy et al. 1994a, b). The biodegradation of 2,4-dinitrotoluene by Pseudomonas sp. has been found to take place via 4-methyl-5-nitrocatechol in a dioxygenase-mediated process (Spanggord et al. 1991). Desulfovibrio sp. (B strain), a sulphate-reducing bacterium, reduced TNT to toluene under anaerobic circumstances (Boopathy et al. 1993). Methanogenic bacteria decreased nitrophenols and nitrobenzoic acids under anaerobic circumstances, according to Gorontzy et al. (1993). Preuss et al. (1993) used Desulfovibrio sp. to convert TNT to triaminotoluene.

132

A. Mallick et al.

5.8 Future Scope Bioremediation is the use of biological treatment processes to remove or reduce the amounts of harmful wastes at a contaminated site. Microorganisms play a crucial role in the bioremediation of heavy metal-contaminated soil and wastewater (Caplan 1993). Intense legislative and public engagement may obstruct the development of regulations that reflect real-world experience. Government regulations that favour proven technologies have slowed the development of rapidly growing technologies notably bioremediation (Day 1993). Despite the obstacles, bioremediation has great market potential. Soil remediation alone is expected to cost more than $30 billion in Europe over the next ten years. This is in comparison with the $1 billion spent thus far. Bioremediation technologies might earn US$1.5 billion if only 5% of this soil was cleaned with bio-treatment. Potential future markets for biological treatment include process waste pre-treatment, industrial dumps, municipal landfill leachates and common chemical spills. These applications are expected to bring in an additional US$2–4 billion in revenue to the global bioremediation industry (Caplan 1993). Table 5.2 summarises the expected global income potential for bioremediation services over the next decade. Plasmids carry chromate resistance determinants in bacteria, which have the ability to detoxify chromate-polluted water (Cervantes 1991); such plasmid can be used to create biomasses that can reduce metal toxicity. Kao et al. (2008) used a MerP-expressing recombinant Escherichia coli to adsorb Ni, Zn and Cr in aqueous solution. The MerP was derived from Gram-positive (Bacillus cereus) and Gramnegative (Pseudomonas sp.) bacteria (Kao et al. 2008). Eichhornia crassipes (water hyacinth) was employed by some Varanasi scientists to extract heavy meals from filthy water (Mishra and Tripathi 2009). Spirulina fusiform has been shown to remove 93–99% of chromium from tannery effluents by others in Chennai. Chlamydomonas reinhardtii, a kind of algae, may detect chromium pollution in effluent (Rodríguez et al. 2007) and water lilies (Nymphaea spontanea) (Choo et al. 2006). Heavy metal toxicity’s environmental impact should be quickly addressed by adopting bioremediation procedures to minimise harmful levels of heavy metals (Pandi et al. 2009). To drain out the toxic metals, we can take good metals like selenium (200 µg per Table 5.2 Approximated worldwide bioremediation market for the next decade

Bioremediation appliance

Revenue potential (US$ billion)

Surface water treatment

2.0

Land farm treatment

2.0

Industrial chemical spills

1.0

Microbial inoculants

0.5

Leaking USTs

5.0

Process waste pre-treatment

1.0

Total

11.5

Adapted and modified from Caplan (1993)

5 Bioremediation: An Effective, Significant and Eco-friendly …

133

day), zinc (20–50 mg per day) and magnesium (350 mg per day) (Florea and Busselberg 2006). As a result, the biogeochemistry of water bodies or soils impacted by companies releasing effluents into them will define the importance of heavy metal bioremediation. Despite the fact that many businesses will fail due to the challenges of a new market, some of today’s modest bioremediation businesses will grow into big players in future. As the industry grows more competitive, others will merge or develop partnerships with both small and large businesses.

5.9 Conclusion Declining water quality has become a global concern as human populations, industrial and agricultural activities expand and climate change threatens to disrupt the hydrological cycle. Surface run-off and sewage and industrial effluents gather contaminants in streams and rivers, which are conveyed to the rivers, lakes and reservoirs that supply our drinking water (Skeat 1969). All of man’s chemicals will eventually find their way into our drinking water. Industry, agriculture and other anthropogenic influences pollute rivers, lakes and underground water, putting our drinking water at risk. Similarly, soil contamination also takes place, affecting the ability of soil to perform some of its critical roles in the ecosystem. Local soil contamination occurs when large levels of contaminants are introduced due to extensive industrial activity, insufficient waste disposal, mining, military activities or accidents. It is clear that present effluent treatment plant procedures are unable to process the wastes they receive, resulting in harmful and persistent contaminants being discharged into rivers and estuaries. They produce poisonous sludge, which must be disposed of. To stop pollution and prevent metal poisoning, a holistic waste treatment approach with the goal of eliminating priority pollutants at the source is clearly needed. Indigenous microorganisms found in a variety of industrial effluents can be employed to resist, process, metabolise and detoxify contaminated soil and water, as well as serve as pollution indicators (Ray and Ray 2009). Bioremediation is a technique for eliminating contaminants by hastening natural biodegradation. We can increase our ability to biodegrade pollutants by better understanding microbial populations and their responses to the natural environment and contaminants, as well as expanding our knowledge of microbe genetics. Identifying the right microbe from the waste to be biodegraded and conducting field trials for bioremediation procedures with these microbes will surely result in cost-effective solutions and significant developments in the area (Divya et al. 2015). There are a variety of conditions that limit bioavailability and impede the movement of certain chemicals into the aqueous phase, where biological uptake is most common. The significance of bioavailability is heavily influenced by the contaminant’s composition, soil chemistry and matrix. Bio-availability may be negligible in some circumstances, but it may be vital in others. Bioremediation must take into account the impact of site-specific bioavailability. Bioactivity takes into account the variables that have long been known to influence the rate of bioremediation. Only a few parameters

134

A. Mallick et al.

can be changed in current bioremediation configurations. This suggests that specific places may be particularly suited to in situ techniques due to the ease with which bioactivity can be maintained (Boopathy 2000). Bioremediation is still regarded as a developing technology. One challenge is that bioremediation takes place in the natural environment, which is full of unknown organisms. The majority of pollutant-degrading bacteria isolated and characterised in the laboratory are currently regarded to contribute only a modest amount to bioremediation. Another issue is that no two environmental problems occur under exactly the same circumstances; for example, differences in pollutant types and levels, climatic factors and hydro-geodynamics all occur. Due to these challenges, the field of bioremediation has fallen behind knowledge-based solutions that are guided by conventional reasoning. Despite the fact that our research is really not sufficient, it is time to move forward with more extensive strategies for determining broad bioremediation rationales. In some cases, such as marine petroleum bioremediation, we have previously observed that similar bacterial populations persist even in geographically distant areas. Taking into account the physiology and genetics of such populations could be immensely useful in the development and evaluation of bioremediation (Watanabe 2001).

References Adhikari T, Manna MC, Singh MV, Wanjari RH (2004) Bioremediation measure to minimize heavy metals accumulation in soils and crops irrigated with city effluent. Food Agric Environ 2:266–270 Ahmad A, Mukherjee P, Mandal D, Senapati S, Khan MI, Kumar R, Sastry M (2002) Enzyme mediated extracellular synthesis of CdS nanoparticles by the fungus, Fusarium oxysporum. J Am Chem Soc 124(41):12108–12109 Ahmad A, Senapati S, Khan MI, Kumar R, Sastry M (2003a) Extracellular biosynthesis of monodisperse gold nanoparticles by a novel extremophilic actinomycete, Thermomonospora sp. Langmuir 19(8):3550–3553 Ahmad A, Senapati S, Khan MI, Kumar R, Ramani R, Srinivas V, Sastry M (2003b) Intracellular synthesis of gold nanoparticles by a novel alkalotolerant actinomycete, Rhodococcus species. Nanotechnology 14(7):824 Ayangbenro AS, Babalola OO (2017) A new strategy for heavy metal polluted environments: a review of microbial biosorbents. Int J Environ Res Public Health 14(1):94 Aziz HA, Tajarudin HA, Wei THL, Alazaiza MYD (2020) Iron and manganese removal from groundwater using limestone filter with iron-oxidized bacteria. Int J Environ Sci Technol (IJEST) 17(5) Azubuike CC, Chikere CB, Okpokwasili GC (2016) Bioremediation techniques–classification based on site of application: principles, advantages, limitations and prospects. World J Microbiol Biotechnol 32(11):1–18 Baker KH, Herson DS (1994) Bioremediation. McGraw-Hili. Inc., New York Baldrian P, Šnajdr J, Merhautová V, Dobiášová P, Cajthaml T, Valášková V (2013) Responses of the extracellular enzyme activities in hardwood forest to soil temperature and seasonality and the potential effects of climate change. Soil Biol Biochem 56:60–68 Bardgett RD, Freeman C, Ostle NJ (2008) Microbial contributions to climate change through carbon cycle feedbacks. ISME J 2(8):805–814

5 Bioremediation: An Effective, Significant and Eco-friendly …

135

Blázquez G, Hernáinz F, Calero M, Martín-Lara MA, Tenorio G (2009) The effect of pH on the biosorption of Cr (III) and Cr (VI) with olive stone. Chem Eng J 148(2–3):473–479 Boopathy R (2000) Factors limiting bioremediation technologies. Bioresour Technol 74(1):63–67 Boopathy R, Kulpa CF, Wilson M (1993) Metabolism of 2, 4, 6-trinitrotoluene (TNT) by Desulfovibrio sp. (B strain). Appl Microbiol Biotechnol 39(2):270–275 Boopathy R, Manning J, Montemagno C, Kulpa C (1994a) Metabolism of 2, 4, 6-trinitrotoluene by a Pseudomonas consortium under aerobic conditions. Curr Microbiol 28(3):131–137 Boopathy R, Wilson M, Montemagno CD, Jnr JM, Kulpa CF (1994b) Biological transformation of 2, 4, 6-trinitrotoluene (TNT) by soil bacteria isolated from TNT-contaminated soil. Bioresour Technol 47(1):19–24 Caplan JA (1993) The worldwide bioremediation industry: prospects for profit. Trends Biotechnol 11(8):320–323 Castro HF, Classen AT, Austin EE, Norby RJ, Schadt CW (2010) Soil microbial community responses to multiple experimental climate change drivers. Appl Environ Microbiol 76(4):999–1007 Cervantes C (1991) Bacterial interactions with chromate. Antonie Van Leeuwenhoek 59(4):229–233 Chakraborty R, O’Connor SM, Chan E, Coates JD (2005) Anaerobic degradation of benzene, toluene, ethylbenzene, and xylene compounds by Dechloromonas strain RCB. Appl Environ Microbiol 71(12):8649–8655 Chakraborty S, Pangga IB, Roper MM (2012) Climate change and multitrophic interactions in soil: the primacy of plants and functional domains. Glob Change Biol 18(7):2111–2125 Chen H, Wang L (2017) Chapter 5-microbial cell refining for biomass conversion. In: Technologies for biochemical conversion of biomass, pp 101–135 Choo TP, Lee CK, Low KS, Hishamuddin O (2006) Accumulation of chromium (VI) from aqueous solutions using water lilies (Nymphaea spontanea). Chemosphere 62(6):961–967 Colberg PJS, Young LY (1995) Anaerobic degradation of nonhalogenated homocyclic aromatic compounds coupled with nitrate, iron, or sulfate reduction. In: Microbial transformation and degradation of toxic organic chemicals, pp 307–330 Da Silva M, Cerniglia CE, Pothuluri JV, Canhos VP, Esposito E (2003) Screening filamentous fungi isolated from estuarine sediments for the ability to oxidize polycyclic aromatic hydrocarbons. World J Microbiol Biotechnol 19(4):399–405 Das N, Vimala R, Karthika P (2008) Biosorption of heavy metals-an overview. Indian J Biotechnol 7:159–169 Day SM (1993) US environmental regulations and policies-their impact on the commercial development of bioremediation. Trends Biotechnol 11(8):324–328 Divya M, Aanand S, Srinivasan A, Ahilan B (2015) Bioremediation—an eco-friendly tool for effluent treatment: a review. Int J Appl Res 1(12):530–537 Earth P (2015) The new top six toxic threats: a priority list for remediation. World’s worst pollution problems report. https://www.worstpolluted.org/docs/WWP15.pdf EPA (2001) Remediation case studies. Federal Remediation Technology Roundtable. Report No. 542-F-01-032 EPA (2002) Handbook on in situ treatment of hazardous waste contaminated soils. https://cfpub. epa.gov/si/si_public_record_Report.cfm?Lab=NRMRL&dirEntryId=124687 Ezzouhri L, Castro E, Moya M, Espinola F, Lairini K (2009) Heavy metal tolerance of filamentous fungi isolated from polluted sites in Tangier, Morocco. Afr J Microbiol Res 3(2):35–48 Florea AM, Büsselberg D (2006) Occurrence, use and potential toxic effects of metals and metal compounds. Biometals 19(4):419–427 Frey SD, Lee J, Melillo JM, Six J (2013) The temperature response of soil microbial efficiency and its feedback to climate. Nat Clim Chang 3(4):395–398 Garbisu C, Alkorta I (2003) Basic concepts on heavy metal soil bioremediation. Eur J Miner Process Environ Prot 3(1):58–66 Gareth ME, Furlong JC (2003) Environmental biotechnology; theory and application. Wiley, Chichester

136

A. Mallick et al.

Gold T (1985) The origin of natural gas and petroleum, and the prognosis for future supplies. Annu Rev Energy 10(1):53–77 Gorontzy T, Küver J, Blotevogel KH (1993) Microbial transformation of nitroaromatic compounds under anaerobic conditions. Microbiology 139(6):1331–1336 Gupta S, Singh D (2017) Role of genetically modified microorganisms in heavy metal bioremediation. In: Advances in environmental biotechnology, pp 197–214 Halden RU, Tepp SM, Halden BG, Dwyer DF (1999) Degradation of 3-phenoxybenzoic acid in soil by Pseudomonas pseudoalcaligenes POB310 (pPOB) and two modified Pseudomonas strains. Appl Environ Microbiol 65(8):3354–3359 Han X, Gu JD (2010) Sorption and transformation of toxic metals by microorganisms. In: Environmental microbiology, pp 153–176 Howe A, Fung LH, Lalor G, Rattray R, Vutchkov M (2005) Elemental composition of Jamaican foods 1: a survey of five food crop categories. Environ Geochem Health 27(1):19–30 Ingham CJ, Sprenkels A, Bomer J, Molenaar D, van den Berg A, van Hylckama Vlieg JE, de Vos WM (2007) The micro-Petri dish, a million-well growth chip for the culture and high-throughput screening of microorganisms. Proc Natl Acad Sci 104(46):18217–18222 Jewett SC, Duffy LK (2007) Mercury in fishes of Alaska, with emphasis on subsistence species. Sci Total Environ 387(1–3):3–27 Jussila MM, Zhao J, Suominen L, Lindström K (2007) TOL plasmid transfer during bacterial conjugation in vitro and rhizoremediation of oil compounds in vivo. Environ Pollut 146(2):510– 524 Juwarkar AA, Nair A, Dubey KV, Singh SK, Devotta S (2007) Biosurfactant technology for remediation of cadmium and lead contaminated soils. Chemosphere 68(10):1996–2002 Kao WC, Huang CC, Chang JS (2008) Biosorption of nickel, chromium and zinc by MerPexpressing recombinant Escherichia coli. J Hazard Mater 158(1):100–106 Kasai Y, Kishira H, Harayama S (2002) Bacteria belonging to the genus Cycloclasticus play a primary role in the degradation of aromatic hydrocarbons released in a marine environment. Appl Environ Microbiol 68(11):5625–5633 Kasai Y, Takahata Y, Hoaki T, Watanabe K (2005) Physiological and molecular characterization of a microbial community established in unsaturated, petroleum-contaminated soil. Environ Microbiol 7(6):806–818 Leonard SS, Harris GK, Shi X (2004) Metal-induced oxidative stress and signal transduction. Free Radical Biol Med 37(12):1921–1942 Lovley DR (1997) Potential for anaerobic bioremediation of BTEX in petroleum-contaminated aquifers. J Ind Microbiol Biotechnol 18(2–3):75–81 Lovley DR (2003) Cleaning up with genomics: applying molecular biology to bioremediation. Nat Rev Microbiol 1(1):35–44 Lovley DR, Woodward JC, Chapelle FH (1994) Stimulated anoxic biodegradation of aromatic hydrocarbons using Fe (III) ligands. Nature 370(6485):128–131 Lovley DR, Coates JD, Woodward JC, Phillips E (1995) Benzene oxidation coupled to sulfate reduction. Appl Environ Microbiol 61(3):953–958 Maier RM, Gentry TJ (2015) Microorganisms and organic pollutants. In: Environmental microbiology. Academic Press, pp 377–413 Maphosa F, Smidt H, De Vos WM, Röling WF (2010) Microbial community-and metabolite dynamics of an anoxic dechlorinating bioreactor. Environ Sci Technol 44(13):4884–4890 Mars AE, Kasberg T, Kaschabek SR, van Agteren MH, Janssen DB, Reineke W (1997) Microbial degradation of chloroaromatics: use of the meta-cleavage pathway for mineralization of chlorobenzene. J Bacteriol 179(14):4530–4537 Mishra VK, Tripathi BD (2009) Accumulation of chromium and zinc from aqueous solutions using water hyacinth (Eichhornia crassipes). J Hazard Mater 164(2–3):1059–1063 Mueller JG, Cerniglia CE, Pritchard PH (1996) Bioremediation of environments contaminated by polycyclic aromatic hydrocarbons. Biotechnol Res Ser 6:125–194

5 Bioremediation: An Effective, Significant and Eco-friendly …

137

Nair B, Pradeep T (2002) Coalescence of nanoclusters and formation of submicron crystallites assisted by Lactobacillus strains. Cryst Growth Des 2(4):293–298 Nair A, Juwarkar AA, Singh SK (2007) Production and characterization of siderophores and its application in arsenic removal from contaminated soil. Water Air Soil Pollut 180(1):199–212 Neubauer U, Furrer G, Kayser A, Schulin R (2000) Siderophores, NTA, and citrate: potential soil amendments to enhance heavy metal mobility in phytoremediation. Int J Phytorem 2(4):353–368 Nie M, Pendall E, Bell C, Gasch CK, Raut S, Tamang S, Wallenstein MD (2013) Positive climate feedbacks of soil microbial communities in a semi-arid grassland. Ecol Lett 16(2):234–241 Nweke CO, Alisi CS, Okolo JC, Nwanyanwu CE (2007) Toxicity of zinc to heterotrophic bacteria from a tropical river sediment. Appl Ecol Environ Res 5(1):123–132 Pandey G, Jain RK (2002) Bacterial chemotaxis toward environmental pollutants: role in bioremediation. Appl Environ Microbiol 68(12):5789–5795 Pandi M, Shashirekha V, Swamy M (2009) Bioabsorption of chromium from retan chrome liquor by cyanobacteria. Microbiol Res 164(4):420–428 Pepper IL, Gentry TJ, Newby DT, Roane TM, Josephson KL (2002) The role of cell bioaugmentation and gene bioaugmentation in the remediation of co-contaminated soils. Environ Health Perspect 110(suppl 6):943–946 Pillay TVR (1992) Nature of environmental impacts. In: Aquaculture and the environment. WileyBlackwell, USA Prenafeta-Boldú FX, Vervoort J, Grotenhuis JTC, Van Groenestijn JW (2002) Substrate interactions during the biodegradation of benzene, toluene, ethylbenzene, and xylene (BTEX) hydrocarbons by the fungus Cladophialophora sp. strain T1. Appl Environ Microbiol 68(6):2660–2665 Preuss A, Fimpel J, Diekert G (1993) Anaerobic transformation of 2, 4, 6-trinitrotoluene (TNT). Arch Microbiol 159(4):345–353 Pritchard PH, Mueller JG, Rogers JC, Kremer FV, Glaser JA (1992) Oil spill bioremediation: experiences, lessons and results from the Exxon Valdez oil spill in Alaska. Biodegradation 3(2):315–335 Puzon GJ, Roberts AG, Kramer DM, Xun L (2005) Formation of soluble organo-chromium (III) complexes after chromate reduction in the presence of cellular organics. Environ Sci Technol 39(8):2811–2817 Rahman KSM, Rahman T, Lakshmanaperumalsamy P, Banat IM (2002) Occurrence of crude oil degrading bacteria in gasoline and diesel station soils. J Basic Microbiol Int J Biochem Physiol Genet Morphol Ecol Microorg 42(4):284–291 Rajendran P, Gunasekaran P (2007) Nanotechnology for bioremediation of heavy metals. In: Environmental bioremediation technologies. Springer, Berlin, pp 211–221 Rajendran P, Muthukrishnan J, Gunasekaran P (2002) Current perspectives in nickel bioremediation strategies. Indian J Microbiol 42(1):1–10 Ravenscroft P, Brammer H, Richards K (2011) Arsenic pollution: a global synthesis, vol 94. Wiley Ray S, Ray MK (2009) Bioremediation of heavy metal toxicity-with special reference to chromium. Al Ameen J Med Sci 2(2):57–63 Robles-González IV, Fava F, Poggi-Varaldo HM (2008) A review on slurry bioreactors for bioremediation of soils and sediments. Microb Cell Fact 7(1):1–16 Rodríguez MC, Barsanti L, Passarelli V, Evangelista V, Conforti V, Gualtieri P (2007) Effects of chromium on photosynthetic and photoreceptive apparatus of the alga Chlamydomonas reinhardtii. Environ Res 105(2):234–239 Saˇg Y, Özer D, Kutsal T (1995) A comparative study of the biosorption of lead (II) ions to Z. ramigera and R. arrhizus. Process Biochem 30(2):169–174 Salem HM, Eweida EA, Farag A (2000) Heavy metals in drinking water and their environmental impact on human health. In: International conference on the environmental hazards mitigation, Cairo University, Egypt, pp 542–556 Sharma S (2012) Bioremediation: features, strategies and applications. Asian J Pharm Life Sci ISSN 2231:4423

138

A. Mallick et al.

Singh A, Kuhad RC, Ward OP (eds) (2009) Advances in applied bioremediation. Springer, Berlin, pp 1–19 Skeat WO (1969) Manual of British water engineering practice. Vol. b: Water quality and treatment. The Institution of Water Engineers, London, England Sowerby A, Emmett B, Beier C, Tietema A, Penuelas J, Estiarte M et al (2005) Microbial community changes in heathland soil communities along a geographical gradient: interaction with climate change manipulations. Soil Biol Biochem 37(10):1805–1813 Spanggord RJ, Spain JC, Nishino SF, Mortelmans KE (1991) Biodegradation of 2, 4-dinitrotoluene by a Pseudomonas sp. Appl Environ Microbiol 57(11):3200–3205 Srivastava J, Naraian R, Kalra SJS, Chandra H (2014) Advances in microbial bioremediation and the factors influencing the process. Int J Environ Sci Technol 11(6):1787–1800 Toyama T, Furukawa T, Maeda N, Inoue D, Sei K, Mori K et al (2011) Accelerated biodegradation of pyrene and benzo[a]pyrene in the Phragmites australis rhizosphere by bacteria–root exudate interactions. Water Res 45(4):1629–1638 Ulrich AC, Edwards EA (2003) Physiological and molecular characterization of anaerobic benzenedegrading mixed cultures. Environ Microbiol 5(2):92–102 Vidali M (2001) Bioremediation. An overview. Pure Appl Chem 73(7):1163–1172 Vivas A, Azcón R, Biró B, Barea JM, Ruiz-Lozano JM (2003) Influence of bacterial strains isolated from lead-polluted soil and their interactions with arbuscular mycorrhizae on the growth of Trifolium pratense L. under lead toxicity. Can J Microbiol 49(10):577–588 Wang JS, Wai CM (2004) Arsenic in drinking water—a global environmental problem. J Chem Educ 81(2):207 Watanabe K (2001) Microorganisms relevant to bioremediation. Curr Opin Biotechnol 12(3):237– 241 Wu P, Zhang LJ, Lin CB, Xie XX, Yong XY, Wu XY (2020) Extracting heavy metals from electroplating sludge by acid and bio-electrical leaching using Acidithiobacillus ferrooxidans. Hydrometallurgy 191:105225

Chapter 6

Exploitation of Arbuscular Mycorrhizal (AM) Fungi as a Sustainable Management Strategy for Remediation of Cadmium-Contaminated Soils Harmanjit Kaur, Tashima, and Bhawna Sunkaria Abstract Cadmium (Cd) is naturally found in soils in divalent state (Cd2+ ). It is one of the most noxious environmental contaminants, being effortlessly absorbed by plants owing to its great water solubility. It is generally discharged into farming soils from manufacturing and mining industries along with agricultural practices like sewage sludge and phosphate fertilizers. One promising strategy for reducing Cd accretion and translocation in plants is the exploitation of microbes, for example, arbuscular mycorrhizal (AM) fungi. AM fungi develop mutualistic association with higher plants and exhibit widespread existence in terrestrial ecosystems, comprising Cd-contaminated regions, thereby recognizing these microbes as a promising technique for enhancing plant tolerance in metal-contaminated soils. Root colonization by AM fungi initiates a cascade of cellular and molecular events resulting in morpho-functional union between the symbiont cells. Cd triggers serious quantitative and qualitative alterations in AM populations by affecting germination of spores, expansion of germ tube and mycelium, colonization degree, and species diversity, though they do not get entirely exterminated from Cd-polluted sites. The probable AM-induced protective mechanisms in plants and/or remediation strategies in Cdcontaminated soils include sequestration by chelating agents like phytochelatins (PCs), metallothioneins (MTs), glutathione (GSH), organic acids, and compartmentalization in vacuoles; adsorption onto fungal cell wall; polyphosphate granules; accrual in spores and extraradical mycelium; and glomalin production. The present chapter briefly summarizes the establishment of mycorrhizal symbiosis, influence of Cd on AM development, AM diversity in contaminated sites contaminated sites and also highlights its role in increasing plant tolerance and restoring Cd-polluted soils. Keywords Cadmium · Arbuscular mycorrhiza · Diversity · Phytochelatins · Glomalin H. Kaur (B) Post Graduate, Department of Botany, Government College for Girls, Ludhiana, Punjab 141001, India e-mail: [email protected]; [email protected] Tashima · B. Sunkaria Department of Botany, Akal University, Talwandi Sabo, Bathinda, Punjab, India © The Author(s), under exclusive license to Springer Nature Switzerland AG 2022 T. Aftab (ed.), Sustainable Management of Environmental Contaminants, Environmental Contamination Remediation and Management, https://doi.org/10.1007/978-3-031-08446-1_6

139

140

H. Kaur et al.

6.1 Introduction Heavy metal pollution is a growing menace which has been recognized as one of the most severe risks for sustainability of agro-ecosystems and ultimately human health (Alekseenko et al. 2018; Kamran et al. 2019). The foremost reasons for this burgeoning problem are the fast rate of urbanization, alterations in land use, and expansion of industrialization, particularly in developing nations with enormously high population density, such as India. Among heavy metals, Cd is acknowledged as an extremely noxious, non-essential, and fairly more soluble compared to other metals, resulting in its great mobility in water–soil–plant system (Kaur and Garg 2017; Chellaiah 2018). It is the fourth most lethal metal for higher plants (ÁlvarezAyuso et al. 2013). The half-life of Cd in soil varies between 15 to 1100 years, whereas in biological systems, it is more than 25 years (Saifullah et al. 2016). Generally, Cd levels in soils vary from 0.1 to 1.0 mg Cd kg−1 soil, based on the source, process of soil formation, geo-morphological, and weather conditions; nevertheless, human actions (agriculture, industries, etc.) have led to major addition of Cd in agricultural soils (Zhang et al. 2010; Abbas et al. 2014; Bojorquez et al. 2016). Morphologically, chlorosis, necrosis, and retarded growth are the most visible symptoms in plants caused by Cd (Jali et al. 2016; Xu et al. 2017). Cd toxicity hinders the carbon-fixing process and reduces the pigment content, thereby affecting photosynthesis in plants (Gallego et al. 2012). Additionally, discharge of Cd into the soil stimulates osmotic stress in plants by lessening leaf water content, transpiration, and stomatal conductance, consequently causing physiological impairment in plants (Rizwan et al. 2016). Further, Cd triggers over-generation of reactive oxygen species (ROS) which results in oxidative injury to plant membranes and deterioration of cellular biomolecules as well as organelles (Abbas et al. 2017). Cd also hampers the uptake and translocation of essential elements such as, Ca, P, Mg, K, Mn, ultimately leading to mineral nutrition imbalance (Nazar et al. 2012). The re-establishment of degraded habitats (including metal contaminated) by means of sustainable, cost-effective techniques/strategies with an objective of raising the productivity of crop plants is receiving considerable attention of the scientific community worldwide. In this context, exploiting the natural potential of beneficial microbes in upholding the soil fertility and plant yield is gaining significance and might prove to be a vital sustainable method for remediating metal-contaminated soils. Arbuscular mycorrhizal (AM) fungi are among the most widespread microbes, forming symbioses with a great majority of higher plants growing in diverse environment conditions (Wang 2017; Shi et al. 2020). These fungi are fundamental endosymbionts performing an important function in several ecological processes, plant output, and ecosystem functioning (Gianinazzi et al. 2010; Garg and Chandel 2011). Many studies have reported considerable potential of AM fungi in increasing the endurance of plants to Cd, thereby improving their capability for remediation of Cd-polluted soils (Garg and Bhandari 2014). Moreover, plants have been found to form symbiosis with AM fungi in Cd-contaminated areas (Gao et al. 2010; Luo et al. 2011), indicating their prospective in alleviating Cd from the polluted soils. It has been documented

6 Exploitation of Arbuscular Mycorrhizal (AM) Fungi as a Sustainable …

141

that AM fungi possess enormous ability to take up metals from the soil and store them in their mycelium (a process called as mycorhizoremediation) which decreases their transportation to aerial parts and accordingly boosts the plant resistance in metalcontaminated environmental conditions (Moreira et al. 2015; Garg and Bhandari 2014). Most of AM species belong to the sub-phylum Glomeromycotina (Phylum Mucoromycota) (Spatafora et al. 2016). Four AM fungi orders, i.e., Archaeosporales, Diversisporales, Glomerales, and Paraglomerales have been recognized in sub-phylum Glomeromycotina which includes 25 diverse genera (Redecker et al. 2013). During initiation of symbiotic association, chemical signals are exchanged between host plant and AM fungi which leads to a phase-specific hormonal signaling and gene expression (Mohanta and Bae 2015; French 2017). Thereafter, germination of AM spore results in the establishment of mycelium which inhabits root system of the host plant (Mohanta and Bae 2015; French 2017). Subsequent to inter- and intracellular colonizations, formation of symbiosis is accomplished with the development of arbuscules and, in few species, vesicles. Vesicles are rounded or elongated structures developed outside and inside root cells and are storage sites of AM fungi, containing lipids and glycogen granules. In turn, the arbuscules formed as a result of extreme hyphal branching are involved in exchange of nutrients between host plant and AM fungus. Finally, mycorrhial symbiosis gets activated, and the fungus initiates growth of extraradical mycelium and a fresh sporulation cycle (Lambais 2006; Miransari 2012). Cd can reduce or even repress spore formation and germination, germ tube growth, mycelium expansion, hyphal branching, development of arbuscules, and root colonization (Shahabivand et al. 2016; Kaur and Garg 2017; Garg and Singh 2018). Though Cd does not eradicate the mycorrhizal symbiosis entirely, yet its toxicity results in remarkable alterations in the AM species diversity (Hu et al. 2013a, b; Moreira et al. 2015). Majority of the reports have documented prevalence of Glomus mosseae (renamed as Funneliformis mosseae) in Cd-polluted soils, indicating the tolerance of this particular AM species to metals (Yang et al. 2015; Colombo et al. 2019). Additionally, Yang et al. (2015) reported Acaulospora to be the second most leading genus following Glomus. The symbiotic association of AM fungi with host plant facilitates the retention of Cd in the hyphal cell walls and underground part of plants. The fungus produces ligands which bind to Cd and reduce its availability in the soil and, hence, decreases the Cd uptake by the plant. Frequently identified AM-mediated mechanisms include production of chelating agents like phytochelatins, metallothioneins, glomalin, malic acid, oxalic acid, and succinic acid; adsorption onto chitin of the cell wall; sequestration and compartmentalization in vacuoles to decrease cytoplasmic levels; build up in extraradical mycelium and spores; and glomalin retention (Abdel Latef et al. 2016; Bhandari and Garg 2017; Mishra et al. 2019). An additional process induced by AM fungi is the elimination or precipitation via polyphosphate granules which bind to the metal (including Cd), thereby reducing its availability to the plant (Garg and Bhandari 2014; Kaur and Garg 2017). The advantages of AM symbiosis to plants comprise of nutritional and non-nutritional effects, the latter occurring from profits of the former. The nutritional impact is the result of the biofertilizing behavior of AM fungi and comprises enhanced mineral nutrient uptake and improved utilization (particularly

142

H. Kaur et al.

P), implicit development of nitrogen fixation, and availability of nutrients in the rhizosphere due to enzymatic activity (Wang 2017; Stürmer et al. 2018). Additionally, AM fungi perform bio-promotory functions, such as increased water absorption and modifications in secondary metabolism of plants. Finally, these microsymbionts also function as bio-controllers supporting enhanced aggregation of soil particles and boosting plant defense strategies against different abiotic stressors (Siqueira et al. 2007). With this background, the present chapter is an attempt to briefly summarize the literature available regarding Cd pollution in soils and effects on plants, formation of mycorrhizal symbiosis with plants, and influence of Cd on AM diversity and development in contaminated sites. Along with this, the various mechanisms employed by AM fungi for increasing plant Cd tolerance with an aim to remediate Cd-contaminated soils are also highlighted.

6.2 An Overview of Cd Contamination in Soil and Impact on Plants Cadmium (Cd) is an extremely carcinogenic, silver-white colored metal, which causes toxicity in biological systems even at low concentrations (Benavides et al. 2005; Khan et al. 2015). Forest fires, volcanic explosions, windblown dust particles, and sea spurt are the common natural causes of Cd input in the atmosphere. Geological weathering of rocks is considered a chief natural origin of Cd in soils (Khan et al. 2010). Mafic along with ultramafic rocks are enriched with Cd, and therefore, during weathering, these rocks discharge considerable amounts of Cd into soils (Shah et al. 2010). Black shales have Cd approximately 100 mg kg−1 , and the soil developed from such rocks possesses large quantities of Cd. Cd levels are higher in sedimentary rocks (0.01–2.6 mg kg−1 ) compared to metamorphic (0.11– 1.0 mg kg−1 ) or igneous rocks (0.07–0.25 mg kg−1 ) (Smolders and Mertens 2013). Besides natural origin, Cd is liberated into the surroundings in erratic quantities by means of different human-based activities, for instance, smelting, mining, irrigation with wastewater, emissions from industries and vehicles, and agro-chemicals (Khan et al. 2016a). Unrestrained and irregular waste removal practices have also drastically enhanced Cd levels in soils (Khan et al. 2017). In several aspects, Cd has turned out to be an essential part of recent technological machinery, with numerous applications in communications, electronics, electricity production, and aerospace sector (Yates 1992, Cadmium Association 1992). Among various sources, application of phosphatic fertilizers is usually regarded as one of the main sources of Cd addition into farming soils (Smolders and Mertens 2013). Moreover, the use of polluted sewage sludge and manure also increases Cd input into arable soils (Khan et al. 2017). According to the British Geological Survey, the Cd production in 2015 was up to 24,900 metric tons worldwide (Brown et al. 2017). In 2016, the global generation of Cd (except US) was roughly 23,000 metric tons (U.S. Geological Survey 2017). Since Cd is quickly activated, soil should not be considered a lasting drain, rather a

6 Exploitation of Arbuscular Mycorrhizal (AM) Fungi as a Sustainable …

143

key temporary storage place for Cd which can easily impact the concentration of this metal in groundwater at diverse timescales, including decadal (dry vs. moist years) and annual (wet vs. dry season) (Sprynskyy et al. 2011). Cd hampers germination rate, hinders seedling physiological processes, growth, and negatively impacts agricultural yield (Guilherme et al. 2015; Raza et al. 2020). Generally, Cd concentrations ranging from 5 to 10 μg Cd g−1 dry matter are toxic to majority of the plants (White and Brown 2010). Cd is extremely cytotoxic and instigates bulging and disintegration of mitochondria, induces chlorosis, necrosis, reddening of leaf veins, inhibits root as well as shoot growth (Khan et al. 2016b). Cd is an oxidative stress inducer that causes increased ROS levels in cells (Jalmi et al. 2018). It also obstructs uptake and translocation of essential minerals in plants, thereby causing nutrient imbalance (Zhang et al. 2019a). Cd inhibits photosynthesis by decreasing total leaf area, chlorophyll content, concentration of ATP, stomatal conductance, affecting the chloroplast structure, and reducing the activity of iron reductase, thereby causing iron (Fe2+ ) deficiency (Abbas et al. 2017; Noor et al. 2018). Further, Cd ions diminish RuBPCase activity and damage its structure by substituting Mg ions, which are important co-factors in carbon dioxide reactions, and shift RuBPCase activity toward oxygenation reactions. Its smaller and larger subunits permanently detach from each other, resulting in absolute disruption of the enzyme activity (Tran and Popova 2013; Noor et al. 2018). The oxygen-evolving complex of PSII is influenced by Cd by interchanging the Ca2+ ions in Ca/Mn clusters (Dinakar et al. 2009) or by certain alterations in the Qb -binding region (Hayat et al. 2011). Cd toxicity reduces meristematic cell division, leading to reduction in root length and biomass, while increased root diameter (Gratao et al. 2009). The enhancement in the volume of cortical tissues and parenchyma cells in turn increases the resistance of cells to flow of solutes and water, ultimately amplifying the root diameter in response to Cd stress (Ismael et al. 2019). It has been reported that different plant organs, viz., roots, stems, and leaves encounter water deficiency under Cd stress (RucinskaSobkowiak 2016). Further aberrations in roots of Cd-stressed plants include reduced root hair surface area, primary root elongation (Gallego et al. 2012), increased root dieback, and hampered secondary development (Lux et al. 2011), which affect plant water relationships in the soil. In roots, Cd causes diminution in water absorption and hinderance in small-distance water transport via apoplast and symplast pathways (Kudoyarova et al. 2015). Cd-induced cell wall thickening with the assistance of incrusting compounds increases the resistance of apoplastic water flow (Hashem 2014). Obstruction in water diffusion via membranes is probably because of the inhibition of aquaporins and deviation in protein expression (Le et al. 2015). These variations change the water passage across the vascular cyclinder and also lessen root sap exudation (Kaznina et al. 2014). It is worth mentioning that Cd toxicity depends on the concentration of Cd in soil and successful activation of different defense strategies by diverse plant species (Vilela and Barbosa 2019).

144

H. Kaur et al.

6.3 Exploiting the Potential of Arbuscular Mycorrhizal (AM) Fungi for Restoring Cd-Polluted Soils The restitution of degraded soils by natural and novel sustainable strategies which can improve yields of crop plants is the need of the hour. Numerous micro-organisms dwell in the rhizosphere, such as nitrogen-fixing bacteria, mycorrhizal fungi, and other plant growth-promoting rhizobacteria (Van-der Putten et al. 2007). Integrating the inborn functions of these beneficial microbes in remediating metal-polluted soils coupled with enhanced plant productivity is receiving considerable importance nowadays. Among soil micro-organisms, association developed between root system of over 80% of higher plant species and arbuscular mycorrhizal (AM) fungi is the most ubiquitous endosymbiosis in the plant kingdom (Helgason and Fitter 2009). The word ‘mycorrhiza’ has its origin from two Greek words mycos, denoting ‘fungus’ and rhiza implying ‘root’, and was initially used in 1885 (Frank 1885) to express the close link between mycorrhizal fungi and roots of plants. Arbuscules are certain ‘tree-shaped’ fungal structures which act as major regions for exchange of nutrients between host plant and fungus (He and Nara 2007) and are formed inside the root cortical cells (Manchanda and Garg 2007). It is believed that mycorrhiza originated around 460 million years ago (Bonfante and Genre 2008).

6.3.1 Establishment of AM Symbiosis The establishment of symbiotic association generally comprises reciprocal recognition along with a high level of synchronization at both morphological and physiological levels, which further depends on constant cellular and molecular communication between the host plant and the fungus. In this section, the process of formation of AM symbiotic association with host plants is briefly summarized: Broadly, the obligatory life cycle of AM fungi can be divided into three phases: (i) the presymbiotic phase involving spore germination and hyphal enlargement, (ii) the symbiotic phase comprising proliferation of hyphae in roots of host plants, and (iii) development of mycelium outside host roots (symbiotic extraradical mycelium growth), followed by spore formation. AM fungal spores are present in the soil and germinate on their own, without assistance from plant signals (Harrison 2005). The establishment of AM symbiosis initiates with the colonization of the host plant root system by the hyphae germinated from AM fungal propagules, asexual spores, or mycorrhizal roots (Requena et al. 1996). The fungal entry into the compatible host plant takes place by means of either a penetration hypha or infection peg derived from the appresorium that vigorously infiltrates the cell or by enzyme synthesis which dissolves the cell wall. Studies in lotus have revealed that fungal attack on the host plant takes place by the development of an epidermal gap between two rhizodermal cells (in close proximity to each other) by means of which the fungus penetrates and then gradually progresses toward the exodermal cells (Parniske 2004). Several

6 Exploitation of Arbuscular Mycorrhizal (AM) Fungi as a Sustainable …

145

researches have also documented the synthesis of diverse cell wall disintegrating enzymes, such as xyloglucanases, cellulases, and pectinases including polygalacturonases, thus indicating that colonization of roots by fungus involves mechanical as well as enzymatic processes together with co-ordination from the plant machinery for penetration. An endotransglucosylase gene, XHT1, recognized from Medicago truncatula was demonstrated to facilitate fungal penetration for establishing symbiosis by altering the structure of plant cell wall (Balestrini and Bonfante 2014). In general, fungal hypha fastens to the host root surface through appressorium. Appressoria are flat, oval tips of hyphae whose inception produces alterations in fungal gene expression. Though the formation of appresoria indicates fungal attachment, yet its propagation and penetration into the plant cell need the synchronized action of the host cells (Paszkowski 2006). Thigmotrophic signals generated from the plant or secondary metabolites synthesized in plants subsequent to perception of the fungus are necessary for formation of appressorium as well as development of AM–plant symbiosis (Requena et al. 2007). The chemicals released by the plant and the thigmotrophic signals from the rhizodermal cells are recognized by the receptor proteins present on the fungal plasma membrane (Requena et al. 2007). In addition, flavonoids have been proposed to play an important role in the symbiosis either by influencing hyphal differentiation and growth or root colonization (Tsai and Phillips 1991). Several flavonoids have been reported to exert an invigorating effect on AM–plant interface, with more apparent impact in the presence of rhizospheric carbon dioxide. Phenolics synthesized by plants also function in the instigation of AM symbiosis, but infiltration of the roots and successful establishment of symbiotic association is reliant on the host plant as well as its interaction with fungus. This has been confirmed through colonization studies performed with genus Glomus on sorghum and clover plants using phenolic compounds such as p-hydroxybenzoic acid, p-coumaric acid, or quercetin as growth promotors. At the same time, strigolactones found in the root exudations of diverse plants also influence AM symbiosis by stimulating its establishment, hyphal branching, or the continuous growth of the fungus (Bouwmeester et al. 2003; Akiyama and Hayashi 2006). Transcript studies of AM fungi during formation of appressorium demonstrated that due to host contact, different genes get activated, for example, many components linked to Ca2C signaling like a calmodulin, P-type Ca2C-ATPase, Ca2C-induced Ras inactivator, and a leucine zipper EF-protein (Requena and Breuninger 2004). After appresorium formation, the fungal hyphae enter into the cortical cells and form discrete specialized structures such as interand intracellular hyphae, loops, and arbuscules. Arbuscules are specialized type of hyphae which develop as intercalary structures connecting the coiled hyphae and are the regions of nutrient and carbon exchange between host plant and the fungus (Requena et al. 2007). It is believed that formation of arbuscule begins when the host cell senses a sugar gradient that arose between the eternal cell layers and the vascular elements. Proteins involved in SYM pathway like LjSYM15, LjSYM 24, LjCASTOR, and LjNup 133 play a key role in development of arbuscules (Kistner et al. 2005). Nodule colonization in leguminous roots by AM fungi initiates with the detection of Nod factors by NFR1 and NFR5 (LysM receptor kinases). Stimulation of the receptor kinases links the symbiotic signaling pathway with symbiosis

146

H. Kaur et al.

receptor-like kinase (SYMRK). Studies have revealed that inactivation of NFR1 or NFR5 hamperes nitrogen-fixation process. Further, it has been identified that MycLCO receptors have structural analogies to NFR5/NFP and NFR1/LYK3 and can execute similar function (Sun et al. 2015). Besides functioning as co-receptors during Nod signaling, SYMRK also acts as a co-receptor for interacting with the specific receptor. Further, SYMRK associates with 3-hydroxy3-methylglutaryl-CoA reductase (HMGR) and mitogen-activated protein kinase (MAPKK), suggesting its role in co-ordinating signals between ion channels connected with nucleus and membranebound receptors. An additional important gene that can play a direct role in AM symbiosis establishment is CYCLOPS which is phosphorylated by calcium and calcium/calmodulin-dependent serine/threonine-protein kinase (CCaMK). Nevertheless, the precise role played by CYCLOPS is largely not clear (Oldroyd 2013). NUP85 and NUP133 are the central nucleoporin proteins engaged in calcium spiking during common symbiosis pathway (CMP) (Balestrini and Bonfante 2014). Moreover, some carotenoid derivatives function at numerous stages in the progression of AM symbiosis, probably by invigorating intraradical fungal branching (Paszkowski 2006). Therefore, it can be inferred that arbuscular development and formation of intracellular fungal structures are intricate physiological processes involving a coordinated system of many genes (Basu et al. 2018). Following host colonization, the fungal mycelium expands out of the root delving into the soil for exploring nutrients and can inhabit other roots. The fungal life phases are completed after development of asexual chlamydospores on the extraradical mycelium (ERM). Therefore, characteristic morphological stages can be recognized in the life cycle of AM fungi.

6.3.2 Impact of Cd on AM Fungal Growth and Development A range of environmental aspects could impact the AM community makeup, and among those, heavy metal soil pollution (Cd) is the major one (Yang et al. 2015). Majority of the studies (Table 6.1) have suggested that high Cd levels can impede AM spore germination and hyphal development (Andrade and Silveira 2008; Yang et al. 2010), but few researches have reported significantly enhanced root colonization and length of ERM at high Cd levels (Janouškova et al. 2005; Audet and Charest 2006; Krishnamoorthy et al. 2015). Simultaneously, some reports revealed no considerable influence of soil Cd pollution on AM growth (Whitfield et al. 2004; Andrade et al. 2008; Liang et al. 2009). The contradictory reports documented by researchers could be attributable to diverse Cd treatments used in their respective trials, indicating that AM grows under Cd stress up to a certain limit after which it starts reducing the symbiosis. Nevertheless, the performance of AM colonization in Cd-polluted soils is a topic of discussion, suggesting the need for understanding the importance of ERM and their metabolic activity in terms of plant growth period and Cd gradient. Whether the growth of AM fungus is increased (indicating enhanced mycorrhizal responsiveness) or retarded with increase in Cd levels is still not clear (Gai et al. 2018). Rask et al. (2019) put forward that mycorrhizal symbiosis is discursively

6 Exploitation of Arbuscular Mycorrhizal (AM) Fungi as a Sustainable …

147

Table 6.1 Effect of different Cd concentrations on growth and development of diverse AM species AMF

Cd concentration

Acaulospora laevis, 0.05, 0.1, 0.5 and Glomus caledonium, 1 mg L−1 and Glomus manihotis

Effect on AM

References

–

No spore Pawlowska germination and and Charvat pre symbiotic (2004) hyphal extension in G. etunicatum at highest Cd concentration whereas spore germination decreased and pre symbiotic hyphal extension stimulated in G. intraradices under highest Cd level

Glomus intraradices Exp.1—40 mg kg−1 Exp.2—0.6 mg L−1

Nicotiana tabacum L., var. Wisconsin 38

Increased root Janouškova colonization rate et al. (2005) and ERM length in Exp. 1 than Exp. 2

Glomus 20 μmol L−1 macrocarpum strain IAC-50

Zea mays L. Root colonization var. Exceller and ERM length decreased dramatically

Andrade and Silveira (2008)

Glomus intraradices 20 μmol L−1 strain IAC-43

Helianthus annuus L. ‘IAC Uruguai’

Andrade et al. (2008)

Glomus etunicatum and Glomus intraradices

0.001, 0.01, 0.1, 1.0 mM

Plant

Zea mays L. G. manihotis > A. Liao et al. laevis > G. (2003) caledonium (spore density)

No significant effect on mycorrhizal colonization and amount of ERM

Glomus mosseae and G. sp

11.75 mg kg−1 28.75 mg kg−1 46.63 mg kg−1 77.13 mg kg−1 (In four test groups)

Zea mays L. No significant differences in HC, VC, and AC in different test groups

Glomus mosseae and Acaulospora laevis

0.1, 0.5 and 1.0 mg L−1

Zea mays L. Spore density of Abdelmoneim G. mosseae was et al. (2014) stimulated at all Cd levels whereas A. laevis showed increase in spore density at low Cd levels and inhibition at higher Cd concentration

Liang et al. (2009)

(continued)

148

H. Kaur et al.

Table 6.1 (continued) AMF

Cd concentration

Plant

Effect on AM

Glomus versiforme and Rhizophagus intraradices

10 and 20 μg g−1

Lonicera japonica

Mycorrhizal Jiang et al. colonization rates (2016) of G. versiforme was higher than R. intraradices

References

Glaroideoglomus etunicatum and Glaroideoglomus claroideum

5, 25 and 50 mg kg−1

Cucumis sativus

ERM length increased at low level but inhibited at high level

Glomus monosporum, G. clarum, Gigaspora nigra, and Acaulospora laevis

2.25 and 6.25 Mm

(Trigonella foenum graecum L.) var. Giza 30

Increase in F %, A Abdelhameed %, and M% at low and Metwally Cd concentration (2019) but decreased at higher Cd levels

Gai et al. (2018)

A% arbuscular frequency, AC arbuscules, ERM extraradical mycelium, F% frequency of mycorrhizal colonization, HC hyphae, M% intensity of mycorrhizal colonization, VC vesicles

impacted by high soil Cd levels via negative influence it exerts on plant growth. The symbiosis shatters, when soil Cd concentration attains a point where plant is not able to support the microbiont. Li et al. (2009) demonstrated depression in activities of alkaline phosphatase (ALP) and succinate dehydrogenase (SDH), especially of Glomus intraradices in the presence of Cd. Further, spores and presymbiotic hyphal development of diverse AM species vary in their sensitivities to Cd (Pawlowska and Charvat 2004). Mycorrhizal colonization has been reported to be suspended, decreased, or even eradicated (Table 6.1) in response to high soil concentrations of Cd (Chen and Zhao 2007; Zhang et al. 2010). Additionally, reduction in AM growth in Cd-contaminated soils may be due to inhibition in processes like spore formation and germination, germ tube growth, mycelium expansion, hyphae branching, arbuscule formation and due to impediment in cell division, protein degradation, DNA damage, cell membrane disruption, and inhibition of transcriptional and translational processes (Moreira et al. 2015; Gupta et al. 2016; Shahabivand et al. 2016; Martins et al. 2017; Wang 2017). Hence, Cd toxicity causes severe alterations in AM life cycle stages and metabolism (Hu et al. 2013a, b; Moreira et al. 2015). Recurrently, Glomus species are richly found in metal-contaminated sites as they make up the biggest group and generally have high sporulation frequency which supports their continued existence in perturbed environments (Wei et al. 2015; Kaur and Garg 2017). Assessment of the effect of Cd on AM growth is scarce, because in majority of cases, heavy metal multi-pollution exists (Ban et al. 2017), thereby resulting in a great difficulty to segregate specific Cd effects on fungal populations. The continuation of germination potential in spite of prolonged contact to the inhibitory metal concentrations suggests that few AM fungal species from low-metal conditions may endure transitory increase in soil metal levels and germinate when

6 Exploitation of Arbuscular Mycorrhizal (AM) Fungi as a Sustainable …

149

situation in soil microhabitats becomes favorable. Moreover, ERM length is considerably dependent on AM species, Cd level, and duration (Gai et al. 2018). Nonetheless, mycorrhizal colonized plants and metal-resistant fungal ecotypes have been reported to occur in metal-contaminated areas (Hildebrandt et al. 2007). In several cases, the AM fungi endeavor to avoid adverse environments by growing mycelium to a greater extent and maintain their role in the existence of lethal elements by improving metabolic activity. This enduring character of AM fungi is a crucial aspect in strengthening the plant tolerance (Hildebrandt et al. 2007; Göhre and Paszkowski 2006). Furthermore, spores from Cd-contaminated grounds have been documented to be more tolerant than spores from unpolluted grounds. This natural endurance is possibly because of phenotypical plasticity instead of genetic alterations in spores, because tolerance is vanished after first generation in the absence of metals. To sum up, for using AM association for soil metal remediation, it is imperative to figure out ways through which fungus tolerates metal toxicity, despite the establishment of the association being influenced by polluted soils.

6.3.3 Diversity of AM Community/Species Richness in Cd-Contaminated Soils AM fungal communities are important during and after soil turmoil due to their function in the establishment and existence of plants. Therefore, alterations in the variability of their populations due to high concentration of metals are assumed to hamper the probable useful outcomes of this symbiotic interaction, since restoration of AM fungal species is a time-consuming process (Pal et al. 2017). Cd pollution is one of the environmental aspects that affects and changes AM fungal community organization in host root system and rhizospheric soil (Table 6.2) relative to those detected in unpolluted grounds (Hassan et al. 2011). Cd decreases AM fungal variability (Table 6.2) in the rhizosphere communities (Martins et al. 2017; Garg and Singh 2018), though they are never totally eradicated from Cd-polluted soils, suggesting great adaptability and the enduring character of these microbes (Liu et al. 2015; Ban et al. 2017; Kaur and Garg 2017). Hassan et al. (2011) observed that few AM ribotypes, viz., Glomus mosseae and Glomus spp. were particularly present in Cd-polluted sites, whereas other ribotypes (G. intraradices, G. etunicatum, G. irregular, and G. viscosum) were identified in Cd polluted as well as unpolluted soil. AM fungal distribution is influenced by various soil factors, for example, soil P, N amounts (Zhao et al. 2017), pH of soil (Melo et al. 2017), moisture content (Deepika and Kothamasi 2015), and organic substances (Wang et al. 2015). Likewise, seasonal variations for instance precipitation (Alguacil et al. 2015) and temperature (Dumbrell et al. 2011) affect AM growth in the soil. The recognition of AM fungi is chiefly dependent upon the eternal morphology of spores (Turnau et al. 2001). Conventionally, investigations on AM fungi abundance and allocation have been carried out through extraction of spores from the soil

Glomus, Gigaspora, Scutellospora and Acaulospora

Glomus spp., Kuklospora spp. (Acaulospora) and Ambispora spp.

Acaulospora longula, A. rugose, A. laevis, A. spinos, A. scrobiculata, A. spp., Glomus spp., Archaeospora leptoticha and Ambispora fennica

R. intraradices, F. Glomeraceae, mosseae and Acaulospora Acaulosporaceae sp.

Slag heaps, Temascaltepec, Mexico

Dabaoshan Mine, China

Ikuno mine, Japan

Qiandongshan mine, China

Acaulosporaceae, Glomeraceae, Archaesporaceae and Ambisporaceae

Glomeraceae, Acaulosporaceae and Ambisporaceae

Glomeraceae, Gigasporaceae and Acaulosporaceae

Glomeraceae and Acaulosporaceae

Glomus sp., G. mosseae, G. fasciculatum, and Acaulospora sp.

River South Tyne, United Kingdom

AMF family Glomeraceae

AMF species detected

Chrzanow, Southern Glomus mosseae, G. intraradices, G. Poland claroideum, Glomus sp. HM-CL4, and Glomus sp. HM-CL5

Cd contaminated site

Robinia pseudoacacia L.

Athyrium yokoscense

Phytolacca americana, Rehmannia glutinosa, Perilla frutescens, Litsea cubeba, and Dysphania ambrosioides

Turnau et al. (2001)

References

Long et al. (2010)

RFLP, sequencing of rRNA (SSU)

(continued)

Yang et al. (2015)

Molecular analysis of Nonomura et al. the 18S rDNA (2011)

Nested PCR and DGGE analysis, sequencing of rRNA (SSU)

Gonzalez-Chavez et al. (2009)

PCR, RFLP and DNA Whitfield et al. sequencing (2004)

Nested PCR

Technique

Pinus sp., Abies religiosa, Buddleia Micro-morphological sp., Quercus sp., and Alnus sp. analysis

Thymus polytrichus

Fragaria vesca L.

Host plant

Table 6.2 Diversity of AM community/species richness in Cd-contaminated sites

150 H. Kaur et al.

Claroideoglomeraceae, Glomeraceae, Gigasporaceae, Ambisporaceae and Acaulosporaceae

C. etunicatum, C. claroideum, R. irregularis, Cetraspora pellucida, Gigaspora margarita, Ambispora leptoticha and A. longula

Glomus, Rhizophagus, Funneliformis, Acaulospora, Diversispora, Claroideoglomus, Scutellopora, Gigaspora, Ambispora, Paraglomus, and Archaeospora

Post-mining area and a natural forest area in Jecheon, Korea

Shimen Realgar Mine, Hunan Province of China

Glomeraceae, Acaulosporaceae, Diversisporaceae, Claroideoglomeraceae, Gigasporaceae, Ambisporaceae, Paraglomeraceae and Archaesporaceae

AMF family

AMF species detected

Cd contaminated site

Table 6.2 (continued)

Sequencing of 18s rDNA and nested PCR

Technique

Digitaria violascens, Eclipta Sequencing of rRNA prostrata, and Veronica didyma (SSU), 454Tenore, Digitaria ciliaris (Retz.) pyrosequencing Koel, Herba seu Radix Amaranthi, Eleusine indica (L.) Gaertn, Solanum nigrum L., Miscanthus floridulu (Labnll.), Allium senescens, Clinopodium chinense (Benth.) O. Ktze, Poa annua L. and Paspalum paspaloides (Michx.)

_

Host plant

(continued)

Sun et al. (2016)

Park et al. (2016)

References

6 Exploitation of Arbuscular Mycorrhizal (AM) Fungi as a Sustainable … 151

Nested PCR, rLSU sequencing

Festuca arvernensis, Koeleria vallesiana, Biscutella laevigata, Silene vulgaris and Thymus vulgaris

Glomus spp., Paraglomus spp., Rhizophagus spp., and Claroideoglom us

Les Avinières, France

Glomeraceae, Paraglomeraceae and Claroideoglomeraceae

Cereals: rice, Sorghum, barley, and Spore identification bajra and count Vegetables: palak, papaya, turmeric, raddish, okra and cauliflower Flowers: marigold, hibiscus, jasmine, rose and bela

Technique

Glomus mosseae, Glomus Glomeraceae fasciculatum and Glomus intraradices

Host plant

Urban fringe, Varanasi city, Eastern gangetic plain, Northern India

AMF family

AMF species detected

Cd contaminated site

Table 6.2 (continued)

(continued)

Sanchez-Castro et al. (2017)

Pal et al. (2017)

References

152 H. Kaur et al.

Glomeraceae, Claroideoglomeraceae

Dominikia iranica, F. constrictum, F. mosseae, R. intraradices, R. irregularis, Septoglomus viscosum and Claroideoglomus sp.

Matanza-Riachuelo river basin, Argentina

Festuca arundinacea, Paspalum distichum, Sorghum halepense, Taraxacum officinale, Senecio bonariensis, Chamaemelum nobile, Trifolium sp., Cyperus eragrostis, Dichondra microcalyx, Salix babylonica, Morusnigra, Ricinus communis, Commelina erecta, Hydrocotyle bonariensis, Conium maculatum and Juncus pallescens

Host plant Molecular, morphological and pyrosequencing

Technique Colombo et al. (2019)

References

Cd cadmium, DGGE denaturing gradient gel electrophoresis, DNA deoxy ribonucleic acid, PCR polymerase chain reaction, rDNA ribosomal deoxy ribonucleic acid, rLSU ribosomal large subunit, rRNA ribosomal ribonucleic acid, SSU smaller subunit, T-RFLP terminal restriction fragment length polymorphism

AMF family

AMF species detected

Cd contaminated site

Table 6.2 (continued)

6 Exploitation of Arbuscular Mycorrhizal (AM) Fungi as a Sustainable … 153

154

H. Kaur et al.

and recognition on the basis of morphology and ontogeny of the spores which are developed around or inside the root structures (Oehl et al. 2010). However, there are few reports which indicate that fungal species variability, dependent upon on spore occurrences, may not be associated with the species mixture aggressively colonizing host roots (Turnau et al. 2001); thus, molecular genomic approaches are being carried out to exemplify the AM fungal DNA inside the roots. Turnau et al. (2001) applied nested PCR technique along with rhodizoniate staining and proposed that it might offer a basis for distinguishing AM fungi with regard to their capability of storing the metals (including Cd) inside the roots under normal environmental conditions. In recent times, molecular study of DNA of AM fungi isolated from soils or host roots through fingerprinting methods, for instance, denaturing gradient gel electrophoresis (DGGE), terminal restriction fragment length polymorphism (T-RFLP), and pyrosequencing have been used to examine AM fungal community arrangement (Symanczik et al. 2014; Krishnamoorthy et al. 2015; Colombo et al. 2019). CruzParedes et al. (2017) evaluated AM fungal molecular variability in Cd-containing regions through phosphate fertilization and proved greater abundance of operational taxonomic units (OTUs) derived from F. caledonium and F. mosseae. These AM fungal species also had more sporulation rates. Majority of the researchers have documented predominance of Glomus mosseae (renamed as Funneliformis mosseae) in Cd-contaminated soil, signifying the endurance of this taxonomic group to metal stress (Krishnamoorthy et al. 2015; Colombo et al. 2019), also Yang et al. (2015) demonstrated in their experimental outcomes the Acaulospora group as the leading genus next to Glomus. Nonetheless, AM symbiotic behavior in Cd-polluted soils varies depending upon the AM species, host species, soil features, and even AM ecotypes (Hildebrandt et al. 2007; Zarei et al. 2010). Similarly, alteration in AM symbiosis with respect to host plants can be associated with characters, for example, plant growth stage, reliance on mycorrhiza, variations in the soil micro-environment, or unidentified host features (Pal et al. 2017). The choice of effectual isolates should, hence, include examination of their symbiosis capabilities in the place where the inoculum is to be introduced.

6.3.4 Various Mechanisms Employed by AM Fungi for Conferring Cd Tolerance to Plants AM fungal symbiosis with plants has been proposed as a conceivable biological way out to enhance plant endurance to metal toxicity and restore fertility of soils contaminated by metals, for example, Cd (Vivas et al. 2005). Several mechanisms implemented by AM fungi to confer Cd tolerance to plants and aid in restoration of Cd-polluted sites are broadly categorized into two categories: extracellular and intracellular:

6 Exploitation of Arbuscular Mycorrhizal (AM) Fungi as a Sustainable …

6.3.4.1

155

Extracellular Mechanisms

Cd Chelation by Root and AM Exudates One of the methods by which plants are capable of decreasing metal content in soils is the exudation of organic acids. Organic acids are chief metabolites produced in plants, generally during the glyoxylate cycle and Krebs cycle as well as in C4 and CAM pathway of photosynthesis (Lopez-Bucio et al. 2000; Igamberdiev and Eprintsev 2016). They can create active cytosolic along with storage vacuolar pools which can be utilized to regulate the ionic equilibrium in plant cells (Osmolovskaya et al. 2007). In general, approximately 50% of photo-assimilates in plants are re-translocated to roots and few of them (roughly 12–40%) are discharged into the rhizosphere throughout the plant developmental stages as exudates: organic acids, amino acids, sugars, polysaccharides, peptides, and proteins (Lin et al. 2003; Hinsinger et al. 2006). Additionally, root exudation also comprises inorganic ligands (e.g., SO4 2− , Cl− , CO3 2− , NH4 + , PO4 3− ). These metabolites not only act as an energy supply of microbes, but also as ligands to be binded with metal ions, thereby changing pH and Eh as well as chemical attributes in the rhizosphere. Certain organic acids can chelate heavy metals and guard the roots from toxic effects (Jones et al. 2003; Jung et al. 2003; Liao and Xie 2004; Schwab et al. 2005). During heavy metal stress, the secretion of amino acids from plant roots boosts drastically (Fu et al. 2017). For instance, the exudation of histidine, methionine, and lysine in rice roots upsurges considerably with the rise in Cd level (Wang et al. 2016). Chen et al. (2016) reported that organic acids exuded by Phyllostachys pubescens roots can improve phosphorus levels in soils. In response to Cd stress, the total organic acid content secreted in Cd-insensitive rice roots was 1.76–2.43 times compared to Cd-sensitive varieties (Fu et al. 2017). The exudation of oxalic acid, tartaric acid, and acetic acid in underground parts of Cd-tolerant pepper varieties was considerably greater compared to Cd-sensitive ones (Xin et al. 2014). Plant cell walls actively gather few soluble solutes, for example, soluble sugars and proteins, whose target is to decrease osmotic potential intracellularly to regulate water supply and normal plant physiological processes during heavy metal stress (Jia et al. 2012). Accordingly, the composition and amount of root exudations may influence the active state of metals. Plant species (e.g., paddy rice) belonging to gramineae family exude phytosiderophores which can develop strong and stable complexes with Cd, Fe, Cu, and Zn compared to carboxylic acids (Chaignon et al. 2002). Furthermore, AM fungi secrete organic acids, for example, malic, citric and oxalic acids along with amino acids into the rhizosphere to endure metal toxicity. The deprotonation of organic acids results in acidification of the rhizosphere and enhances the movement of metal ions or restricts their mobility and detoxifies them via precipitation and complexation (Saraswat and Rai 2011). Similarly, the vital function of amino acid, viz., tryptophan has been reported with respect to plant Cd tolerance (Sanjaya et al. 2008). Tryptophan is presumed to execute a chelating role with regard to the Cd. It has been revealed that the increased tryptophan level in the transgenic Arabidopsis thaliana plants was able to restrain the expression of genes encoding metal transporters. These findings unlock remarkable prospective for breeding crop species with improved Cd tolerance, decreased Cd accumulation, and increased content of tryptophan.

156

H. Kaur et al.

The fundamental strategy of metal detoxification with the aid of organic acids is the capability of acids, for example, malate, citrate, malonate, oxalate, aconitate, and tartrate to develop strong bonds with metal ions through chelation by carboxyl groups performing the function of donor oxygen in metal–ligands (Anjum et al. 2015). In contrast, Cd-stimulated the exudation of oxalic acid from the tips of tomato roots which was linked with the prohibition of Cd tolerance (Zhu et al. 2011). An inhibitor of anion channel PG stopped the exudation of oxalate, and external application of oxalate successfully eradicated Cd toxicity, blocking the entry of Cd into the root, possibly via development of extracellular Cd-oxalate complex (Zhu et al. 2011). The Cd-oxalate complex is moderately soluble and thus decreases the Cd bioavailability and its absorption by the root tip, especially in the soil, where the contribution of exudates in the various soil processes is possible (Zhu et al. 2011). The phenomenon of reduced metal absorption by plants under the influence of organic acids exuded by roots is generally ascribed to decline in the level of ionized bioavailable states of metals in the rhizosphere and enhanced antagonism of H+ and metal ions for the adsorption regions on the root cell wall (Dong et al. 2007) and with the development of less bioavailable chelate complexes, which eventually plays a role in improving plant tolerance to metals (Hall 2002). AM-Induced Glomalin Secretion The glomalin-related soil protein (GRSP) is a glycoprotein yielded by the mycelium of AM fungus belonging to Glomerales (Khan 2006; Saleh and Al-Garni 2006; Cornejo et al. 2008). It is a stable compound resistant to heat, produced mainly in the internal layer of the fungal cell walls, and is secreted into the soil in the course of hyphal turnover or subsequent to the fungal death (Driver et al. 2005). Except Glomeromycota, no other fungal group produces these glycoproteins in large amounts (Singh et al. 2012). The formation of glomalin is determined by the content of metal ions present in the soil (Singh et al. 2012; Sidhu et al. 2019). Production of glomalin by fungal hyphae to alleviate Cd toxicity has been documented in numerous findings (Wu et al. 2014; Malekzadeh et al. 2016; Jia et al. 2018). Glomalin (homolog of heat shock proteins) also possess a remarkable ability to sequester Cd and hence can decrease cytosolic Cd damage (Fig. 6.1). The efficacy of protection is determined by the content of metal immobilized in extraradical hyphae, which promotes adaptation in host plants facing stressful conditions (Zhang et al. 2019b). Furthermore, this may act as a defensive strategy against Cd toxicity through regulated Cd translocation by extraradical hyphae toward the host root system (Shahabivand et al. 2012), since external hyphae are the primary site for the expression of gene responsible for glomalin production (Gadkar and Rillig 2006). The existence of specific functional groups in the glomalin helps in binding with heavy metals. In addition to sequestering Cd, glomalin carries out various functions such as increasing the firmness of soil masses, decreasing soil erosion, and promoting soil quality. Furthermore, glomalin assists in maintaining soil water level by regulating the rate of water transport between plants and the soil, eventually improving the plant growth. AM fungi have been documented to regulate production of glomalin depending on intensity of contamination. In Robinia pseudoacacia, entire and easily extractable glomalin level augmented according to Cd levels, which

6 Exploitation of Arbuscular Mycorrhizal (AM) Fungi as a Sustainable …

157

led to an increase in the content of glomalin-bound Cd over time (Jia et al. 2016). In bermudagrass, inoculation with Diversispora spurcum and Funneliformis mosseae raised the soil pH, thus lowering the level of available Cd (Zhan et al. 2019). Binding of Cd on Fungal Structures In mycorrhiza associated plants, Cd tolerance is associated with the production of mycelial biomass and fungal development, as metal gets accumulated in the fungal mycelium. Mycorrhizal roots function as a barricade against transportation of metals, decreasing their transfer, and increasing root/shoot Cd ratios (Andrade et al. 2008). This is ascribed to adsorption of metal on hyphal cell walls (chitin and polysaccharides), which contain valuable metal-binding ability (Christie et al. 2004; Liu et al. 2008). Presence of free amino acids in the cell walls and functional groups, for example, amino groups, imidazole carboxyl groups, and free hydroxyl groups offer binding regions for metals and develop negatively charged structures which can adsorb metals in the soil and prevent their transfer to plant (Meier et al. 2012). Moreover, AM fungi accumulate metals within their spores (Gonzalez-Guerrero et al. 2008; Cornejo et al. 2013). At high metal concentrations, less amount of metal crosses the cell wall, gets accumulated in the fungal cell membrane, or is transferred to the fungal cytoplasm, thus decreasing

Fig. 6.1 Diagrammatic representation of AM-mediated (phyto)-remediation of Cd-contaminated soils a AM-induced alterations in the morphological and physiological aspects of host plant increase the plant tolerance toward Cd2+ ; glomalin produced by fungal mycelium helps in Cd2+ sequestration in soil and prevents its translocation from root to shoot b uptake of Cd2+ occurs through zinc/ironregulated transporters (ZIPs) which then enters the cytosol and stimulates the synthesis of metal chelators like glutathione (GSH), phytochelatins (PCs), and metallothioniens (MTs). PCs bind cytosolic Cd2+ and form PC-Cd2+ complexes which are transported into the vacuole via adenosine triphosphate–binding cassette (ABC) transporters present in tonoplast. GSH and MTs also facilitate buffering of the cytosolic Cd2+

158

H. Kaur et al.

the content of metal ions in the plants. AM fungi promote root cell wall synthesis in the host plant, which improves metal diminution since with enhancement in the width of cell wall, the area for metal absorption also increases (Zhang et al. 2019b). Numerous researchers have demonstrated that with rise in metal content, the fungal cell walls function as the first line of defense as they block the metal entry (Hall 2002; Emamverdian et al. 2015). Compartmentalization of metals inside fungal structures is also well described. X-ray fluorescence imaging with a synchrotron irradiation microbeam of Rhizophagus irregularis under Cd stress showed large amounts of this metal inside the fungal cell wall and vacuoles of extraradical mycelium compared to those detected in the cytoplasm (Nayuki et al. 2014). The AM inoculation of Aster tripolium roots allowed the fungi to accumulate Cd in the mycelium and stimulate plant tolerance towards Cd (Carvalho et al. 2006). The AM colonization of Melastoma malabathricum plants resulted in an upsurge in the absorbing area of the host roots in the soil, thereby improving plant growth (Jankong and Visoottiviseth 2008).

6.3.4.2

Intracellular Mechanisms

Metal Chelators A distinctive amelioration approach employed by AM fungi is the metal chelation with the assistance of ligands possessing great affinity for metal ions in the cytoplasm. Cd compartmentalization linked with intracellular complexation signifies a crucial strategy for decreasing Cd toxic effects on plants. It arises due to the association of Cd with chelating agents, which accumulate Cd in cellular compartments like vacuoles (Guimarães et al. 2008). The generation of chelating compounds takes place if the content of toxic metals goes beyond the threshold value within the cells. Chelation assists in decreasing metal content by making them less available in the cytosol and by reducing their solubility and reactivity. Chelation through glutathione (GSH), phytochelatins (PCs), and metallothioneins (MTs) (Fig. 6.1) signifies a frequently employed Cd detoxification approach by several plant species (Garg and Bhandari 2014). Besides these plant processes, Cd can also form complexes with the binding proteins, abundantly possessing cysteines having large affinity for metals (Ma et al. 2005). GSH and PCs possess sulfhydryl (–SH) groups, which participate in the sequestration and metal detoxification. GSH, a tripeptide and an amino acid derivative, comprising cysteine, glutamic acid, and glycine, is acknowledged as a strategy not only for carrying out key roles in the antioxidant defense mechanism but also as a metal-chelator which reduces the toxicity of metals (Guo et al. 2012). Zhang et al. (2019b) demonstrated that mycorrhizal colonization in Zea mays reduced the Cd toxicity and its movement by converting it into an inactive state and attributed it to the enhanced level of PC and GSH. It has been reported that colonization with F. mosseae increased the content of GSH in Nicotiana tabacum, further decreasing the Cd and As level in the leaves and roots (Degola et al. 2015). AM fungi have potential of increasing the production of PCs (Garg and Chandel 2012; Begum et al. 2019).

6 Exploitation of Arbuscular Mycorrhizal (AM) Fungi as a Sustainable …

159

GSH is crucial for biosynthesis of PCs and is an important metabolic regulator of PCs (Seth et al. 2012). PCs, a lineage of linked thiolate peptides, chelate metals in cytosol via metal-PC complexes (Brunetti et al. 2011; Zitka et al. 2011). PCs are Cys-rich polypeptides which comprise duplicate units of γ-glutamyl-cysteine, subsequently one glycine (Gly) in the C-terminal [(γ-Glu-Cys)n -Gly] having 2-11 recurring units. Based on the plant species, Gly in the C-terminal can be replaced by Ser, Ala, Glu, or Gln. These metal chelators are enzymatically produced by γGlu-Cys dipeptide transpeptidase (also known as PC synthase) from GSH in the cytoplasm (Filiz et al. 2019). PC synthase is stimulated by binding of Cd to the enzyme (Vatamaniuk et al. 2001). When the Cd level in the cytoplasm is increased, AM fungi boost the synthesis of PCs (Cao et al. 2018; Zhang et al. 2019b). Particularly, among metals, Cd is recognized as a strong activator of PCs in various plant species (Anjum et al. 2015). Garg and Kaur (2013) reported that G. mosseae colonization markedly improved PCs amounts in pigeonpea under Cd and/or Zn stress. Similarly, Jiang et al. (2016) found increased PCs level in mycorrhizal plants of Lotus japonica and inferred that AM was effective in decreasing Cd toxicity. PCs combine with Cd and form a stable complex which is less toxic compared to free Cd ions present in the cells. When Cd-PC complexes are synthesized inside the cytoplasm, they are ultimately compartmentalized in vacuoles via ATP-binding cassette (ABC) transporters (Fig. 6.1) present in the tonoplast (Franchi et al. 2014). Three kinds of vacuolar ABC transporters, AtABCC1, AtABCC2 (Park et al. 2012), and AtABCC3 (Brunetti et al. 2015), have been identified in Arabidopsis thaliana that are engaged in the transportation of Cd-PC complexes through the tonoplast into the vacuole and facilitate Cd tolerance (Fu et al. 2019). Because of the low pH inside the vacuoles, Cd-PC complexes dissociate, and afterward, Cd can combine with ligands, comprising organic acids and possibly amino acids (Hossain et al. 2012). In addition, both PCs and GSH may play a crucial role in the long-distance Cd transportation between root and shoot, transferring the metal in the form of PC-Cd or GSH-Cd complexes, respectively (Mendoza-Cózatl et al. 2011). An alternative group of ligands, i.e., MTs, is also engaged in the compartmentalization of heavy metals (Fig. 6.1). MTs, a cluster of metal-proteins, have a low molecular mass and non-enzymatic, cysteine-containing, extended polypeptide chains which comprise of a huge number of amino acids (Ziller and FraissinetTachet 2018). MTs possess a common arrangement, i.e., Cys-X-Cys, wherein X is an amino acid excluding cysteine. They are metal chelators which bind metal ions in metal thiolate in the cytoplasm or sub-cellular parts for accumulating and sequestering metals inside plant vacuoles (Jia et al. 2012). Few researchers have reported different classes of MT genes stimulated by metals (Xu et al. 2007; Liu et al. 2009). GmarMT1, a cDNA-encoding MT-like functional polypeptide, was recognized from the germinating spores of Gigaspora margarita to impart tolerance against Cu and Cd (Lanfranco et al. 2002). Moreover, it has also been documented that metals upregulate the expression of GmarMT1 in the symbiotic mycelium. GmarMT1 codes for MTs identified in G. margarita (BEG34), retains the redox potential of the fungus and defends against oxidative stress. In Gigaspora rosea, GrosMT1 expression has been observed (Stommel et al. 2001). Plants colonized with AM fungi during metal

160

H. Kaur et al.

stress exhibit expression of certain genes, which are accountable for the generation of proteins (including MTs) improving the tolerance of plants. MTs are produced in various organisms when subjected to high concentration of heavy metals such as Zn, Cu, and Cd, and AM regulates the transcription of MT genes, thereby increasing the plant endurance to heavy metals (Miransari 2010; Guo et al. 2013). MTs are produced by mRNA transcription and are stimulated under metal stress conditions (Cobbett and Goldsbrough 2002; Emamverdian et al. 2015). MT gene can be expressed at various phases of plant development, responding to the stress of diverse heavy metal ions (Singh et al. 2019). So far, four kinds of MTs have been identified in plants, comprising MT1, MT2, MT3, and MT4, which are classified according to the sequence of Cys residues in their C- and N-terminal domains (Pan et al. 2018). MTs have a remarkable capability of binding to heavy metals, comprising Zn, Cd, Cu, and As, and can remove them even at low concentrations; nonetheless, in terms of a Cd chelator, MTs are placed after PCs (Li et al. 2016). Additional method adopted by AM fungi is the elimination or precipitation by secreting polyphosphate granules which form complexes with the metal, making it inaccessible to the plant (Kaur and Garg 2017; Abdelhameed and Metwally 2019; Shi et al. 2019).

6.4 Conclusions and Future Prospects The concentrations of cadmium (Cd) in the environment have augmented drastically in recent decades. Cd sources in food crops differ in the developing and developed countries. The use of industrial wastes and sewage sludge as fertilizers is the major sources of metal entry into the soil–crop systems in developed nations. Nevertheless, in developing countries, irrigation with insufficiently treated waste effluents or sludge is the major contamination cause for food crops. Cd transportation from soil to crop plants is complicated and involves intricate mechanisms. Soil microbes, for example, AM fungi function as an effectual and eco-friendly sustainable method for retrieval of Cd-polluted sites. Though Cd, as one of the most noxious elements in the soil and environment, can impact AM fungal growth, development, and functional variability, nevertheless, these microbes possess certain inbuilt intrinsic mechanisms (extracellular and intracellular) that effectively play a role in bio-(or phyto-)remediation of Cd-polluted areas. Therefore, mycorrhizal symbiosis is an excellent contender for phytostabilization and re-establishment of Cd-contaminated sites. In forthcoming times, precise recognition of AM taxa or strains present in the rhizosphere of plants cultivated on metal-polluted areas could prove to be a crucial step toward enriching bioremediation. Moreover, for complete exploitation of AM advantages, large-scale field experiments must be performed, employing different permutations of AM fungi and host plants. Besides this, there is lack of in-depth information about the genomic, metabolomic, and proteomic aspects of AM fungi in Cd-polluted areas. Hence, it is imperative to understand molecular basis of the establishment, regulation, and functioning of symbiosis under Cd stress environments.

6 Exploitation of Arbuscular Mycorrhizal (AM) Fungi as a Sustainable …

161

References Abbas SZ, Rafatullah M, Ismail N, Lalung J (2014) Isolation, identification, and characterization of cadmium resistant Pseudomonas sp. M3 from industrial wastewater. J Waste Manage 1–6 Abbas T, Rizwan M, Ali S, Adrees M, Zia-ur-Rehman M, Qayyum MF, Ok YS, Murtaza G (2017) Effect of biochar on alleviation of cadmium toxicity in wheat (Triticum aestivum L.) grown on Cd-contaminated saline soil. Environ Sci Pollution Res 25(26):25668–25680 Abdel Latef AAH, Hashem A, Rasool S, AbdAllah EF, Egamberdieva D, Jan S, Anjum NA, Ahmad P (2016) Arbuscular mycorrhizal symbiosis and abiotic stress in plants: a review. J Plant Biol 59(5):407–426 Abdelhameed RE, Metwally RA (2019) Alleviation of cadmium stress by arbuscular mycorrhizal symbiosis. Int J Phytorem 21(7):663–671 Abdelmoneim TS, Moussa TA, Almaghrabi OA, Abdelbagi I (2014) Investigation the effect of arbuscular mycorrhizal fungi on the tolerance of maize plant to heavy metals stress. Life Sci J 11(4):255–263 Akiyama K, Hayashi H (2006) Strigolactones: chemical signals for fungal symbionts and parasitic weeds in plant roots. Ann Bot 97(6):925–931 Alekseenko VA, Bech J, Alekseenko AV, Shvydkaya NV, Roca N (2018) Environmental impact of disposal of coal mining wastes on soils and plants in Rostov Oblast, Russia. J Geochem Explor 184:261–270 Alguacil MM, Torrecillas E, Lozano Z, Roldán A (2015) Arbuscular mycorrhizal fungi communities in a coral cay system (Morrocoy, Venezuela) and their relationships with environmental variables. Sci Total Environ 505:805–813 Álvarez-Ayuso E, Otones V, Murciego A, García-Sánchez A, Rodriguez ISR (2013) Zinc, cadmium and thallium distribution in soils and plants of an area impacted by sphalerite-bearing mine wastes. Geoderma 207–208(1):25–34 Andrade SAL, Silveira A (2008) Mycorrhiza influence on maize development under Cd stress and P supply. Braz J Plant Physiol 20(1):39–50 Andrade SAL, da Silveira APD, Jorge RA, de Abreu MF (2008) Cadmium accumulation in sunflower plants influenced by arbuscular mycorrhiza. Int J Phytorem 10(1):1–13 Anjum NA, Hasanuzzaman M, Hossain MA, Thangavel P, Roychoudhury A, Gill SS, Merlos Rodrigo MA, Adam V, Fujita M, Kizek R, Duarte AC, Pereira E, Ahmad I (2015) Jacks of metal/metalloid chelation trade in plants—an overview. Front Plant Sci 6:192 Audet P, Charest C (2006) Effects of AM colonization on ‘“wild tobacco”’ plants grown in zinccontaminated soil. Mycorrhiza 16(4):277–283 Balestrini R, Bonfante P (2014) Cell wall remodeling in mycorrhizal symbiosis: a way towards biotrophism. Front Plant Sci 5(4):237 Ban Y, Jiang Y, Li M, Zhang X, Zhang S, Wu Y, Xu Z (2017) Homogenous stands of a wetland grass living in heavy metal polluted wetlands harbor diverse consortia of arbuscular mycorrhizal fungi. Chemosphere 181:699–709 Basu N, Horvat M, Evers DC, Zastenskaya I, Weihe P, Tempowski J (2018) A state-of-the-science review of mercury biomarkers in human populations worldwide between 2000 and 2018. Environ Health Perspect 126(10):106001–106014 Begum N, Qin C, Ahanger MA, Raza S, Khan MI, Ashraf M, Ahmed N, Zhang L (2019) Role of arbuscular mycorrhizal fungi in plant growth regulation: Implications in abiotic stress tolerance. Front Plant Sci 10:1068 Benavides MP, Gallego SM, Tomaro ML (2005) Cadmium toxicity in plants. Braz J Plant Physiol 17(1):21–34 Bhandari P, Garg N (2017) Arbuscular mycorrhizal symbiosis: a promising approach for imparting abiotic stress tolerance in crop plants. In: Plant-microbe interactions in agro-ecological perspectives. Springer, Singapore, pp 377–402

162

H. Kaur et al.

Bojorquez C, Frias-Espericueta MG, Voltolina D (2016) Removal of cadmium and lead by adapted strains of Pseudomonas aeruginosa and Enterobacter cloacae. Revista Internacional De Contaminacion Ambiental 32(4):407–412 Bonfante P, Genre A (2008) Plants and arbuscular mycorrhizal fungi: an evolutionary developmental perspective. Trends Plant Sci 13(9):492–498 Bouwmeester HJ, Matusova R, Zhongkui S, Beale MH (2003) Secondary metabolite signalling in host-parasitic plant interactions. Curr Opin Plant Biol 6(4):358–364 Brown TJ, Idoine NE, Raycraft ER, Shaw RA, Deady EA, Hobbs SF, Bride T (2017) World Mineral Production 2011–2015. In: British geological survey. Keyworth, Nottingham Brunetti P, Zanella L, de Paolis A, di Litta D, Cecchetti V, Falasca G, Barbieri M, Altamura MM, Costantino P, Cardarelli M (2015) Cadmium-inducible expression of the ABC-type transporter AtABCC3 increases phytochelatin-mediated cadmium tolerance in Arabidopsis. J Exp Bot 66(13):3815–3829 Brunetti P, Zanella L, Proia A, de paolis A, Falasca G, Altamura MM, di toppi LS, Costantino P, Cardarelli M (2011) Cadmium tolerance and phytochelatin content of Arabidopsis seedlings over-expressing the phytochelatin synthase gene AtPCS1. J Experimental Botany 62(15):5509– 5519 Cao ZZ, Qin ML, Lin XY, Zhu ZW, Chen MX (2018) Sulfur supply reduces cadmium uptake and translocation in rice grains (Oryza sativa L.) by enhancing iron plaque formation, cadmium chelation and vacuolar sequestration. Environ Pollut 238:76–84 Carvalho L, Cacador I, Martins-Loucao MA (2006) Arbuscular mycorrhizal fungi enhance root cadmium and copper accumulation in the roots of the salt marsh plant Aster tripolium L. Plant Soil 285(1):161–169 Chaignon V, Di Malta D, Hinsinger P (2002) Fe-deficiency increases Cu acquisition by wheat cropped in a Cu-contaminated vineyard soil. New Phytol 154(1):121–130 Chellaiah ER (2018) Cadmium (heavy metals) bioremediation by Pseudomonas aeruginosa: a mini-review. Appl Water Sci 8:154 Chen L, Zhang D, Yang W, Liu Y, Zhang L, Gao S (2016) Sex-specific responses of Populus deltoides to Glomus intraradices colonization and Cd pollution. Chemosphere 155:196–206 Chen XH, Zhao B (2007) Arbuscular mycorrhizal fungi mediated uptake of lanthanum in Chinese milk vetch (Astragalus sinicus L.). Chemosphere 68(8):1548–1555 Christie P, Li X, Chen B (2004) Arbuscular mycorrhiza can depress translocation of zinc to shoots of host plants in soils moderately polluted with zinc. Plant Soil 261(1):209–217 Cobbett C, Goldsbrough P (2002) Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annu Rev Plant Biol 53(1):159–182 Colombo RP, Benavidez ME, Bidondo LF, Silvani VA, Bompadre MJ, Statello M, Scorza VM, Scotti A, Godeas AM (2019) Arbuscular mycorrhizal fungi in heavy metal highly polluted soil in the Riachuelo river basin. Rev Argent Microbiol 52(2):145–149 Cornejo P, Meier S, Borie G, Rillig MC, Borie F (2008) Glomalin-related soil protein in a Mediterranean ecosystem affected by a copper smelter and its contribution to Cu and Zn sequestration. Sci Total Environ 406(1–2):154–160 Cornejo P, Pérez-Tienda J, Meier S, Valderas A, Borie F, Azcón-Aguilar C, Ferrol N (2013) Copper compartmentalization in spores as a survival strategy of arbuscular mycorrhizal fungi in Cupolluted environments. Soil Biol Biochem 57:925–928 Cruz-Paredes C, López-García Á, Rubæk GH, Hovmand MF, Sørensen P, Kjøller R (2017) Risk assessment of replacing conventional P fertilizers with biomass ash: residual effects on plant yield, nutrition, cadmium accumulation and mycorrhizal status. Sci Total Environ 575:1168–1176 Degola F, Fattorini L, Bona E, Sprimuto CT, Argese E, Berta G, di Toppi LS (2015) The symbiosis between Nicotiana tabacum and the endomycorrhizal fungus Funneliformis mosseae increases the plant glutathione level and decreases leaf cadmium and root arsenic contents. Plant Physiol Biochem 92:11–18 Deepika S, Kothamasi D (2015) Soil moisture—a regulator of arbuscular mycorrhizal fungal community assembly and symbiotic phosphorus uptake. Mycorrhiza 25:67–75

6 Exploitation of Arbuscular Mycorrhizal (AM) Fungi as a Sustainable …

163

Dinakar N, Nagajyothi PC, Suresh S, Damodharam T, Suresh C (2009) Cadmium induced changes on proline, antioxidant enzymes, nitrate and nitrite reductases in Arachis hypogaea L. J Environ Biol 30(2):289–294 Dong J, Mao WH, Zhang GP, Wu FB, Cai Y (2007) Root excretion and plant tolerance to cadmium toxicity—a review. Plant Soil Environ 53(5):193–200 Driver JD, Holben WE, Rillig MC (2005) Characterization of glomalin as a hyphal wall component of arbuscular mycorrhizal fungi. Soil Biol Biochem 37(1):101–106 Dumbrell AJ, Ashton PD, Aziz N, Feng G, Nelson M, Dytham C, Fitter AH, Helgason T (2011) Distinct seasonal assemblages of arbuscular mycorrhizal fungi revealed by massively parallel pyrosequencing. New Phytol 190(3):794–804 Emamverdian A, Ding Y, Mokhberdoran F, Xie Y (2015) Heavy metal stress and some mechanisms of plant defense response. Sci World J 2015:756120 Filiz E, Saracoglu IA, Ozyigit II, Yalcin B (2019) Comparative analyses of phytochelatin synthase (PCS) genes in higher plants. Biotechnol Biotechnol Equip 33(1):178–194 Franchi N, Piccinni E, Ferro D, Basso G, Spolaore B, Santovito G, Ballarin L (2014) Characterization and transcription studies of a phytochelatin synthase gene from the solitary tunicate Ciona intestinalis exposed to cadmium. Aquat Toxicol 152:47–56 Frank B (1885) Über die auf Wurzelsymbiosen beruhende Ernährung gewisser Bäume durch unterirdische Pilze. Berichte Der Deutschen Botanischen Gesellschaft 3(4):128–145 French KE (2017) Engineering mycorrhizal symbioses to alter plant metabolism and improve crop health. Front Microbiol 8:1403 Fu H, Yu H, Li T, Zhang X (2017) Influence of cadmium stress on root exudates of high cadmium accumulating rice line (Oryza sativa L.). Ecotoxicol Environ Saf 150:168–175 Fu S, Lu Y, Zhang X, Yang G, Chao D, Wang Z, Shi M, Chen J, Chao D, Li Y, Rongbai L, Jian FM, Jixing X (2019) The ABC transporter ABCG36 is required for cadmium tolerance in rice. J Experimental Botany 70(20):5909–5918 Gadkar V, Rillig MC (2006) The arbuscular mycorrhizal fungal protein glomalin is a putative homolog of heat shock protein 60. FEMS Microbiol Lett 263(1):93–101 Gai JP, Fan JQ, Zhang SB, Mi NN, Christie P, Li XL, Feng G (2018) Direct effects of soil cadmium on the growth and activity of arbuscular mycorrhizal fungi. Rhizosphere 7:43–48 Gallego SM, Pena LB, Barcia RA, Azpilicueta CE, Iannone MF, Rosales EP, Zawoznik MS, Groppa MD, Benavides MP (2012) Unravelling cadmium toxicity and tolerance in plants: insight into regulatory mechanisms. Environ Exp Bot 83:33–46 Gao Y, Miao C, Mao L, Zhou P, Jin Z, Shi W (2010) Improvement of phytoextraction and antioxidative defense in Solanum nigrum L. under cadmium stress by application of cadmium-resistant strain and citric acid. J Hazardous Mater 181(1–3):771–777 Garg N, Bhandari P (2014) Cadmium toxicity in crop plants and its alleviation by arbuscular mycorrhizal (AM) fungi: an overview. Plant Biosyst 148(4):609–621 Garg N, Chandel S (2011) Arbuscular mycorrhizal networks: process and functions. Sustain Agric 2:907–930 Garg N, Chandel S (2012) Role of arbuscular mycorrhizal (AM) fungi on growth, cadmium uptake, osmolyte, and phytochelatin synthesis in Cajanus cajan (L.) Millsp. under NaCl and Cd stresses. J Plant Growth Regul 31:292–308 Garg N, Kaur H (2013) Response of antioxidant enzymes, phytochelatins and glutathione production towards Cd and Zn stresses in Cajanus cajan (L.) Millsp. genotypes colonized by arbuscular mycorrhizal fungi. J Agron Crop Sci 199(2):118–133 Garg N, Singh S (2018) Arbuscular mycorrhiza Rhizophagus irregularis and silicon modulate growth, proline biosynthesis and yield in Cajanus cajan L. Millsp. (pigeonpea) genotypes under cadmium and zinc stress. J Plant Growth Regulation 37(6):46–63 Gianinazzi S, Gollotte A, Binet MN, van Tuinen D, Redecker D, Wipf D (2010) Agroecology: the key role of arbuscular mycorrhizas in ecosystem services. Mycorrhiza 20(8):519–530 Göhre V, Paszkowski U (2006) Contribution of the arbuscular mycorrhizal symbiosis to heavy metal Phytoremediation. Planta 223(6):1115–1122

164

H. Kaur et al.

Gonzalez-Chavez MC, Carrillo-Gonzalez R, Gutierrez-Castorena MC (2009) Natural attenuation in a slag heap contaminated with cadmium: the role of plants and arbuscular mycorrhizal fungi. J Hazard Mater 161(2–3):1288–1298 Gonzalez-Guerrero M, Melville LH, Ferrol N, Lott JNA, Azcon-Aguilar C, Peterson RL (2008) Ultrastructural localization of heavy metals in the extraradical mycelium and spores of the arbuscular mycorrhizal fungus Glomus intraradices. Can J Microbiol 54(2):103–110 Gratao PL, Monteiro CC, Rossi ML, Martinelli AP, Peres LEP, Medici LO, Lea PJ, Azevedo RA (2009) Differential ultrastructural changes in tomato hormonal mutants exposed to cadmium. Environ Exp Bot 67(2):387–394 Guilherme MDFS, Oliveira HM, Silva E (2015) Cadmium toxicity on seed germination and seedling growth of wheat Triticum aestivum. Acta Scientiarum. Biol Sci 37(4):499 Guimarães MDA, de Santana TA, Silva EV, Zenzen I, Loureiro ME (2008) Cadmium toxicity and tolerance in plants. Revista Trópica-Ciências Agrárias e Biológicas 2:58–68 Guo J, Xu W, Ma M (2012) The assembly of metals chelation by thiols and vacuolar compartmentalization conferred increased tolerance to and accumulation of cadmium and arsenic in transgenic Arabidopsis thaliana. J Hazard Mater 199–200:309–313 Guo W, Zhao R, Zhao W, Fu R, Guo J, Bi N, Zhang J (2013) Effects of arbuscular mycorrhizal fungi on maize (Zea mays L.) and sorghum (Sorghum bicolor L. Moench) grown in rare earth elements of mine tailings. Appl Soil Ecol 72:85–92 Gupta A, Joia J, Sood A, Sood R, Sidhu C, Kaur G (2016) Microbes as potential tool for remediation of heavy metals: a review. J Microbial Biochem Technol 8(4):364–372 Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53(366):1–11 Harrison MJ (2005) Signaling in the arbuscular mycorrhizal symbiosis. Annu Rev Microbiol 59:19– 42 Hashem HA (2014) Cadmium toxicity induces lipid peroxidation and alters cytokinin content and antioxidant enzyme activities in soybean. Botany 92(1):1–7 Hassan SED, Boon E, Arnaud M, Hijri M (2011) Molecular biodiversity of arbuscular mycorrhizal fungi in trace metal-polluted soils. Mol Ecol 20(16):3469–3483 Hayat S, Hasan SA, Aqil A (2011) Growth, nitrate reductase activity and antioxidant system in Cd stressed tomato (Lycopersicon esculentum Mill.) cultivars. Biotechnol Agron Soc Environ 15:401–414 He X, Nara K (2007) Element biofortification: can mycorrhizas potentially offer a more effective and sustainable pathway to curb human malnutrition? Trends Plant Sci 12(8):331–333 Helgason T, Fitter A (2009) Natural selection and the evolutionary ecology of the arbuscular mycorrhizal fungi (Phylum Glomeromycota). J Exp Bot 60(9):2465–2480 Hildebrandt U, Regvar M, Bothe H (2007) Arbuscular mycorrhiza and heavy metal tolerance. Phytochemistry 68(1):139–146 Hinsinger P, Plassard C, Jaillard B (2006) Rhizosphere: a new frontier for soil biogeochemistry. J Geochem Explor 88(1–3):210–213 Hossain MA, Piyatida P, da Silva JAT, Fujita M (2012) Molecular mechanism of heavy metal toxicity and tolerance in plants: central role of glutathione in detoxification of reactive oxygen species and methylglyoxal and in heavy metal chelation. J Bot 2012:1–37 Hu J, Chan PT, Wu F, Wu S, Zhang J, Lin X, Wong MH (2013a) Arbuscular mycorrhizal fungi induce differential Cd and P acquisition by Alfred stonecrop (Sedum alfredii Hance) and upland kangkong (Ipomoea aquatica Forsk.) in an intercropping system. Appl Soil Ecol 63:29–35 Hu J, Wu S,Wu F, Leung HM, Lin X, Wong MH (2013b) Arbuscular mycorrhizal fungi enhance both absorption and stabilization of Cd by Alfred stonecrop (Sedum alfredii Hance) and perennial ryegrass (Lolium perenne L.) in a Cd-contaminated acidic soil. Chemosphere 93(7):1359–1365 Igamberdiev AU, Eprintsev AT (2016) Organic acids: the pools of fixed carbon involved in redox regulation and energy balance in higher plants. Front Plant Sci 7:1042 Ismael MA, Elyamine AM, Moussa MG, Cai M, Zhao X, Hu C (2019) Cadmium in plants: uptake, toxicity, and its interactions with selenium fertilizers. Metallomics 11(2):255–277

6 Exploitation of Arbuscular Mycorrhizal (AM) Fungi as a Sustainable …

165

Jali P, Pradhan C, Das AB (2016) Effects of cadmium toxicity in plants: a review article. Scholars Acad J Biosci 4:1074–1081 Jalmi SK, Bhagat PK, Verma D, Noryang S, Tayyeba S, Singh K, Sharma D, Sinha AK (2018) Traversing the links between heavy metal stress and plant signaling. Front Plant Sci 9:12 Jankong P, Visoottiviseth P (2008) Effects of arbuscular mycorrhizal inoculation on plants growing on arsenic contaminated soil. Chemosphere 72(7):1092–1097 Janouškova M, Pavlíková D, Macek T, Vosátka M (2005) Arbuscular mycorrhiza decreases cadmium phytoextraction by transgenic tobacco with inserted metallothionein. Plant Soil 272(1):29–40 Jia D, Li Y, Hao LIC (2012) Advances in metallothionein studies in forest trees. Plant Omics J 5:46–51 Jia X, Zhao Y, He Y, Chang Y (2018) Glomalin-related soil protein in the rhizosphere of Robinia pseudoacacia L. seedlings under higher air temperature combined with Cd-contaminated soil. Eur J Soil Sci 69(4):634–645 Jia X, Zhao Y, Liu T, Huang S, Chang Y (2016) Elevated CO2 increases glomalin-related soil protein (GRSP) in the rhizosphere of Robinia pseudoacacia L. seedlings in Pb-and Cd-contaminated soils. Environ Pollut 218:349–357 Jiang QY, Zhuo F, Long SH, Zhao HD, Yang DJ, Ye ZH, Li S, Jing YX (2016) Can arbuscular mycorrhizal fungi reduce Cd uptake and alleviate Cd toxicity of Lonicera japonica grown in Cd-added soils? Sci Rep 6:21805 Jones DL, Dennis PG, Owen AG, van Hees PAW (2003) Organic acid behavior in soilsmisconceptions and knowledge gaps. Plant Soil 248(1):31–41 Jung C, Maeder V, Funk F, Frey B, Sticher H, Frossard E (2003) Release of phenols from Lupinus albus L. roots exposed to Cu and their possible role in Cu detoxification. Plant Soil 252(2):301–312 Kamran M, Malik Z, Parveen A, Zong Y, Abbasi GH, Rafiq MT, Shaaban M, Mustafa A, Bashir S, Rafay M, Mehmood S, Ali M (2019) Biochar alleviates Cd phytotoxicity by minimizing bioavailability and oxidative stress in pak choi (Brassica chinensis L.) cultivated in Cd-polluted soil. J Environ Manage 250:109500 Kaur H, Garg N (2017) Recent perspectives on cross talk between cadmium, zinc, and arbuscular mycorrhizal fungi in plants. J Plant Growth Regul 37:1–14 Kaznina NM, Titov AF, Batova YV, Laidinen GF (2014) The resistance of plants Setaria veridis (L.) Beauv. to the influence of cadmium. Biol Bull 41:428–433 Khan AG (2006) Mycorrhizoremediation—an enhanced form of phytoremediation. J Zhejiang Univ Sci B 7(7):503–514 Khan S, Munir S, Sajjad M, Li G (2016a) Urban park soil contamination by potentially harmful elements and human health risk in Peshawar City, Khyber Pakhtunkhwa, Pakistan. J Geochem Explor 165:102–110 Khan A, Khan S, Alam M, Khan MA, Aamir M, Qamar Z, Rehman ZU, Perveen S (2016b) Toxic metal interactions affect the bioaccumulation and dietary intake of macro-and micro-nutrients. Chemosphere 146:121–128 Khan A, Khan S, Khan MA, Qamar Z, Waqas M (2015) The uptake and bioaccumulation of heavy metals by food plants, their effects on plants nutrients, and associated health risk: a review. Environ Sci Pollut Res Int 22(18):13772–13799 Khan MA, Khan S, Khan A, Alam M (2017) Soil contamination with cadmium, consequences and remediation using organic amendments. Sci Total Environ 601–602:1591–1605 Khan S, Rehman S, Khan AZ, Khan MA, Shah MT (2010) Soil and vegetables enrichment with heavy metals from geological sources in Gilgit, Northern Pakistan. Ecotoxicol Environ Saf 73(7):1820–1827 Kistner C, Winzer T, Pitzschke A, Mulder L, Sato S, Kaneko T, Tabata S, Sandal N, Stougaard J, Webb KJ, Szczyglowski K, Parniske M (2005) Seven Lotus japonicus genes required for transcriptional reprogramming of the root during fungal and bacterial symbiosis. Plant Cell 17(8):2217–2229

166

H. Kaur et al.

Krishnamoorthy R, Kim CG, Subramanian P, Kim KY, Selvakumar G, Sa TM (2015) Arbuscular mycorrhizal fungi community structure, abundance and species richness changes in soil by different levels of heavy metal and metalloid concentration. PLoS ONE 10(6):e0128784 Kudoyarova GR, Dodd IC, Veselov DS, Rothwell SA, Veselov SY (2015) Common and specific responses to availability of mineral nutrients and water. J Exp Bot 66(8):2133–2144 Lambais MR (2006) Unraveling the signaling and signal transduction mechanisms controlling arbuscular mycorrhiza development. Scientia Agricola 63(4):405–413 Lanfranco L, Bolchi A, Ros EC, Ottonello S, Bonfante P (2002) Differential expression of a metallothionein gene during the presymbiotic versus the symbiotic phase of an arbuscular mycorrhizal fungus. Plant Physiol 130(1):58–67 Le GH, Philippe F, Domon J-M, Gillet F, Pelloux J, Rayon C (2015) Cell wall metabolism in response to abiotic stress. Plants 4:112–166 Li LS, Meng YP, Cao QF, Yang YZ, Wang F, Jia SH, Wu SB, Liu XG (2016) Type 1 metallothionein (ZjMT) is responsible for heavy metal tolerance in Ziziphus jujuba. Biochemistry 81:565–573 Li Y, Peng J, Shi P, Zhao B (2009) The effect of Cd on mycorrhizal development and enzyme activity of Glomus mosseae and Glomus intraradices in Astragalus sinicus L. Chemosphere 75(7):894–899 Liang CC, Li T, Xiao YP, Liu MJ, Zhang HB, Zhao ZW (2009) Effects of inoculation with arbuscular mycorrhizal fungi on maize grown in multi-metal contaminated soils. Int J Phytorem 11(8):692– 703 Liao JP, Lin XG, Cao ZH, Shi YQ, Wong MH (2003) Interactions between arbuscular mycorrhizae and heavy metals under sand culture experiment. Chemosphere 50:847–853 Liao M, Xie XM (2004) Cadmium release in contaminated soils due to organic acids. Pedosphere 14(2):223–228 Lin Q, Chen YX, Chen HM, Zheng CM (2003) Study on chemical behavior of root exudates with heavy metals. Plant Nutrition Fertilizer Sci 9:425–431 Liu H, Yuan M, Tan SY, Yang XP, Lan Z, Jiang QY, Ye ZH, Jing YX (2015) Enhancement of arbuscular mycorrhizal fungus (Glomus versiforme) on the growth and Cd uptake by Cd-hyperaccumulator Solanum nigrum. Appl Soil Ecol 89:44–49 Liu T, Liu SY, Guan H, Ma LG, Chen ZL, Gu HY, Qu LJ (2009) Transcriptional profiling of Arabidopsis seedlings in response to heavy metal lead (Pb). Environ Experimental Botany 67(2):377–386 Liu YG, Feng BY, Fan T, Pan C, Peng LJ (2008) Study on the biosorption of heavy metals by fungi. J Hunan Univ 35(1):71–74 Long LK, Yao Q, Guo J, Yang RH, Huang YH, Zhu HH (2010) Molecular community analysis of arbuscular mycorrhizal fungi associated with five selected plant species from heavy metal polluted soils. Eur J Soil Biol 46(5):288–294 Lopez-Bucio J, Nieto-Jacobo MF, Ramırez-Rodriguez V, Herrera-Estrella L (2000) Organic acid metabolism in plants: from adaptive physiology to transgenic varieties for cultivation in extreme soils. Plant Sci 160(1):1–13 Luo H, Li H, Zhang X, Fu J (2011) Antioxidant responses and gene expression in perennial ryegrass (Lolium perenne L.) under cadmium stress. Ecotoxicology 20(4):770–778 Lux A, Martinka M, Vaculı KM, White PJ (2011) Root responses to cadmium in the rhizosphere: a review. J Exp Bot 62(1):21–37 Ma JF, Ueno D, Zhao FJ, Mcgrath SP (2005) Subcellular localisation of Cd and Zn in the leaves of a Cd-hyperaccumulating ecotype of Thlaspi caerulescens. Planta 220:731–736 Malekzadeh E, Aliasgharzad N, Majidi J, Aghebati-Maleki L, Abdolalizadeh J (2016) Cd-induced production of glomalin by arbuscular mycorrhizal fungus (Rhizophagus irregularis) as estimated by monoclonal antibody assay. Environ Sci Pollut Res 23(20):20711–20718 Manchanda G, Garg N (2007) Endomycorrhizal and rhizobial symbiosis: how much do they share? J Plant Interactions 2(2):79–88

6 Exploitation of Arbuscular Mycorrhizal (AM) Fungi as a Sustainable …

167

Martins RMS, Melloni R, Melloni EGP (2017) Crescimento micelial de fungos micorrízicos arbusculares e formação de micorriza em solo contaminado por cádmio. Scientia Agraria 18:48–60 Meier S, Borie F, Bolan N, Cornejo P (2012) Phytoremediation of metal-polluted soils by arbuscular mycorrhizal fungi. Crit Rev Environ Sci Technol 42(7):741–775 Melo CD, Luna S, Krüger C, Walker C, Mendonça D, Fonseca MAC, Jaizme-Vega M, Machado AC (2017) Arbuscular mycorrhizal fungal community composition associated with Juniperus brevifolia in native Azorean forest. Acta Oecologica 79:48–61 Mendoza-Cózatl DG, Jobe TO, Hauser F, Schroeder JI (2011) Long-distance transport, vacuolar sequestration, tolerance, and transcriptional responses induced by cadmium and arsenic. Curr Opin Plant Biol 14(5):554–562 Miransari M (2010) Contribution of arbuscular mycorrhizal symbiosis to plant growth under different types of soil stress. Plant Biol 12(4):563–569 Miransari M (2012) Signaling molecules in the Arbuscular Mycorrhizal Fungi. In: Biotechnology of fungal genes. CRC Press, Boca Raton, pp 310–319 Mishra A, Bhattacharya A, Mishra N (2019) Mycorrhizal symbiosis: an effective tool for metal bioremediation. In: New and future developments in microbial biotechnology and bioengineering, pp 113–128 Mohanta TK, Bae H (2015) Functional genomics and signaling events in mycorrhizal symbiosis. J Plant Interactions 10(1):21–40 Moreira FMDS, Ferreira PAA, Vilela LAF, Carneiro MAC (2015) Symbioses of plants with Rhizobia and Mycorrhizal Fungi in heavy metal-contaminated tropical soils. In: Heavy metal contamination of soils. Springer, Switzerland, pp 215–243 Nayuki K, Chen B, Ohtomo R, Kuga Y (2014) Cellular imaging of cadmium in resin sections of arbuscular mycorrhizas using synchrotron micro X-ray fluorescence. Microbes Environ 29(1):60– 66 Nazar R, Iqbal N, Masood A, Khan MIR, Syeed S, Khan NA (2012) Cadmium toxicity in plants and role of mineral nutrients in its alleviation. Am J Plant Sci 3:1476–1489 Nonomura N, Kawada Y, Minamiya Y, Hayakawa H, Fukuda T, Kang Y, Sakurai K (2011) Molecular identification of arbuscular mycorrhizal fungi colonizing Athyrium yokoscense of the Ikuno mine site, Japan. J Jpn Botany 86(2):73–81 Noor W, Umar S, Mir MY, Shah D, Majeed G, Hafeez S, Yaqoob S, Gulzar A, Kamili AN (2018) Effect of cadmium on growth, photosynthesis and nitrogen metabolism of crop plants. J Res Dev 18:100–106 Oehl F, Laczko E, Bogenrieder A, Stahr K, Bösch R, Heijden MVD, Sieverding E (2010) Soil type and land use intensity determine the composition of arbuscular mycorrhizal fungal communities. Soil Biol Biochem 42(5):724–738 Oldroyd GED (2013) Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nat Rev Microbiol 11(4):252–263 Osmolovskaya NG, Kuchaeva LN, Novak VA (2007) Role of organic acids in the formation of the ionic composition in developing glycophyte leaves. Russ J Plant Physiol 54(3):336–342 Pal S, Singh HB, Farooqui A (2017) Diversity of arbuscular mycorrhiza associated with long term wastewater irrigation in the peri-urban soil of Varanasi. Int J Agric Environ Biotechnol 10(6):779 Pan Y, Zhu M, Wang S, Ma G, Huang X, Qiao C, Wang R, Xu X, Liang Y, Lu K, Li J, Qu C (2018) Genome-wide characterization and analysis of metallothionein family genes that function in metal stress tolerance in Brassica napus L. Int J Mol Sci 19(8):2181 Park H, Lee EH, Ka KH, Eom AH (2016) Community structures of arbuscular mycorrhizal fungi in soils and plant roots inhabiting abandoned mines of Korea. Mycobiology 44(4):277–282 Park J, Song WY, Ko D, Eom Y, Hansen TH, Schiller M, Lee TG, Martinoia E, Lee Y (2012) The phytochelatin transporters AtABCC1 and AtABCC2 mediate tolerance to cadmium and mercury. Plant J 69(2):278–288 Parniske M (2004) Molecular genetics of the arbuscular mycorrhizal symbiosis. Curr Opin Plant Biol 7(4):414–421

168

H. Kaur et al.

Paszkowski U (2006) A journey through signaling in arbuscular mycorrhizal symbioses. New Phytol 172(1):35–46 Pawlowska TE, Charvat I (2004) Heavy-metal stress and development patterns of arbuscular mycorrhizal fungi. Appl Environ Microbiol 70(11):6643–6649 Rask KA, Johansen JL, Kjøller R, Ekelund F (2019) Differences in arbuscular mycorrhizal colonisation influence cadmium uptake in plants. Environ Exp Bot 162:223–229 Raza AH, Madiha K, Shiva N, Zahid Z, Zahra N, Sharif R, Hasanuzzaman M (2020) Phytoremediation of cadmium: physiological, biochemical, and molecular mechanisms. Biology 9(7):177 Redecker D, Schüßler A, Stockinger H, Stürmer SL, Morton JB, Walker C (2013) An evidence-based consensus for the classification of arbuscular mycorrhizal fungi (Glomeromycota). Mycorrhiza 23:515–531 Requena N, Breuninger M (2004) The old Arbuscular mycorrhizal symbiosis in the light of the molecular era. In: Progress in plant botany. Springer, Heidelberg, pp 323–356 Requena N, Jeffries P, Barea JM (1996) Assessment of natural mycorrhizal potential in a desertified semiarid ecosystem. Appl Environ Microbiol 62(3):842–847 Requena N, Serrano E, Ocón A, Breuninger M (2007) Plant signals and fungal perception during arbuscular mycorrhizal establishment. Phytochemistry 68(1):33–40 Rizwan M, Ali S, Qayyum MF, Ibrahim M, Zia-ur-Rehman M, Abbas T, Ok YS (2016) Mechanisms of biochar-mediated alleviation of toxicity of trace elements in plants: a critical review. Environ Sci Pollut Res 23:2230–2248 Rucinska-Sobkowiak R (2016) Water relations in plants subjected to heavy metal stresses. Acta Physiologiae Plantarum 38 Saifullah Javed H, Naeem A, Rengel Z, Dahlawi S (2016) Timing of foliar Zn application plays a vital role in minimizing Cd accumulation in wheat. Environ Sci Pollution Res 23(16):16432–16439 Saleh M, Al-Garni S (2006) Increased heavy metal tolerance of cowpea plants by dual inoculation of an arbuscular mycorrhizal fungi and nitrogen-fixer rhizobium bacterium. Afr J Biotech 5:132–144 Sanchez-Castro I, Gianinazzi-Pearson V, Cleyet-Marel JC, Baudoin E, Tuinen DV (2017) Glomeromycota communities survive extreme levels of metal toxicity in an orphan mining site. Sci Total Environ 598:121–128 Sanjaya P, Hsiao P, Su R, Ko S (2008) Overexpression of Arabidopsis thaliana tryptophan synthase beta 1 (AtTSB1) in Arabidopsis and tomato confers tolerance to cadmium stress. Plant Cell Environ 31(8):1074–1085 Saraswat S, Rai JPN (2011) Mechanism of metal tolerance and detoxification in mycorrhizal fungi. In: Biomanagement of metal-contaminated soils. Springer, Netherlands, pp 225–240 Schwab AP, He YH, Banks MK (2005) The influence of organic ligands on the retention of lead in soil. Chemosphere 61(6):856–866 Seth CS, Remans T, Keunen E, Jozefczak M, Gielen H, Opdenakker K, Weyens N, Vangronsveld J, Cuypers A (2012) Phytoextraction of toxic metals: a central role for glutathione. Plant Cell Environ 35(2):334–346 Shah MT, Begum S, Khan S (2010) Pedo and biogeochemical studies of mafic and ultramfic rocks in the Mingora and Kabal areas, Swat, Pakistan. Environ Earth Sci 60(5):1091–1102 Shahabivand S, Aliloo AA, Maivan HZ (2016) Wheat biochemical response to cadmium toxicity under Funneliformis mosseae and Piriformospora indica symbiosis. Botanica Lithuanica 22(2):169–177 Shahabivand S, Maivan H, Goltapeh E, Sharifi M, Aliloo AA (2012) The effects of root endophyte and arbuscular mycorrhizal fungi on growth and cadmium accumulation in wheat under cadmium toxicity. Plant Physiol Biochem 60:53–58 Shi W, Zhang Y, Chen S, Polle A, Rennenberg H, Luo ZB (2019) Physiological and molecular mechanisms of heavy metal accumulation in nonmycorrhizal versus mycorrhizal plants. Plant Cell Environ 42:1087–1103 Shi Z, Li K, Zhu X, Wang F (2020) The worldwide leaf economic spectrum traits are closely linked with mycorrhizal traits. Fungal Ecol 43:100877

6 Exploitation of Arbuscular Mycorrhizal (AM) Fungi as a Sustainable …

169

Sidhu GPS, Bali AS, Bhardwaj R (2019) Use of fungi in mitigating cadmium toxicity in plants. In: Cadmium toxicity and tolerance in plants. Academic Press, Cambridge, pp 397–426 Singh G, Pankaj U, Chand S, Verma RK (2019) Arbuscular mycorrhizal fungi assisted phytoextraction of toxic metals by Zea mays L. from tannery sludge. Soil Sediment Contamination 28(8):729–746 Singh PK, Singh M, Tripathi BN (2012) Glomalin: an arbuscular mycorrhizal fungal soil protein. Protoplasma 250:663–669 Siqueira J, Soares C, Santos JD, Schneider J, Carneiro M (2007) Micorrizas e degradação do solo: caracterização, efeitos e ação recuperadora. Tópicos Em Ciência Do Solo 5:219–306 Smolders E, Mertens J (2013) Cadmium. In: Heavy metals in soils—trace metals and metalloids in soils and their bioavailability. Springer, Dordrecht, pp 283–299 Spatafora JW, Chang Y, Benny GL, Lazarus K, Smith ME, Berbee ML, Bonito G, Corradi N, Grigoriev IV, Gryganskyi A, James TY, O’Donnell K, Roberson RW, Taylor TN, Uehling J, Vilgalys R, White MM, Stajich JE (2016) A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data. Mycologia 108:1028–1046 Sprynskyy M, Kowalkowski T, Tutu H, Cozmuta LM, Cukrowska EM, Buszewski B (2011) The adsorption properties of agricultural and forest soils towards heavy metal ions (Ni, Cu, Zn and Cd). Soil Sediment Contamination 20(1):12–29 Stommel M, Mann P, Franken P (2001) EST-library construction using spore RNA of the arbuscular mycorrhizal fungus Gigaspora rosea. Mycorrhiza 10(6):281–285 Stürmer SL, Bever JD, Morton JB (2018) Biogeography of arbuscular mycorrhizal fungi (Glomeromycota): a phylogenetic perspective on species distribution patterns. Mycorrhiza 28(7):587– 603 Sun J, Miller JB, Granqvist E, Wiley-lil A, Gobbato E, Maillet F, Cottaz S, Samain E, Venkateshwaran M, Fort S, Morris JR, Ane J-M, Denarie J, Oldroyd GED (2015) Activation of symbiosis signaling by arbuscular mycorrhizal fungi in legumes and rice. Plant Cell 27(3):823–838 Sun Y, Zhang X, Wu Z, Hu Y, Wu S, Chen B (2016) The molecular diversity of arbuscular mycorrhizal fungi in the arsenic mining impacted sites in Hunan province of China. J Environ Sci 39:110–118 Symanczik S, Błaszkowski J, Koegel S, Boller T, Wiemken A, Al-Yahya’Ei MN (2014) Isolation and identification of desert habituated arbuscular mycorrhizal fungi newly reported from the Arabian Peninsula. J Arid Land 6(4):488–497 Tran TA, Popova LP (2013) Functions and toxicity of cadmium in plants: recent advances and future prospects. Turk J Bot 37(1):1–13 Tsai SM, Phillips DA (1991) Flavonoids released naturally from alfalfa promote development of symbiotic glomus spores in vitro. Appl Environ Microbiol 57(5):1485–1488 Turnau K, Ryszka P, Gianinazzi-Pearson V, van Tuinen D (2001) Identification of arbuscular mycorrhizal fungi in soils and roots of plants colonizing zinc wastes in Southern Poland. Mycorrhiza 10:169–174 Van-der Putten WH, Klironomos JN, Wardle DA (2007) Microbial ecology of biological invasions. ISME J 1:28–37 Vatamaniuk OK, Bucher EA, Ward JT, Rea PA (2001) A new pathway for heavy metal detoxification in animals: phytochelatin synthase is required for cadmium tolerance in Caenorhabditis elegans. J Biol Chem 276(24):20817–20820 Vilela LAF, Barbosa MV (2019) Contribution of Arbuscular mycorrhizal fungi in promoting cadmium tolerance in plants. In: Cadmium tolerance in plants: agronomic, molecular, signaling, and omic approaches. Elsevier, pp 553–856 Vivas A, Barea JM, Azcon R (2005) Interactive effect of Brevibacillus brevis and Glomus mosseae both isolated from Cd contaminated soil, on plant growth, physiological mycorrhizal fungal characteristics and soil enzymatic activities in Cd polluted soils. Environ Pollut 134(2):257–266 Wang F (2017) Occurrence of arbuscular mycorrhizal fungi in mining-impacted sites and their contribution to ecological restoration: mechanisms and applications. Crit Rev Environ Sci Technol 47(20):1–57

170

H. Kaur et al.

Wang F, Liu X, Shi Z, Tong R, Adams CA, Shi X (2016) Arbuscular mycorrhizae alleviate negative effects of zinc oxide nanoparticle and zinc accumulation in maize plants—a soil microcosm experiment. Chemosphere 147:88–97 Wang Q, Wang W, He X, Zhang W, Song K, Han S (2015) Role and variation of the amount and composition of glomalin in soil properties in farmland and adjacent plantations with reference to a primary forest in North-Eastern China. PloS one 10(10) Wei Y, Chen Z, Wu F, Li J, Shangguan Y, Li F, Zeng QR, Hou H (2015) Diversity of arbuscular mycorrhizal fungi associated with a Sb accumulator plant, Ramie (Boehmeria nivea), in an active Sb mining. J Microbiol Biotechnol 25:1205–1215 White PJ, Brown PH (2010) Plant nutrition for sustainable development and global health. Ann Bot 105(7):1073–1080 Whitfield L, Richards AJ, Rimmer DL (2004) Relationships between soil heavy metal concentration and mycorrhizal colonisation in Thymus polytrichus in Northern England. Mycorrhiza 14(1):55– 62 Wu Z, McGrouther K, Huang J, Wu P, Wu W, Wang H (2014) Decomposition and the contribution of glomalin-related soil protein (GRSP) in heavy metal sequestration: field experiment. Soil Biol Biochem 68:283–290 Xin J, Huang B, Dai H, Liu A, Zhou W, Liao K (2014) Characterization of cadmium uptake, translocation, and distribution in young seedlings of two hot pepper cultivars that differ in fruit cadmium concentration. Environ Sci Pollut Res Int 21(12):7449–7456 Xu XY, McGrath SP, Zhao FJ (2007) Rapid reduction of arsenate in the medium mediated by plant roots. New Phytol 176(3):590–599 Xu ZM, Li QS, Yang P, Ye HJ, Chen ZS, Guo SH, Wang LL, He BY, Zeng EY (2017) Impact of osmoregulation on the differences in Cd accumulation between two contrasting edible amaranth cultivars grown on Cd-polluted saline soils. Environ Pollut 224:89–97 Yang RH, Yao Q, Guo J, Liangkun L, Yongheng H, Honghui Z (2010) Influence of P and Cd on the spore germination, hyphal growth and polyphosphate accumulation in extraradical hyphae of Glomus intraradices. Mycosystema 29(3):421–428 Yang Y, Song Y, Scheller HV, Ghosh A, Ban Y, Chen H, Tang M (2015) Community structure of arbuscular mycorrhizal fungi associated with Robinia pseudoacacia in uncontaminated and heavy metal contaminated soils. Soil Biol Biochem 86:146–158 Yates EM (1992) The world needs cadmium—a Miner’s viewpoint. In: Cadmium, vol 92. Cadmium Association, London. Technical notes on cadmium. Cadmium production, properties and uses, pp 1–7 Zarei M, Hempel S, Wubet T, Schafer T, Savaghebi G, Jouzani GS, Nekouei MK, Buscot F (2010) Molecular diversity of arbuscular mycorrhizal fungi in relation to soil chemical properties and heavy metal contamination. Environ Pollut 158(8):2757–2765 Zhan F, Li B, Jiang M, Li T, He Y, Li Y, Wang Y (2019) Effects of arbuscular mycorrhizal fungi on the growth and heavy metal accumulation of bermudagrass [Cynodon dactylon (L.) Pers.] grown in a lead-zinc mine wasteland. Int J Phytoremediation 21(9):849–856 Zhang F, Liu M, Li Y, Che Y, Xiao Y (2019a) Effects of arbuscular mycorrhizal fungi, biochar and cadmium on the yield and element uptake of Medicago sativa. Sci Total Environ 655:1150–1158 Zhang XF, Hu ZH, Yan TX, Lu RR, Peng CL, Li SS, Jing YX (2019b) Arbuscular mycorrhizal fungi alleviate Cd phytotoxicity by altering Cd subcellular distribution and chemical forms in Zea mays. Ecotoxicol Environ Saf 171(4):352–360 Zhang HH, Tang M, Chen H, Zheng C, Niu ZC (2010) Effect of inoculation with AM fungi on lead uptake, translocation and stress alleviation of Zea mays L. seedlings planting in soil with increasing lead concentrations. Eur J Soil Biol 46(5):306–311 Zhao H, Li XZ, Zhang Z, Zhao Y, Yang J, Zhu Y (2017) Species diversity and drivers of arbuscular mycorrhizal fungal communities in a semi-arid mountain in China. PeerJ 5 Zhu XF, Zheng C, Hu YT, Jiang T, Liu Y, Dong NY, Yang JL, Zheng SJ (2011) Cadmiuminduced oxalate secretion from root apex is associated with cadmium exclusion and resistance in Lycopersicon esulentum. Plant Cell Environ 34(7):1055–1064

6 Exploitation of Arbuscular Mycorrhizal (AM) Fungi as a Sustainable …

171

Ziller A, Fraissinet-Tachet L (2018) Metallothionein diversity and distribution in the tree of life: a multifunctional protein. Metallomics 10(11):1549–1559 Zitka O, Krystofova O, Sobrova P, Adam V, Zehnalek J, Beklova M, Kizek R (2011) Phytochelatin synthase activity as a marker of metal pollution. J Hazard Mater 192(2):794–800

Chapter 7

Medicinal and Aromatic Plant Species with Potential for Remediation of Metal(loid)-Contaminated Soils Katarína Král’ová and Josef Jampílek

Abstract High contamination of soils with heavy metals, mainly due to increasing anthropogenic activity, significantly contributed to the reduction of soil fertility worldwide and has an adverse impact on crop production and non-target organisms. In addition, toxic metals accumulating in the consumable parts of plants in quantities exceeding permissible levels pose a serious risk to human and animal health. Phytoremediation presents an environment-friendly green approach to clean areas contaminated with toxic metals. Metal-tolerant medicinal and aromatic plants have been found to be suitable candidates for this purpose because they can grow on metal-contaminated soils without significant adverse effects on plants, whereas the metal-induced stress has a positive effect on the quantity and possibly also on the quality of the essential oil without translocation of metals into essential oil, which ensures an economic profit of such a solution. In this chapter, attention is focused on the impact of heavy metals on the growth and physiological and biochemical characteristics of plants, classification of plants in terms of metal accumulation capacity, phytoremediation techniques and the impact of soil metal contamination on the yield of essential oils of medicinal and aromatic plants. The potential of individual medicinal and aromatic plants (herbs, succulents, shrubs and trees) for decontamination of soils polluted with heavy metals by phytoextraction or phytostabilization and the impact of microorganisms and chelating agents on the phytoremediation efficiency is discussed. The pharmacological activities of some medicinal shrubs and trees are briefly mentioned as well. Keywords Essential oils · Heavy metals · Hyperaccumulators · Medicinal and aromatic plants · Metal accumulation · Metalloids · Oxidative stress · Phytoremediation · Phytostabilization K. Král’ová (B) Institute of Chemistry, Faculty of Natural Sciences, Comenius University, Ilkoviˇcova 6, Bratislava 842 15, Slovakia e-mail: [email protected] J. Jampílek Department of Analytical Chemistry, Faculty of Natural Sciences, Comenius University, Ilkoviˇcova 6, Bratislava 842 15, Slovakia © The Author(s), under exclusive license to Springer Nature Switzerland AG 2022 T. Aftab (ed.), Sustainable Management of Environmental Contaminants, Environmental Contamination Remediation and Management, https://doi.org/10.1007/978-3-031-08446-1_7

173

174

K. Král’ová and J. Jampílek

7.1 Introduction The rapid growth of industrial production and overuse of fertilizers and pesticides in agriculture, especially in the twentieth century, pronouncedly contributed to soil degradation, reduction of its fertility and increased concentrations of toxic metals in soils. In addition, significant soil contamination by metals and metalloids is associated with natural processes, including mineral weathering, erosion or volcanic eruptions (Su et al. 2014; Saxena et al. 2019; Kumar et al. 2021). Maps of heavy metals (HM) in the topsoil of the European Union showed higher concentrations of toxic metals (Hg, Cd, As, Pb) for historical and recent industrial and mining areas indicating adverse impact of anthropogenic activities on soil quality (Tóth et al. 2016). Due to high soil HM concentrations in the vicinity of active as well as old abandoned mines, lands near steelworks, and smelting or electroplating factories and industrial effluent discharges only HM-tolerant plant species can grow on these areas (Pratas et al. 2013; Frutos et al. 2017; Kumar et al. 2021; Pasricha et al. 2021); however, after uptake of higher amounts of toxic metals from soil in bioavailable form, some metalaccumulating tolerant plant species can store them in aerial tissues, which presents a risk for animal and human population consuming these plants; high concentrations of HM in environmental matrices also pose a great risk for non-target organisms (Ali and Khan 2018; Kráˇlová et al. 2019; Kumar et al. 2020; Wang et al. 2020; Alengebawy et al. 2021). In contrast to organic pollutants, HM cannot be degraded, and their toxicity can be reduced only by changing their oxidation state to less toxic form, by formation of complexes with chelate-forming agents or by immobilization preventing their migration in soils, subsequent entry in watercourses and lakes, and ultimately their entry in the food chain (Ali and Khan 2018; Ali et al. 2019).

Phytovolatilization Phytodegradation (Phytotransformation)

Phytoextraction (Phytoaccumulation)

Rhizodegradation (Phytostimulation) Phytostabilization Rhizofiltration Hydraulic control Fig. 7.1 Phytoremediation techniques

7 Medicinal and Aromatic Plant Species with Potential for Remediation …

175

Essential metals, similarly to toxic metals, which are not involved in plant metabolism, exhibit phytotoxicity when applied in excess whether in bulk or nanoform and show adverse effect on plant growth and development due to induction of reactive oxygen species (ROS) causing oxidative stress (Masaroviˇcová et al. 2010a, 2014; Masaroviˇcová and Kráˇlová 2012; Jampílek and Kráˇlová 2019a; Kráˇlová et al. 2019, 2021; Kráˇlová and Jampílek 2021). Therefore, remediation of HMcontaminated soils is highly desirable. For this purpose HM-tolerant plants are suitable, whether those showing ability hyperaccumulate HM in levels exceeding by two order or more the accumulated HM concentrations compared to non-accumulating plants or fast-growing plants with a huge root system, which despite their lower HM accumulating ability can translocate significant HM amounts to rich aerial biomass resulting in soil decontamination (Masaroviˇcová et al. 2010b; Masaroviˇcová and Kráˇlová 2018; Saxena et al. 2019; Kumar et al. 2021). These plants can withstand to metal-induced stress by effective defense system able to increase biosynthesis of metal-chelating biomolecules, such as phytochelatins or metallothioneins and effective antioxidants, whether enzymatic or non-enzymatic (Verbruggen et al. 2009; Singh and Santal 2015; Panda et al. 2016; Masaroviˇcová et al. 2019; Talukder et al. 2020; Kráˇlová and Jampílek 2021; Ozyigit et al. 2021; Varma et al. 2021). Medicinal and aromatic plants (MAPs) have been used by the human population for medicinal purposes and in cosmetic preparations since ancient times, during the centuries BC (Masaroviˇcová and Kráˇlová 2007; Masaroviˇcová et al. 2019). At that time, based on experience the humans used for therapy indigenous plants from the surrounding nature, whereby the seeds, dried roots and leaves as well as extracts of plant organs and bark were the most popular (Alamgir 2020). Receipts dealing with healing properties of plants were recorded already in Sumerian tablets (300 BC), and more than 850 plants showing healing effects were described in Ebers Papyrus (1500 BC) (Ahn 2017). Beside ancient Egypt, the use of plants or their essential oils was widely used in traditional medicine also in China, India, or Persia (Schnaubelt 2005; Morgan 2021). Dioscorides (40–90 AD), a Greek physician, botanist and pharmacologist in his work De materia medica published more than 1000 recipes for medicines prepared from >600 medicinal plants (Ahn 2017). During antique and in Middle Age the widespread use of medicinal plants by humans continued, and current knowledge concerning healing effects of about 600 medicinal plants summarized John Gerarde in 1597 in his work The Herball or Generall Historie of Plantes (Singer 1923). Some medicinal plants containing volatile secondary metabolites with distinct fragrance were frequently used as ritual plants in religious ceremonies (Yaniv and Dudai 2014; Dafni et al. 2020). The use of biochemical analysis from nineteenth century pronouncedly contributed to discovery of pharmacologically active metabolites of MAPs and increased interest in their use in pharmacy. Since then, several secondary metabolites of medicinal plants have served as leads for development of new drugs (Jampílek 2017; Zhang and Jampílek 2017; Dolab et al. 2018; Dehyab et al. 2020). Some aromatic substances produced by aromatic plants also show pharmacological activities (i.e., antioxidant. antimicrobial) and found application in culinary recipes as

176

K. Král’ová and J. Jampílek

well as in liqueur and food industries (Zhao et al. 2015; Bhavaniramya et al. 2019; Inoue et al. 2019; Amiri et al. 2020; Nieto 2020; Do Nascimento et al. 2020). According to the “Royal Botanic Gardens” (KEW, United Kingdom), in 2016 17,810 plant species were used for medicinal purposes, whereby for 30,000 plants their healing properties were recorded (Anonymus 2016). On the other hand, FAO in 2002 declared that even 50,000 plant species are used globally for therapy of various diseases (Schippmann et al. 2002). For healing properties of MAPs their secondary metabolites showing a wide scale of biological effects, including antioxidant, anti-inflammatory and anticancer activities, are responsible (Alamgir 2020; Aftab and Hakeem 2021; Husen 2022). In thirdworld countries, it is less expensive to use preparations prepared from medicinal plants as medicines than industrially produced medicines. However, also in developed countries is increasingly noticeable interest to take medicinal plants or their secondary metabolites in form of tea or dietary supplements (Miroddi et al. 2013; Matic et al. 2018; Saper 2021). In 2005, WHO published a global survey concerning national policy on traditional medicine and regulation of herbal medicines (WHO 2005) and in 2013 presented WHO Traditional medicine strategy 2014–2023 (WHO 2013). Regarding Covid-19 pandemics in last two years, the research focused also on the search of medicinal plants or their metabolites, which would be beneficial in the therapy of this viral disease (Khadka et al. 2021; Khan et al. 2021; Lim et al. 2021; Phumthum et al. 2021). Numerous secondary metabolites of MAPs exhibiting healing activities are situated in essential oils (EOs). Based on the findings that HM stress stimulates production of EO secondary metabolites and enhances EO yield (Lafmejani et al. 2018; Rezaizad et al. 2019; Shabbir et al. 2019; Gohari et al. 2020; Shahhoseini et al. 2020; Kráˇlová and Jampílek 2021) along with fact that EOs are frequently derived from wild growing plants, testing of EOs for the presence of toxic contaminants such as HM is inevitable. As predominant majority of the laboratory experiments performed in hydroponium or as pot experiments and field experiments showed that the presence of HM in the cultivation medium/substrate did not cause translocation of HM into EO in non-permissible toxic levels or HM content was below detection limit (Zheljazkov et al. 2006; Angelova et al. 2015; Kunwar et al. 2015; Sosa et al. 2016; Szakova et al. 2018; Angelova 2020; Raveau et al. 2021), the use of MAPs for phytoremediation of HM-polluted environmental matrices became also interesting from an economic point of view. Moreover, the residues of some medicinal plants grown on metal-contaminated sites can be used after recovery of EO for production of energy, biofuels or fibers (Saxena et al. 2019; Kumar et al. 2021). On the other hand, species suitable for phytostabilization can immobilize HM and prevent their migration in soil, considerably contributing to restoration of contaminated areas (Andreazza et al. 2015; Shackira and Puthur 2017; Rani et al. 2018; Masaroviˇcová et al. 2019). Improved phytoremediation effectiveness of MAPs can be achieved by inoculating them with suitable microorganisms, or application of amendments such as biochar or

7 Medicinal and Aromatic Plant Species with Potential for Remediation …

177

manure as well as with application of chelating agents such as 2,2' ,2'' ,2''' -(ethane-1,2diyldinitrilo)tetraacetic acid (EDTA), ethylenediamine-N,N ' -disuccinic acid (EDDS) or organic acids (citric acid (CA), tartaric acid, etc.) (Abbaslou et al. 2018; Saxena et al. 2019; Saffari and Saffari 2020; Ul Khair et al. 2020; Kumar et al. 2021; Li et al. 2021; Pasricha et al. 2021). The effectiveness of phytoremediation can be significantly increased also by using transgenic plants (Fasani et al. 2018; Gunarathne et al. 2019; Prasad 2019; Boechat et al. 2021; Ozyigit et al. 2021). In this chapter, attention is focused on the impact of heavy metals on the growth and physiological and biochemical characteristics of plants, classification of plants in terms of metal accumulation capacity, phytoremediation techniques and the impact of soil metal contamination on the yield of EOs of MAPs. The potential of individual MAPs (herbs, succulents, shrubs and trees) for decontamination of soils polluted with heavy metals by phytoextraction or phytostabilization and the impact of microorganisms and chelating agents on the phytoremediation efficiency is discussed. The pharmacological activities of some medicinal shrubs and trees are briefly mentioned as well.

7.2 Impact of Heavy Metals on Growth and Physiological and Biochemical Characteristics of Plants Heavy metals are elements characterized by specific metal properties and a density >5 g/cm3 . In environmental chemistry, some metalloids, selenium and transition metals (lanthanides, actinides) are also considered HM, although Se density is only 4.8 g/cm3 (Duffus 2002; Emsley 2011; Rasic-Milutinovic and Jovanovic 2013; Vernon 2013). Some metals such as Zn, Cu, Fe, Mn, B, Mo and Ni, which are catalytic and structural cofactors in many enzymes, or are present in photosynthetic apparatus, are indispensable for healthy development and growth of plants (Maksymiec 1997; Yruela 2005, 2009; Broadley et al. 2007; Rout and Sahoo 2015; Shahzad et al. 2018; Shireen et al. 2018; Schmidt and Husted 2019; Rana et al. 2020). These metals when applied at optimal dose serve as essential micronutrients of plants and are used as nanofertilizers to ensure improved yield and nutritional quality of plants (Marschner 1995; IFA 2020a; Luo et al. 2020). Their beneficial impact is reflected in improved germination, enhanced content of photosynthetic pigments, improved photosynthesis, increased membrane stability and increased levels and activities of antioxidant enzymes resulting in improved plant growth and fitness (Masaroviˇcová and Kráˇlová 2017; Jampílek and Kráˇlová 2019b; Kráˇlová et al. 2021). Moreover, also application of some non-essential micronutrients from the group of HM such as Co (Marschner 1995; Akeel and Jahan 2020; IFA 2020a), Si (Luyckx et al. 2016; Souri et al. 2021) and Se (Hasanuzzaman et al. 2010; El-Ramady et al. 2016; IFA 2020b) can be favorable for plant growth. Deficiency in essential metals results in impaired plant growth and reduced productivity and nutritional quality of crops (Marschner 1995; Aftab and

178

K. Král’ová and J. Jampílek

Hakeem 2020; IFA 2020a). On the other hand, higher concentrations of these essential metal nutrients are phytotoxic, similarly to highly toxic effect of HM such as Cd, Hg and Pb. Higher concentrations of HM, whether in ionic or nanoform, induce oxida1 tive stress and generate reactive oxygen species (• OH, O•− 2 , O2 ) causing inhibition of photosynthetic electron transport as well as activity of many enzymes, including ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco), enhanced peroxidation of lipids resulting in the damage of cellular membranes and subsequent electrolyte leakage, oxidation of carbohydrates, denaturation of proteins and can damage DNA, resulting in impaired plant growth (Masaroviˇcová et al. 2010a; Fryzova et al. 2018; Berni et al. 2019; Kráˇlová et al. 2021). Therefore, plants developed defense strategies to cope with oxidative stress induced by HM, including increased biosynthesis of antioxidant enzymes, non-enzymatic antioxidants such as glutathione, enhanced synthesis of phytochelatins and metallothioneins as well as amino acid proline, whereby the metal excess in plants is sequestered primarily in vacuoles and stored in old leaves with reduced photosynthetic activity (Panda et al. 2016; Almehdi et al. 2019; Masaroviˇcová et al. 2019; Talukder et al. 2020; Kráˇlová et al. 2021). Increasing amounts of HM in environmental matrices due to anthropogenic activities such as mining, industrial activities, agriculture and intensive traffic have detrimental impact on soil quality resulting in adverse impact on plant growth, including growth of MAPs (Nagajyoti et al. 2010; Gonzalez-Valdez et al. 2016; Wang et al. 2017; Pirzadah et al. 2019; Charvalas et al. 2021; Pasricha et al. 2021). The plants can uptake HM only in bioavailable form, and increased levels of toxic metals in plant tissues, especially in photosynthesizing plant parts due to effective metal translocation from root to shoot, can adversely affect growth and development of plants (Masaroviˇcová et al. 2004, 2019; Masaroviˇcová et al. 2014; Kráˇlová et al. 2021). Negative impact of higher HM concentrations on growth of MAPs was observed as well (e.g., Masaroviˇcová et al. 2004; Kummerová et al. 2010; He et al. 2018a; Kovacik et al. 2018; Dinu et al. 2021; Kráˇlová and Jampílek 2021; Zarinkamar et al. 2021).

7.3 Classification of Plants from the Aspect of Metal Accumulation Ability From the aspect of plant strategies used for phytoremediation of metal-contaminated matrices characteristics as bioconcentration factor (BCF), biological accumulation factor (BAF) and translocation factor (TF) are decisive. BCF is defined as a ratio of metal concentration in root dry mass (d.m.; μg/g) to this in the soil (μg/g); BAF is evaluated as the ratio of metal concentration in shoot dry mass (μg/g) to this in the soil (μg/g) and TF is a ratio of the metal concentration in the shoot tissue to the metal concentration in the root tissue. Some researchers also evaluated bioconcentration factor for the whole plant as a ratio of metal concentration in plant dry mass to this in the soil (Tu and Ma 2002; Masaroviˇcová et al. 2010b; Kumar et al. 2021).

7 Medicinal and Aromatic Plant Species with Potential for Remediation …

179

Metallophytes, i.e., plants able to tolerate considerable amounts of HM and survive on HM-contaminated substrates can be classified as (a) metal indicators accumulating metals in above-ground parts using intracellular chelator for the binding of metals or store them in non-sensitive plant parts; accumulated metal concentrations correlate with metal concentration in soil and TF is ca. 1; (b) metal accumulators actively accumulating excess metal levels from the soil in the aboveground plant parts, mainly in leaves, without signs of phytotoxicity; and (c) metal excluders accumulating metals in their roots, whereby translocation of metals into shoots is inhibited via modifying the permeability of cell membranes and metal binding capacity of cell wall or by increased releasing of chelating compounds in exudates into soil (van der Ent et al. 2013; Saxena et al. 2019; Wójcik et al. 2017; Kumar et al. 2021; Pasricha et al. 2021). Metallophytes are plants suitable to be used for phytoremediation of HMcontaminated environmental matrices, whereby their phytoremediation efficiency can be pronouncedly improved by the presence of microorganisms (Khan et al. 2015; Ruscitti et al. 2017; Banarjee 2018; Saxena et al. 2019; Kumar et al. 2021; Li et al. 2021; Ozyigit et al. 2021; Pasricha 2021) or by application of various chelating agents such as EDTA, EDDS, CA and salicylic acid (Kráˇlová and Masaroviˇcová 2008; Sinhal et al. 2010; Cay et al. 2016; Chen et al. 2019; Saffari and Saffari 2020; Gul et al. 2021). Hyperaccumulators are plant species showing extreme appetite for toxic metals/metalloids and can accumulate in leaves 100–1000-fold higher metals/metalloids concentrations compared to those observed in non-accumulating closely related plant species; they achieve higher metal concentrations in the tissues compared to those occurring in the metal-polluted soil (Ghosh and Singh 2005; Lee 2013; Saxena et al. 2019). Hyperaccumulators are characterized with improved mobilization and uptake of metals by roots, increased xylem loading from roots to shoots and effective detoxification of metals in the shoots (Verbruggen et al. 2009; Masaroviˇcová et al. 2010b; Pasricha et al. 2021). Their uncommon metal-accumulating properties are associated with overexpression and regulation of genes coding transport systems common to non-hyperaccumulator plants (HM transporting ATPase) and transporters involved in sequestration of HM (ATP-binding cassette (ABC) transporters, cation diffusion facilitator transporters, HM ATPases transporters, etc.) and with overexpression of antioxidant genes (Pirzadah et al. 2019; Kumar et al. 2021; Dar et al. 2020; Kumar et al. 2021). The hormetic biphasic dose-dependent responses, i.e., stimulatory at exposure to low and inhibitory/toxic ones at exposure to high metal concentrations observed in several hyperaccumulating plant species, can be associated with the up- and down-regulation of adaptive mechanisms, particularly those, which are involved in antioxidative enzymatic processes (Calabrese and Agathokleous 2021). Mean metal concentrations in standard plants are 200 μg Mn/g, 50 μg Zn/g, 10 μg Cu/g, 1.5 μg Ni/g, 1.5 μg Cr/g, 1 μg Pb/g, 0.2 μg Co/g, 0.1 μg As/g, 0.05 μg Cd/g, 0.02 μg Tl/g and 0.02 μg Se/g (Markert 1994; Dunn 2007). On the other hand, hyperaccumulators were defined as plant species containing in the dry mass of their leaf tissues >100 μg/g Cd, Tl or Sr; >300 μg/g Co, Cu or Cr; >1000 μg/g Ni, As, Pb or rare earth elements; and >10,000 μg/g Zn and Mg when growing in

180

K. Král’ová and J. Jampílek

their natural habitat (Reeves and Baker 2000; Reeves 2006; van der Ent et al. 2013; Reeves et al. 2018; Shrivastava et al. 2019). Metal hyperaccumulating ability was reported for ca. 500 taxa (450 taxa are Ni hyperaccumulators occurring on serpentine (ultramafic) soils (van der Ent et al. 2013). Plants species hyperaccumulating metals, distribution of which is restricted to metalliferous soils, are known as obligate hyperaccumulators (85–90% of hyperaccumulator plant species), while facultative hyperaccumulators are plants species hyperaccumulating HM when growing on metalliferous soils but also occur frequently on normal, non-metalliferous soils (Pollard et al. 2002, 2014). Numerous experiments investigating phytoremediation potential of HM and metalloids was performed in hydroponic solutions or in pots with soils artificially supplemented with various concentrations of HM. Although in these experiments some plants, including MAPs achieved accumulated metal concentrations required for hyperaccumulation (e.g., Schneider and Marquard 1996; Marquard and Schneider 1998; Kráˇlová and Masaroviˇcová 2003; Pavloviˇc et al. 2006; Masaroviˇcová and Kráˇlová 2012, 2017; Lydakis-Simantiri et al. 2016; Han et al. 2021; Zarinkamar et al. 2021), the obtained results must be critically analyzed because such experimental conditions significantly differ from those of natural HM-polluted areas and the hyperaccumulating ability of individual species must be subsequently confirmed by cultivating them in soils naturally contaminated with HM originating from mining or industrial activities. Several researchers published lists of hyperaccumulating MAPs (Banarjee 2018; Saxena et al. 2019; Kumar et al. 2021; Pasricha et al. 2021) and some hyperaccumulators from these plant groups are shown in Table 7.1. Aromatic and medicinal plant species with potential to remediate soils polluted with metals, metalloids and radionuclides are listed in Table 7.2.

7.4 Phytoremediation Techniques Phytoremediation is a green, environment-friendly method using plants for decontamination of environmental matrices from inorganic and organic pollutants via contaminant degradation, contaminant removal via accumulation or dissipation, or by immobilization, whereby phytoremediation techniques such as phytoextraction, phytovolatilization, rhizofiltration, rhizodegradation, phytodegradation, phytostabilization and hydraulic control (see Fig. 7.1) can be used. Several researchers comprehensively discussed phytoremediation techniques emphasizing that different forms of phytoremediation may be applied to particular types of contaminants or contaminated environmental matrices and may require different types of plants (Ansari et al. 2015, 2016, 2017; Erickson and Pidlisnyuk 2021; Flores 2021). Therefore, only brief characterizations of individual phytoremediation techniques are presented here. Phytoextraction (phytoaccumulation): The metal contaminants are removed from soil and water by plant roots and are allocated in shoots, whereby the contaminant

Silene viscidula Corrigiola telephiifolia Pteris vittata

As

Andreazza et al. (2015)

Bidens pilosa, Plantago lanceolata

Urtica dioica Potentilla griffithii

Cu

Zn

Wang et al. (2009) Wang et al. (2009) Liu et al. (2019)

Lysimachia deltoids Silene viscidula Lantana camara

Cd

References

Wang et al. (2009) Garcia-Salgado et al. (2012) Wu et al. (2007, 2009)

Viktorova et al. (2016) Wang et al. (2009)

Liu et al. (2010a) Cudic et al. (2016)

Plant species

Phytolacca americana Verbascum thapsus

Metal

Various

Table 7.1 Some aromatic and medicinal plants hyperaccumulating metals and metalloids

(continued)

7 Medicinal and Aromatic Plant Species with Potential for Remediation … 181

Golubkina et al. (2020)

Tamarix ramosissim, Paliurus spina-christi, Artemisia dracunculus cv. Izumrudny, Anthemis tranzscheliana, Astragalus arnacantha, Limonium gerbera

Se

Brooks (1977), Morrison et al. (1979) Xue et al. (2004) Pollard et al. (2009) Both et al. (1862)

Haumaniastrum robertii

Phytolacca acinosa Phytolacca americana Cardamine violifolia

Co

Sajad et al. (2020) Zhang et al. (2007)

Allium griffithianum Catharanthus roseus, Himalaiella heteromalla, Geranium rotundifolium, Marrubium vulgare, Solanum nigrum, Leersia hexandra

Cr

Mn

Fuente et al. (2016)

Imperata cylindrica

Fe

Pratas et al. (2013) Benis et al. (2015) Angelova et al. (2016) Wang et al. (2009)

Mentha suavolens, Ruscus ulmifolius

Alhagi pseudalhagi Salvia aristata Stipa barbata, Salsola kali, Salvia sclarea, Silene viscidula

Ag

Serrano et al. (2017)

Plantago coronopus

Al

Pb

References

Plant species

Metal

Table 7.1 (continued)

182 K. Král’ová and J. Jampílek

Cheraghi et al. (2013), Ghazaryan et al. (2019) Pecina et al. (2020) Steindor and Palowski (2011) Gorelova et al. (2011) Mohebzadeh et al. (2021) Khalid et al. (2020) Jaison and Muthukumar (2017) Por˛ebska and Ostrowska (1999) Sasmaz and Sasmaz (2009) Frutos et al. (2017) Kaewtubtim et al. (2017)

Cu Cd, Cu, Pb, Zn, U Cd, Pb Cd, Ni, As, Pb Ni, Pb Cu, Co Cr Cd, Cu, Ni, Pb, Zn Sr Cd, Cu, Pb 226 Ra, 232 Th

Cd, Ni, Fe, Zn, Mn Cd, Cu, Ni, Cr, Pb, Fe. Zn, Mn Cd, Cu, Cr, Pb, Zn Cu, Pb, Fe, Zn, Mn Fe, Mn Cr As Fe, Zn, Mn, Sr Cd, Ni, Pb Cd, Ni, Cr Cd, Cr, Fe Cu, Ni, Cr, Pb,Co, Zn As Cd, Cr, Cu, Fe, Mn, Ni, Zn Cd, Cu, Ni, Cr, Pb, Fe, Zn, Mn As

Achillea milefolium

Aesculus hippocastanum

Ailanthus altissima

Alternanthera bettzickiana

Amaranthus viridis, Amaranthus spinosus

Artemisia vulgaris

Astragalus gummifer, Euphorbia macroclada, Verbascum cheiranthifolium

Atriplex halimus

Avicennia marina, Plutea indica

Azadirachta indica

Calotropis procera

Cannabis sativa

Cassia fistula

Qadir et al. (2021) Pant et al. (2011)

Linger et al. (2002) Citterio et al. (2003) Irshad et al. (2015) Malik et al. (2010) Picchi et al. (2022) Zielonka et al. (2020)

Rani et al. (2018) Varun et al. (2012) Almehdi et al. (2019)

Ruhela et al. (2019) Qadir et al. (2021) Thangaswamy et al. (2015) Arise et al. (2021) Umer e al. (2022)

(continued)

Abbasi et al. (2017)

Pb

Acer cappadocicum, Fraxinus excelsior, Platycladus orientalis

Ruhela et al. (2019)

Cd, Ni, Fe, Zn, Mn

Acacia nilotica

References

Metals

Plant species

Table 7.2 Medicinal and aromatic plants suitable for phytoremediation of soils contaminated with metals, metalloids and radionuclides

7 Medicinal and Aromatic Plant Species with Potential for Remediation … 183

Irshad et al. (2015) Varun et al. (2012) Sharma and Adholeya (2011) Datta et al. (2011) Mangkoedihardjo and Triastuti (2011) Pandey et al. (2019a) Lago-Vila et al. (2019) Varun et al. (2012) Ibrahim et al. (2013) Mbanga et al. (2019) Moreno-Jimenez et al. (2009) El-Khatib et al. (2020a) Xing et al. (2019) Hamzach et al. (2016) Varun et al. (2012)

Cd, Cr, Fe, Cd, Cu, Zn, Mn Cr As Hg Cd, Ni, Cr, Pb Cd, Pb, Zn Cu, Cr, As, Mn Cu, Ni Hg Fe, Mn, Cu, Zn, Cd Cd, Cu, Pb Cd, Cu Cd As Pb, Zn, Cu, Ni, Cd Cd, Cu, Pb Pb, As, Sb, Zn, Cu Cd, Pb Cu, Zn Cu, Pb, Zn Cu, Zn

Centaurea jacea

Chenopodium album

Chenopodium murale

Chrysopogon zizanioides

Cymbopogon flexuosus

Cytisus scoparius

Datura stramonium

Digitalis thapsi

Eucalyptus globules

Euphorbia hirta

Euphorbia cheiradenia

Ficus nitida

Globularia alypum

Glycyrrhiza glabra

Hibiscus cannabinus

Hibiscus mutabilis

Vincent et al. (2018) Shang et al. (2020)

Aishah et al. (2019)

Tabrizi et al. (2021)

Testiati et al. (2013)

El-Khatib et al. (2020a)

Chehregani and Malayeri (2007)

Antonijevic et al. (2012)

As, Pb, Mn

Catharantus roseus

References Pandey et al. (2007) Ahmad and Mishra (2014) Fulekar et al. (2010)

Metals Cd, Pb Ni, Cr, Pb 137 Cs

Plant species

Table 7.2 (continued)

(continued)

184 K. Král’ová and J. Jampílek

Mataruga et al. (2020) Jaison and Muthukumar (2017) Ye et al. (2020) Guo et al. (2020) Golubkina et al. (2020) Szakova et al. (2018) Stancheva et al. (2014a), Bagheri et al. (2021) Lydakis-Simantiris et al. (2016) Mohebzadeh et al. (2021) Zemiani et al. (2021) Sá et al. (2014) Zheljazkov et al. (2006) Dinu et al. (2021)

Cd, Cu, Ni, Zn Fe, Zn, Mn, Cu Cd Cu Fe, Mn, Cu, Zn, Cd Ni, Cr, As, Pb Cr Cr Cd Se Cd, As, Pb, Zn Cd, Pb Cd, Ni, Pb Ni, Pb Cd Pb Cd, Cu, Pb Cd, Ni, As, Pb Cd, Cu, Pb Cd V, Cr Pb

Hippophae rhamnoides

Hypericum perforatum

Juglans regia, Salix alba

Lantana camara

Lavendula dentata

Linum usitatissimum

Limonium gerberi, Pistacia atlantica, Cotinus coggygria

Matricaria recutita

Melia azedarach

Mentha crispa

Mentha piperita

Ocimum basilicum

Pinus nigra, Vitis vinifera, Robinia pseudoacacia, Thuja

Plantago lanceolata

Salas-Luevano et al. (2017)

Akkus et al. (2017)

Zheljazkov et al. (2006) Putwattana et al. (2010)

Shi et al. (2016) Bogatu et al. (2007)

Vincent et al. (2018)

(continued)

Schneider and Marquard (1998) Ghazaryan et al. (2019) Moreno-Jimenez et al. (2009)

Cu, Pb, Zn

Hibiscus syriacus

References

Hibiscus sabdarifa Ramana et al. (2016)

Metals Cr

Plant species

Table 7.2 (continued)

7 Medicinal and Aromatic Plant Species with Potential for Remediation … 185

Midhat et al. (2019) Ibrahim et al. (2013) Bauddh and Singh (2012) Galal et al. (2021) Jaison and Muthukumar (2017), Rani et al. (2018) Ananthi and Manikandan (2013) Shi et al. (2016) Abbaslou et al. (2018) Affholder et al. (2020) Testiati et al. (2013) Adiloglu (2020) Lydakis-Simantiris et al. (2016) Antonijevic et al. (2012)

Lajayer et al. (2017) Shi et al. (2016)

Zn, Cu, Pb, Cd Cd, Pb Cd Cu, Ni, Fe, Zn, Mn Cr Pb Cd, Cu, Ni, Zn Cd, Cu. Pb, Fe, Zn, Mn As, Pb, Zn, Sb Pb, As, Sb, Zn, Cu Cd, Cu, Cr, Pb Cd, Ni, Pb As, Pb, Mn Cd, Cu, Zn Cd, Ni, Pb Cd, Pb Cd, Ni, Cr, Co Cd, Cu, Ni, Zn Cr Pb As, Pb, Mn Hg Cd, Cr, Fe,

Portulaca oleracea

Rhazya stricta

Ricinus communis

Robinia pseudoacacia

Rosmarinus officinalis

Rumex patientia

Salvia officinalis

Saponaria officinalis

Taraxacum officinale

Thymus vulgaris

Trigonella foenum-graecum

Ulmus pumila

Urtica dioica

Verbascum phlomoides

Verbascum thapsus

Xanthium stramonium

References

Plantago major

Irshad et al. (2015)

Sasmaz et al. (2016)

Antonijevic et al. (2012)

Shams et al. (2010) Grubor (2008)

Lydakis-Simantiris et al. (2016) Zhou et al. (2020)

Rosselli et al. (2006)

Galal and Shehata (2015)

Metals Cd, Fe, Pb, Al, Mn, V, Co, Ni, Cr, Zn, Cu, Sr

Plant species

Table 7.2 (continued)

186 K. Král’ová and J. Jampílek

7 Medicinal and Aromatic Plant Species with Potential for Remediation …

187

is stepwise mobilized in rhizosphere, taken up by plant roots and after translocation to shoots, it is sequestered in plant tissue (Ali et al. 2013). The ultimate elimination of accumulated non-biodegradable toxic metals from the environment can be then realized by harvesting the shoots or collection of fallen leaves (Sheoran et al. 2016; Yan et al. 2021). For effective phytoextraction, high tolerance of plant tissues to the contaminant suppressing adverse impact on plant health is required. The metal tolerance of plants can be achieved by binding of metals to cell wall, transport of metal ions into the vacuoles, and by chelating of metal ions with plant biomolecules (Memon and Schröder 2009). Phytoextraction efficiency can be ameliorated by external application of chelating agents such as EDTA, EDDS or CA. Phytovolatilization: Contaminants, which were taken up by roots from soil, are moved to the leaves and released by plants into the atmosphere in a volatile, less toxic form via transpiration (Kumar et al. 2017; Khan et al. 2019; Khalid et al. 2017). Beside organic contaminants, this technique is also suitable for removal of As, Se and Hg, which exist as gaseous species in the environment (Pajevi´c et al. 2016; Wang et al. 2021a). Improved ability of plants to volatilize metals can be achieved using genetically modified plants converting metals into volatilized forms more efficiently compared to naturally occurring non-transgenic plants (Khalid et al. 2017). Phytodegradation: The organic contaminants, which were taken up by plants, are degraded via metabolic processes in tissues of plant organs. The degradation can be accelerated by enzymes produced by plants, which catalyze the transformation of organic pollutants by inserting functional groups such as –OH moieties, thereby increasing their polarity; reduced toxicity is achieved by following conjugation with plant biomolecules resulting in further polarity increase (Mahar et al. 2016; Pajevi´c et al. 2016; Muthusaravanan et al. 2018; Kráˇlová and Jampílek 2022). This technique is also known as phytotransformation. Phytostabilization: Reduction of the mobility of toxic metals in soil due to their accumulation by plant roots, absorption onto roots or precipitation within the root zone (Radziemska et al. 2017; Schachtschneider et al. 2017). Toxic metals accumulated in roots show no or only limited translocation to shoots, whereby as efficient phytostabilizers plants showing BCF > 1 and TFs < 1 exhibiting tolerance to multiple metals/metalloids contamination can be considered (Fitz and Wenzel 2002; Maestri et al. 2010; Shackira and Puthur 2017). Phytostabilization using metal-tolerant plant species can contribute to re-establish vegetation cover at contaminated sites; however, the disadvantage of this remediation method is the persistence of metals in soils or in the root system, primarily in the rhizosphere. Rhizodegradation: degradation of organic contaminants in the rhizosphere by rhizospheric microorganisms (yeast, fungi or bacteria), utilizing the contaminants as a source of energy and nutrition, whereby their activity is enhanced by the presence of plant roots. Moreover, carbon-containing substances released by plants serve as additional nutrients for microorganisms and promote their activity. Transgenic plants showing powerful ability to secrete compounds simulating the microbial activity could contribute to effective rhizodegradation of organic pollutants (Fasani et al. 2018; Gunarathne et al. 2019; Boechat et al. 2021).

188

K. Král’ová and J. Jampílek

Rhizofiltration: Contaminants are adsorbed or precipitated from solution surrounding the root zone or absorbed into the roots (Khan et al. 2019). Certain chemicals synthesized within the roots enable the adsorption of contaminants, whereby the binding capacity of metal ions is improved by phytochelatins (Singh and Santal 2015). For rhizofiltration plants with rapidly growing roots, extensive root architecture and fibrous roots able to remove contaminants from the ground water and rhizospheric zone are suitable (Dhanam 2017; Khan et al. 2019). Rhizofiltration technique is also suitable for decontamination of effluents and contaminated waterways. Hydraulic control is based on the uptake and transpiration of large volumes of water by plants, thereby reducing leaching of contaminants from the vadose zone and preventing migration of contaminated wastewater into adjacent uncontaminated areas. For hydraulic control of ground water, deep-rooted phreatophyte species such as tamarisk or eucalyptus able to draw large volumes of water from a deep-water table are desirable (Pivetz 2001). Thus, it can be concluded that phytoextraction, phytovolatilization, phytostabilization and hydraulic control are convenient for phytoremediation of soils contaminated with toxic metals, while rhizofiltration can be used for removal of toxic metals from the aqueous environment. On the other hand, for removal of organic contaminants from environmental matrices rhizodegradation and phytodegradation are suitable. Comprehensible review papers focused on phytoremediation of metal-contaminated environmental matrices were published by several researchers (Ali et al. 2013; Yan et al. 2020; Khalid et al. 2021; Ozyigit et al. 2021), while some researchers discussed in detail the potential of MAPs to be used for decontamination of metal-polluted areas (Gupta et al. 2013; Pruteanu and Muscalu 2014; Jisha et al. 2017; Pirzadah et al. 2019; Saxena et al. 2019; Kumar et al. 2021; Lone and Gaffar 2021). Factors affecting metal accumulation in plants cultivated in soil are presented in Fig. 7.2. Potential implications of HM-contaminated medicinal plants on human health were analyzed by Asiminicesei et al. (2020).

7.5 Phytoremediation of Metal/Metalloid-Contaminated Soils Using Medicinal and Aromatic Plants Medicinal plants can by classified on the basis of their growth habit (e.g., trees, shrubs or herbs), nutrition (autotrophs, heterotrophs, etc.) or habitat (e.g., (hydrophytes, xerophytes, halophytes), whereby from medicinal plans 33% belong to trees, 20% to shrubs and 32% to herbs, while climbers represent 12%. The pharmacologically active secondary metabolites of MAPs can be situated in seeds, bark, stem and wood, leaves, rhizome or corm (Alamgir 2020). Chemotaxonomic classification of medicinal plants was discussed by Singh and Geetanjali (2018). The healing properties of medicinal and some aromatic plants were described in several monographs and review papers (e.g., Alamgir 2020; Aftab and Hakeem 2021; Husen 2022). As the general public knows mainly the healing effects of herbs, in Table 7.3 we

7 Medicinal and Aromatic Plant Species with Potential for Remediation …

soil pH

organic matter eontent in soil

presence of other metals in soil presence of microorganisms in soil

Plant species

Metal accumulation in plant

189

life stage of plant species

genetic modification of plants/microbes

application of chelators

biological wastederived amendments

application of electric field on soil

Fig. 7.2 Factors affecting metal accumulation in plants in plants cultivated in soil

present the pharmacological effects of some medicinal trees and shrubs used for phytoremediation of HM-contaminated soils.

7.5.1 Phytoremediation of Soils by Medicinal and Aromatic Herbs Investigation of Cd phytoextraction by Calendula officinalis L. grown in Cd-spiked calcareous soil (50 and 100 mg Cd/kg) without and in the presence of chelating agents, EDTA, CA and tartaric acid showed that BCFs ranged from 1.3 to 2.90 and TF values of Cd from 1.28 to 1.58. In all treated and untreated plants, the TF values of Cd were >1 and the accumulated Cd concentrations >100 mg Cd/kg. As excellent chelating agent improving the efficiency of Cd phytoextraction by C. officinalis CA can be considered, which beside increased translocation of Cd to shoots showed positive impact on plant biomass due to reduced oxidative stress (Saffari and Saffari 2020). At combined treatment of marigold plants grown in pots with 30 mg Cd/kg, +2 g/kg humic acid (HA) + 5 mmol EDTA/kg the plants accumulated up to 115.96, 56.65 and 13.85 mg Cd/kg in roots, shoots and flowers, respectively, and only slightly lower values were observed using more eco-friendly chelator, EDDS, instead of EDTA. Maximum remediation ratio was achieved with application of 15 mg Cd/kg + 2 g/kg HA and 5 mmol EDDS/kg (Mani et al. 2014). Treatment of C. officinalis

190

K. Král’ová and J. Jampílek

Table 7.3 Pharmacological activities of some medicinal trees and shrubs Plant species

Activity/therapy

References

Acacia auriculiformis

Antioxidant activity; treatment of cancer, cardiovascular and inflammatory diseases

Krishnaiah et al. (2011)

Acacia farnesiana

Moderate anti-inflammatory, antituberculotic and anticancer activities; treatment of dysentery

Lin et al. (2009), Hernandez-Konwar and Das (2014), Hernandez-Garcia et al. (2019)

Acacia nilotica

Antimicrobial, antiparasitic, antidiabetic, antihyperlipidemic, anticancer, antimutagenic, antipyretic, anti-inflammatory, antinociceptive, antiulcer, antihypertensive, antispasmodic, antidiarrheal, antioxidant, antidiarrheal, antihypertensive and antispasmodic, antibacterial, anthelmintic, anticancer and acetyl cholinesterase (AChE) inhibitory activities

Rather et al. (2015), Abduljawad (2020)

Aesculus hippocastanum

Anti-inflammatory and anti-edematous and anticancer activities; used for treatment of chronic venous insufficiency

Dudek-Makuch et al. (2014), Cheong et al (2018)

Albizzia lebbeck

Antihyperglycemic, antihyperlipidemic and antioxidant activities; pancreas/renal/hepatic/cardiac protective action; treatment of asthma

Ahmed et al. (2014), Yim et al. (2014), He et al. (2020)

Atriplex halimus

Antiproliferative and antidiabetic effects

Kadan et al. (2013), Al-Senosy et al. (2018)

Avicennia spp.

Antimicrobial, antioxidant, anticancer, antidiabetic and anti-inflammatory activities

Thatoi et al. (2016)

Azadirachta indica

Antifertility, antispermatogenic, Patil et al. (2021), Sandhir et al. antiovulation, hormone altering, (2021), Sarkar et al. (2021) contraceptive, abortifacient, anti-inflammatory, antiangiogenic, immunomodulatory and apoptotic activities; neuroprotective effects (continued)

7 Medicinal and Aromatic Plant Species with Potential for Remediation …

191

Table 7.3 (continued) Plant species

Activity/therapy

Calotropis procera

Anticancer, antifertility and Ali-Seyed and Ayesha (2020), antiscabietic activities; the Pathania et al. (2020) antidote for snakebite; treatment of skin infections, inflammation and cardiovascular problems

References

Capsicum annuum

Lipid-lowering, antihypertensive, antidiabetic and anti-obesity effects; beneficial effects on metabolic syndrome cardiovascular diseases

Salehi et al. (2018), Sanati et al. (2018)

Cassia fistula

Antioxidant, antimicrobial, antidiabetic, anti-inflammatory, hypolipidemic, hepatoprotective, antiulcer, antitumor, antimelasmic, antipyretic, analgesic and laxative activities; treatment of Leucoderma, and intestinal disorder

Ali (2014), Zhao et al. (2016), Sharma et al. (2021)

Cytisus scoparius

Antidiabetic, antioxidant, Nirmal et al. (2008), Luis et al. hypnotic and sedative, antistress (2009) and moderate anxiolytic activities

Elaeagnus commutata

Anticancer activity

Majinski (2020)

Eucalyptus camaldulensis

Activity against Vibrio spp., antituberculotic activity

Rangra et al. (2019), Ghosh et al. (2021)

Eucalyptus globulus

Antibacterial, antifungal, antidiabetic, anticancer, anthelmintic, antiviral, antioxidant and anti-inflammatory activities; protection against UV-B irradiation; wound healing and stimulating the immune response effect

Jafariet al. (2021), Surbhi et al.(2021)

Euphorbia macroclada

Anti-inflammatory, antimicrobial, anticancer and wound-healing activities

Kirbag et al. (2013), Tas et al. (2018), Ozbilgin et al. (2019)

Euphorbia milii

Antimicrobial and antioxidant activities

Rauf et al. (2014)

Globularia alypum

cardioprotective, antigenotoxic and antioxidant activities

Harzallah et al. (2010), Nacira et al. (2011) (continued)

192

K. Král’ová and J. Jampílek

Table 7.3 (continued) Plant species

Activity/therapy

References

Hibiscus mutabilis

Antiproliferative and HIV-1 reverse transcriptase inhibitory activities; allergy-preventive effects

Iwaoka et al. (2009), Lam and Ng (2009)

Hippophae rhamnoides

Antioxidant, anti-inflammatory Jastrzab and Skrzydlewska and cardioprotective properties; (2019), Wang et al. (2022) protective effect on skin cells

Jatropha spp.

Antimicrobial, antifungal, anti-inflammatory, antioxidant and anticancer activities

Limoniastrum monopetalum Antioxidant activity

Das et al. (2018), Cavalcante et al. (2020) Trabelsi et al. (2010)

Olea europaea

Antidiabetic, anti-inflammatory Tahraoui et al. (2007), Bilal and antioxidant activity; limits et al. (2021) the risk of liver damage; prevents the progression of steatohepatitis

Platycladus orientalis

Anti-inflammatory, antifibrotic, Shan et al. (2014) antioxidant, antimicrobial, disinsection, anticancer, diuretic, hair growth-promoting and neuroprotective activities

Ricinus communis

Anti-inflammatory, anthelmintic Franke et al. (2019), Polito and antibacterial activities; used et al. (2019) as laxative, abortifacient and for healing of wounds and ulcers

Robinia pseudoacacia

Cytotoxic, antioxidant, antitumor, antiviral and immunomodulatory activities

Thespesia populnea

Hepatoprotective, antitumor, Chellappandian et al. (2018), antioxidant, wound-healing and Gopalakrishnan et al. (2019) antidermatophytic activities

Tilia cordata

Treatment of symptoms of the common cold and mental stress

Symma et al. (2021)

Ulmus pumila

Hepatoprotective and neuroprotective activities; attenuates adipogenesis; used for prevention of hormone-dependent tumors

Hartmann et al. (2011), Ghosh et al. (2012), Ma et al. (2019)

Guo et al. (2019), Sun et al. (2019), Bratu et al. (2021)

plants grown in Cd-contaminated soil with sodium dodecyl sulfate and ethylenegluatarotriacetic acid (EGTA) resulted in increased accumulation of Cd in plant organs, whereby root Cd concentrations were higher than those of shoot; application of EGTA increased the total Cd accumulation by plants up to 217% (Liu et al. 2010b). If the marigold plants cultivated in pots and exposed to Cd stress of 80 mg Cd/kg soil were inoculated with mycorrhizal fungi, they accumulated 833.3 and 1585.8 mg

7 Medicinal and Aromatic Plant Species with Potential for Remediation …

193

Cd in their shoots and roots, respectively (Tabrizi et al. 2015). Claroideoglomus claroideum isolates and Funneliformis mosseae (derived from metal-contaminated soils) enhanced synthesis of valuable secondary metabolites, including total phenols, flavonoids and carotenoids in C. officinalis flowers resulting in improved antioxidant capacity, whereby in flowers neither Pb nor Cd was detected (Hristozkova et al. 2016). In C. officinalis used for Pb/Cd remediation in contaminated loess the plants accumulated 104.85 mg Cd/kg at Cd concentration of 50 mg/kg, and although the plants accumulated only low concentrations of Pb, its presence showed beneficial impact on Cd accumulation by plants (Fan et al. 2016a). The methylation of pectins and lipids, and coordination effect between Pb/Cd and OH groups were supposed to contribute to the adaptation process of C. officinalis plants exposed to Pb/Cd stress (Fan et al. 2016b). Mani et al. (2015) recommended application of hyperaccumulator oilcake manure as an alternative for chelate-induced phytoremediation of Cd and Pb by C. officinalis grown in alluvial soils contaminated with toxic metals. C. officinalis plants cultivated in hydroponium in the presence of Cu and Pb achieved the average Cu and Pb concentration of 1473.4 mg Cu/kg and 4303.6 mg Pb/kg, suggesting their suitability to be used for remediation of soils contaminated with both tested metals (Shao et al. 2019). Co-application of Kocuria rhizophila bacterium and CA (5 mM) ameliorated Ni phytoextraction efficiency of C. officinalis (Anum et al. 2019). Application of 5 mM CA to young Mentha piperita plants exposed to Ni stress (100–500 μM) considerably ameliorated adverse impact of Ni on morphophysiological and biochemical characteristics of plants and increased Ni accumulation in plant organs achieving 138.2, 54.2 and 38% higher values in roots, stems and leaves, respectively, compared to plants exposed only to Ni (Ul Khair et al. 2020). Potential of Mentha longifolia (wild mint) to be used for phytostabilization of wetlands contaminated with toxic metals (Cu, Zn, Mn, Ni and Cd) was reported by Gharib et al. (2021). In pot experiments using soil contaminated with As(III) and As(V) M. piperita phytoaccumulated more As than Melissa officinalis and Salvia officinalis, whereby the bioavailability of the oxidized As form was greater (Jablonska-Czapla et al. 2019). Treatment with CA enhanced U content in Salvia officinalis grown in pots in soil artificially contaminated with 470 mg U/kg by 3.53fold (Ibragic et al. 2020). Salvia sclarea can tolerate high concentrations of Zn and accumulate it in leaves at increasing levels of essential metal (Fe, Ca and Mn) ions in its tissues, which contribute to improved activities of photosystem (PS) I and PS II by increased synthesis of non-enzymatic antioxidants such as phenolics and anthocyanins in the leaves, which detoxify excess Zn, ensuring protection against oxidative stress. This medicinal plant is suitable to be used for the phytoextraction/ phytostabilization of soils contaminated with Zn (Dobrikova et al. 2021). Clary sage plants grown for two seasons in soil containing 394 ppm Pb, 443 ppm Zn and 7 ppm Cd considerably increased the abundance of plant-growth-promoting rhizobacteria in roots during the second growing season but mycorrhizal inoculation practically did not alter bacterial diversity and community structure (Raveau et al. 2020). In an outdoor pot experiment, Origanum vulgare plant cultivated in soils containing 150–200 mg Cr(VI)/kg accumulated in roots and shoots up to 4300 and 1,200 mg Cr/kg d.w. However, it was found that oregano plant can be effective Cr remediatior

194

K. Král’ová and J. Jampílek

showing no adverse impact on plant growth when soil Cr concentrations are below 100 mg Cr(VI)/kg. At these conditions, Cr uptake from soil by roots increases but Cr translocation to shoots is reduced and reduction of Cr(VI) to Cr(III) is faster in shoots but slower in roots (Levizou et al. 2019). Levandula dentata plants grown in soil originating from Qingdao in Eastern China, which was highly contaminated with Cr, accumulated in roots 817.5 mg Cr/kg d.w. and in shoots 843.9 mg Cr/kg d.w., suggesting high tolerance of this plant to Cr. Although plant growth was negatively affected by the high Cr concentration, due to Cr-free essential oil L. dentata can be considered as an appropriate phytoextractor plant to remediate Cr-contaminated soils (Ye et al. 2020). Ocimum basilicum L. and Origanum vulgare L. plants cultivated in pots in soil containing high Cd and Pb amounts accumulated Cd predominantly in the roots, while Pb was observed only in O. vulgare shoots. In contrast to basil plants, which responded to metal stress by improved gas exchange, stomatal conductivity, transpiration and reduced water use efficiency, oregano plants showed enhanced water use efficiency but reduced gas exchange and transpiration. Differences were also found in metabolites biosynthesized under metal stress: In basil more phenols and flavonoids were estimated, while in oregano higher levels of ascorbate, glutathione and phenols were observed (Stancheva et al. 2014b). Ruzickova et al. (2015) at investigating accumulation of Cd, As and Pb grown on soil spiked with 40 mg Cd/kg, 100 mg As/kg and 2000 mg Pb/kg found that the metals were accumulated in O. basilicum roots and their translocation to shoots was restrained. Reduced accumulation of Mo in plants suggested As–Mo and Cd–Mo antagonism and anthocyanins were found to play a role in the tolerance of plants to monitored HM. Predominant accumulation of Cd in roots of O. basilicum was observed also at exposure of plants cultivated in an environmental chamber to both Cd2+ ions and nanosized CdSSe particles (Alamo-Nole et al. 2017). O. basilicum. plants cultivated on soil supplemented with 40 mg Cd/kg showed reduced levels of Cu, Zn and Cd, in the shoot, although Fe concentration in shoots showed an increase. Treatment of plants with potassium fertilizers resulted in enhanced Cd accumulation in plants; this enhancement was higher at application of K salts (KCl, K2 SO4 ) compared to K-nanochelate application (Zahedifar et al. 2019). O. basilicum plants cultivated in multimetal-contaminated soil reflecting metal levels of soil from mining area were characterized with improved growth and increased chlorophyll (Chl) levels, whereby Cd, Co, Cr and Pb were accumulated mainly in roots, in contrast to Cu, Ni and Zn, which accumulated in flowers. However, in the mature plants the levels of Cd and Pb concentrations were higher than the legal limits for the mature plants and thus, they would be not suitable for consumption (Dinu et al. 2020). Prapagdee et al. (2015) in a field study performed on Cd-contaminated soil found that inoculation of soil with Cd-resistant Arthrobacter sp. enhanced Cd accumulation in Ocimum gratissimum roots and shoots by 20% and 40%, respectively. The most efficient Cd removal can be achieved in soil, in which EDTA-treated O. gratissimum plants were cultivated. The highest percentage of Cd removal was found in soil when cultivation of EDTA-treated O. gratissimum was succeeded by plants inoculated by Arthrobacter sp. Potential of basil plants to accumulate Cs from hydroponic solution during a period of 60 days was assessed by Ko et al. (2018).

7 Medicinal and Aromatic Plant Species with Potential for Remediation …

195

Cs concentrations in basil leaves increased with prolongation of the treatment and applied Cs concentration; the highest Cs concentration was observed in leaf margin, the lowest one in veins. However, exposure of plants to 1000 ng/mL of Cs resulted in considerable growth inhibition. Medicinal plants cultivated in pots using soil supplemented with 30 ppm Cd accumulated in leaves/roots 2.31/51.7 ppm Cd (Salvia officinalis), 8.55/0.8.56 ppm Cd (Thymus vulgaris) and 27.1/48.6 ppm Cd (Matricatia recutita), and chamomile flowers contained 9.27 ppm Cd. Using soil containing 1800 ppm Pb, the respective accumulated Pb levels in leaves/roots of chamomile, sage and thyme were 29.2/153, 5.31/177 and 12.2/156 ppm, respectively, while in soil contaminated with 600 ppm Ni the corresponding accumulated Ni concentrations were 61.2/288, 29.5/248.5 and 46.5/154 ppm (Lydakis-Simantiris et al. 2016). Evaluation of HM uptake by M. recutita cultivated in pots with four soils containing different concentrations of As, Cd, Pb and Zn showed that in contrast to As, Pb and Zn, which accumulated in roots, Cd translocated to the aboveground parts of plants, including anthodia, whereby adverse toxic effect was not observed. Increasing Cd content in anthodia resulted in reduced Cd extractability to infusion (Szakova et al. 2018). Foliar-fertilized chamomile plants grown on industrially contaminated soil containing 4.6- and 2-fold higher Cd and Pb levels compared to permissible concentrations showed reduced dry biomass of plant roots and shoots, while higher biomass of flowers and increased levels of peroxidases was observed (Stancheva et al. 2014a). Comparison of diploid chamomile cultivar “Novbona” with tetraploid cv. “Lutea” cultivated on an experimental field showed that accumulation of K, Ca, Mg, Al, Cu, Cr, Hg and Cd in anthodia was higher in diploid plants, while ploidy did not affect accumulation of Fe, Zn and Ni. In addition, tetraploid cultivar showed reduced levels of amino acids but higher concentrations of phenolic metabolites compared to diploid cultivar (Kovacik et al. 2012). Pronounced impact of actual climatic relations on Cd concentrations accumulated in anthodia of M. recutita plants cultivated in Eastern Slovakia in field conditions in the period 1995–2002 was estimated by Šalamon et al. (2007); the highest Cd accumulation (0.505 mg/kg) was observed in 2021, which was characterized with above-average precipitation quantity compared to 0.003 mg/kg in 2000 (year with markedly below-average precipitation quantity). Enhanced levels of As and Sb in some medicinal plants naturally growing on old mining site in Poproc (Slovakia) containing 539 mg/kg As and 4462.9 mg/kg Sb were observed; the estimated shoot/root concentrations of As were 518.6/919.9 mg/kg in Fragaria vesca and 166.7/369.1 mg/kg in Taraxacum officinale, while those of Sb were 241.0/436.9 mg/kg in T. officinale and 269.6/703.6 mg/kg in F. vesca. Enhanced levels of these toxic metals in biomass of medicinal plants suggested that their use for medicinal purposes can threaten human health (Vaculik et al. 2013). Tagetes minuta grown near a battery recycling plant was found to be resistant to high Pb concentrations and accumulated it in shoots, whereby EO of this plant was free of Pb (Sosa et al. 2016). Taraxacum ohwianum Kitam. grown 6 months on soil supplemented with 100 mg Cd/kg accumulated in roots and leaves 520.35 and 100.11 mg Cd/kg d.w., respectively, and the respective BAF (leaves), BCF and TF values were 1.0, 5.2 and 0,19; at this treatment stem and root biomass increased by 35.3% and 47%,

196

K. Král’ová and J. Jampílek

respectively. Hence, dandelion showed excellent Cd-accumulating capacity close to this of a hyperaccumulator and can be recommended for phytoremediation purposes. It was found that in dandelion leaves Cd was accumulated mainly in epidermis cells, the laticifer groups of phloem, parenchyma cell inclusions and non-glandular hairs (Cheng et al. 2019). Dandelion clones sampled from plants growing in HM-polluted site accumulated in their tissues 4.2-, 17,76 and 4.2-fold higher concentrations of Cu, Pb and Zn than the clones originating from unpolluted area; considerably higher levels of Cu, Pb and Zn were allocated in roots compared to those in shoots (Collier et al. 2017). In hydroponic experiments, dandelion was found to be more tolerant to Cd achieving 489 and 2486 μg Cd/g d.w. in shoots and roots, respectively, compared to Ni showing lower accumulated metal concentrations (165 and 858 μg Ni/g d.w). Ni strongly reduced mineral nutrients in the shoots and accumulation of thiols but with prolongation of the exposure total soluble phenols and phenolic acids showed an increase (Kovacik et al. 2019). Cannabis sativa plants grown on As-polluted industrial soil showed mean As root concentration of 1473 mg/kg and achieved up to 189 and 47.0 mg As/kg in stem and leaves (Picchi et al. 2022). This plants species also accumulated pronounced Cr concentration in roots (1233.3 mg/kg) from Cr-contaminated soil (Sajad et al. 2020). Potential of hemp plants to be used in phytomanagement for both phytoremediation and bioenergy production was highlighted by Rheay et al (2021). Phytoremediation potential of flax (Linum usitatissimum L.) in metalcontaminated soils and aqueous environment was discussed by Saleem et al. (2020). Investigation of Cd accumulation from Cd-contaminated soil by flax cultivars in a field experiment showed 2–4-fold higher accumulation by phloem compared to roots, xylems and capsules, whereby accumulated Cd levels achieved 45–55% of Cd accumulated by plant. The most effective cultivars were able to extract 60 g Cd/ha suggesting their suitability to be used for phytoremediation purposes (Guo et al. 2020). Moreover, L. usitatissimum plants exposed to Cd stress and inoculated with bacterial strain Serratia sp. CP-13 sequestered Cd in plant rhizospheric zone and inhibited the Cd uptake (Shahid et al. 2019). In Cd-tolerant flax cultivars phytochelatins were involved in the response of plants to Cd stress and reduced Cd translocation to shoots was due to formation of high-molecular weight Cd complexes (Najmanova et al. 2012). Investigation of Hg bioaccumulation in Achillea millefolium and Macleaya cordata plants grown in the Wanshan mercury mining district of China showed that these plants are able to be used for phytoremediation purposes, whereby positive correlation was observed between Hg concentration in roots and bioavailable Hg concentration in the soil as well as between Hg levels in shoots and total gaseous Hg in ambient air. However, it could be mentioned that Hg content in plants exceeded the permissible limits, and therefore they were not suitable to be used as fodder or for medicinal purposes (Wang et al. 2011). Treatment of Solanum nigrum L. plants exposed to Cd and Pb with 10% water fruit extract of Phyllanthus emblica L. increased Cd accumulation in shoots and roots by 32.5% and 65.2%, respectively, and that of Pb by 38.7% and 39.6%, respectively, compared to control, without affecting plant biomass. Increased metal accumulation

7 Medicinal and Aromatic Plant Species with Potential for Remediation …

197

was likely also due to the chelating ability of the extract associated with high levels of polyphenolic compounds. On the other hand, enhanced accumulation of Cd ad Pb observed at application of EDTA was accompanied with biomass reduction (Han et al. 2021). In a hydroponics experiment, Panax notoginseng accumulated 1402.1 mg Cu/kg and 2710.4 mg Pb/kg, the accumulated metal concentrations were higher in roots compared to shoots, and it would be desirable to investigate phytoremediation potential of this medicinal plant also in metal-contaminated soil (Shao et al. 2019). Hypericum perforatum plants grown on soil originating from a mining valley in NW Madrid (Spain) highly contaminated with HM accumulated in their shoots 10.22, 59.18, 16.11, 230.2 and 108.11 μg/g d.w. of Cd, Zn, Cu, Mn and Fe, respectively, while the respective accumulated metal levels in Digitalis thapsi were 13.28, 245.3, 23.5, 182.7 and 422.1 μg/g d.w., respectively; hence, both medicinal plants can be used for HM phytoextraction from metal-contaminated soils (Moreno-Jimenez et al. 2009). Digitalis purpurea plants grown on soils contaminated with toxic metals from the vicinity of an abandoned Pb mine in Portugal accumulated 4450 mg Fe/kg and 1017 mg Zn/kg, while medicinal plants Ruscus ulmifolius and Mentha suavolens accumulating Ag in concentrations 1.0 and 1.9 mg Ag/kg were evaluated as Ag hyperaccumulators (Pratas et al. 2013). On the other hand, Digitalis thapsi grown in soils contaminated with metals originating from mining activities showed TF > 1 for Zn, Cu, As, Cr and Pb, although the respective BAF values were low (2200 g Cu /ha. For Bidens pilosa plants BCF and TF of 4.08 and 0.04 were observed and the plants can

198

K. Král’ová and J. Jampílek

extract even >3.500 g Cu/ha. Both medicinal plants, B. pilosa and P. lanceolata, can be used for phytostabilization and phytoremediation of Cu-contaminated vineyard soils (Andreazza et al. 2015). Penstemon digitalis grown on U tailing ponds receiving waste from ores mines at several mine stations effectively phytoaccumulated Al, V, Ni and Co achieving leaf concentrations of 48.3, 0.4, 2.7 and 0.5 mg/kg, respectively, and can be used for phytoremediation of such multimetal-contaminated areas. However, among native plant species grown on this area as the best metal accumulator Pteris vittata was evaluated, accumulating in leaves 70.6 mg Al, 197.6 mg Mn, 108.6 mg Fe, 0.7 mg V and 0.6 mg Co per kilogram (Singh et al. 2015). Cobalt phytoextraction by Astragalus sinicus can be increased by application of chelators. Treatment with 2.5 mmol/kg EDDS resulted in 6.51-fold greater shoot Co accumulation compared to control plants, and TF of 1.76 was estimated. The Co phytoextraction enhancements by other tested chelators such as nitrilotriacetic acid (NTA) and CA were lower (Chen et al. 2019). The tolerance of Astragalus tragacantha providing the natural gum tragacanth to metals and metalloids can be associated with its phytometabolites, plant antioxidant activity and plant nutrientuptake strategy, utilizing association with arbuscular mycorrhizal fungi and dark septate endophytes (Salducci et al. 2019). Medicago sativa and Astragalus adsurgens were reported to be suitable species for rhenium phytoextraction from alkaline soils amended with coal fly ash containing Re (He et al. 2018b). In pot experiments, Borago officinalis and Sinapis alba plants grown in soil containing 180 mg Cd/kg accumulated 109 mg Cd/kg in B. officinalis and 123 mg Cd/kg in S. alba, respectively, while in soil containing 2400 mg Pb/kg the accumulated metal concentrations were 25 mg Pb/kg (B. officinalis) and 29 mg Cd/kg (S. alba), respectively. (Evangelou et al. 2007).

7.5.2 Phytoremediation of Soils by Medicinal Succulents Succulent plants, which are characterized with thickened, fleshy and engorged plant parts adapted to drought, during regular drought utilize stored water for sustain metabolism. Drought-tolerant succulents can be used to attenuate adverse impact of climate change (Males 2017; Grace 2019). Plant parts of some succulents contain valuable secondary metabolites, which can be used in therapies as alternative medicines (Pattanayak et al. 2016), and some succulent plants were also shown to accumulate toxic metals, and therefore can be considered as potential phytoremediators of HM-contaminated arid and semi-arid soils (Ziarati et al. 2015; Vijayaraghavan et al. 2017; Sanchez-Gavilan et al. 2021). Investigation of phytoremediation of welding sites soil contaminated with Cr, Ni, Cu, Co, Pb and Cd using Aloe vera plants showed that BAF values for all HM were >1, and after 20 days the plants were able to take up Pb and Cu more efficiently than the other tested metals (Ziarati et al. 2015). On the other hand, A. vera plants grown on Cata mine tailing depot located in the outskirts of the city of Guanajuato, Mexico, accumulated only minute concentrations of Ag, Sn and B, but they reduced wind

7 Medicinal and Aromatic Plant Species with Potential for Remediation …

199

and water erosion (Cano-Resendiz et al. 2011). A. vera plants grown for one year in arid soils contaminated with 1500 ppm of toxic metals (As, Cd, Cr, Cu, Pb, Hg and Ni) and irrigated once a month with clean water accumulated the tested metals in plant organs, whereby the BAF values decreased in following order: Cr 2.478 (Cr) > 2.219 (Cd) > 2.197 (Hg) > 2.184 (As) > 1.992 (Ni) > 1.71 (Cu) > 1.578 (Pb) and the TF increased as follows: 0.677 (Cr) < 0.820 (Cd) < 0.836 (Hg) < 0.845 (As) < 1.008 (Ni) < 1.402 (Cu) < 1.729 (Pb); the percentage of accumulated metal allocated in A. vera shoots decreased as follows: 63% (Pb) > 58% (Cu) > 50% (Ni) > 46% (Hg and As) > 45% (Cd) > 40% (Cr). The highest metal accumulation was estimated for As; however, it decreased after 9 months of cultivation. The researchers did not recommend using this medicinal plant for phytoremediation of Hg-polluted soils (Elhag et al. 2018). Five plants of A. vera plants cultivated in 200 mL of nutrient solution containing 2 μg/L Hg accumulated in roots, stems and leaves 4.443, 0.245 and 0.771 μg Hg, respectively, whereby transfer rate of Hg from roots to shoots was 22.87%. With increasing Hg concentration in the nutrient medium the transfer rate decreased, suggesting that A. vera can be used for remediation of soils containing low Hg levels (Liu et al. 2017). The BCF for As estimated in Aloe barbadensis grown in soils contaminated with As and Sb were in the range of 0.05–0.07 and BCF of 0.07 observed for Sb suggested low transfer of metals from the soil to the roots. On the other hand, more effective translocation of metals from root to shoot was reflected in TF values of 0.29–0.67 and 0.51–0 0.89 evaluated for As and Sb, respectively. The levels of both toxic metals in A. barbadensis did not pose a threat for human consumption (Ong et al. 2018). In A. barbadensis exposed to sublethal doses of Zn the phytochelatins and metallothioneins detoxified metal ions by chelating and played considerable role in Zn phytoremediation. However, Zn doses >800 μM exhibited adverse impact on plants causing a pronounced reduction in the expression of the genes (Talukder et al. 2020). Medicinal drought-tolerant succulent plant Furcraea gigantea Vent. cultivated on Cr-spiked soil showed tolerance up to 50 mg Cr/kg soil and accumulated in its tissues 80%, suggesting that this medicinal shrub can be used for decontamination of soils containing low or medium Cr levels (up to 50 mg Cr/kg soil) (Ramana et al. 2015b). On the other hand, Euphorbia macroclada grown on soil containing 398 mg Sr/kg accumulated in shoots and roots 453 and 243 mg Sr/kg, respectively, while Sr concentrations in respective plant organs of the small woody evergreen shrub Astragalus gummifer grown in soil containing 469 mg Sr/kg soil were 278 and 223 mg/kg, respectively. As the mean observed TFs were 2.08 for E. macroclada and 1.18 for A. gummifer, these species can be used for remediation of Sr-polluted soils (Sasmaz and Sasmaz 2009). Echeveria elegans, a semi-desert succulent plant with pharmacological activity, cultivated on soil enriched with toxic metals and 137 Cs accumulated these elements predominantly in roots with BCF >1, and most effective accumulation was observed

200

K. Král’ová and J. Jampílek

for Pb and 137 Cs; BAF > 1 was estimated for Zn, Cu, Fe and Mn. Thus, E. elegans can be used to monitor soil contamination with HM and 137 Cs (Ortiz-Oliveros et al. 2021). Salicornia patula, an euhalophyte annual succulent species, is an edible plant containing high levels of essential minerals, and when cultivated on metalcontaminated soil it was found to uptake Zn, Cu, Pb, As and Sr in roots, however, without their translocation into the aboveground part, suggesting ability of S. patula to be used for phytostabilization of metal-polluted soils (Sanchez-Gavilan et al. 2021). Medicinal succulent plant Portulaca grandiflora grown 40 days on metal-spiked green roof substrate accumulated per kilogram 811 mg Al, 87.2 mg Cd, 416 mg Cr, 459 mg Cu, 746 mg Fe, 357 mg Ni, 565 mg Pb and 596 mg Zn, respectively; TF > 1 was observed for Zn, Fe, Cu and Al (Vijayaraghavan et al. 2017). Carpobrotus rossii (Haw.) Schwantes, a prostrate, succulent perennial medicinal herb, which accumulated 87 mg Cd/kg in shoots, doubled the accumulated Cd amount in the presence of salts (sulfates or nitrates) by increasing Cd mobility in soils. Consequently, this succulent plant can be used for removing Cd from soils showing high salinity (Zhang et al. 2016). Moreover, from soils showing multiple HM contamination this succulent plant efficiently accumulated beside Cd also other HM (Cu, Zn, Ni, Mn, Cr and Pb) (Zhang et al. 2015).

7.5.3 Phytoremediation of Soils by Medicinal Shrubs Medicinal shrubs cultivated on soil of Alacran gold-mining site, one of the most important artisanal and small-scale Au mining sites in Colombia, showing total Hg concentration (THg) 6022 ng/g (Jatropha curcas), 6267 ng/g (Ricinus communis) and 340.4 mg/g (Capsicum annuum) were evaluated for Hg levels in plants organs. The leaves of J. curcas contained 2782 ng Hg/g and estimated BCF, BAF and TF were 0.99, 0.62 and 0.62, respectively. The leaves of R. communis accumulated 1900 ng Hg/g, and BCF, BAF and TF were 0.83, 0.41 and 1.49, respectively; mean Hg level in leaves of C. annuum was 229.2 ng/g, and respective BCF, BAF and TF values were 0.83, 1.00 and 1.19, respectively. J. curcas and C. annuum were reported as promising to be used in the phytoremediation of soils in tropical areas. However, whereas root Hg concentrations were related to the soil Hg concentration, foliar uptake of Hg was mostly affected by Hg occurring in the atmosphere, and consequently, evaluated TF values are not a very accurate (Marrugo-Negrete et al. 2016). Chen et al. (2020) investigated Cd and Pb accumulations of low and high Cd in C. annuum cultivars exposed to 0.3 mg/kg Cd and 250 mg/kg Pb as well as to fivefold and tenfold higher concentrations of both metals. The treatment with the highest dose of Cd and Pb resulted in higher stimulation of the nitrate content in fruits than treatment with lower doses. Positive correlations were observed between Cd and Pb fruit concentrations with the shoot Cd and Pb concentrations as well as with TF in contrast to root Cd and Pb concentrations. At treatments with both lower doses of Cd and Pb, more effective Cd translocation from shoots to fruits was observed in

7 Medicinal and Aromatic Plant Species with Potential for Remediation …

201

high Cd cultivars compared to low Cd cultivars. According to the researchers, the movement of Cd and Pb into fruits occurs likely via phloem. Plant growth-promoting rhizobacteria Bacillus amyloliquefaciens ameliorated growth and fitness of C. capsicum plants exposed to abiotic stress, showed enhanced expression of XTH genes and reduced expression of WRKY2, BI-1, PTI1 and binding immunoglobulin protein genes. Consequently, it can be assumed that inoculation with B. amyloliquefaciens can exhibit beneficial impact on phytoremediation efficiency of pepper plants grown on metal-contaminated soil (Kazerooni et al. 2021). Shrubs Globularia alypum (showing beneficial effect to muscles and kidneys, able to reduce lipid peroxidation and improve antioxidant enzymes) and Rosmarinus officinalis grown in semi-arid area of a former lead smelting site (Marseille, France) showing a multicontamination by Pb, As, Sb, Zn and Cu were found to be tolerant to these HM and accumulated them in plant organs. Based on the low BCF and TF values, these species can be used for phytostabilization (Testiati et al. 2013). Application of CA (4 g/L, pH 2.9) and nutrient solution daily for 60 days to R. officinalis grown on pruning wastes and biosolids compost containing HM (Cd, Cu, Fe, Mn, Pb and Zn) resulted in 1.22-, 1.56- and 1.58-fold enhancement of leaf Cu, Fe and Mn concentrations, while the same treatment of Atriplex halimus shrub increased only Mn concentration (by 1.66-fold), suggesting that increased Fe and Mn solubility by CA ameliorated nutrition of plants (Tapia et al. 2013). R. officinalis is a Mediterranean shrub with strong pungent aroma. Its extracts are used in folk medicine to treat urinary diseases, chronic weakness, nervous disorder and peripheral vascular diseases (Anadón et al. 2021). In rosemary plants grown on soil contaminated with Pb, As, Sb, Zn and Cu, translocation of these contaminants to aerial parts was limited and the concentrations of Pb, As and Cu were below international regulation limits. EOs of these plants, which were characterized with enhanced synthesis of antioxidant compounds compared to control plants, can be considered as safe (Affholder et al. 2013). The translocation of As, Pb, Sb and Zn to shoots of R. officinalis plants was reduced with increasing soil contamination with monitored metals/metalloids, achieving saturation of 0.37, 7.9, 41 and 51.3 mg/kg for Sb, Pb, As and Zn, respectively; correlation was found between concentrations of accumulated metals/metalloids in shoots and the levels of thiols and phenols. Thiols were reported as crucial in ensuring rosemary tolerance to As, Pb and Sb. R. officinalis was recommended as suitable species for phytostabilization of metal-contaminated areas in the Mediterranean (Affholder et al. 2020). Phytoremediation of Fe ore mine soil containing HM performed using R. officinalis with assisting mycorrhizal arbuscular fungi Glomus mosseae and Glomus intraradices reduced toxic levels of Cd, Pb, Zn and Cu in soil to non-toxic levels; the accumulation of monitored metals in rosemary shoots and roots decreased in following order: Cu > Zn > Mn > Cd > Pb > Fe. The plants showing moderate tolerance to salinity and aridity absorbed toxic metals mostly via phytoextraction. Co-application of fibrous clay minerals immobilizing the metal contaminants to soil planted with R. officinalis can ameliorate soil remediation (Abbaslou et al. 2018). Limoniastrum monopetalum shrub, which leaf infusion shows antidysenteric properties against infectious diseases, exhibited good Cu tolerance; it accumulated

202

K. Král’ová and J. Jampílek

Cu in roots and was characterized with low Cu translocation to shoots, and consequently, as a Cu-excluder plant it is suitable for revegetation of Cu-polluted soils (Cambrolle et al. 2013a). In another paper, the researchers reported about hypertolerance of L. monopetalum to Zn stress when at leaf Zn levels of 1400 mg/kg d.m. its growth was practically unaffected; treatment with 130 mmol Zn/L resulted even in leaf concentrations of up to 1700 mg Zn/kg d.m. suggesting its potential to be used in the phytoremediation of Zn-contaminated soils. (Cambrolle et al. 2013b). Leaves of medicinal shrub Hibiscus mutabilis show anodyne, antidotal, demulcent, expectorant and refrigerant properties (Raut et al. 2014), while leaves of Hibiscus syriacus are diuretic, expectorant and stomachic (Hibiscus syriacus 2013). These shrubs show high yield when grown on soil spiked with Cu, Pb and Zn. Therefore, despite of low BCF and TF values, the observed final quantity of phytoextracted metals suggests that H. mutabilis and H. syriacus can be used for decontamination of soils containing HM (Vincent et al. 2018). Similar findings were obtained by Shang et al. (2020) at investigating phytoextraction of Cu and Zn by H. mutabilis. Hibiscus sabdarifa woody-based subshrub used in folk medicine as a diuretic, mild laxative, and for treatment of cardiac and nerve disease, which was grown on Cr polluted soil, accumulated only 10 mg/kg were phytotoxic and considerably reduced the growth of plants (Ramana et al. 2016). Sebania sesban is a deciduous, short-lived perennial shrub showing antidiabetic, anti-inflammatory and anthelmintic effects. In S. sesban plants cultivated in hydroponium in the presence of 50 mM Cd the addition of 0.2 mM Ca increased Cd uptake into roots, thereby increasing phytotoxicity of Cd; however, Cd translocation to the shoots was higher at application of 2 mM Ca compared to that observed with 10fold lower Ca concentration (Eller and Brix 2016). Cytisus scoparius is a deciduous leguminous shrub, which due to the presence of sparteine can be used as a cathartic and cardiac stimulant, and tips of its flowering shoots have diuretic, emetic and vasoconstrictor activity (Cytisus scoparius 2016). C. scoparius grown in soils from the abandoned Pb/Zn mine of Rubiais (NW Spain) with high Cd, Pb and Zn content accumulated Zn and Pb in roots, while Zn was also accumulated in the aerial part, and Cd was mostly excluded from C. scoparius tissues. It can be used for the restoration of mine soils acting simultaneously as Zn accumulator, Pb phytostabilizer and as Cd excluder (Lago-Vila et al. 2019). Acacia farnesiana showing various uses in traditional medicine is a As-tolerant shrub, which accumulated approx. 940 and 4380 mg As/kg d.m. in shoots and roots, respectively, when exposed for 60 days to 0.58 mM As(V). Treated A. farnesiana plants showed a growth delay during the first two weeks of the experiment, when the As uptake rate was fastest (reaching 117 mg/kg per day), indicating strong lipid peroxidation and the strongest up-regulation of activities of peroxidases and glutathione S-transferases (GST) enzymes. Strong correlation was observed between activity of GST and bioaccumulated As. The high tolerance of A. farnesiana to As(V) was reflected in half-inhibitory concentration (IC50 ) of ca. 2.8 mM (Alcantara-Martinez et al. 2016).

7 Medicinal and Aromatic Plant Species with Potential for Remediation …

203

Purshia mexicana is a blooming cliffrose shrub, leaves of which are used as a cold remedy, taken as a laxative, for arthritis, and for venereal diseases. P. mexicana growing in mine tailings in Zacatecas, Mexico, containing HM accumulated in shoots 268 mg As/kg and was reported to be suitable for revegetation of the mining wastes in arid and semi-arid regions (Salas-Luevano et al. 2021). The phytoremediation efficiency of Atriplex halimus L, a xero-halophyte shrub exhibiting hypoglycemic activity, which was tested in two mine soils containing HM (Cd, Pb and Cu) contaminants, was enhanced by the addition of spent mushroom compost (SMC). At the presence of SMC soil pH increased, the mobility of the metals was reduced, growth of A. halimus plants was ameliorated, whereby the metals were primarily immobilized in roots and their translocation to shoots showed a decrease, suggesting that addition of SMC enhanced phytostabilization potential of A. halimus in acidic mine soils (Frutos et al. 2017). A. halimus growing in a pine bark compost substrate (pH 5.6) supplemented with 100 mg Cd/kg for 70 days accumulated in its roots, stems and leaves 20.6, 35.2 and 34.7 mg Cd/kg d.w., respectively. The respective BAF of 0.36, TF of 1.68 and 86% of the total accumulated Cd amount allocated in shoots suggested phytoextraction potential of this plant for Cd (Tapia et al. 2011). Elaeagnus commutata shrub grown on Alaska military training lands was able effectively bioconcentrate Sb, Ni and Cr with low TF, and it can be used in combination with forb and grass for phytostabilization of HM in Alaska soils (Busby et al. 2020). Strong decoction of the bark of this shrub mixed with oil can be used as a salve for children with frostbite. Calotropis procera Linn. shrub with lavender flowers and cork-like bark is an Ayurvedic plant, powered roots of which were traditionally used to treat bronchitis, asthma, leprosy or eczema, and can also act as a laxative (Meena et al. 2011); it is also nowadays intensively investigated for its potential pharmacological applications (Kaur et al. 2021). C. procera is suitable for phytostabilization of soils contaminated with As and HM (Varun et al. 2012) and can be also used for phytostabilization of tannery contaminated soil (Rani et al. 2018). Roots of C. procera grown at a traffic-polluted site accumulated Fe, Mn, Sr and Zn with low translocation of metals to aboveground parts. However, metabolically less-active old leaves of C. procera accumulated considerably higher levels of metals (particularly Fe and Sr) than other plant parts and served as sinks for HM, whereby bioconcentration and accumulation of Fe and Sr exceeded that observed for Zn and Mn (Almehdi et al. 2019). Avicennia marina is a mangrove shrub, leaf extracts of which show antibacterial, antiulcer, anti-inflammatory, antiviral/anti-HIV, anticancer and antidiabetic activities, and were also used for treatment of smallpox lesions in Persian folk medicine (Thatoi et al. 2016). Leaf and root extracts of Plutea indica shrub exhibit similar biological activities as A. marina (Cho et al. 2017). Both shrub species grown in mangrove forests in Pattani Bay, Thailand, were tested for accumulation of radionuclides. In roots of A. marina 232 Th and 40 K activity concentrations of 24.6 Bq/kg and 227.9 Bq/kg, respectively, were estimated, while in P. indica roots 232 Th and 40 K activity concentrations were 18.0 and 220.7 Bq/kg, respectively. Both medicinal

204

K. Král’ová and J. Jampílek

shrubs were evaluated as excluder species suitable to be used for mangrove forest restoration in radionuclide-contaminated environment (Kaewtubtim et al. 2017). Pharmacological activities of some medicinal shrubs are shown in Table 7.3.

7.5.4 Phytoremediation of Soils by Medicinal Trees Trees play important role in moderating the climate because they remove CO2 from the atmosphere, are able to store great amounts of C and release substantive O2 amounts into the atmosphere (Masaroviˇcová and Kráˇlová 2018; Lewis et al. 2019; Domke et al. 2020). For example, the net annual carbon sequestration rate observed for fast-growing Eucalyptus plantations was 6000 kg C/ha per year (Kaul et al. 2010). Leaves, bark and roots of medicinal tree species containing valuable secondary metabolites have been used since ancient times for healing purposes (Alamgir 2020) and served as inspiration for the design of modern synthetic drugs. For example, salicin (β-O-glucoside of saligenin) extracted from Salix alba bark is converted to salicylic acid by the liver and has fewer side effects than aspirin (Banu and Lunghar 2021). Pharmacological activities of some medicinal trees are shown in Table 7.3. Trees, including medicinal trees, can be particularly useful for phytoremediation of soils contaminated with HM, e.g., mine tailings, sewage sludge, land near mining areas or for biomonitoring of trace elements and radionuclides in urban air (Anicic et al. 2011; Todorovic et al. 2013; Prasad et al. 2015; Mleczek et al. 2019; Deng et al. 2020). To achieve the best possible restoration of areas polluted with toxic metals using trees thoughtful selection of the mixture of tree species, including medicinal trees capable efficiently retain these metals, is needed (Samara et al. 2020; Deng et al. 2020; Mleczek et al. 2019). Using trees producing large biomass can be despite of their lower metal accumulation in shoots considered as an alternative to metal hyperaccumulating plant species for environment-friendly removal of toxic metals from soils. Soil pH < 9 and extreme high Ca concentration can contribute to improved ability of trees to survive in harsh conditions characterized with high contamination with toxic metals (Budzynska et al. 2022). On the other hand, an extensive root system of fast-growing trees enables them efficacious uptake of water contaminated with toxic metals from the substrate situated in greater depth (Stomp et al. 1993; Masaroviˇcová and Kráˇlová 2018). Six medicinal tree species, Acer platanoides L., A. pseudoplatanus L., Betula pendula Roth, Quercus robur L., Tilia cordata Miller and Ulmus laevis Pall. grown on mining sludge containing As, Cd, Cu, Pb, Tl and Zn accumulated As, Cd, Cu, Pb and Tl mostly in roots, while Zn was allocated mainly in shoots, achieving even 5732 mg /kg and 5801 mg/kg for A. platanoides and U. laevis, respectively. A. platanoides showed BCF of 1.41 for Tl but TF < 1, suggesting that it could be used for phytostabilization of this trace element (Mleczek et al. 2017). Seven investigated medicinal tree species grown close to the Pb and Zn smelting industrial complexes had considerably higher mean metal contents in leaves than control species, and high

7 Medicinal and Aromatic Plant Species with Potential for Remediation …

205

correlation was observed with respective metal concentrations in soils. Thuja orientalis was evaluated as the best phytoextractor for Fe, Populus nigra accumulated the highest amounts of Mn, Zn and Cd and as best Pb accumulator Cupressus sempervirens var. arizonica was appreciated (Saba et al. 2015). Comparison of the ability of elder, linden and pine leaves for biomonitoring of the atmospheric deposition of metals near Cu smelter showed that elder leaves were the most suitable. While As accumulated in leaves/needles of the investigated trees mainly from atmosphere, accumulated Cu and Pb originated from soil (Kalinovic et al. 2016). Tilia cordata (2-year-old) trees grown in pots on mining sludge showing high pH, salinity and huge As concentration accumulated Ba, Nb, Rb and Se, and were able to phytostabilize Pd, Ru, Sc and Sm, whereby translocation of metals to leaves was limited. T cordata was less tolerant to metal contaminants as A. platanoides, which showed ability to phytostabilize Pd, Ru, Sc, Sm, Ba and Nd (Drzewiecka et al. 2019). Evaluation of phytoremediation ability of some medicinal tree species in six European cities and towns showed that Aesculus hippocastanum can effectively accumulate Ni, Cu, As and Pb, while T. cordata accumulated Al, Fe and Cu (Gorelova et al. 2011). Based on the evaluation of the uranium contamination levels of riparian forest stands in U mining areas, A. hippocastanum accumulating in leaves 51.8 mg U/kg dry ash (DA) along with 0.73 mg Cd/kg DA, 24.7 mg Cu/kg DA, 326 mg Pb/kg DA and 38.6 mg Zn/kg DA was recommended as appropriate species for phytoremediation (Pecina et al. 2020). Comparison of metal bioaccumulating ability of Sambucus nigra, Salix sp. and Alnus glutinosa grown on location with high occurrence of As and Sb at abandoned Sb mining deposits showed that Sambucus nigra accumulated the highest amounts of Pb and Sb, while Salix sp. were able to accumulate high As, Cd and Zn concentrations in leaves (Molnarova et al. 2018). As suitable candidate for phytoremediation of Pb- (Abbasi et al. 2017) and Cd-polluted soil (Zeng et al. 2018), medicinal tree Platycladus orientalis was reported. The presence of growth-promoting bacteria in the rhizosphere of Salix species pronouncedly increased growth of Salix genotypes resulting in increased Cd accumulation from Cd-contaminated soil, since these microbes significantly increased willow growth. On the other hand, the impact of arbuscular mycorrhizal fungi in the rhizosphere on the Cd content in plant tissues depended on individual willow genotype (Wang et al. 2021b). Co-inoculation of Salix integra Thunb plants with either Bacillus sp. or Aspergillus niger resulted in improved plant growth, although increase in Pb accumulation was observed only by single inoculation, when also accumulation of Pb in aerial plant part was stimulated. Inoculation enhanced antioxidant defenses of S. integra and modified bioavailability of Pb, and the researchers assumed simultaneous colonization of the soil and plants by microbial strains, whereby the different living condition affected the metabolite profiles (Niu et al. 2021). Azadirachta indica plants grown in soils of various towns containing 6716– 9119 mg Fe/kg and 354–746 mg Mn/kg accumulated in leaves 1583–2315 mg Fe/kg d.w. and 93.8–159 mg Mn/kg d.w. (Umer et al. 2022). In A. indica trees gown in soils contaminated by industrial effluent discharge and containing high levels of Fe, Cu, Zn, Pb and Mn, TF > 1 was observed for Cd, Cu, Fe, Pb and Zn and BAF

206

K. Král’ová and J. Jampílek

(leaves) > 1 was estimated for all monitored metals except for Zn and Ni. Thus, A. indica can be recommended for phytoextraction of HM in polluted soils (Arise et al. 2021). A.indica trees irrigated in greenhouse with industrial wastewater accumulated in leaves, stem and roots 108.5, 46.2, 180.5 mg Pb/kg, showed approximately 148% increase in H2 O2 production, and effective antioxidative defense mechanism of metal-stressed plants was reflected in pronouncedly increased levels of antioxidant enzymes (Hussain et al. 2021). Values of BAF related to metals accumulated in A. indica and Cassia fistula grown on fly ash-contaminated soils in suburban area decreased in following order: Fe > Cd > Cr > Zn > Ni > Mn > Cu > Pb. On the other hand, for the decrease of BCF following rank was observed: Fe > Cd > Zn > Ni > Mn > Pb > Cu > Cr for A. indica and Fe > Cd > Zn > Ni > Cr > Cu > Mn > Pb for Cassia fistula (Qadir et al. 2021). From five medicinal trees tested for Cr phytoextraction from Cr-containing tannery effluent-contaminated soil higher amounts of Cr in both the roots and stems were observed in A. auriculiformis, while Dalbergia sisso and Thespesia populnea accumulated more Cr in the roots, in contrast to A. indica, Albizzi richardiana and Albizzia lebbeck, which accumulated higher Cr concentrations in stems (Manikandan et al. 2016). Fast-growing medicinal trees A. indica, Acacia mangium, Eucalyptus camaldulensis and Senna siamea tested for phytoextraction of Pb in hydroponium containing 10 mg Pb/L achieved BCF of 869.7, 1836, 1808 and 905.2, respectively, while the respective TF values were low (0.19, 0.02, 0.02 and 0.03, respectively) suggesting suitability of these trees to be used for phytostabilization of Pb-contaminated areas (Yongpisanphop et al. 2017). Metal-polluted Hindon river water containing 11.27 ppm Fe, 4.00 ppm Mn, 0.08 ppm Cd, 0.63 ppm Ni, 1.46 ppm Zn affected mean concentrations of these metals in two riparian species, A. indica and Acacia nilotica trees, which reached 1.44-, 1.39-, 2.50-, 5.13- and 1.72-fold higher levels of Fe, Mn, Cd, Ni and Zn in A. indica than in control and 1.65–1.85–1.40-, 1.74- and 1.49-fold higher levels in A. nilotica compared to control. However, with the exception of Zn, the absolute accumulated concentrations of Fe, Mn, Cd and Ni were higher in A. nilotica (Ruhela et al. 2019). Eucalyptus globulus planted with rotation period of 9 years, when E. globulus plants were not cut, was shown as best solution for remediation of soil contaminated with Cd, Pb and Cu and brought the highest economic benefit (Xing et al. 2019). Eight-month-old E. globulus plants grown in pots and treated for four times (every 2 months) with 100 and 200 μg As/mL, accumulated after 6 months period 8.19 and 8.91 mg As, respectively; the majority of accumulated As was allocated in roots and treatment with a higher dose caused pronounced reduction of root biomass but did not affect leaf biomass. Root uptake of As by E. globulus showed antagonistic effect on Zn root uptake (Reboredo et al. 2021). In E. globulus grown on mine-contaminated soil higher metal concentration was accumulated in roots compared to leaves. The respective values for metal accumulation in roots/leaves in μg/g were 0.325/0.081 for Cr, 0.401/0.250 for Cu, 1.787/0.904 for Zn, 0.290/0.021 for Pb and 213.392/4.304 for Fe. Cd was estimated only in roots (0.019 μg/g) showing BCF of 0.0006. Values of BCF estimated for individual metals increased as follows: Cd < Cr < Fe < Cu < Zn < Pb, while BAF related to plant leaves increased in following order: Fe < Cr < Zn
Zn (0.506) > Cr (0.249) > Pb (0.072) > Fe (0.034). Considering that the photosynthetic efficiency, pigment content and growth of E. globulus were not considerably affected it can be stated that this tree is suitable to be used for phytoremediation of soils contaminated with HM (El Rasafi et al. 2021). Treatment with EDTA can contribute to more effective phytoextraction of Cd, Pb and Cu from contaminated soil by E. globulus but such treatment is accompanied with more leachate and has adverse impact on living organisms. However, by foliar spraying of cytokinin, which accelerates the transpiration rate of the plant, the negative effects of EDTA can be suppressed, biomass yield will be enhanced, and leachate volume reduced (Luo et al. 2017). The biomass of E. globulus treated by electric field voltage of 6.5 V supplied by storage battery and solar cell, respectively, increased 1.33- and 1.63-fold compared to control, and phytoextraction of Cd, Pb and Cu increased as well. On the other hand, volume of leachate was reduced to 29.6 and 32.2% of the control, and the leaching mass of monitored metals decreased as well. The researchers stated that application of solar cells could be good alternative for amelioration of phytoremediation efficiency in metal-contaminated soil and can reduce energy consumption from conventional power sources (Luo et al. 2019c). Direct current field with moderate voltage increased the root and shoot metal contents in E. globulus used for phytoremediation of contaminated e-waste recycling site, and more metals accumulated in soil surface compared to treatment with alternating current (Luo et al. 2018a). Although chelator-assisted phytoremediation efficiency was stimulated more by using alternating current field compared to application of direct current field, due to higher leaching risk, it is less favorable than treatment with direct current field with moderate voltage (Luo et al. 2018b). Luo et al. (2018c) also recommended a moderate harvest protocol using the medium planting density of E. globulus to achieve good remediation efficiency for phytoremediation of sites contaminated with e-waste containing HM. The amelioration of phytoremediation efficiency of E. globulus grown in HM-polluted soil along with alleviation of leaching risk was observed at irradiation of red and blue light combined in varying proportions. Using such irradiation, the Cu removal increased by 28.9– 70.6%, and the removal of Pb and Cd by 71.1–88.7% and 50.6–65.6%, respectively, and the leachate volume was reduced by 46.7–66.0% compared to control irradiated with blue/red light combination with a ratio 1:9. On the other hand, irradiation with monochromic red light inhibited shoot growth, which was reflected in increasing remediation time by 137.9% (Pb), 218.7% (Cu) and 338.9% (Cd), respectively (Luo et al. 2019a). E. globulus treated by static magnetic field of 150 mT before sowing enhanced its phytoremediation efficiency, shortened the time needed to remove Cd, Pb and Cu by 27.8–73.2%, 27.3– 74.7% and 2.5–50.6%, respectively, and ceased 31.6–86.1% of the leachate. At application 150 mT biomass yield increased by 60.9%; due to higher transpiration rate resulting in lower soil moisture content it was able to reduce the leachate volume (Luo et al. 2019b). E. globulus trees cultivated in polluted areas produced more biomass and take up more Cd and Hg per year compared to individuals cultivated in clean soils (Luo et al. 2016). Mughini et al. (2013) recommended the use of hybrid Eucalyptus clones producing large biomass and effectively accumulating As, Cd, Cr, Pb, Cu and Zn in leaves, stems and branches

208

K. Král’ová and J. Jampílek

for both biomass production and phytoremediation in Mediterranean-type environments. The concentration of HM in the tissues of Eucalyptus hybrid trees grown in reclaimed overburden dumps of 30 years age was 1.12–105-fold higher compared to trees grown on control soils; based on observed BCF > 1 and TFs estimated for leaves and stem bark, the trees can be recommended for phytoextraction of Mn. On the other hand, for Cu BCF > 1 was estimated and TFs for leaf, stem bark and wood of aboveground part were < 1, suggesting suitability of this tree species for phytostabilization of Cu (Bandyopadhyay and Maiti 2019). In another study, it was found that Eucalyptus hybrid grown in metal-contaminated reclaimed mine soil showed higher metal accumulation in plant organs compared to trees grown on control soils, reaching 3-fold higher levels of Pb in bark, 4.5- and 19-fold higher levels of Zn and Mn in leaves, and 1.4-fold higher Cu concentration in roots (Maiti and Rana 2017). Clones of Eucalyptus camaldulensis Dehnh. x E. globulus subsp. bicostata, which were cultivated in hydroponic solution for 3 weeks in the presence of 50 μM CdSO4 accumulated Cd mostly in roots with low translocation to shoots, showed good tolerance to Cd and can be also used in phytoremediation of Cd-contaminated wastewaters, whereby by harvesting of root biomass absorbed Cd can be removed (Iori et al. 2017). Following inoculation of endophytic strain, Chaetomium cupreum in E. globulus expression of 663 genes was changed, 369 of which were up-regulated and 294 were down-regulated; increased tolerance to metals and growth stimulation of inoculated plants was observed (Ortiz et al. 2019). The shoot dry weight, tolerance to Zn and Zn uptake of E. globulus inoculated by arbuscular mycorrhizal fungus Glomus deserticola can be enhanced by the presence of saprophytic fungi Trametes versicolor and Coriolopsis rigida (Arriagada et al. 2010). El-Khatib et al. (2020a) evaluated the composition of HM in soil and atmospheric dust as well as in leaves and bark of Ficus nitida and E. globulus trees grown in urban areas with heavy traffic load and industrial zones. They found that in tested samples, the metal concentrations decreased as follows: Pb > Cu > Cd, whereby accumulated Pb originated primarily from the atmospheric dust but the accumulation of Cu by trees was low (in contrast to Pb and Cd captured from air), suggesting the suitability of both trees to be used for remediation of areas with atmospheric pollutants. In another study, El-Khatib et al. (2020b) found that Cd, Pb and Cu inhibited the growth, leaf area and specific leaf area of F. nitida and E. globulus and increasing concentrations of metals resulted in reduced water content, Chla and Chlb levels and soluble carbohydrate content, while considerable increase of Chla/Chlb ratio and concentration of carotenoids was observed. In general, F. nitida showed less tolerance to monitored HM than E. globulus. In olive trees (Olea europea L.) grown under high levels of atmospheric Hg and irrigated with mineral water, which was free of Hg, the total concentrations in leaves ranged from 26 to 333 ng Hg/g (mean: 145 ng Hg/g), whereby continuous Hg exchange at the leaf-atmosphere interface occurred. After relocation of these trees in environment with low levels of atmospheric Hg, desorption process was observed suggesting that Hg bioaccumulation by plant is likely a reversible process (Naharro et al. 2019).

7 Medicinal and Aromatic Plant Species with Potential for Remediation …

209

Robinia pseudoacacia and Ulmus pumila medicinal trees, and deciduous shrub Hippophae rhamnoides characterized with noticeable biomass, which were grown in soil contaminated by HM in coal mine wastelands showing moderate Cd contamination and high levels of Ni, Zn, and Cu, were evaluated as species suitable for vegetation restoration (Shi et al. 2016). After exposure of R. pseudoacacia seedlings to elevated levels of CO2 and Cd for 4 years the abundance of soil microbial communities in the rhizosphere increased and changes in microbial diversity were observed due to enhanced nutrient content in rhizosphere soils; under elevated levels of CO2 total and soluble Cd levels in rhizosphere soils showed a decrease (Jia et al. 2020). Inoculation of R. pseudoacacia with the endophyte Enterobacter sp. YG-14 pronouncedly enhanced Cd accumulation, which was explained with chelating of huge amounts of Cd in the roots with siderophores released by the strain YG-14 or by formation of Cd complexes with organic acids released by the endophyte under Cd stress resulting ultimately in suppressed Cd translocation into the shoots. Moreover, enhanced phytostabilization of Cd in the soil can be achieved by co-application of biochar resulting not only in improved plant growth but also in considerable enhancement of Cd accumulation along with reduction of TF (Zhang et al. 2021). Evaluation of the impact of R. pseudoacacia planting on a Zn smelting slag site after 7 years showed that phytostabilization markedly decreased available concentrations of As and Sb in soil as well as their accumulated amounts in plants, the lowest concentrations being observed in stems (Sun et al. 2021). Based on the investigation of the impact of Pb(NO3 )2 and Pb(CH3 COO)2 on seed germination, growth of roots and stems, and seedling fresh biomass, seedlings of medicinal trees Amaorpha fruticosa and Platycladus orientalis were found to be tolerant to Pb contamination and can be used for phytoremediation purposes. On the other hand, low tolerance of Hippophae rhamnoides to Pb predestines it to be used as an indicative plant able to detect Pb toxicity (Yang et al. 2016).

7.6 Impact of Soil Metal Contamination on Essential Oils of Medicinal and Aromatic Plants Essential oils (EOs) are concentrated hydrophobic liquids consisting of lipophilic volatile secondary plant metabolites, predominantly of mono- and sesquiterpenes, but they can contain also compounds such as allyl and isoallyl phenols, coumarins, anthraquinones and alkaloids. EOs contain a mixture of fragrant and odorless compounds, whereby fragrant compounds are volatile under normal conditions (Rios 2016). Numerous compounds from EOs show pronounced pharmacological activities, and EOs were used from ancient time for religious purposes and healing. Manniche (2006) described 94 plant and tree species, which were used before, during and after the Pharaonic period in Egypt. In ancient Egypt, great number of plants were utilized for medicinal application perfumes, cosmetics, food or funerals, which is also confirmed by some 4000 years old medical texts. Aromatherapy was also

210

K. Král’ová and J. Jampílek

first used in the Temple of Edfu ca. 265 BC, where soothing or healing ointments were prepared according to recipes written on the walls of the Laboratory (DePrado 2018). In ancient times, the use of EOs was popular throughout the world, including China, India, Persia and Greece (Schnaubelt 2005; Morgan 2021). Biochemical pathways and enzymatic reactions involved in biosynthesis of EOs in aromatic plants were reviewed by Rehman et al. (2016). Many wild MAPs producing EOs grow on soils polluted with HM. Beside promising results obtained with such species in remediation of HM-polluted areas, it was observed that the presence of toxic metals in soils and hydroponic solution or foliar applied metals, whether in bulk of nanoform, considerably improved EO yields (Lafmejani et al. 2018; Rezaizad et al. 2019; Shabbir et al. 2019; Gohari et al. 2020; Shahhoseini et al. 2020; Kráˇlová and Jampílek 2021). However, use of EOs for healing purposes or their application in food industry requires EOs free from toxic metals, and therefore increased attention of researchers was focused on investigation of the impact of soil HM contamination on quantity and quality of produced EOs as well as on potential contamination of EOs with metals. In the majority of performed investigations, significant increase of EO yields in plants cultivated in HM-polluted soils was observed, and in numerous cases also the quality of EOs was improved; presence of toxic metals in EOs was not detected or achieved only negligible levels, which do not threat human health (Zheljazkov et al. 2008; Pandey et al. 2019b). Beneficial impact on yield and quality of EOs in geranium plants cultivated in contaminated sludge was reported by Mazee et al. (2020), and free of HM were also EOs of medicinal plants (thyme, sage and chamomile) grown on HM-contaminated soils (Lydakis-Simantiris et al. 2016). Investigation of the impact of soil Cr and Pb concentrations on EO yield and composition of mint species showed that EO yield of Mentha piperita increased but decreased in M. citrata. At Cr and Pb concentrations of 30 and 60 mg/kg soil the levels of α-pinene, β-pinene, sabinene, β-myrcene, limonene, menthone and isomenthone in EOs of M. arvensis and M. piperita and those of sabinene, pinene and linalyl acetate in the EO of M. citrata were considerably affected compared to respective EOs of control plants (Prasad et al. 2010). In the composition of Mentha spicata EO grown on Cu-, Cd- and Pb-amended soil no pronounced change compared to control was observed and the metal levels were below detectable limit, but the yield of EOs increased from 0.3 to 0.6 and 1%, respectively. In O. basilicum EO the Cu, Cd and Pb concentrations also were below detectable limit, and EO yield increased from 0.4 to 0.7 and 0.5%, respectively (Kunwar et al. 2015). Cd stress affected EO composition in M. piperita plants and with increasing Cd concentration reduced menthol levels were observed, while the levels of menthofuran and pulegone increased (Azimychetabi et al. 2021). Positive impact of Cd stress on the increase of EO yield and carvacrol levels in Satureja hortensis plants was also reported by Azizollahi et al. (2019). However, reduction of menthol concentrations in M. piperita due to Cd stress can be mitigated by treatment with salicylic acid (Ahmad et al. 2018). EO yield of O. basilicum plants grown on Cd (5–20 mg/kg soil) and Pb (100–400 mg/kg soil)spiked soils varied from 0.28 to 0.39% (v/w), although higher metal concentrations adversely affected seed germination and morphological traits of plants (Fattahi et al.

7 Medicinal and Aromatic Plant Species with Potential for Remediation …

211

2019). Similar results concerning EO of basil plants grown on soils amended with Cd and Pb were obtained by Youssef (2021). Tagetes minuta plants grown near a battery recycling plant in soil highly contaminated with Pb were tolerant to Pb and accumulated Pb it in their tissues, however, in the EOs extracted by hydrodistillation detectable Pb levels were not observed, although β-ocimene and α-thujone levels showed correlation with soil Pb content (Sosa et al. 2016). In M. piperita, O. basilicum and Anethum graveolens plants, which were grown in soil and watered with solutions of HM (Cu, Pb and Cu), the EO content in leaves and the composition of their EOs was not pronouncedly changed compared to control plants, although menthol content showed a decrease. Reduced EO content in dill was observed at treatment with 150 mg/L of Cu, and reduction of EO content in basil was observed at simultaneous exposure to all three metals. On the other hand, no detectable concentrations of HM in EO of tested plants were found suggesting that during steam distillation the HM were not removed from plant tissues (Zheljazkov et al. 2006). In EO of Artemisia absinthum L. grown in soil originating from a NonFerrous-Metal Works near Plovdiv, which was contaminated with HM such as Cd, Pb and Zn, the levels of α-myrcene, sabinene, β-linalool, (E)-β-cryophyllene, cembrene, β-elemene, lavandulol and cis-sabinene hydrate showed a decrease, while terpinene-4-ol, phytol, γ-terpinene, p-cymene, α-terpinene, α-pinene and (E)-9-epicaryophyllene significantly increased compared to control. The HM content in the EOs was significantly lower than in leaves and flowering tips of plants, and HM concentrations in EOs were lower than the accepted maximum values (Angelova 2020). Previously, it was found that the HM did not affect quality and quantity of EO of Lavandula vera L. plants grown on abovementioned HM-contaminated area near Plovdiv (Angelova et al. 2015). In EOs of coriander and sage grown on HM-contaminated agricultural soil containing 394 ppm Pb, 443 ppm Zn and 7.2 ppm Cd, the detected HM concentrations were below or close to the limit of quantification of the used method (Raveau et al. 2021). Similar results were obtained with EOs of Salvia sclarea and Coriandrum sativum grown on an area contaminated with Cu, Zn, Ni, Cd, Pb, As and Sb; however, the coriander distillation residues contained increased levels of Cd, which limited their further use (Perlein et al. 2021). Whereas EO quality and quantity was affected not even in M. recutita (Stancheva et al. 2014a) or Salvia officinalis plants (Stancheva et al. 2010) grown on soil industrially contaminated with HM, reduced yield of EOs was observed in O. basilicum grown on soil polluted with HM (Stancheva et al. 2014b). No detectable concentrations of As, Cd, Pb and Zn in EO of M. recutita plants grown on HM-contaminated soils were found by Szakova et al. (2018), although the abundance of the individual compounds in EO was changed. Harvesting season and soil HM contamination were found to affect the yield and composition of the EO of Mentha longifolia in the Egyptian watercourses (Gharib et al. 2021). It can be stated that MAPs cultivated on HM-contaminated areas mostly achieved higher EO yield with convenient or improved EO composition compared to plants

212

K. Král’ová and J. Jampílek

grown on uncontaminated soil, whereby their EOs were free of toxic metals and thus, can be utilized as a marketable product providing economic return.

7.7 Conclusion Massive contamination of the soil with heavy metals worldwide, mostly due to intensified anthropogenic activities, contributes significantly to reduced crop yields and can endanger the health of the human population when consuming crops accumulating higher levels of toxic metals in the edible parts of plants. Due to the wide application of harmful chemicals in industrial production and agriculture, the use of low-cost ecological methods such as phytoremediation is desirable for cleaning environmental matrices from toxic metals. Effective phytoremediation requires careful selection of suitable plant species showing high tolerance to the metal contaminants to be removed, considering the chemical properties of the contaminants, the soil properties and the presence of the contaminant in the soil layers (surface of deeper layers). Therefore, fast-growing, non-edible and deep-rooting metal-tolerant plants with an extensive root system and rich biomass as well as hyperaccumulator plant species capable of storing significant concentrations of toxic metals in their aerial parts without adversely affecting plant growth and fitness are favorable. Metal-tolerant MAPs have the potential to be used to clean soils containing low and medium levels of toxic metals, because metal stress induces defense mechanisms in the plants, leading to increased production of essential oils containing medicinal secondary metabolites and antioxidant compounds. In addition, after recovery of essential oils, the residues of some MAPs can be used to produce energy and biofuels, thus increasing the economic profit from cultivation of these plants on areas contaminated with metals. Plants, which are capable selectively concentrate specific metals in their aboveground parts, can also be used for phytomining enabling commercial exploitation of these metals after harvest. Cleaning soils from toxic metal contaminants using MAPs is a long-term process, the effectiveness of which can be improved by the application of microbially assisted and chelate-assisted phytoremediation. This requires ensuring an optimal selection of microorganisms with regard to the plant and the metal(s) to be removed. However, the selection of suitable chelating agents must consider their potential adverse environmental impact, and therefore, application of biodegradable chelators is desirable. It may also be advantageous to apply soil treatments, such as using of biochar to reduce the bioavailability of metals and prefer the use of plant species tolerant to multimetal stress. Advances in genetic engineering techniques make it possible to create transgenic plants with excellent metal accumulation/hyperaccumulation properties that can be used to effectively decontaminate metal-polluted soils. On the other hand, it is highly desirable to focus on phytoremediation experiments performed “in situ” in field conditions on metal-contaminated soils, as so far most published experiments have been performed in laboratory conditions, whether in hydroponics or in pots with artificially supplemented metals. Continuous search for new effective metal-accumulating/hyperaccumulating native

7 Medicinal and Aromatic Plant Species with Potential for Remediation …

213

MAPs is desirable as well. Intensive multidisciplinary research concerning molecular mechanisms involved in toxic metal stress can also help to achieve improved plant phytoremediation efficiency. In addition, cultivation of MAPs on metal-contaminated areas can also prevent the extinction of some endangered wild species. The United Nations General Assembly has declared 2020 the International Year of Plant Health and emphasized the important role of healthy plants in protecting the environment, economic development and raising people’s living standards. It can be stated that MAPs excellently meet these requirements by being able to produce essential oils with medicinal secondary metabolites, have the ability to decontaminate environmental matrices from metal contaminants and after recovery of essential oils allow further use of plant residues for energy or biofuel production, thereby enhancing economic profit.

References Abbasi H, Pourmajidian MR, Hodjati SM, Fallah A, Nath S (2017) Effect of soil-applied lead on mineral contents and biomass in Acer cappadocicum, Fraxinus excelsior and Platycladus orientalis seedlings. iForest 10:722–728 Abbaslou H, Bakhtiari S, Hashemi SS (2018) Rehabilitation of iron ore mine soil contaminated with heavy metals using rosemary phytoremediation-assisted mycorrhizal arbuscular fungi bioaugmentation and fibrous clay mineral immobilization. Iran J Sci Technol Trans A Sci 42(A2):431–441 Abduljawad EA (2020) Review of some evidenced medicinal activities of Acacia nilotica. J Pharm Pract 11(4):20–25 Adiloglu S (2020) Interaction of some heavy metals with copper content in dock plant. KSU J Agric Nat 23(4):1078–1084 Affholder MC, Prudent P, Masotti V, Coulomb B, Rabier J, Nguyen-The B, Laffont-Schwob I (2013) Transfer of metals and metalloids from soil to shoots in wild rosemary (Rosmarinus officinalis L.) growing on a former lead smelter site: human exposure risk. Sci Total Environ 454:219–229 Affholder MC, Laffont-Schwob I, Coulomb B, Rabier J, Borla A, Boudenne JL, Demelas C, Prudent P (2020) Implication of phytometabolites on metal tolerance of the pseudo-metallophyteRosmarinus officinalis-in a Mediterranean brownfield. Chemosphere 249:126159 Aftab T, Hakeem KR (2020) Plant micronutrients; deficiency and toxicity management. Springer, Cham Aftab T, Hakeem KR (2021) Medicinal and aromatic plants: expanding their horizons through omics. Elsevier, Amsterdam Ahatovic A, Cakar J, Subasic M, Hasanovic M, Murtic S, Durmic-Pasic A (2020) Plantago lanceolata L. from serpentine soils in Central Bosnia tolerates high levels of heavy metals in soil. Water Air Soil Pollut 231(4):169 Ahmad R, Misra N (2014) Evaluation of phytoremediation potential of Catharanthus roseus with respect to chromium contamination. Am J Plant Sci 5(15):2378–2388 Ahmad B, Jaleel H, Sadiq Y, Khan MMA, Shabbir A (2018) Response of exogenous salicylic acid on cadmium induced photosynthetic damage, antioxidant metabolism and essential oil production in peppermint. Plant Growh Regul 86(2):273–286 Ahmed D, Kumar V, Verma A, Gupta PS, Kumar H, Dhingra V, Mishra V, Sharma M (2014) Antidiabetic, renal/hepatic/pancreas/cardiac protective and antioxidant potential of methanol/dichloromethane extract of Albizzia lebbeck Benth. Stem bark (ALEx) on streptozotocin induced diabetic rats. BMC Complement Altern Med 14:243

214

K. Král’ová and J. Jampílek

Ahn K (2017) The worldwide trend of using botanical drugs and strategies for developing global drugs. BMB Rep 50:111–116 Aishah RM, Shamshuddin J, Fauziah CI, Arifin A, Panhwar QA (2019) Using plant species for phytoremediation of highly weathered soils contaminated with zinc and copper with application of sewage sludge. BioResources 14(4):8701–8727 Akeel A, Jahan A (2020) Role of cobalt in plants: its stress and alleviation. In: Naeem M, Ansari AA, Gill SS (eds) Contaminants in agriculture. Springer, Cham, pp 339–357 Akkus SO, Yaman B, Yaman M (2017) Assessment of phytoextraction potential of thirteen plant species for chromium and vanadium and their relationship with sulfur and histidine. J Elem 22(4):1387–1400 Alamgir ANM (2020) Pharmacological botany: classification of medicinal and aromatic plants (MAPs), botanical taxonomy, morphology, and anatomy of drug plants. In: Alamgir ANM (ed) Therapeutic use of medicinal plants and their extracts, vol 1. Springer, Cham, pp 177–293 Alamo-Nole L, Su YF (2017) Translocation of cadmium in Ocimum basilicum at low concentration of CdSSe nanoparticles. Appl Mater Today 9:314–318 Alcantara-Martinez N, Guizar S, Rivera-Cabrera F, Anicacio-Acevedo BE, Buendia-Gonzalez L, Volke-Sepulveda T (2016) Tolerance, arsenic uptake, and oxidative stress in Acacia farnesiana under arsenate-stress. Int J Phytorem 18(7):671–678 Alengebawy A, Abdelkhalek ST, Qureshi SR, Wang MQ (2021) Heavy metals and pesticides toxicity in agricultural soil and plants: ecological risks and human health implications. Toxics 9(3):42 Ali MA (2014) Cassia fistula Linn: a review of phytochemical and pharmacological studies. Int J Pharm Sci Res 5(6):2125–2130 Ali H, Khan E, Sajad MA (2013) Phytoremediation of heavy metals-concepts and applications. Chemosphere 91:869–881 Ali H, Khan E (2018) Trophic transfer, bioaccumulation and biomagnification of non-essential hazardous heavy metals and metalloids in food chains/webs: concepts and implications for wildlife and human health. Hum Ecol Risk Assess 25(6):1353–1376 Ali H, Khan E, Ilahi I (2019) Environmental chemistry and ecotoxicology of hazardous heavy metals: environmental persistence, toxicity, and bioaccumulation. J Chem 2019:6730305 Ali-Seyed M, Ayesha S (2020) Calotropis-a multi-potential plant to humankind: special focus on its wound healing efficacy. Biocatal Agric Biotechnol 28:101725 Almehdi A, El-Keblawy A, Shehadi I, El-Naggar M, Saadoun I, Mosa KA, Abhilash PC (2019) Old leaves accumulate more heavy metals than other parts of the desert shrub Calotropis procera at a traffic-polluted site as assessed by two analytical techniques. Int J Phytorem 21(12):1254–1262 Al-Senosy NK, Abou-Eisha A, Ahmad ES (2018) Cytotoxic effects of Atriplex halimus extract on human cancer cell lines. Biosci Res 15(3):1718–1728 Amiri A, Mottaghipisheh J, Jamshidi-Kia F, Saeidi K, Vitalini S, Iriti M (2020) Antimicrobial potency of major functional foods’ essential oils in liquid and vapor phases: a short review. Appl Sci 10:8103 Anadón A, Martínez-Larrañaga MR, Ares I, Aránzazu Martínez M (2021) Interactions between nutraceuticals/nutrients and nutrients and therapeutic drugs. In: Gupta RC, Lall R, Srivastava A (eds) Nutraceuticals, 2nd edn. Efficacy, safety and toxicity. Elsevier, Amsterdam, pp 1175–1197 Ananthi TAS, Manikandan PNA (2013) Potential of rhizobacteria for improving lead phytoextraction in Ricinus communis. Remediation 24(1):99–106 Andreazza R, Bortolon L, Pieniz S, Bento FM, Camargo FAO (2015) Evaluation of two Brazilian indigenous plants for phytostabilization and phytoremediation of copper-contaminated soils. Braz J Biol 75(4):868–877 Angelova V, Grekov D, Kisyov V, Ivanov K (2015) Potential of lavender (Lavandula vera L.) for phytoremediation of soils contaminated with heavy metals. Int J Biol Biomolec Agric Food Biotechnol Eng 9(5):522–529 Angelova VR, Ivanova RV, Todorov GM, Ivanov KI (2016) Potential of Salvia sclarea L. for phytoremediation of soils contaminated with heavy metals. World Acad Sci Eng Technol 780–790

7 Medicinal and Aromatic Plant Species with Potential for Remediation …

215

Angelova V (2020) Heavy metal accumulation and chemical composition of essential oils of wormwood (Artemisia absinthum) cultivated on heavy metal contaminated soils. Scientific papers. Series E. Land reclamation, earth observation & surveying. Environ Eng IX:44–52 Anicic M, Spasic T, Tomasevic M, Rajsic S, Tasic M (2011) Trace elements accumulation and temporal trends in leaves of urban deciduous trees (Aesculus hippocastanum and Tilia spp.) Arch Biol Sci 11(3):824–830 Anonymous (2016) State of the world’s plants, report 2016. KEW, Royal Botanic Gardens. Retrieved September 25, 2017 Ansari AA, Gill SS, Gill R, Lanza GR, Newman L (2015) Phytoremediation, vol 2. Springer, Cham Ansari AA, Gill SS, Gill R, Lanza GR, Newman L (2016) Phytoremediation, vol 4. Springer, Cham Ansari AA, Gill SS, Gill R, Lanza GR, Newman L (2017) Phytoremediation, vol 5. Springer, Cham Antonijevic MM, Dimitrijevic MD, Milic SM, Nujkic MM (2012) Metal concentrations in the soils and native plants surrounding the old flotation tailings pond of the Copper Mining and Smelting Complex Bor (Serbia.). J Environ Monit 14(3):866–877 Anum S, Khan SM, Chaudhary HJ, Ahmad Z, Afza R (2019) Phytoremediation of nickel polluted ecosystem through selected ornamental plant species in the presence of bacterium Kocuria rhizophila. Bioremediation J 23(3):215–226 Arise RO, Basiru DI, Olufemi O, Adeoye RI (2021) Biochemical transmutation in Lumbricus terrestris and phytoextraction of heavy metals from the swamp of Challawa industrial layout, Kano Nigeria. SN Appl Sci 3(3):362 Arriagada C, Pereira G, Garcia-Romera I, Ocampo JA (2010) Improved zinc tolerance in Eucalyptus globulus inoculated with Glomus deserticola and Trametes versicolor or Coriolopsis rigida. Soil Biol Biochem 42:118–124 Asiminicesei DM, Vasilachi OC, Gavrilescu M (2020) Heavy metal contamination of medicinal plants and potential implications on human health. Rev Chim 71(7):16–36 Azimychetabi Z, Nodehi MS, Moghadam TK, Motesharezadeh B (2021) Cadmium stress alters the essential oil composition and the expression of genes involved in their synthesis in peppermint (Mentha piperita L.). Ind Crops Prod 168:113602 Azizollahi Z, Ghaderian SM, Ghotbi-Ravandi AA (2019) Cadmium accumulation and its effects on physiological and biochemical characters of summer savory (Satureja hortensis L.). Int J Phytorem 21(12):1241–1253 Bagheri M, Javanmard HR, Naderi MR (2021) Soil cadmium and lead affecting biochemical properties of Matricaria chamomilla L. at different growth stages in the greenhouse and field. Biometals 34(4):881–893 Banarjee P (2018) Phytoremediation: using natural strength for curing nature. Acta Sci Agric 2(12):144–153 Bandyopadhyay S, Maiti SK (2019) Heavy metals distribution in Eucalyptus tree in 30 years old reclaimed overburden dumps. In: Bora P, Phukan BR, Bora D (eds) Current trends in renewable and alternative energy. Book series: AIP Conference Proceedings 2091:020008 Banu AT, Lunghar J (2021) Supplements and diets for antiinflammation. In: Gopi S, Kunnumakkara A, Amalraj A, Thomas S (eds) Inflammation and natural products. Elsevier, Amsterdam, pp 359–376 Bauddh K, Singh RP (2012) Growth, tolerance efficiency and phytoremediation potential of Ricinus communis (L.) and Brassica juncea (L.) in salinity and drought affected cadmium contaminated soil. Ecotoxicol Environ Saf 85:13–22 Benis MRS, Hassani AH, Nouri J, Mehregan I, Moattar F (2015) The effect of soil properties and plant species on the absorption of heavy metals in industrial sewage contaminated soil: a case study of Eshtehard Industrial Park. Bulg Chem Commun 47:211–219 Berni R, Luyckx M, Xu X, Legay S, Sergeant K, Hausman JF, Lutts S, Cai G, Guerriero G (2019) Reactive oxygen species and heavy metal stress in plants: impact on the cell wall and secondary metabolism. Environ Exp Bot 161:98–106 Bhavaniramya S, Vishnupriya S, Saleh AA, Vijayakumar R, Baskaran D (2019) Role of essential oils in food safety: antimicrobial and antioxidant applications. Grain Oil Sci Technol 2:49–55

216

K. Král’ová and J. Jampílek

Bilal RM, Liu CJ, Zhao HH, Wang YZ, Farag MR, Alagawany M, Hassan FU, Elnesr SS, Elwan HAM, Qiu HJ (2021) Olive oil: nutritional applications, beneficial health aspects and its prospective application in poultry production. Front Pharmacol 12:723040 Boechat CL, Miranda RD, Lacerda JJD, Coelho DG, Sobrinho LS, Saraiva PC (2021) Transgenic plants and rhizosphere associated microbiota in phytoremediation of heavy metals and organic pollutants. In: Kumar V, Saxena G, Shah MP (eds) Bioremediation for environmental sustainability. Elsevier, Amsterdam, pp 299–328 Bogatu C, Lazarovici M, Masu S, Negrea A, Mosoarca G, Ciopec M, Dragomir N (2007) Mobilization of heavy metals from mining wastes by their covering with soil and phytoremediation. Chem Bull “POLITEHNICA” Univ (Timi¸soara) 52(66):27–30 Both EB, Shao SX, Xiang JQ, Jokai Z, Yin HQ, Liu YF, Magyar A Dernovics M (2018) Selenolanthionine is the major water-soluble selenium compound in the selenium tolerant plant Cardamine violifolia. Biochim Biophys Acta 11:2354–2362 Bratu MM, Birghila S, Stancu LM, Cenariu MC, Emoke P, Popescu A, Radu MD, Zglimbea L (2021) Evaluation of the antioxidant, cytotoxic and antitumoral activities of a polyphenolic extract of Robinia pseudoacacia L. flowers. J Sci Arts 2:547–556 Broadley MR, White PJ, Hammond JP, Zelko I, Lux A (2007) Zinc in plants. New Phytol 173(4):677–702 Brooks RR (1977) Copper and cobalt uptake in Hauminiastrum species. Plant Soil 48:541–544 Budzynska S, Kubiak A, Szostek M, Budka A, Gasecka M, Niedzielski P, Zheng L, Mleczek M (2022) Trees and shrubs from a post-industrial area high in calcium and trace elements: the potential of dendroremediation. Int J Phytorem 24(5):493–495 Busby RR, Douglas TA, LeMonte JJ, Ringelberg DB, Indest KJ (2020) Metal accumulation capacity in indigenous Alaska vegetation growing on military training lands. Int J Phytorem 22(3):259–266 Calabrese EJ, Agathokleous E (2021) Accumulator plants and hormesis. Environ Pollut 274:116526w Cambrolle J, Mancilla-Leyton JM, Munoz-Valles S, Figueroa-Luque E, Luque T, Figueroa ME (2013) Effects of copper sulfate on growth and physiological responses of Limoniastrum monopetalum. Environ Sci Pollut Res 20(12):8839–8847 Cambrolle J, Mancilla-Leyton JM, Munoz-Valles S, Figueroa-Luque E, Luque T, Figueroa ME (2013) Evaluation of zinc tolerance and accumulation potential of the coastal shrub Limoniastrum monopetalum (L.) Boiss. Environ Exp Bot 85:50–57 Cano-Resendiz O, de la Rosa G, Cruz-Jimenez G, Gardea-Torresdey JL, Robinson BH (2011) Evaluating the role of vegetation on the transport of contaminants associated with a mine tailing using the Phyto-DSS. J Hazard Mater 189(1–2):472–478 Cavalcante NB, Santos ADD, Almeida JRGD (2020) The genus Jatropha (Euphorbiaceae): A review on secondary chemical metabolites and biological aspects. Chem Biol Interact 318:108976 Cay S, Uyanik A, Engin MS (2016) EDTA supported phytoextraction of Cd from contaminated soil by four different ornamental plant species. Sediment Contam 25(3):346–355 Charvalas G, Solomou AD, Kyriakos KD, Skoufogianni E, Bartzialis D, Emmanouil C, Danalatos NG (2021) Determination of heavy metals in the territory of contaminated areas of Greece and their restoration through hyperaccumulators. Environ Sci Pollut Res Int 28(4):3858–3863 Chehregani A, Malayeri BE (2007) Removal of heavy metals by native accumulator plants. Int J Agric Biol 9(3):462–465 Chellappandian M, Saravanan M, Pandikumar P, Harikrishnan P, Thirugnanasambantham K, Subramanian S, Hairul-Islam VI, Ignacimuthu S (2018) Traditionally practiced medicinal plant extracts inhibit the ergosterol biosynthesis of clinically isolated dermatophytic pathogens. J Mycol Med 28(1):143–149 Chen L, Wanga D, Zenga C, Longa C (2019) Improving cobalt phytoextraction by Astragalus sinicus L. grown in co-contaminated soils using biodegradable chelators. Soil Sediment Contam 28(5):461–472

7 Medicinal and Aromatic Plant Species with Potential for Remediation …

217

Chen L, Cui ZX, Wang D (2020) Variations in Cd and Pb accumulations of hot pepper (Capsicum annuum L.) cultivars for screening pollution- and nitrate-safe cultivars. Pol J Environ Stud 29(4):2597–2607 Cheng HT, Liu Q, Ma M, Liu Y, Wang WT, Ning W (2019) Cadmium tolerance, distribution, and accumulation in Taraxacum ohwianum Kitam. As a potential Cd-hyperaccumulator. Int J Phytorem 21(6):541–549 Cheong DHJ, Arfuso F, Sethi G, Wang LZ, Hui KM, Kumar AP, Thai T (2018) Molecular targets and anti-cancer potential of escin. Cancer Lett 422:1–8 Cheraghi M, Mosavinia SM, Lorestani B (2013) Heavy metal contamination in soil and some medicinal plant species in Ahangaran lead-zinc mine Iran. J Adv Environ Health Res 1(1):29–34 Cho CL, Lee YZ, Tseng CN, Cho J, Cheng YB, Wang KW, Chen HJ, Chiou SJ, Chou CH, Hong YR (2017) Hexane fraction of Pluchea indica root extract inhibits proliferation and induces autophagy in human glioblastoma cells. Biomed Rep 7(5):416–422 Citterio S, Santagostino A, Fumagalli P, Prato N, Ranalli P, Sgorbati S (2003) Heavy metal tolerance and accumulation of Cd, Cr and Ni by Cannabis sativa L. Plant Soil 256(2):243–252 Collier MH, Boughter SA, Dameron MP, Gribbins KM, Keane B, Shann JR, Rogstad SH (2017) Uptake and distribution of copper, lead, and zinc in dandelions (Taraxacum officinale; Asteraceae) sampled from polluted and nonpolluted soils. J Torrey Bot Soc 144(1):47–57 Cudic V, Stojiljkovic D, Jovovic A (2016) Phytoremediation potential of wild plants growing on soil contaminated with heavy metals. Arh Hig Rada Toksikol 67(3):229–239 Cytisus scoparius. Practical Plants, 2016. https://practicalplants.org/wiki/Cytisus_scoparius Dafni A, Petanidou T, Vallianatou I, Kozhuharova E, Blanche C, Pacini E, Peyman M. Stevanovic ZD, Franchi GG, Benitez G (2020) Myrtle, basil, rosemary, and three-lobed sage as ritual plants in the monotheistic religions: An historical-ethnobotanical comparison. Econ Bot 74:330–355 Dar FA, Pirzadah TB, Malik B (2020) Accumulation of heavy metals in medicinal and aromatic plants. In: Aftab T, Hakeem KR (eds) Plant micronutrients. Springer, Cham, pp 113–127 Das B, Salvanna N, Reddy PR, Paramesh J, Das R (2018) Our phytochemical research on Jatropha species. Arkivoc 2018 (Part 1):114–133 Datta R, Quispe MA, Sarkar D (2011) Greenhouse study on the phytoremediation potential of vetiver grass, Chrysopogon zizanioides L., in arsenic-contaminated soils. Bull Environ Contam Toxicol 86:124–128 Dehyab AS, Bakar MFA, AlOmar MK, Sabran SF (2020) A review of medicinal plant of Middle East and North Africa (MENA) region as source in tuberculosis drug discovery. Saudi J Biol Sci 27(9):2457–2478 Deng JJ, Yin Y, Zhu WX, Zhou YB (2020) Response of soil environment factors and microbial communities to phytoremediation with Robinia pseudoacacia in an open-cut magnesite mine. Land Degrad Dev 31(16):2340–2355 DePrado L (2018) Aromatherapy in ancient Egypt has linked to today’s booming alternative medicine practices. Final touch plantscaping. https://eu.mycentraljersey.com/story/news/local/ how-we-live/2018/06/19/aromatherapy-alternative-medicine-ancient-eygpt/709857002/ Dhanam S (2017) Strategies of bioremediation of heavy metal pollutants toward sustainable agriculture. In: Dhanarajan A (ed) Sustainable agriculture towards food security. Springer Nature, Singapore, pp 349–358 Dinu C, Vasile GG, Buleandra M, Popa DE, Gheorghe S, Ungureanu EM (2020) Translocation and accumulation of heavy metals in Ocimum basilicum L. plants grown in a mining-contaminated soil. J Soil Sediment 20(4):2141–2154 Dinu C, Gheorghe S, Tenea AG, Stoica C, Vasile GG, Popescu RL, Serban EA, Pascu LF (2021) Toxic metals (As, Cd, Ni, Pb) impact in the most common medicinal plant (Mentha piperita). Int J Environ Res Public Health 18(8):3904 Dobrikova A, Apostolova E, Hanc A, Yotsova E, Borisova P, Sperdouli I, Adamakis IDS, Moustakas M (2021) Tolerance mechanisms of the aromatic and medicinal plant Salvia sclarea L. to excess zinc. Plants 10(2):194

218

K. Král’ová and J. Jampílek

Dolab JG, Lima B, Spaczynska E, Kos J, Cano NH, Feresin G, Tapla A, Garibotto F, Petenatti E, Olivella M, et al (2018) Antimicrobial activity of Annona emarginata (Schltdl.) H. Rainer and most active isolated compound against clinically important bacteria. Molecules 23:1187 Domke GM, Oswalt SN, Walters BF, Morin RS (2020) Tree planting has the potential to increase carbon sequestration capacity of forests in the United States. PNAS 117(40):24649–24651 Do Nascimento LD, de Moraes AAB, da Costa KS, Galucio JMP, Taube PS, Costa CML, Cruz JN, Andrade EHD, de Faria LJG (2020) Bioactive natural compounds and antioxidant activity of essential oils from spice plants: new findings and potential applications. Biomolecules 10:988 Drzewiecka K, Piechalak A, Golinski P, Gasecka M, Magdziak Z, Szostek M, Budzynska S, Niedzielski P, Mleczek M (2019) Differences of Acer platanoides L. and Tilia cordata Mill. Response patterns/survival strategies during cultivation in extremely polluted mining sludge—a pot trial. Chemosphere 229:589–601 Dudek-Makuch M, Studzinska-Sroka E (2014) Horse chestnut-efficacy and safety in chronic venous insufficiency: an overview. Rev Bras Pharmacogn 25(5):533–541 Duffus JH (2002) Heavy metals a meaningless term? Pure Appl Chem 74(5):793–807 Dunn CE (2007) New perspectives on biogeochemical exploration. Paper 12. Advances in prospectscale geochemical methods. In: Milkereit B (ed) Proceedings of Exploration 07: fifth decennial international conference on mineral exploration, pp 249–261 Elhag M, Al-Ghamdi AAM, Galal HK, Dahlan A (2018) Evaluation of Aloe vera L. as phytoremediator of heavy metals contaminated soils in arid environments. Appl Ecol Environ Res 16(5):6033–6045 El-Khatib AA, Barakat NA, Youssef NA, Samir NA (2020a) Bioaccumulation of heavy metals air pollutants by urban trees. Int J Phytorem 22:210–222 El-Khatib AA, Youssef NA, Barakat NA, Samir NA (2020b) Responses of Eucalyptus globulus and Ficus nitida to different potential of heavy metal air pollution. Int J Phytorem 22:986–999 Eller F, Brix H (2016) Influence of low calcium availability on cadmium uptake and translocation in a fast-growing shrub and a metal-accumulating herb. AOB Plants 8:plv143 El-Ramady H, Abdalla N, Taha HS, Alshaal T, El-Henawy A, Faizy SEDA, Shams MS, Youssef SM et al (2016) Selenium and nano-selenium in plant nutrition. Environ Chem Lett 14:123–147 El Rasafi T, Pereira R, Pinto G, Goncalves FJM, Haddioui A, Ksibi M, Roembke J, Sousa JP, Marques CR (2021) Potential of Eucalyptus globulus for the phytoremediation of metals in a Moroccan iron mine soil-a case study. Environ Sci Pollut Res 28:15782–15793 Emsley J (2011) Nature’s building blocks, new. Oxford University Press, Oxford Erickson LE, Pidlisnyuk V (2021) Phytotechnology with Biomass Production. CRC Press, Boca Raton, FL Evangelou MWH, Kutschinski-Kloess S, Ebel M, Schaeffer A (2007) Potential of Borago officinalis, Sinapis alba L. and Phacelia boratus for phytoextraction of Cd and Pb from soil. Water Air Soil Pollut 182(1–4):407–416 Fan CH, Du B, Zhang YC, Gao YL, Chang M (2016a) Determination of lead and cadmium in Calendula officinalis seedlings for phytoremediation of multi-contaminated loess by using flame atomic absorption spectrometry with wet digestion. Spectrosc Spect Anal 36(8):2625–2628 Fan CH, Chang M, Zhang YC, Gao YL (2016b) FTIR analysis of secondary abiotic stress response of Calendula officinalis seedlings to lead and cadmium in multi-contaminated loess. Spectrosc Spect Anal 36(8):2442–2446 Fasani E, Manara A, Martini F et al (2018) The potential of genetic engineering of plants for the remediation of soils contaminated with heavy metals. Plant Cell Environ 41:1201–1232 Fattahi B, Arzani K, Souri MK, Barzegar M (2019) Effects of cadmium and lead on seed germination, morphological traits, and essential oil composition of sweet basil (Ocimum basilicum L.). Ind Crops Prod 138:111584 Fitz WJ, Wenzel WW (2002) Arsenic transformations in the soil-rhizosphere-plant system: fundamentals and potential application to phytoremediation. J Biotech 99:259–278 Flores JC (2021) The future of phytoremediation. Nova Science Publishers, New York, USA

7 Medicinal and Aromatic Plant Species with Potential for Remediation …

219

Franke H, Scholl R, Aigner A (2019) Ricin and Ricinus communis in pharmacology and toxicologyfrom ancient use and “Papyrus Ebers” to modern perspectives and “poisonous plant of the year 2018.” Naunyn Schmiedebergs Arch Pharmacol 392(10):1181–1208 Frutos I, Garcia-Delgado C, Cala V, Garate A, Eymara E (2017) The use of spent mushroom compost to enhance the ability of Atriplex halimus to phytoremediate contaminated mine soils. Environ Technol 38(9):1075–1084 Fryzova R, Pohanka M, Martinkova P, Cihlarova H, Brtnicky M, Hladky J, Kynicky J (2018) Oxidative stress and heavy metals in plants. Rev Environ Contam Toxicol 245:129–156 Fuente V, Rufo L, Juárez BH, Menéndez N, García-Hernández M, Salas-Colera E, Espinosa A (2016) Formation of biomineral iron oxides compounds in a Fe hyperaccumulator plant: Imperata Cylindrica (L.) P. Beauv. J Struct Biol 193(1):23–32 Fulekar MH, Singh A, Thorat V, Kaushik CP, Eapen S: Phytoremediation of 137 Cs from low level nuclear waste using Catharanthus roseus. Indian J Pure Appl Phys 48(7):516–519 Galal TM, Shehata HS (2015) Bioaccumulation and translocation of heavy metals by Plantago major L. grown in contaminated soils under the effect of traffic pollution. Ecol Indic 48:244–251 Galal TM, Essa B, Al-Yasi H (2021) Heavy metals uptake and its impact on the growth dynamics of the riparian shrub Ricinus communis L. along Egyptian heterogenic habitats. Environ Sci Pollut Res 28(28):37158–37171 Grace OM (2019) Succulent plant diversity as natural capital. Plants People Planet 1(4):336–345 Garcia-Salgado S, Garcia-Casillas D, Quijano-Nieto MA, Bonilla-Simon MM (2012) Arsenic and heavy metal uptake and accumulation in native plant species from soils polluted by mining activities. Water Air Soil Pollut 223(2):559–572 Gharib FA, Mansour KH, Ahmed EZ, Galal TM (2021) Heavy metals concentration, and antioxidant activity of the essential oil of the wild mint (Mentha longifolia L.) in the Egyptian watercourses. Int J Phytorem 23(6):641–651 Ghazaryan K, Movsesyan H, Ghazaryan N, Watts BA (2019) Copper phytoremediation potential of wild plant species growing in the mine polluted areas of Armenia. Environ Pollut 249:491–501 Ghosh M, Singh SP (2005) A review on phytoremediation of heavy metals and utilization of its byproducts. Appl Ecol Environ Res 3:1–18 Ghosh C, Chung HY, Nandre RM, Lee JH, Jeond TI, Kim IS, Yang SH, Hwang SG (2012) An active extract of Ulmus pumila inhibits adipogenesis through regulation of cell cycle progression in 3T3-L1 cells. Food Chem Toxicol 50(6):2009–2015 Ghosh AK, Panda SK, Luyten W (2021) Anti-vibrio and immune-enhancing activity of medicinal plants in shrimp: a comprehensive review. Fish Shellfish Immunol 117:192–210 Gohari G, Mohammadi A, Akbari A, Panahirad S, Dadpour MR, Fotopoulos V, Kimura S (2020) Titanium dioxide nanoparticles (TiO2 NPs) promote growth and ameliorate salinity stress effects on essential oil profile and biochemical attributes of Dracocephalum moldavica. Sci Rep 10:912 Golubkina N, Lapchenko V, Ryff L, Lapchenko H, Naumenko T, Bagrikova N, Krainuk K, Kosheleva O, Caruso G (2020) Medicinal plants as sources of selenium and natural antioxidants. Banats J Biotechnol 11(22):48–59 Gonzalez-Valdez E, Alarcon A, Ferrera-Cerrato R, Vega-Carrillo HR, Maldonado-Vega M, SalasLuevano MA (2016) Seed germination and seedling growth of five plant species for assessing potential strategies to stabilizing or recovering metals from mine tailings. Water Air Soil Pollut 227(1):112051 Gopalakrishnan A, Kariyil BJ, John R, Usha PTA (2019) Phytochemical evaluation and cytotoxic potential of chloroform soluble fraction of methanol extract of Thespesia populnea in human breast cancer cell lines. Pharmacogn Mag 15(62):150–154 Gorelova SV, Frontasyeva MV, Yurukova L, Coskun M, Pantelica A, Saitanis CJ, Tomasevic M, Anicic M (2011) Revitalization of urban ecosystems through vascular plants: preliminary results from the BSEC-PDF project. Agrochimica 55(2):65–84 Grubor M (2008) Lead uptake, tolerance, and accumulation exhibited by the plants Urtica dioica and Sedum spectabile in contaminated soil without additives. Arch Biol Sci 60(2):239–244

220

K. Král’ová and J. Jampílek

Gul I, Manzoor M, Hashim N, Shah GM, Waani SP, Shahid M, Antoniadis V, Rinklebe J, Arshad M (2021) Challenges in microbially and chelate-assisted phytoextraction of cadmium and lead—a review. Environ Pollut 28:117667 Gupta AK, Verma SK, Khan K, Verma RK (2013) Phytoremediation using aromatic plants: a sustainable approach for remediation of heavy metals polluted sites. Environ Sci Technol 47:10115–10116 Guo H, Wan XH, Niu FJ, Sun JJ, Shi CX, Ye JM, Zhou CZ (2019) Evaluation of antiviral effect and toxicity of total flavonoids extracted from Robinia pseudoacacia cv. idaho. Biomed Pharmacother 118:109335 Guo Y, Qiu CS, Long SH, Wang H, Wang YF (2020) Cadmium accumulation, translocation, and assessment of eighteen Linum usitatissimum L. cultivars growing in heavy metal contaminated soil. Int J Phytorem 22(5):490–496 Gunarathne V, Mayakaduwa S, Ashiq A, Weerakoon SR, Biswas JK, Vithanage M (2019) Transgenic plants: benefits, applications, and potential risks in phytoremediation. In: Prasad MNV (ed) Transgenic plant technology for remediation of toxic metals and metalloids. Academic Press, London, pp 89–102 Hamzah A, Hapsari RI, Wisnubroto EI (2016) Phytoremediation of cadmium-contaminated agricultural land using indigenous plants. Int J Environ Agric Res (IJOEAR) 2(1):8–14 Han R, Dai HP, Guo B, Noori A, Sun WC, Wei SH (2021) The potential of medicinal plant extracts in improving the phytoremediation capacity of Solanum nigrum L. for heavy metal contaminated soil. Ecotoxicol Envrion Saf 220:112411 Hartmann AM, Abarzua S, Schlichting A, Richter DU, Leinweber P, Briese V (2011) Effects of elm bark extracts from Ulmus laevis on human chorion carcinoma cell lines. Arch Gynecol Obstet 284(5):1265–1269 Harzallah HJ, Neffati A, Skandrani I, Maaloul E, Chekir-Ghedira L, Mahjoub T (2010) Antioxidant and antigenotoxic activities of Globularia alypum leaves extracts. J Med Plant Res 4(19):2048– 2053 Hasanuzzaman M, Hossain MA, Fujita M (2010) Selenium in higher plants: physiological role, antioxidant metabolism and abiotic stress tolerance. J Plant Sci 5:354–375 He A, Gu M, Wang X, He X (2018a) The effects of lead on photosynthetic performance of waxberry seedlings (Myrica rubra). Photosynthetica 56(4):1147–1153 He HH, Dong ZG, Pang JY, Wu GL, Zheng JY, Zhang XC (2018b) Phytoextraction of rhenium by lucerne (Medicago sativa) and erect milkvetch (Astragalus adsurgens) from alkaline soils amended with coal fly ash. Sci Total Environ 630:570–577 He YF, Wang QW, Ye YP, Liu ZY, Sun HX (2020) The ethnopharmacology, phytochemistry, pharmacology and toxicology of genus Albizia: A review. J Ethnopharmacol 257:112677 Hernandez-Garcia E, Garcia A, Garza-Gonzalez E, Avalos-Alanis FG, Rivas-Galindo VM, Rodriguez-Rodriguez J, Alcantar-Rosales VM, Delgadillo-Puga C, Camacho-Corona MD (2019) Chemical composition of Acacia farnesiana (L) wild fruits and its activity against Mycobacterium tuberculosis and dysentery bacteria. J Ethnopharmacol 230:74–80 Hibiscus syriacus (2013) Practical plants https://practicalplants.org/wiki/Hibiscus_syriacus2013 Hristozkova M, Geneva M, Stancheva I, Boychinova M, Djonova E (2016) Contribution of arbuscular mycorrhizal fungi in attenuation of heavy metal impact on Calendula officinalis development. Appl Soil Ecol 101:57–63 Husen A (2022) Traditional herbal therapy for the human immune system. CRC Press, Boca Raton, FL Hussain Z, Rasheed F, Tanvir MA, Zafar Z, Rafay M, Mohsin M, Pulkkinen P, Ruffner C (2021) Increased antioxidative enzyme activity mediates the phytoaccumulation potential of Pb in four agroforestry tree species: a case study under municipal and industrial wastewater irrigation. In J Phytorem 23(7):704–714 Ibragic S, Smjecanin N, Hodzic S, Ramcic S, Nuhanovic M (2020) Study of uranium bioaccumulation capacity of Salvia officinalis L. and Ocimum basilicum L. enhanced by citric acid. Glas Hem Tehnol Bosne Herceg 2020(55):1–6

7 Medicinal and Aromatic Plant Species with Potential for Remediation …

221

Ibrahim MM, Alsahli AA, El-Gaaly G (2013) Evaluation of phytoremediation potential of six wild plants for metal in a site polluted by industrial wastes: a field study in Riyadh. Saudi Arabia. Pakistan J Bot 45(2):571–576 IFA (2020a) Micronutrients: how fertilizers help to address the problems of hunger and malnutrition. Assessed 10 Sept 2021 at https://www.fertilizer.org/Public/Stewardship/Publication_Det ail.aspx?SEQN=5894&PUBKEY=0065B481-B6E7-47C1-BD5C-56F6519B9462 IFA (2020b) 19 Essential nutrients for improving and protecting plant health. Assessed 10 Sept 2021 at https://www.fertilizer.org/public/resources/publication_detail.aspx?SEQN=5898&PUB KEY=72A2904A-2C9A-4A5E-9696-55E45C60EE12 Inoue M, Hayashi S, Craker LE (2019) Role of medicinal and aromatic plants: Past, present, and future. In: Perveen S, Al-Taweel A (eds) Pharmacognosy–medicinal plants. IntechOpen, Rijeka, Croatia, 2019. https://www.intechopen.com/chapters/65477 (Accessed on 15 Nov 2020) Iori V, Pietrini F, Bianconi D, Mughini G, Massacci A, Zacchini M (2017) Analysis of biometric, physiological, and biochemical traits to evaluate the cadmium phytoremediation ability of eucalypt plants under hydroponics. iForest 10:416–421 Irshad M, Ruqia B, Hussain Z (2015) Phytoaccumulation of heavy metals in natural vegetation at the municipal wastewater site in Abottabad. Pakistan. Int J Phytorem 17(12):1269–1273 Iwaoka E, Oku H, Takahashi Y, Ishiguro K (2009) Allergy-preventive effects of Hibiscus mutabilis “Versicolor” and a novel allergy-preventive flavonoid glycoside. Biol Pharm Bull 32(3):509–512 Jablonska-Czapla M, Michalski R, Nocon K, Grygoyc K (2019) The mobility of arsenic and its species in selected herbs. Arch Environ Protect 45(3):86–98 Jafari F, Ramezani M, Nomani H, Amiri MS, Moghadam AT, Sahebkar A, Emami SA, Mohammadpour AH (2021) Therapeutic effect, chemical composition, ethnobotanical profile of Eucalyptus globulus: A review. Lett Org Chem 18(6):419–452 Jaison S, Muthukumar T (2017) Chromium accumulation in medicinal plants growing naturally on tannery contaminated and non-contaminated soils. Biol Trace Elem Res 175(1):223–235 Jampilek J (2017) Design of antimalarial agents based on natural products. Curr Org Chem 21:1824– 1846 Jampílek J, Kráˇlová K (2019a) Impact of nanoparticles on photosynthesizing organisms and their use in hybrid structures with some components of photosynthetic apparatus. In: Prasad R (ed) Plant nanobionics, nanotechnology in the life sciences. Springer Nature, Cham, pp 255–332 Jampílek J, Kráˇlová K (2019b) Beneficial effects of metal- and metalloid-based nanoparticles on crop production. In: Panpatte DG, Jhala YK (eds) Nanotechnology for agriculture. Springer Nature, Singapore, pp 161–219 Jastrzab A, Skrzydlewska E (2019) Composition and biomedical relevance of sea buckthorn. Acta Pol Pharm 76(6):959–969 Jia X, Wang L, Zhao YH, Zhang CY, Li XD (2020) Soil microbial communities in the rhizosphere of Robinia pseudoacacia L. after being exposed to elevated atmospheric CO2 and cadmium for 4 years. Appl Ecol 154:103661 Jisha CK, Bauddh K, Shukla SK (2017) Phytoremediation and bioenergy production efficiency of medicinal and aromatic plants. In: Bauddh K, Singh B, Korstad J (eds) Phytoremediation potential of bioenergy plants. Springer Nature, Singapore, pp 287–304 Kadan S, Saad B, Sasson Y, Zaid H (2013) In vitro evaluations of cytotoxicity of eight antidiabetic medicinal plants and their effect on GLUT4 translocation. Evid Based Complement Alternat Med 2013:549345 Kaewtubtim P, Meeinkuirt W, Seepom S, Pichtel J (2017) Radionuclide (226 Ra, 232 Th, 40 K) accumulation among plant species in mangrove ecosystems of Pattani Bay, Thailand. Mar Pollut Bull 115(1–2):391–400 Kalinovic TS, Serbula SM, Radojevic AA, Kalinovic JV, Steharnik MM, Petrovic JV (2016) Elder, linden and pine biomonitoring ability of pollution emitted from the copper smelter and the tailings ponds. Geoderma 262:266–275 Kaul M, Mohren GMJ, Dadhwal VK (2010) Carbon storage and sequestration potential of selected tree species in India. Mitig Adapt Strateg Glob Chang 15:489–510

222

K. Král’ová and J. Jampílek

Kaur A, Batish DR, Kaur S, Chauhan BS (2021) An overview of the characteristics and potential of Calotropis procera from botanical, ecological, and economic perspectives. Front Plant Sci 12:690806 Kazerooni EA, Maharachchikumbura SSN, Adhikari A, Al-Sadi AM, Kang SM, Kim LR, Lee IJ (2021) Rhizospheric Bacillus amyloliquefaciens protects Capsicum annuum cv. Geumsugangsan from multiple abiotic stresses via multifarious plant growth-promoting attributes. Front Plant Sci 12:669693 Khadka D, Dhamala MK, Li F, Aryal PC, Magar PR, Bhatta S, Thakur MS, Basnet A, Cui D, Shi S (2021) The use of medicinal plants to prevent COVID-19 in Nepal. J Ethnobiol Ethnomedicine 17:26 Khalid S, Shahid M, Niazi NK, Murtaza B, Bibi I, Dumat C (2017) A comparison of technologies for remediation of heavy metal contaminated soils. J Geochem Explor 182:247–268 Khalid A, Farid M, Zubair M, Rizwan M, Iftikhar U, Ishaq HK, Farid S, Latif U, Hina K, Ali S (2020) Efficacy of Alternanthera bettzickiana to remediate copper and cobalt contaminated soil physiological and biochemical alterations. Int J Environ Res 14(3):243–255 Khalid M, Ur-Rahman S, Hassani D, Hayat K, Zhou P, Hui N (2021) Advances in fungal-assisted phytoremediation of heavy metals: A review. Pedosphere 31(3):475–495 Khan AR, Ullah I, Khan AL, Park GS, Waqas M, Hong SJ, Jung BK, Kwak Y, Lee IJ, Shin JH (2015) Improvement in phytoremediation potential of Solanum nigrum under cadmium contamination through endophytic-assisted Serratia sp RSC-14 inoculation. Environ Sci Pollut Res 22(18):14032–14042 Khan I, Iqbal M, Shafiq F (2019) Phytomanagement of lead-contaminated soils: critical review of new trends and future prospects. Int J Environ Sci Technol 16:6473–6488 Khan T, Khan MA, Mashwani ZUR, Ullah N, Nadhman A (2021) Therapeutic potential of medicinal plants against COVID-19: The role of antiviral medicinal metabolites. Biocatal Agric Biotechnol 31:101890 Kirbag S, Erecevit P, Zengin F, Guvenc AN (2013) Antimicrobial activities of some Euphorbia species. Afr J Tradit Complement Altern Med 10(5):305–309 Ko JA, Furuta N, Lim HB (2018) Quantitative mapping of elements in basil leaves (Ocimum basilicum) based on cesium concentration and growth period using laser ablation ICP-MS. Chemosphere 190:368–374 Konwar M, Das S (2014) Comparative study of antidiabetic and antioxidant activities of the ethanolic extracts of leaves and bark of Acacia farnesiana (L.) Willd. in streptozocin-nicotinamide induced type 2 diabetic experimental animal models. Indian J Pharmacol 46(4):S4–S4 Kovacik J, Gruz J, Klejdus B, Stork F, Hedbavny J (2012) Accumulation of metals and selected nutritional parameters in the field-grown chamomile anthodia. Food Chem 13(1):55–62 Kovacik J, Dresler S, Wojciak-Kosior M, Hladky J, Babula P (2018) Metabolic changes induced by manganese in chamomile. Plant Physiol Biochem 133:127–133 Kovacik J, Bujdos M, Ketzer P, Babula P, Peterkova V, Krenn L (2019) Dandelion is more tolerant to cadmium than to nickel excess. Chemosphere 224:884–891 Krishnaiah D, Sarbatly R, Nithyanandam R (2011) A review of the antioxidant potential of medicinal plant species. Food Bioprod Process 89(C3):217–233 Kráˇlová K, Masaroviˇcová E (2003) Hypericum perforatum L and Chamomilla recutita (L.) Rauschaccumulators of some toxic metals. Pharmazie 58:359–360 Kráˇlová K, Masaroviˇcová E (2008) EDTA-assisted phytoextraction of copper, cadmium and zinc using chamomile plants. Ecol Chem Engin A 15(3):213–220 Kráˇlová K, Masaroviˇcová E, Jampílek J (2019) Plant responses to stress induced by toxic metals and their nanoforms. In: Pessarakli M (ed) Handbook of plant and crop stress, 4th edn. CRC Press, Boca Raton, pp 479–522 Kráˇlová K, Jampílek J (2021) Responses of medicinal and aromatic plants to engineered nanoparticles. Appl Sci 11:1813

7 Medicinal and Aromatic Plant Species with Potential for Remediation …

223

Kráˇlová K, Masaroviˇcová E, Jampílek J (2021) Risks and benefits of metal-based nanoparticles for vascular plants. In: Pessarakli M (ed) Handbook of plant and crop physiology, 4th edn. CRC Press, Boca Raton, FL, pp 923–963 Kráˇlová K, Jampilek J (2022) Phytoremediation of environmental matrices contaminated with photosystem II-inhibiting herbicides. In: Solana AC, de Castro LFMV NN (eds) Pesticides bioremediation. Springer Cham, pp 31–80 Kumar SS, Kadier A, Malyan SK, Ahmad A, Bishnoi NR (2017) Phytoremediation and rhizoremediation: uptake, mobilization and sequestration of heavy metals by plants. In: Singh D, Singh H, Prabha R (eds) Plant-microbe interactions in agro-ecological perspectives. Springer, Singapore, pp 367–394 Kumar A, Kumar A, Cabral-Pinto M, Chaturvedi AK, Shabnam AA, Subrahmanyam G, Mondal R, Gupta DK, Malyan SK, Kumar SS et al (2020) Lead toxicity: health hazards, influence on food chain, and sustainable remediation approaches. Int J Environ Res Public Health 17:2179 Kumar J, Malik NA, Atri NS (2021) Aromatic and medicinal plants for phytoremediation: a sustainable approach. In: Aftab Y, Hakeem KR (eds) Medicinal and aromatic plants. Springer, Cham, pp 485–543 Kummerová M, Zezulka S, Kráˇlová K, Masaroviˇcová E (2010) Effect of zinc and cadmium on physiological and production characteristics in Matricaria recutita. Biol Plant 54(2):308–314 Kunwar G, Pande C, Tewari G, Singh C, Kharkwal GC (2015) Effect of heavy metals on terpenoid composition of Ocimum basilicum L. and Mentha spicata L. J Essent Oil-Bear Plants 18(4):818– 825 Lafmejani ZN, Jafari AA, Moradi P, Moghadam AL (2018) Impact of foliar application of ironchelate and iron nano particles on some morpho-physiological traits and essential oil composition of peppermint (Mentha piperita L.). J Essent Oil Bear Plants 21:1374–1384 Lago-Vila M, Arenas-Lago D, Rodriguez-Seijo A, Andrade ML, Vega FA (2019) Ability of Cytisus scoparius for phytoremediation of soils from a Pb/Zn mine: assessment of metal bioavailability and bioaccumulation. J Environ Manag 235:152–160 Lajayer BA, Ghorbanpour G, Nikabadi S (2017) Heavy metals in contaminated environment, Destiny of secondary metabolite biosynthesis. Ecotoxicol Environ Safe 145:377–390 Lam SK, Ng TB (2009) Novel galactonic acid-binding hexameric lectin from Hibiscus mutabilis seeds with antiproliferative and potent HIV-1 reverse transcriptase inhibitory activities. Acta Biochim Pol 56(4):649–654 Lee JH (2013) An overview of phytoremediation as a potentially promising technology for environmental pollution control. Biotechnol Bioprocess Eng 18:431–439 Levizou E, Zanni AA, Antoniadis V (2019) Varying concentrations of soil chromium (VI) for the exploration of tolerance thresholds and phytoremediation potential of the oregano (Origanum vulgare). Environ Sci Pollut Res 26(1):14–23 Lewis SL, Wheeler CE, Mitchard ETA, Koch A (2019) Restoring natural forests is the best way to remove atmospheric carbon. Nature 568:25–28 Li JJ, Yang L, Miao CP, Teng YJ, Fu ZH, Cheng CL, Chang XX, Qian Y, Zhao LX (2021) Impact of rhizosphere microorganisms on arsenic (As) transformation and accumulation in a traditional Chinese medical plant. Environ Sci Pollut Res 28(43):60923–60934 Lim XY, Teh BP, Tan TYC (2021) Medicinal plants in COVID-19: potential and limitations. Front Pharmacol 12:611408 Lin AS, Lin CR, Du YC, Luebken T, Chiang MY, Chen IH, Wu CC, Hwang TL, Chen SL, Yen MH (2009) Acasiane A and B and farnesirane A and B, diterpene derivatives from the roots of Acacia farnesiana. Planta Med 75(3):256–261 Linger P, Müssig J, Fischer H, Kobert J (2002) Industrial hemp (Cannabis sativa L.) growing on heavy metal contaminated soil: fibre quality and phytoremediation potential. Ind Crop Prod 16(1):33–42 Liu X, Peng K, Wang A, Lian C, Shen Z (2010a) Cadmium accumulation and distribution in populations of Phytolacca americana L. and the role of transpiration. Chemosphere 78:1136– 1141

224

K. Král’ová and J. Jampílek

Liu J, Zhou QX, Wang S (2010b) Evaluation of chemical enhancement on phytoremediation effect of Cd-contaminated soils with Calendula officinalis L. Int J Phytorem 12(5):503–515 Liu ZC, Wang LA, Xu JH, Ding SM, Feng XH, Xiao HY (2017) Effects of different concentrations of mercury on accumulation of mercury by five plant species. Ecol Eng 106(Part A):273–278 Liu SL, Ali S, Yang RJ, Tao JJ, Ren B (2019) A newly discovered Cd-hyperaccumulator Lantana camara L. J Hazard Mater 371:233–242 Lone IA, Gaffar M (2021) Phytoremediation potential of medicinal and aromatic plants. In: Aftab T, Hakeem KR (eds) Medicinal and aromatic plants. Springer Nature, Cham, pp 741–760 Luis A, Domingues F, Gil C, Duarte AP (2009) Antioxidant activity of extracts of Portuguese shrubs: Pterospartum tridentatum, Cytisus scoparius and Erica spp. J Med Plant Res 3(11):886–893 Luo J, Qi SH, Peng L, Wang JJ (2016) Phytoremediation efficiency of Cd by Eucalyptus globulus transplanted from polluted and unpolluted sites. Int J Phytorem 18:308–314 Luo J, Cai LM, Qi SH, Wu J, Gu XWS (2017) Improvement effects of cytokinin on EDTA assisted phytoremediation and the associated environmental risks. Chemosphere 185:386–393 Luo J, Wu J, Huo SY, Qi SH, Gu XS (2018a) A real scale phytoremediation of multi-metal contaminated e-waste recycling site with Eucalyptus globulus assisted by electrical fields. Chemosphere 201:262–268 Luo J, Cai LM, Qi SH, Wu J, Gu XS (2018b) Influence of direct and alternating current electric fields on efficiency promotion and leaching risk alleviation of chelator assisted phytoremediation. Ecotoxicol Environ Saf 149:241–247 Luo J, He M, Qi SH, Wu J, Gu XS (2018c) Effect of planting density and harvest protocol on fieldscale phytoremediation efficiency by Eucalyptus globulus. Environ Sci Pollut Res 25:11343– 11350 Luo J, He WX, Wu J, Gu XWS (2019a) Sensitivity of Eucalyptus globulus to red and blue light with different combinations and their influence on its efficacy for contaminated soil phytoremediation. J Environ Manag 241:235–242 Luo J, He WX, Xing XL, Wu J, Gu XWS (2019b) The phytoremediation efficiency of Eucalyptus globulus treated by static magnetic fields before sowing. Chemosphere 226:891–897 Luo J, He M, Wu J, Huo SY, Gu XWS (2019c) Comparing storage battery and solar cell in assisting Eucalyptus globulus to phytoremediate soil polluted by Cd, Pb, and Cu. Int J Phytorem 21:181– 190 Luo XQ, Zhang CL, Xu WH, Peng Q, Jiao LC, Deng JB (2020) Effects of nanometer magnesium hydroxide on growth, cadmium (Cd) uptake of Chinese cabbage (Brassica campestris) and soil Cd form. Int J Agric Biol 24:1006–1016 Luyckx M, Hausman JF, Lutts S, Guerriero G (2016) Silicon and plants: current knowledge and technological perspectives. Front Plant Sci 8:411 Lydakis-Simantiris N, Fabian M, Skoula M (2016) Cultivation of medicinal and aromatic plants in heavy metal-contaminated soils. Glob Nest J 18(3):630–642 Ma QG, Wei RR, Shang DL, Sang ZP, Liu WM, Cao ZL (2019) Hepatoprotective and neuroprotective flavanes from the fruits of Ulmus pumila L. (Ulmaceae). Pak J Pharm Sci 32(5):2059–2064 Maestri E, Marmiroli M, Visioli G, Marmiroli N (2010) Metal tolerance and hyperaccumulation: costs and trade-offs between traits and environment. Environ Exp Biol 68:1–13 Mahar A, Wang P, Ali A, Awasthi MK, Lahori AH, Wang Q, Li R, Zhang Z (2016) Challenges and opportunities in the phytoremediation of heavy metals contaminated soils: a review. Ecotoxicol Environ Saf 126:111–121 Maiti SK, Rana V (2017) Assessment of heavy metals contamination in reclaimed mine soil and their accumulation and distribution in Eucalyptus hybrid. Bull Environ Contam Toxicol 98:97–104 Majinski R (2020) Asymmetric synthesis of the anticancer agent (+)-elacomine. UWM Undergraduate Research Symposium, 2020. https://dc.uwm.edu/uwsurca/2020/virtual/128/ Maksymiec W (1997) Effect of copper on cellular processes in higher plants. Photosynthetica 33(13):321–342 Males J (2017) Secrets of succulence. J Exp Bot 68(9):2121–2134

7 Medicinal and Aromatic Plant Species with Potential for Remediation …

225

Malik RN, Husain SZ, Nazir I (2010) Heavy metal contamination and accumulation in soil and wild plant species from industrial area of Islamabad Pakistan. Pak J Bot 42(1):291–301 Mangkoedihardjo S, Triastuti Y (2011) Vetiver in phytoremediation of mercury polluted soil with the addition of compost. J Appl Sci Res 7(4):465–469 Mani D, Patel NK (2014) Humic acid, EDDS and EDTA induced phytoremediation of cadmium contaminated alluvial soil by Calendula officinalis L. J Indian Chem Soc 91(11):2073–2082 Mani D, Kumar C, Patel NK (2015) Hyperaccumulator oilcake manure as an alternative for chelateinduced phytoremediation of heavy metals contaminated alluvial soils. Int J Phytorem 17(3):256– 263 Manikandan M, Kannan V, Mahalingam K, Vimala A, Chun S (2016) Phytoremediation potential of chromium-containing tannery effluent-contaminated soil by native Indian timber-yielding tree species. Prep Biochem Biotechnol 46(1):100–108 Manniche L (2006) An ancient Egyptian herbal, 2nd ed. British Museum Press Markert B (1994) Progress report on the element concentrations cadastre project (ECCP) of INTERCOL/IUBS, International Union of Biological Sciences, 25th General Assembly, Paris Marquard R, Schneider M (1998) Zur Cadmiumproblematik im Arzneipflanzenanbau. In: Marquard R, Schubert E (eds) Fachtagung, Arznei- und Gewürzpflanzen. Justus-Liebig-Universität, Gießen, pp 9–15 Marrugo-Negrete J, Marrugo-Madrid S, Pinedo-Hernandez J, Durango-Hernandez J, Diez S (2016) Screening of native plant species for phytoremediation potential at a Hg-contaminated mining site. Sci Total Environ 542:809–816 Marschner H (1995) Mineral nutrition of higher Plants, 2nd ed. Academic Press Masaroviˇcová E, Kráˇlová K, Kummerová M, Kmentová E (2004) The effect of cadmium on root growth and respiration rate of two medicinal plant species. Biologia 59:211–214 Masaroviˇcová E, Kráˇlová K (2007) Medicinal plants—past, nowadays, future. Acta Horticult 749:19–27 Masaroviˇcová E, Kráˇlová K (2017) Essential elements and toxic metals in some crops, medicinal plants, and trees. In: Ansari A, Gill S, Gill R, Lanza G, Newman L (eds) Phytoremediation, vol 5. Springer International Publishing AG, Cham, pp 183–255 Masaroviˇcová E, Kráˇlová K, Šeršeˇn (2010a) Plant responses to toxic metal stress. In: Pessarakli M (ed) Handbook of plant and crop stress, 3rd. CRC Press, Boca Raton, FL, pp 595–634 Masaroviˇcová E, Kráˇlová K, Kummerová M (2010b) Principles of classification of medicinal plants as hyperaccumulators or excluders. Acta Physiol Plant 32:823–829 Masaroviˇcová E, Kráˇlová K (2012) Plant-heavy metal interaction: phytoremediation, biofortification and nanoparticles. In: Montanaro G, Dichio B (eds) Advances in selected plant. physiology aspects. InTech, Rijeka, Croatia, pp 75–102 Masaroviˇcová E, Kráˇlová K, Zinjarde SS (2014) Metal nanoparticles in plants. Formation and action. In: Pessarakli M (ed) Handbook of plant and crop physiology, 3rd edn. CRC Press, Boca Raton, FL, pp 683–731 Masaroviˇcová E, Kráˇlová K (2018) Woody species in phytoremediation applications for contaminated soils. In: Ansari A, Gill S, Gill R, Lanza G, Newman L (eds) Phytoremediation. Springer Nature, Cham, pp 319–373 Masaroviˇcová E, Kráˇlová K, Vykouková I, Kriššáková Z (2019) Responses of medicinal plants to abiotic stresses. In: Pessarakli M (ed) Handbook of plant and crop stress, 4th edn. CRC Press, Boca Raton, FL, USA, pp 713–753 Matanzas N, Afif E, Diaz TE, Gallego JLR (2021) Screening of pioneer metallophyte plant species with phytoremediation potential at a severely contaminated Hg and As mining site. Environments 8(7):63 Mataruga Z, Jaric S, Markovic M, Pavlovic M, Pavlovic D, Jakovljevic K, Mitrovic M, Pavlovic P (2020) Evaluation of Salix alba, Juglans regia and Populus nigra as biomonitors of PTEs in the riparian soils of the Sava River. Environ Monit Assess 192(2):131 Matic J, Guidi A, Kenzo M, Mattei M, Galgani A (2018) Investigation of medicinal plants traditionally used as dietary supplements: a review on Moringa oleifera. J Publ Health Afr 9(3):841

226

K. Král’ová and J. Jampílek

Mazeed A, Lothe NB, Kumar A, Sharma SK, Srivastav S, Verma RK (2020) Evaluation of phytoaccumulation potential of toxic metals from sewage sludge by high-value aromatic plant geranium. J Environ Biol 41(4):761–769 Mbanga O, Ncube S, Tutu H, Chimuka L, Cukrowska E (2019) Mercury accumulation and biotransportation in wetland biota affected by gold mining. Environ Monit Assess 191(3):186 Meena AK, Yadav A, Rao MM (2011) Ayurvedic uses and pharmacological activities of Calotropis procera Linn. Asian J Tradit Med 6(2):45–53 Memon AR, Schröder P (2009) Implications of metal accumulation mechanisms to phytoremediation. Environ Sci Pollut Res 16:162–175 Midhat L, Ouazzani N, Hejjaj A, Ouhammon A, Mandi L (2019) Accumulation of heavy metals in metallophytes from three mining sites (Southern Centre Morocco) and evaluation of their phytoremediation potential. Ecotoxicol Environ Saf 169:150–160 Miroddi M, Mannucci C, Mancari F, Navarra M, Calapai G (2013) Research and development for botanical products in medicinals and food supplements market. Evid Based Complementary Altern Med 2013:649720 Mleczek M, Golinski P, Krzeslowska M, Gasecka M, Magdziak Z, Rutkowski P, Budzynska S, Waliszewska B, Kozubik T, Karolewski Z (2017) Phytoextraction of potentially toxic elements by six tree species growing on hazardous mining sludge. Environ Sci Pollut 24(28):22183–22195 Mleczek M, Rutkowski P, Kaniuczak J, Szostek M, Budka A, Magdziak Z, Budzynska S, KuczynskaKippen N, Niedzielski P (2019) The significance of selected tree species age in their efficiency in elements phytoextraction from wastes mixture. Int J Environ Sci Technol 16(7):3579–3594 Mohebzadeh F, Motesharezadeh B, Jafari M, Zare S, Aman MS (2021) Remediation of heavy metal polluted soil by utilizing organic amendments and two plant species (Ailanthus altissima and Melia azedarach). Arabian J Geosci 14(13):1211 Molnarova M, Ruzickova J, Lehotska B, Takacova A, Fargasova A (2018) Determining As, Cd, Cu, Pb, Sb, and Zn in leaves of trees collected near mining locations of Male Karpaty Mts. in the Slovak Republic. Pol J Environ Stud 27(5):2179–2191 Moreno-Jimenez E, Penalosa JM, Manzano R, Carpena-Ruiz RO, Gamarra R, Esteban E (2009) Heavy metals distribution in soils surrounding an abandoned mine in NW Madrid (Spain) and their transference to wild flora. J Hazard Mater 162(2–3):854–859 Morgan L (2021) History of essential oils. In: Aromatherapy Guide. https://healingscents.net/blogs/ learn/18685859-history-of-essential-oils Morrison RS, Brooks RR, Reeves RD, Malaisse F (1979) Copper and cobalt uptake by 601 metallophytes from Zaïre. Plant Soil 53:535–539 Mughini G, Alianiello F, Benedetti A, Gras LM, Gras MA, Salvati L (2013) Clonal variation in growth, arsenic and heavy metal uptakes of hybrid Eucalyptus clones in a Mediterranean environment. Agrofor Syst 87:755–766 Muthusaravanan S, Sivarajasekar N, Vivek JS, Paramasivan T, Naushad MU, Prakashmaran J, Gayathri V, Al-Duaij OK (2018) Phytoremediation of heavy metals: mechanisms, methods and enhancements. Environ Chem Lett 16:1339–1359 Nacira A, Fatima K, Wahiba K, Safia I, Cherifa B, Zahia K (2011) Cardioprotective effect of Algerian medicinal plant Globularia alypum extract against cardiotoxicity of Adriamycin in rats. Planta Med 77(12):1454–1454 Nagajyoti PC, Lee KD, Sreekanth TVM (2010) Heavy metals, occurrence and toxicity for plants: a review. Environ Chem Lett 8(3):199–216 Naharro R, Esbri JM, Amoros JA, Garcia-Navarro FJ, Higueras P (2019) Assessment of mercury uptake routes at the soil-plant-atmosphere interface. Geochem Expolr Environ Anal 19:146–154 Najmanova J, Neumannova E, Leonhardt T, Zitka O, Kizek R, Macek T, Mackova M, Kotrba P (2012) Cadmium-induced production of phytochelatins and speciation of intracellular cadmium in organs of Linum usitatissimum seedlings. Ind Crops Prod 36(1):536–542 Nieto G (2020) A review on applications and uses of Thymus in the food industry. Plants 9:961

7 Medicinal and Aromatic Plant Species with Potential for Remediation …

227

Nirmal J, Babu CS, Harisudhan T, Ramanathan M (2008) Evaluation of behavioural and antioxidant activity of Cytisus scoparius Link in rats exposed to chronic unpredictable mild stress. BMC Complement Altern Med 8:15 Niu XY, Wang SK, Zhou J, Di DL, Sun P, Huang DZ (2021) Inoculation with indigenous rhizosphere microbes enhances aboveground accumulation of lead in Salix integra Thunb. by improving transport coefficients. Front Microbiol 12:686812 Ong GH, Cheng WH, Wong LS (2018) Accumulation of arsenic and antimony in Aloe barbadensis: a transplantation study. Remediation J 29(1):53–57 Ortiz J, Soto J, Fuentes A, Herrera H, Meneses C, Arriagada C (2019) The endophytic fungus Chaetomium cupreum regulates expression of genes involved in the tolerance to metals and plant growth promotion in Eucalyptus globulus roots. Microorganisms 7:490 Ortiz-Oliveros HB, Cruz D, Flores-Espinosa RM, Santillan-Malaquias I, Zarazua-Ortega G, Villalva A (2021) Evaluation of the bioaccumulation of heavy metals and 137 Cs in succulent plants Echeveria elegans. Int J Environ Sci Technol 2021:126849 Ozbilgin S, Akkol EK, Suntar I, Tekin M, Iscan GS (2019) Wound-healing species of Euphorbia L. Rec Nat Prod 13(2):104–113 Ozyigit II, Can H, Dogan I (2021) Phytoremediation using genetically engineered plants to remove metals: a review. Environ Chem Lett 19:669–698 Pajevi´c S, Borišev M, Nikoli´c N, Arsenov DD, Orlovi´c S, Župunski M (2016) Phytoextraction of heavy metals by fast-growing trees: a review. In: Ansari A, Gill S, Gill R, Lanza G, Newman L (eds) Phytoremediation. Springer, Cham, pp 29–64 Panda SK, Choudhary S, Patra HK (2016) Heavy-metal induced oxidative stress in plants: physiological and molecular perspectives. In: Tuteja N, Gill SS (eds) Abiotic stress response in plants. Wiley VCH Verlag, pp 219–232 Pandey S, Gupta K, Mukherjee AK (2007) Impact of cadmium and lead on Catharanthus roseus a phytoremediation study. J Environ Biol 28(3):655–662 Pandey J, Verma RK, Singh S (2019a) Screening of most potential candidate among different lemongrass varieties for phytoremediation of tannery sludge contaminated sites. Int J Phytorem 21(6):600–609 Pandey J, Verma RK, Singh S (2019b) Suitability of aromatic plants for phytoremediation of heavy metal contaminated areas: a review. Int J Phytorem 21(5):405–418 Pant PP, Tripathi AK, Gariola S (2011) Phytoremediation of arsenic using Cassia fistula Linn Seedling. Int J Res Chem Environ 1(1):24–28 Pasricha S, Mathur V, Garg A, Lenka S, Verma K, Agarwal S (2021) Molecular mechanisms underlying heavy metal uptake, translocation and tolerance in hyperaccumulators-an analysis. Heavy metal tolerance in hyperaccumulators. Environ Challenges 4:100197 Pathania S, Bansal P, Gupta P, Rawal RK (2020) Genus Calotropis: a hub of medicinally active phytoconstituents. Curr Tradit Med 6(4):312–331 Patil SM, Shirahatti PS, Kumari VBC, Ramu R, Prasad MNN (2021) Azadirachta indica A. Juss (neem) as a contraceptive: An evidence-based review on its pharmacological efficiency. Phytomedicine 88:153596 Pattanayak S, Mandal TK, Bandyopadhyay SK (2016) Validation and therapeutic use ofd succulent plant parts—opening of new horizon of alternative medicine. Explor Anim Medical Res 6(1):8–14 Pavloviˇc A, Masaroviˇcová E, Kráˇlová K, Kubová J (2006) Response of chamomile plants (Matricaria recutita L.) to cadmium treatment. Bull Environ Contam Toxicol 77:763–771 Pecina V, Juricka D, Kynicky J, Baltazar T, Komendova R, Brtnicky M (2020) The need to improve riparian forests management in uranium mining areas based on assessment of heavy metal and uranium contamination. Forests 11(9):952 Perlein A, Zdanevitch I, Gaucher R, Robinson B, Papin A, Sahraoui ALH, Bert V (2021) Phytomanagement of a metal(loid)-contaminated agricultural site using aromatic and medicinal plants to produce essential oils: analysis of the metal(loid) fate in the value chain. Environ Sci Pollut Res Article Number 147944

228

K. Král’ová and J. Jampílek

Phumthum M, Nguanchoo V, Bakskey H (2021) Medicinal plants used for treating mild COVID-19 symptoms among Thai Karen and Hmong. Front Pharmacol 12:699897 Picchi C, Giorgetti L, Morelli E, Landi M, Rosselini I, Grifoni M, Franchi E, Petruzzelli G, Barbafieri M (2022) Cannabis sativa L. and Brassica juncea L. grown on arsenic-contaminated industrial soil: potentiality and limitation for phytoremediation. Environ Sci Pollut Res 29(11):15983– 15998 Pirzadah TB, Malik B, Dar FA (2019) Phytoremediation potential of aromatic and medicinal plants: a way forward to green economy. J Stress Physiol Biochem 15(3):62–75 Pivetz BE (2001) Phytoremediation of contaminated soil and ground water at hazardous waste sites. United States Environmental Protection Agency, Office of Solid Waste and Emergency Response. EPA/540/S-01/500, February 2001 Polito L, Bortolotti M, Battelli MG, Calafato G, Bolognesi A (2019) Ricin: an ancient story for a timeless plant toxin. Toxins 11(6):324 Pollard AJ, Powell KD, Harper FA, Smith JAC (2002) The genetic basis of hyperaccumulation in plants. Crit Rev Plant Sci 21:539–566 Pollard AJ, Stewart HS, Roberson CB (2009) Manganese hyperaccumulation in Phytolacca americana L. from the southeastern United States. Northeast Naturalist 16(5):155–162 Pollard AJ, Reeves RD, Baker AJM (2014) Facultative hyperaccumulation of heavy metals and metalloids. Plant Sci 217–218:8–17 Por˛ebska G, Ostrowska A (1999) Heavy metal accumulation in wild plants: implications for phytoremediation. Pol J Environ Stud 8(6):433–442 Prapagdee B, Khonsue N (2015) Bacterial-assisted cadmium phytoremediation by Ocimum gratissimum L. in polluted agricultural soil: a field trial experiment. Int J Environ Sci Technol 12:3843–3852 Prasad A, Singh AK, Chand S, Chanotiya CS, Patra DD (2010) Effect of chromium and lead on yield, chemical composition of essential oil, and accumulation of heavy metals of mint species. Commun Soil Sci Plant Anal 41(18):2170–2186 Prasad B, Kumar D, Sinha P, Kumari R, Singh S, Swati S (2015) Bioaccumulation of heavy metals in plants near mining and non-mining areas. Asian J Water Environ Pollut 12(1):53–59 Prasad MNV (2019) Transgenic plant technology for remediation of toxic metals and metalloids. Elsevier, Amsterdam Pratas J, Favas PJC, D’Souza R, Varun M, Paul MS (2013) Phytoremedial assessment of flora tolerant to heavy metals in the contaminated soils of an abandoned Pb mine in Central Portugal. Chemosphere 90(8):2216–2225 Pruteanu A, Muscalu A (2014) Phytoremediation using medicinal plants—a review. Ann Univ Craiova—Agric Montanol Cadastre Ser 44:186–193 Putwattana N, Kruatrachue M, Pokethitiyook P, Chaiyarat R (2010) Immobilization of cadmium in soil by cow manure and silicate fertilizer, and reduced accumulation of cadmium in sweet basil (Ocimum basilicum). ScienceAsia 36:349–354 Qadir SU, Raja V, Siddiqi WA, Alyemeni MN, Wijaya L, Ahmad P (2021) Heavy metal bioaccumulation by selected plants from fly ash-contaminated soils in suburban area. Arab J Geosci 14(2):116 Radziemska M, Vaverkova MD, Baryla A (2017) Phytostabilization-management strategy for stabilizing trace elements in contaminated soils. Int J Environ Res 14(9):958 Ramana S, Biswas AK, Singh AB, Ajay, Ahirwar NK, Prasad RD, Srivastava S (2015a) Potential of Mauritius hemp (Furcraea gigantea Vent.) for the remediation of chromium contaminated soils. Int J Phytorem 17(7):709–715 Ramana S, Biswas AK, Singh AB, Ajay ANK, Rao AS (2015b) Tolerance of ornamental succulent plant crown of thorns (Euphorbia milli) to chromium and its remediation. Int J Phytorem 17(4):363–368 Ramana S, Biswas AK, Ajay SAB, Srivastava S, Naqvi A (2016) Potential of mestha (Hibiscus sabdarifa) for remediation of soils contaminated with chromium. J Nat Fibers 13(5):597–602

7 Medicinal and Aromatic Plant Species with Potential for Remediation …

229

Rana MS, Bhantana P, Imran M, Saleem MH, Moussa MG, Khan Z, Khan I, Alam M, Abbas M, Binyamin R, Afzal J, Syaifudin M, Din IU, Younas N, Ahmad I, Hu SMA, Hu CX (2020) Molybdenum potential vital role in plants metabolism for optimizing the growth and development. Ann Environ Sci Toxicol 4(1):032–044 Rangra NK, Samanta S, Pradhan KK (2019) A comprehensive review on phytopharmacological investigations of Acacia auriculiformis A. Cunn. ex Benth. Asian Pac J Trop Biomed 9(1):1–11 Rani P, Kumar A, Arya RC, Tripti (2018) Ricinus communis and Calotropis procera as putative plant species for the phytostabilization of tannery contaminated soil: a dynamic approach. In: Tretyakova AS, Veseelkn DV (eds) Fourth international scientific conference ecology and geography of plants and plant communities. Book Series: KnE Life Sciences, pp 10–18 Rasic-Milutinovic Z, Jovanovic D (2013) Toxic metals. In: Ferrante M, Oliveri Conti G, RasicMilutinovic Z, Jovanovic D (eds) Health effects of metals and related substances in drinking water. IWA Publishing, London, pp 6–9 Rather LJ, Shahid-ul-Islam, Mohammad, F (2015) Acacia nilotica (L.): a review of its traditional uses, phytochemistry, and pharmacology. Sustain Chem Pharm 2:12–30 Rauf A, Khan A, Uddin N, Akram M, Arfan M, Uddin G, Qaisar M (2014) Preliminary phytochemical screening, antimicrobial and antioxidant activities of Euphorbia milli. Pak J Pharm Sci 27(4):947–951 Raut DN, Mandal SC, Pal SC (2014) Phytochemical and pharmacological overview of Hibiscus mutabilis Linn. Int J Pharm Res Biosci 3(3):236–241 Raveau R, Fontaine J, Hijri M, Sahraoui ALH (2020) The aromatic plant clary sage shaped bacterial communities in the roots and in the trace element-contaminated soil more than mycorrhizal inoculation—a two-year monitoring field trial. Front Microbiol 11:586050 Raveau R, Fontaine J, Bert V, Perlein A, Tisserant B, Ferrant P, Sahraoui ALH (2021) In situ cultivation of aromatic plant species for the phytomanagement of an aged-trace element polluted soil: Plant biomass improvement options and techno-economic assessment of the essential oil production channel. Sci Total Environ 789:147944 Reboredo FH, Pelica J. Lidon FC, Pessoa MF, Silva MM, Guerra M, Leitao R, Ramalho JC (2021) The tolerance of Eucalyptus globulus to soil contamination with arsenic. Plants-Basel 10:627 Reeves RD, Baker AJM (2000) Metal-accumulating plants. In: Raskin I, Ensley BD (eds) Phytoremediation of toxic metals: using plants to clean-up the environment. K John Wiley and Sons, New York, pp 193–230 Reeves R (2006) Hyperaccumulation of trace elements by plants. In: Morel JL, Echevarria G, Goncharova N (eds) Phytoremediation of metal-contaminated soils. Springer, Dordrecht, pp 25– 52 Reeves RD, Baker AJM, Jaffré T, Erskine PD, Echevarria G, van der Ent (2018) A global database for plants that hyperaccumulate metal and metalloid trace elements. New Phytologist 218(2):407–411 Rehman R, Hanif MA, Mustaq Z, Mohammed Ak-Sadi AM (2016) Biosynthesis of essential oils in aromatic plants: A review. Food Rev Int 32(2):117–160 Rezaizad M, Hashemi-Moghaddam H, Abbaspour H, Gerami M, Mueller A (2019) Photocatalytic effect of TiO2 nanoparticles on morphological and photochemical properties of stevia plant (Stevia rebaudiana Bertoni). Sugar Tech 21:1024–1030 Rheay HT, Omondi EC, Brewer CE (2021) Potential of hemp (Cannabis sativa L.) for paired phytoremediation and bioenergy production. GCB Bioenergy 13:525–536 Rios JL (2016) Essential oils: what they are and how the terms are used and defined. In: Preedy VR (ed) Essential oils in food preservation, flavor and safety. Elsevier, Amsterdam, pp 3–10 Rosselli W, Rossi M, Sasu I (2006) Cd, Cu and Zn contents in the leaves of Taraxacum officinale. For Snow Landsc Res 80(3):361–366 Rout GR, Sahoo S (2015) Role of iron in plant growth and metabolisms. Rev Agric Sci 3:1–24 Ruhela M, Bhutiani R, Ahamad F, Khanna DR (2019) Impact of Hindon river water on selected riparian flora (Azadirachta indica and Acacia nilotica) with special reference to heavy metals. Pollution 5(4):749–760

230

K. Král’ová and J. Jampílek

Ruscitti M, Arango M, Beltrano J (2017) Improvement of copper stress tolerance in pepper plants (Capsicum annuum L.) by inoculation with arbuscular mycorrhizal fungi. Theor Exp Plant Physiol 29(1):37–49 Ruzickova P, Szakova J, Havlik J, Tlustos P (2015) The effect of soil risk element contamination level on the element contents in Ocimum basilicum L. Arch Environ Protect 41(2):47–53 Sá RA, Sá RA, Alberton O, Gazim ZC, Laverde A Jr, Caetano J, Amorin AC, Dragunski DC (2014) Phytoaccumulation and effect of lead on yield and chemical composition of Mentha crispa essential oil. Desalin Water Treat 53(11):3007–3017 Saba G, Parizanganeh AH, Zamani A, Saba J (2015) Phytoremediation of heavy metals contaminated environments: screening for native accumulator plants in Zanjan-Iran. Int J Environ Res 9(1):309– 316 Saffari VR, Saffari M (2020) Effects of EDTA, citric acid, and tartaric acid application on growth, phytoremediation potential, and antioxidant response of Calendula officinalis L. in a cadmiumspiked calcareous soil. Int J Phytorem 22(11):1204–1214 Sajad MA, Khan MS, Bahadur S, Naeem A, Ali H, Batool F, Shuaib M, Khan MAS, Batool S (2020) Evaluation of chromium phytoremediation potential of some plant species of Dir Lower, Khyber Pakhtunkhwa, Pakistan. Acta Ecol Sin 40:158–165 Salas-Luevano MA, Mauricio-Castillo JA, Gonzalez-Rivera ML, Vega-Carrillo HR, Salas-Munoz S (2017) Accumulation and phytostabilization of As, Pb and Cd in plants growing inside mine tailings reforested in Zacatecas Mexico. Environ Earth Sci 76(23):806 Salas-Luevano MA, Puente-Cuevas R, Vega-Carrillo HR (2021) Concentrations of heavy metals and measurement of 40 K in mine tailings in Zacatecas Mexico. Environ Earth Sci 80(5):186 Salducci MD, Folzer H, Issartel J, Rabier J, Masotti V, Prudent P, Affre L, Hardion L, Tatoni T, Laffont-Schwob I (2019) How can a rare protected plant cope with the metal and metalloid soil pollution resulting from past industrial activities? Phytometabolites, antioxidant activities and root symbiosis involved in the metal tolerance of Astragalus tragacantha. Chemosphere 217:887–896 Saleem MH, Ali S, Hussain S, Kamran M, Chattha MS, Ahmad S, Aqeel M, Rizwan M, Aljarba NH, Alkahtani S (2020) Flax (Linum usitatissimum L.): a potential candidate for phytoremediation? Biological and economical points of view. Plants 9(4):496 Šalamon I, Kráˇlová K, Masaroviˇcová E (2007) Accumulation of cadmium in chamomile plants cultivated in Eastern Slovakia regions. Acta Hort (ISHS) 749:217–22 Salehi B, Hernandez-Alvarez AJ, Contreras MD, Martorell M, Ramirez-Alarcon K, Melgar-Lalanne G, Matthews KR, Sharifi-Rad M, Setzer WN, Nadeem M (2018) Potential phytopharmacy and food applications of Capsicum spp.: a comprehensive review. Nat Prod Commun 13(11):1543– 1556 Samara T, Spanos I, Platis P, Papachristou TG (2020) Heavy metal retention by different forest species used for restoration of post-mining landscapes. N. Greece. Sustainability 12(11):4453 Sanati S, Razavi BM, Hosseinzadeh H (2018) A review of the effects of Capsicum annuum L. and its constituent, capsaicin, in metabolic syndrome. Iran J Basic Med Sci 21(5):439–448 Sanchez-Gavilan I, Rufo L, Rodriguez N, de la Fuente V (2021) On the elemental composition of the Mediterranean euhalophyte Salicornia patula Duval-Jouve (Chenopodiaceae) from saline habitats in Spain (Huelva, Toledo and Zamora). Environ Sci Pollut Res 28(3):2719–2727 Sandhir R, Khurana M, Singhal NK (2021) Potential benefits of phytochemicals from Azadirachta indica against neurological disorders. Neurochem Int 146:105023 Saper BR (2021) Overview of herbal medicine and dietary supplements. UpToDate; https://www. uptodate.com/contents/overview-of-herbal-medicine-and-dietary-supplements. Accessed on 28 Nov 2021 Sarkar S, Singh RP, Bhattacharya G (2021) Exploring the role of Azadirachta indica (neem) and its active compounds in the regulation of biological pathways: an update on molecular approach. 3Biotech 11(4):178 Sasmaz A, Sasmaz M (2009) The phytoremediation potential for strontium of indigenous plants growing in a mining area. Environ Exp Bot 67(1):139–144

7 Medicinal and Aromatic Plant Species with Potential for Remediation …

231

Sasmaz M, Akgül B, Yıldırım D, Sasmaz A (2016) Mercury uptake and phytotoxicity in terrestrial plants grown naturally in the Gumuskoy (Kutahya) mining area, Turkey. Int J Phytorem 18:69–76 Saxena G, Purchase D, Mulla SI, Saratale GD, Bharagava RN (2019) Phytoremediation of heavy metal-contaminated sites: eco-environmental concerns, field studies, sustainability issues and future prospects. In: de Voogt P (ed) Reviews of environmental contamination and toxicology, vol 249. Springer, Cham, pp 71–131 Schachtschneider K, Chamier J, Somerset V (2017) Phytostabilization of metals by indigenous riparian vegetation. Water SA 43(2):177–185 Schippmann U, Leaman DJ, Cunningham AB (2002) Impact of cultivation and gathering of medicinal plants on biodiversity: Global trends and issues. In: FAO 2002 biodiversity and the ecosystem approach in agriculture, forestry and fisheries. Satellite event on the occasion of the Ninth Regular Session of the Commission on Genetic Resources for Food and Agriculture, Rome, October 12–13 Schmidt SB, Husted S (2019) The biochemical properties of manganese in plants. Plants 8(10):381 Schnaubelt K (2005) Essential oil therapy according to traditional Chinese medical concepts. Int J Aromather 15(2):98–105 Schneider M, Marquard R (1996) Investigation on the uptake of cadmium in Hypericum perforatum L. (St. John’s wort). Acta Hortic 426:435–442 Serrano HC, Cotrim H, Pinto MJ, Martins-Loucao MA, Branquinho C (2017) Metal hyperaccumulation patterns within Plantago phylogeny (Plantaginaceae). Plant Soil 411(1–2):227–241 Shabbir A, Khan MMA, Ahmad B, Sadiq Y, Jaleel H, Uddin M (2019) Efficacy of TiO2 nanoparticles in enhancing the photosynthesis, essential oil and khusimol biosynthesis in Vetiveria zizanioides L. Nash. Photosynthetica 57:599–606 Shackira AM, Puthur JT (2017) Enhanced phytostabilization of cadmium by a halophyte—Acanthus ilicifolius L. Int J Phytoremediation 19:319–326 Shahhoseini R, Azizi M, Asili J, Moshtaghi N, Samiei L (2020) Effects of zinc oxide nanoelicitors on yield, secondary metabolites, zinc and iron absorption of Feverfew (Tanacetum parthenium (L.) Schultz Bip.). Acta Physiol Plant 42:52 Shahid M, Javed MT, Masood S, Akram MS, Azeem M, Ali, Gilani R, Basit F, Abid A, Lindberg S (2019) Serratia sp. CP-13 augments the growth of cadmium (Cd)-stressed Linum usitatissimum L. by limited Cd uptake, enhanced nutrient acquisition and antioxidative potential. J Appl Microbiol 126(6):1708–1721 Shahzad B, Tanveer M, Rehman A, Cheema SA, Fahad S, Rehman S, Sharma S (2018) Nickel; whether toxic or essential for plants and environment—a review. Plant Physiol Biochem 132:641– 651 Shams KM, Tichy G, Fischer A, Sager M, Peer T, Bashar A, Filip K (2010) Aspects of phytoremediation for chromium contaminated sites using common plants Urtica dioica, Brassica napus and Zea mays. Plant Soil 328:175–189 Shan MQ, Shang J, Ding AW (2014) Platycladus orientalis leaves: a systemic review on botany, phytochemistry and pharmacology. Am J Chinese Med 42(3):523–542 Shang KK, Hu YH, Vincent G, Labrecque M (2020) Biomass and phytoextraction potential of three ornamental shrub species tested over three years on a large-scale experimental site in Shanghai, China. Int J Phytorem 22(1):10–19 Shao ZQ, Lu WL, Nasar J, Zhang JJ, Yan L (2019) Growth responses and accumulation characteristics of three ornamentals under copper and lead contamination in a hydroponic-culture experiment. Bull Environ Contam Toxicol 103(6):854–859 Sharma S, Adholeya A (2011) Phytoremediation of Cr-contaminated soil using Aloe vera and Chrysopogon zizanioides along with AM fungi and filamentous saprobe fungi: a research study towards possible practical application. Mycorrhiza News 22(4):16–20 Sharma A, Kumar A, Jaitak V (2021) Pharmacological and chemical potential of Cassia fistula L—a critical review. J Herb Med 26:100407 Sheoran V, Sheoran AS, Poonia P (2016) Factors affecting phytoextraction: a review. Pedosphere 26(2):148–166

232

K. Král’ová and J. Jampílek

Shi YK, Mu XK, Li KR, Shao HB (2016) Soil characterization and differential patterns of heavy metal accumulation in woody plants grown in coal gangue wastelands in Shaanxi China. Environ Sci Pollut Res 23(13):13489–13497 Shireen F, Nawaz MA, Chen C, Zhang Q, Zheng ZH, Sohail H, Sun JY, Cao HS, Huang Y, Bie ZL (2018) Boron: functions and approaches to enhance its availability in plants for sustainable agriculture. Int J Mol Sci 19(7):1856 Shrivastava M, Khandelwal A, Srivastava S (2019) Heavy metal hyperaccumulator plants: the resource to understand the extreme adaptations of plants towards heavy metals. In: Srivastava S, Srivastava AK, Suprasanna P (eds) Plant-metal interaction. Springer, Cham, pp 79–97 Singer C (1923) Herbals. Edinburg Rev 237:95–112 Singh NP, Santal AR (2015) Phytoremediation of heavy metals: the use of green approaches to clean the environment. In: Ansari A, Gill S, Gill R, Lanza G, Newman L (eds) Phytoremediation. Springer, Cham, pp 115–129 Singh KL, Sudhakar G, Swaminathan SK, Rao CM (2015) Identification of elite native plants species for phytoaccumulation and remediation of major contaminants in uranium tailing ponds and its affected area. Environ Dev Sustain 17(1):57–81 Singh R, Geetanjali (2018) Chemotaxonomy of medicinal plants: possibilities and limitations. In: Mandal SC, Mandal V, Konishi T (eds) Natural products in drug discovery: an integrated approach. Elsevier, Amsterdam, pp 119–136 Sinhal VK, Srivastava A, Singh VP (2010) EDTA and citric acid mediated phytoextraction of Zn, Cu, Pb and Cd through marigold (Tagetes erecta). J Environ Biol 31(3):255–259 Sosa MD, Salazar MJ, Zygadlo JA, Wannaz ED (2016) Effects of Pb in Tagetes minuta L. (Asteraceae) leaves and its relationship with volatile compounds. Ind Crops Prod 82:37–43 Souri Z, Khanna K, Karimi N, Ahmad P (2021) Silicon and plants: current knowledge and future prospects. J Plant Growth Regul 40:906–925 Stancheva I, Geneva M, Hristozkova M, Markovska Y, Salamon I (2010) Antioxidant capacity of sage grown on heavy metal-polluted soil. Russ J Plant Physiol 57(6):799–805 Stancheva I, Geneva M, Boychinova M, Mitova I, Markovska Y (2014a) Physiological response of foliar fertilized Matricaria recutita L. grown on industrially polluted soil. J Plant Nutr 37(12):1952–1964 Stancheva I, Geneva M, Markovska Y, Tzvetkova N, Mitova I, Todorova M, Petrov P (2014b) A comparative study on plant morphology, gas exchange parameters, and antioxidant response of Ocimum basilicum L. and Origanum vulgare L. grown on industrially polluted soil. Turk J Biol 38(1):89–102 Steindor K, Palowski B (2011) Cadmium and lead accumulation in organs of chosen urban tree species. Ecol Chem Eng A 18(3):453–460 Stomp AM, Han KH, Wilbert S, Gordon MP (1993) Genetic improvement of tree species for remediation of hazardous wastes. In Vitro Cell Dev Biol Plant 29:227–232 Su C, Jiang L, Zhang W (2014) A review on heavy metal contamination in the soil worldwide: situation, impact and remediation techniques. Environ Skept Critics 3:24–38 Sun QY, Li F, Wang CX, Shen M (2019) Immunomodulatory effects of Robinia pseudoacacia polysaccharides on live vaccine against infectious bronchitis in immunosuppressive chickens. Int J Polym Sci 2019:9542759 Sun H, Li XL, Wu YG (2021) Effects of four woody plant species revegetation on habitat improvement and the spatial distribution of arsenic and antimony in zinc smelting slag. Int J Phytorem 23(14):1506–1518 Surbhi KA, Singh S, Kumari P, Rasane P (2021) Eucalyptus: phytochemical composition, extraction methods and food and medicinal applications. Adv Trad Med. https://doi.org/10.1007/s13596021-00582-7 Symma N, Buetergerds M, Sendker J, Petereit F, Hake A, Duefer M, Hensel A (2021) Novel piperidine and 3,4-dihydro-2H-pyrrole alkaloids from Tilia platyphyllos and Tilia cordata flowers. Planta Med 87(09):686–700

7 Medicinal and Aromatic Plant Species with Potential for Remediation …

233

Szakova J, Dziakova M, Kozakova A, Tlustos P (2018) The risk element uptake by chamomile (Matricaria recutita (L.) Rauschert) growing in four different soils. Arch Environ Protect 44(4):12–21 Tabrizi L, Mohammadi S, Delshad M, Zadeh BM (2015) Effect of arbuscular mycorrhizal fungi on yield and phytoremediation performance of pot marigold (Calendula officinalis L.) under heavy metals stress. Int J Phytorem 17(12):1244–1252 Tabrizi L, Lakzaei M, Motesharezadeh B (2021) The yield potential and growth responses of licorice (Glycyrrhiza glabraL.) to mycorrhization under Pb and Cd stress. Int J Phytorem 23(3):316–327 Tahraoui A, El-Hilaly J, Israili ZH, Lyoussi B (2007) Ethnopharmacological survey of plants used in the traditional treatment of hypertension and diabetes in south-eastern Morocco (Errachidia province). J Ethnopharmacol 110(1):105–117 Talukder P (2020) Role of phytochelatin and metallothionein in phytoremediation of heavy metals by Aloe vera L. (Aloe barbadensis Miller). J Indian Chem Soc 97(4):685–691 Tapia Y, Cala V, Eymar E, Frutos I, Garate A, Masaguer A (2011) Phytoextraction of cadmium by four Mediterranean shrub species. Int J Phytorem 13(6):567–579 Tapia Y, Eymar E, Garate A, Masaguer A (2013) Effect of citric acid on metals mobility in pruning wastes and biosolids compost and metals uptake in Atriplex halimus and Rosmarinus officinalis. Environ Monit Assess 185(5):4221–4229 Tas A, Sahin-Bolukbasi S, Cevik E, Ozmen E, Gumus E, Silig Y (2018) An in vitro study of cytotoxic activity of Euphorbia macroclada Boiss on MCF-7 cells. Indian J Pharm Educ Res 52(4):S119–S123 Testiati E, Parinet J, Massiani C, Laffont-Schwob I, Rabier J, Pfeifer HR, Lenoble V, Masotti V, Prudent P (2013) Trace metal and metalloid contamination levels in soils and in two native plant species of a former industrial site: evaluation of the phytostabilization potential. J Hazard Mater 248:131–141 Thangaswamy S, Manjunatha B, Suarez JP, Babu M, Ponnuswamy G, Reddy GVS, Mariadoss S (2015) Phytoremediation of tannery effluent polluted soils of Dindigul, Tamil Nadu, using arbuscular mycorrhizal fungi inoculated Azadirachta indica. J Chem Pharm Res 7(7):905–914 Thatoi H, Samantaray D, Das SK (2016) The genus Avicennia, a pioneer group of dominant mangrove plant species with potential medicinal values: a review. Front Life Sci 9(4):267–291 Todorovic D, Popovic D, Ajtic JV, Nikolic J (2013) Leaves of higher plants as biomonitors of radionuclides (137 Cs, 40 K, 210 Pb and 7 Be) in urban air. Environ Sci Pollut Res 20(1):525–532 Tóth G, Hermann T, Szatmári G, Pásztor L (2016) Maps of heavy metals in the soils of the European Union and proposed priority areas for detailed assessment. Sci Total Environ 565:1054–1062 Trabelsi N, Megdiche W, Ksouri R, Falleh H, Oueslati S, Soumaya B, Hajlaoui H, Abdelly C (2010) Solvent effects on phenolic contents and biological activities of the halophyte Limoniastrum monopetalum leaves. LWT-Food Sci Technol 43(4):632–639 Tu C, Ma LQ (2002) Effects of arsenic concentrations and forms on arsenic uptake by the hyperaccumulator ladder brake. J Environ Qual 31:641–647 Ul Khair K, Farid M, Ashraf U, Zubair M, Rizwan M, Farid S, Ishaq HK, Iftikhar U, Ali S (2020) Citric acid enhanced phytoextraction of nickel (Ni) and alleviate Mentha piperita (L.) from Ni-induced physiological and biochemical damages. Environ Sci Polut Res 27(21):27010–27022 Umer S, Hussain M, Arfan M, Rasul F (2022) Spatiotemporal variations of metals in urban roadside soils and ornamental plant species of Faisalabad Metropolitan, Pakistan. Int J Sci Environ Technol 19:6491–6498 Vaculik M, Jurkovic L, Matejkovic P, Molnarova M, Lux A (2013) Potential risk of arsenic and antimony accumulation by medicinal plants naturally growing on old mining sites. Water Air Soil Pollut 224(5):1546 van der Ent A, Baker AJM, Reeves RD, Pollard AJ, Schat H (2013) Hyperaccumulators of metal and metalloid trace elements: facts and fiction. Plant Soil 362:319–334 Varma S, Ekta, Jamgra M (2021) Heavy metals stress and defense strategies in plants: an overview. J Pharmacogn Phytochem 10(1):608–614

234

K. Král’ová and J. Jampílek

Varun M, D’Souza R, Pratas J, Paul MS (2012) Metal contamination of soils and plants associated with the glass industry in North Central India: prospects of phytoremediation. Environ Sci Pollut Res 19(1):269–281 Verbruggen N, Hermans C, Schat H (2009) Molecular mechanisms of metal hyperaccumulation in plants. New Phytol 181:759–776 Vernon RE (2013) Which elements are metalloids. J Chem Educ 90(12):1703–1707 Vijayaraghavan K, Arockiaraj J, Kamala-Kannan S (2017) Portulaca grandiflora as green roof vegetation: plant growth and phytoremediation experiments. Int J Phytorem 19(6):537–544 Viktorova J, Jandova Z, Madlenakova M, Prouzova P, Bartunek V, Vrchotova B, Lovecka P, Musilova L, Macek T (2016) Native phytoremediation potential of Urtica dioica for removal of PCBs and heavy metals can be improved by genetic manipulations using constitutive CaMV 35S promoter. PLoS ONE 11(12):e0167927 Vincent G, Shang K, Zhang GW, Labrecque M (2018) Preliminary results of the tolerance to inorganic contaminants and phytoextraction potential of twelve ornamental shrub species tested on an experimental contaminated site. iForest 11:442–448 Wang SL, Liao WB, Yu FQ, Liao B, Shu WS (2009) Hyperaccumulation of lead, zinc, and cadmium in plants growing on a lead/zinc outcrop in Yunnan Province. China Environ Geol 58:471 Wang JX, Feng XB, Anderson CWN, Zhu W, Yin RS, Wang H (2011) Mercury distribution in the soil-plant-air system at the Wanshan mercury mining district in Guizhou. Southwest China. Environ Toxicol Chem 30(2):2725–2731 Wang L, Ji B, Hu YH, Liu RQ, Sun W (2017) A review on in situ phytoremediation of mine tailings. Chemosphere 184:594–600 Wang F, Guan Q, Tian J, Lin J, Yang Y, Yang L, Pan N (2020) Contamination characteristics, source apportionment, and health risk assessment of heavy metals in agricultural soil in the Hexi Corridor. CATENA 191:104573 Wang M, Chen SB, Jia XY, Chen L (2021a) Concept and types of bioremediation. In: Hasanuzzaman M, Prasad MNV (eds) Handbook of bioremediation. Physiological, molecular and biotechnological interventions. Elsevier, Amsterdam, pp 3–8 Wang GB, Zhang QQ, Du WC, Ai FX, Yin Y, Ji R, Guo HY (2021b) Microbial communities in the rhizosphere of different willow genotypes affect phytoremediation potential in Cd contaminated soil. Sci Total Environ 769:145224 Wang KW, Xu ZZ, Liao XJ (2022) Bioactive compounds, health benefits and functional food products of sea buckthorn: a review. Crit Rev Food Sci Nutr 62(24):6761–6782 WHO (2005) National policy on traditional medicine and regulation of herbal medicines : report of a WHO global survey. https://apps.who.int/iris/handle/10665/43229. Accessed on 28 Nov 2021 WHO (2013) WHO Traditional Medicine Strategy 2014–2023. http://apps.who.int/medicinedocs/ documents/s21201en/s21201en.pdf. Accessed on 28 Nov 2021 Wójcik M, Gonnelli C, Selvi F, Dresler S, Rosta´nski A, Vangronsveld J (2017) Metallophytes of serpentine and calamine soils–their unique ecophysiology and potential for phytoremediation. Adv Bot Res 83:1–42 Wu FY, Ye ZH, Wu SC, Wong MH (2007) Metal accumulation and arbuscular mycorrhizal status in metallicolous and nonmetallicolous populations of Pteris vittata L. and Sedum alfredii Hance. Planta 226:1363–1378 Wu FY, Leung HM, Wu SC, Ye ZH, Wong MH (2009) Variation in arsenic, lead and zinc tolerance and accumulation in six populations of Pteris vittata L. from China. Environ Pollut 157:2394– 2404 Xing YZ, Wang ZL, Zhang C, He WX, Luo J (2019) Balance between soil remediation and economic benefits of Eucalyptus globulus. Bull Environ Contam Toxicol 102:887–891 Xue SG, Chen YX, Reeves RD, Lin Q, Fernando DR (2004) Manganese uptake and accumulation by the hyperaccumulator plant Phytolacca acinosa Roxb. (Phytolaccaeae). Environ Pollut 131:393– 399 Yan A, Wang YM, Tan SN, Yusof MLM, Ghosh S, Chen Z (2020) Phytoremediation: a promising approach for revegetation of heavy metal-polluted land. Front Plant Sci 11:359

7 Medicinal and Aromatic Plant Species with Potential for Remediation …

235

Yan LJ, Le QY, Sonne C, Yang YF, Yang H, Gu HP, Ma NL, Lam SS, Peng WX (2021) Phytoremediation of radionuclides in soil, sediments and water. J Hazard Mater 407:124771 Yang N, Zhou FR, Wang JX (2016) Eco-toxicological effects of two kinds of lead compounds on forest tree seed in alkaline soil. Environ Monitor Assess 188(3):201 Yaniv Z, Dudai N (2014) Medicinal and aromatic plants of the Middle-East. Springer, Dordrecht Ye LL, Chen YS, Chen YD, Qian LW, Xiong WL, Xu JH, Jiang JP (2020) Phytomanagement of a chromium-contaminated soil by a high-value plant: phytostabilization of heavy metal contaminated sites. BioResources 15(2):3545–3565 Yim M, Sarma BP, Sinha S, Deka H, Deka H, Parida P, Ghosh A, Johari S (2014) Exploring the possible mechanism of Albizzia lebbeck compounds binding with dug targets of bronchial asthma—an in silico and clinical analysis. Int J Pharm Sci Res 5(11):5042–5051 Yongpisanphop J, Babel S, Kruatrachue M, Pokethitiyook P (2017) Hydroponic screening of fast-growing tree species for lead phytoremediation potential. Bull Environ Contam Toxicol 99(4):518–523 Youssef NA (2021) Changes in the morphological traits and the essential oil content of sweet basil (Ocimum basilicum L.) as induced by cadmium and lead treatments. Int J Phytorem 23(3):291–299 Yruela I (2005) Copper in plants. Braz J Plant Physiol 17:145–156 Yruela I (2009) Copper in plants acquisition, transport and interactions. Funct Plant Biol 6:409–430 Zahedifar M, Moosavi AA, Zarei Z, Shafigh M, Karimian F (2019) Heavy metals content and distribution in basil (Ocimum basilicum L.) as influenced by cadmium and different potassium sources. Int J Phytorem 21(5):435–447 Zarinkamar F, Moradi A, Davoodpour M (2021) Ecophysiological, anatomical, and apigenin changes due to uptake and accumulation of cadmium in Matricaria chamomilla L. flowers in hydroponics. Environ Sci Pollut Res 28(39):55154–55165 Zemiani A, Boldarini MTB, Anami MH, de Oliveira EF, da Silva AF (2021) Tolerance of Mentha crispa L. (garden mint) cultivated in cadmium-contaminated oxisol. Environ Sci Pollut Res 28(31):42107–42120 Zhang XH, Liu J, Huang HT, Chen J, Zhu YN, Wang DQ (2007) Chromium accumulation by the hyperaccumulator plant Leersia hexandra Swartz. Chemos 67:1138–1143 Zhang CJ, Sale PWG, Clark GJ, Liu WX, Doronila AI, Kolev SD, Tang CX (2015) Succulent species differ substantially in their tolerance and phytoextraction potential when grown in the presence of Cd, Cr, Cu, Mn, Ni, Pb, and Zn. Environ Sci Pollut Res 22(23):18824–18838 Zhang CJ, Sale PWG, Tang CX (2016) Cadmium uptake by Carpobrotus rossii (Haw.) Schwantes under different saline conditions. Environ Sci Pollut Res 23(13):13480–13488 Zhang HJ, Jampilek J (2017) Anti-infective drug discovery based on diversified plant natural compounds. Curr Org Chem 21:1775–1776 Zhang X, Yu JL, Huang ZL, Li H, Liu XM, Huang J, Zhuo R, Wu ZJ, Qin XL, Gao Y (2021) Enhanced Cd phytostabilization and rhizosphere bacterial diversity of Robinia pseudoacacia L. by endophyte Enterobacter sp. YG-14 combined with sludge biochar. Sci Total Environ 787:147660 Zhao Y, Wu Y, Wang M (2015) Bioactive substances of plant origin. In: Cheung P, Mehta B (eds) Handbook of food chemistry. Springer, Berlin/Heidelberg, Germany, pp 967–1008 Zhao Y, Zhao K, Jiang K, Tao SS, Li YX, Chen WW, Kou SM, Gu CR, Li ZR, Guo LS (2016) A review of flavonoids from Cassia species and their biological activity. Curr Pharm Biotechnol 17(13):1134–1146 Zeng P, Guo ZH, Xiao XY, Cao X, Peng C (2018) Response to cadmium and phytostabilization potential of Platycladus orientalis in contaminated soil. Int J Phytorem 20(13):1337–1345 Zheljazkov VD, Craker LE, Xing BS (2006) Effects of Cd, Pb, and Cu on growth and essential oil contents in dill, peppermint, and basil. Environ Exp Bot 58(1–3):9–16 Zheljazkov VD, Jeliazkova EA, Kovacheva N, Dzhurmanski A (2008) Metal uptake by medicinal plant species grown in soils contaminated by a smelter. Environ Exp Bot 64(3):207–216 Zhou M, Zhi Y, Dai YY, Lv JL, Li YJ, Wu ZH (2020) The detoxification mechanisms of lowaccumulating and non-low-accumulating medicinal plants under Cd and Pb stress. RSC Adv 10(71):43882–43893

236

K. Král’ová and J. Jampílek

Ziarati P, Nazif M, Khandehrouy M (2015) Decreasing bio-toxicity of fume particles produced in welding process by Aloe vera L. Orient J Chem 31:113–120 Zielonka D, Szulc W, Skowronska M, Rutkowska B, Russel S (2020) Hemp-based phytoaccumulation of heavy metals from municipal sewage sludge and phosphogypsum under field conditions. Agronomy 10(6):907

Chapter 8

Heavy Metal Toxicity and Phytoremediation by the Plants of Brassicaceae Family: A Sustainable Management Kakan Ball, Zerald Tiru, Arka Pratim Chakraborty, Parimal Mandal, and Sanjoy Sadhukhan Abstract Heavy metals (Pb, Cd, Ni, Co, Fe, Zn, Cr, As, Ag, platinum group, etc.) in trace amounts are natural components of the environment. However, their presence in excess may cause a serious threat to the stability of the ecosystem by inducing a drastic change in the quality and yield of crop products. Heavy metal toxicity in the agro-ecosystem has now become a major challenge for the planet. To increase crop productivity, it is necessary to evolve efficient, low-cost technologies for reducing metal toxicity. Many appropriate technologies are available for removing or reducing such toxicants but as a cost-effective, eco-friendly, and sustainable method—phytoremediation is gaining worldwide attention for its effectiveness. In the present book chapter, we attempt an overview of current knowledge on the roles of several species of plants from the family Brassicaceae as metal hyper-accumulators. Characteristics of plant species of Brassicaceae as phytoremediators of heavy metals, detailed mechanisms of phytoremediation by plants from the Brassicaceae family, and methods to enhance heavy metal phytoextraction by using chelating chemicals or through biotechnology and genetic engineering have been focused. Keywords Heavy metals · Metal toxicity · Brassicaceae · Metal hyper-accumulators · Phytoremediation

Kakan Ball and Zerald Tiru: Both the authors contributed equally. K. Ball · S. Sadhukhan (B) Plant Molecular Biology Laboratory, Department of Botany, Raiganj University, Raiganj, Uttar Dinajpur, West Bengal 733134, India e-mail: [email protected] Z. Tiru Plant Physiology Laboratory, Department of Botany, Raiganj University, Raiganj, Uttar Dinajpur, West Bengal 733134, India A. P. Chakraborty · P. Mandal Mycology and Plant Pathology Laboratory, Department of Botany, Raiganj University, Raiganj, Uttar Dinajpur, West Bengal 733134, India © The Author(s), under exclusive license to Springer Nature Switzerland AG 2022 T. Aftab (ed.), Sustainable Management of Environmental Contaminants, Environmental Contamination Remediation and Management, https://doi.org/10.1007/978-3-031-08446-1_8

237

238

K. Ball et al.

8.1 Introduction The availability of heavy metals (HMs) in the environment has increased dramatically in recent decades as a result of the expansion of industries and urbanisation, raising serious concerns around the world (Ashraf et al. 2019; Suman et al. 2018). Heavy metals are a class of metallic elements with high density, atomic weights, and atomic numbers. Heavy metals include arsenic (As), cadmium (Cd), chromium (Cr), copper (Cu), lead (Pb), mercury (Hg), nickel (Ni), and zinc (Zn). The transition elements, lanthanides, actinides, and metalloids are among the HMs, which are potentially harmful even at low concentrations. These heavy metals/metalloids come from both natural and artificial (man-made) sources, such as water produced from the oil and gas industry (Neff et al. 2011; Pichtel 2016), enormous use of phosphate fertilisers in the agriculture industry (Hamzah et al. 2016; Rafique and Tariq 2016), application of pesticides (Iqbal et al. 2016), electroplating, and burning of fossil fuel (Muradoglu et al. 2015). Heavy metals are not degraded by biological or physical means, and they persist in the soil for a long period, creating a prolonged environmental hazard (Suman et al. 2018). Heavy metals may be categorised depending on the requirement of plants as essential and non-essential elements. Cu, Fe, Mn, Zn, and Ni are grouped under essential metals as they are needed in the plant life cycle (Cempel and Nikel 2006) although the essential metals become toxic to plants if they accumulate in excess amounts. Pb, Cd, As, and Hg are some non-essential heavy metals, highly toxic for plants (Fasani et al. 2018). Heavy metals can pollute the environment, disrupt a variety of physiological and biochemical processes in crops, and lower agricultural yield (Clemens 2006). When heavy metals reach inside the human body and accumulate through biomagnification by the food chain, they pose a major health hazard (Sarwar et al. 2010; ur Rehman et al. 2017). As a result, remediation measures are critical in stopping heavy metals to reach the land, air, and marine habitats, as well as for improving polluted soil (Gerhardt et al. 2017; Hasan et al. 2019). To reclaim heavy metal-contaminated soil, a range of remediation procedures have been developed. These interventions are implemented via mechanical or physio-chemical processes involving soil burning, removal and disposal, soil washing, solidification, as well as an electric field treatment (DalCorso et al. 2019; Sheoran et al. 2010; Wuana and Okieimen 2011). These physicochemical techniques have limitations like exorbitant prices, incompetence when pollutants are present at low levels, permanent transformation of soil physicochemical and biological characters, leading to soil ecosystem damage, and the emergence of subsequent pollutions (Ali et al. 2013; DalCorso et al. 2019). To retrieve heavy metal-contaminated soil, cost-effective, efficient, and eco-friendly remediation solutions are needed. Phytoremediation is a low-cost, environmentally acceptable method of eliminating or lowering hazardous contaminants from various components of the environment (Sarma 2011; Sharma et al. 2021; Tangahu et al. 2011). The term “phytoremediation” is derived from remediation the Greek phrase Phyto, meaning “plant,” and the Latin word remedium, meaning remediation, i.e. to correct or remove an evil. In this technique, plants are utilised to remove, sequester,

8 Heavy Metal Toxicity and Phytoremediation by the Plants …

239

and/or detoxify contaminants and are known as accumulator plants (Erakhrumen and Agbontalor 2007; Tangahu et al. 2011). Phytoremediation employs the unique and selective absorption capabilities of plant root systems, as well as excellent translocation, bioaccumulation, and pollutant breakdown capacities of accumulator plants. Several plant species have been reported for phytoremediation, and many of them are hyper-accumulators, capable of storing phytotoxic substances at concentrations 50–500 times higher than ordinary plants (Baker et al. 1994; Mellem et al. 2012; Palmer et al. 2001; Sarma 2011; Tangahu et al. 2011). If a plant can accumulate 1000 μg nickel (Ni) per Kg of leaf dry mass, 10,000 μ-g (zinc) Zn or manganese (Mn) g−1 shoot dry mass, 100 μ-g Cd g−1 shoot dry matter, and 1000 μ-m Co/Cu/Pb or Se g−1 shoot dry matter, it is called a hyper-accumulator of certain metals (Baker et al. 2020; Brooks et al. 1977). Approximately, 500 plant species are reported as bioaccumulator, most of these are angiosperms which include Asteraceae, Brassicaceae, Caryophyllaceae, Cyperaceae, Cunoniaceae, Fabaceae, Flacourtiaceae, Lamiaceae, Poaceae, Violaceae, and Euphorbiaceae families have the most hyper-accumulators (Vara Prasad and de Oliveira Freitas 2003). The family Brassicaceae is a hyperaccumulating angiosperm family which represents about 25% of total angiosperms (Dar et al. 2015; Krämer 2010; Palmer et al. 2001; Sarma 2011). Brassicaceae members are known due to their capacity to collect a considerable amount of heavy metals (Broadley et al. 2001). Brassicaceae plants are well known for their large biomass and ability to store large amounts of heavy metals (Dushenkov et al. 1995; Kumar et al. 1995). It is reported Brassicaceae plants include Brassica nigra Koch, Brassica oleracea L, Brassica campestris L., and Brassica napus L. With a high growth rate capable of accumulating heavy metals (Kumar et al. 1995), B. juncea accumulates as well as transports metals like Cu, Cr, Cd, Ni, Pb, and Zn towards their stems. All Brassicaceae species, on the other hand, have the same propensity to store and transport heavy metals towards their stems (Boye 2002). While most Brassica crop research has focused on oilseed and vegetable biotypes, rapid cycling Brassica biotypes of diverse species have recently received attention.

8.2 Sources and Toxicity of Heavy Metals Heavy metals (HMs) after entering the soil pose a substantial hazard to soil quality and have a negative impact on biological activities. HMs are non-biodegradable, i.e. intrinsic mechanisms of nature cannot remove them out of the biosphere. The major sources of heavy metals in the environment are mainly of two types: (i) geogenic (volcanic eruptions, leaching, and weathering of rocks) and (ii) anthropogenic (industrial, intensive metal mining, smelting, combustion of fossil fuels, use of pesticides, and sewage sludge, agricultural, pharmaceutical, household effluents), and atmospheric sources (Alloway 2013; Kumar et al. 2015; Wuana and Okieimen 2011). HMs cause soil dysfunction, plant developmental disorders, and even human health hazard through food chain contamination (Sidhu 2016). Heavy metals have been found to influence cellular organelles including the cell membrane, mitochondria, lysosomes,

240

K. Ball et al.

endoplasmic reticulum, nuclei, and several enzymes related to metabolism, detoxification, and damage repair in living organisms. Metal ions have been discovered to react with cellular constituents like DNA and nuclear proteins, inducing DNA damage and conformational changes which may result in cell cycle regulation, cancer, or apoptosis (Kaur et al. 2019; Tchounwou et al. 2012). Plants being sessile organisms are unable to avoid unfavourable environmental changes. Since heavy metals accumulate in crop plants, they diminish the yield of plants and pose serious health risks to humans (Rai et al. 2019). The harmful effects of HMs produce a wide array of physiological and biochemical modifications, and plants should develop and/or acquire several strategies to cope with the negative consequences. Plants, like other living beings, are often reactive to both a lack of and an abundance of some HM ions as critical micronutrients, whereas the same HM at larger concentrations such as Cd, Hg, and As are very harmful to metabolic functions. The phytotoxicity of Zn and Cd is manifested in diverse plant species by a reduction in growth and development, metabolism, as well as the generation of oxidative stress (Haider et al. 2021) (Fig. 8.1). Excessive Cu in the soil is cytotoxic, stimulates stress, and it causes leaf chlorosis and slowdowns plant growth (Arif et al. 2016). Lead has a negative impact on plant shape, growth, and physiological functions, i.e. photosynthetic mechanisms. It affects cell membrane permeability, hormonal changes, inhibition of certain sulfhydryl-containing enzymes, water content decrease, and mineral nutrition. Fig. 8.1 Diverse adverse effects on plants caused by heavy metals

8 Heavy Metal Toxicity and Phytoremediation by the Plants …

241

Plants resist heavy metal stress, through detoxification processes which include phytochelation of metals, vacuolar sequestration of chelated complexes, and stimulation of the enzymatic and non-enzymatic antioxidant systems (Kumar and Trivedi 2016).

8.3 Heavy Metal Uptake and Phytoremediation Potential When HMs build up in the plant, a series of physiological activities occur, including absorption, cellular compartmentation, mobilisation, root uptake, root-to-shoot transit, and xylem loading. Heavy metal is often found in soil as an insoluble form that is not accessible to plants. Plants can boost their accessibility by generating a range of root exudates that can alter the pH of the rhizosphere and the solubilisation of heavy metals (Yan et al. 2020). Plants can affect soil qualities by regulating the content of root exudates, allowing them to adapt and survive in harsh situations. They employ a variety of techniques, including (1) altering soil pH to solubilise nutrients into assimilable forms and (2) chelating harmful chemicals including HMs (Vives-Peris et al. 2020). The accessible metal adheres to the root surface and passes through the cell membrane to enter the root cells. Heavy metals infiltrate roots largely through two mechanisms: (a) apoplastic (passive diffusion) and (b) symplastic (active diffusion) (active transport against electrochemical potential gradients and concentration across the plasma membrane) (Luo and Zhang 2021). The ATP-dependent symplastic route regulates the general uptake of heavy metals using metal ion carriers or crosslinking molecules. Upon entering root cells, HM ions may develop complexes with different chelators, like organic acids. Carbonate, sulphate, and phosphate precipitate into complexes which are then fixed in the extracellular area (apoplastic cellular walls) or intracellular regions (symplastic compartments, such as vacuoles) (Broadley et al. 2007). Metal ions get encapsulated in vacuoles that might well be transported into the vascular bundles and then into the xylem channel via the root symplasm where they are then translocated to the shoots via xylem vessels (Yamaguchi et al. 2012). They are transported and dispersed in leaves via apoplast or symplast, where the ions are trapped in extracellular spaces (cell walls) or plant vacuoles, avoiding the build-up of unbound metal ions in the cytoplasm.

8.4 Heavy Metal Transporters Plants have developed numerous methods to deal with metal stress challenges, such as extrusion, exclusion, and detoxification. Excessive levels of heavy metals in soil suppress plant growth and expose plants to oxidative stress. All metals produce reactive oxygen species (ROS) when accumulated in excess, which trigger downstream plant responses such as phytohormones and mitogen-activated protein kinases

242

K. Ball et al.

(MPKs). Metal transporters may be involved in the activation of these pathways, which are similar to biotic stress circumstances in that they prevent or reduce the detrimental effects of heavy metal stress (Jonak et al. 2004; Liu et al. 2018; Opdenakker et al. 2012). Metal stress influences callose accumulation or decomposition near plasmodesmata, as well as aids in metal transport, through modifying genes involved in callose production, i.e. callose synthases and β-1, 3-glucanases (O’Lexy et al. 2018). Plants use a variety of carriers to seclude metal ions inside cell organelles presumably in a chelated or free ionic state. To reduce metallic harmful impacts, metal chelators are used in the metal-binding proteins or compounds including amino acids, amino acid derivatives, or organic acids (Clemens 2001; Hall 2002; Polle and Schützendübel 2003). Phytochelatins are among the most widely used plant metal chelators (PCs). These are glutathione polymers, which are small versions of the antioxidant chemical glutathione. PCs play a significant role in heavy metal detoxification (Yadav 2010). The Fe-chelator nicotianamine (NA) is another essential metal chelator. Heavy metals are transported and stored in roots and leaves in tomatoes thanks to NA, which also helps to reduce metal stress (Pich and Scholz 1996). The Fe-NA transporters YSL1 and YSL3 play an important role in Fe-long-distance sensing by regulating Fe levels in the phloem. Metal chelators are used not only for metal detoxification but also for transporting metals to a specific transporter system. Arsenic homeostasis in grains and leaves is maintained by transporters like NOD26-like intrinsic protein (OsNIP2; 1) and low silicon rice1 (LSI1) and LSI2. LSI2 that has been mutated, has a lower level of arsenic in grains (Ma and Yamaji 2008). Another study revealed that the calcium-dependent protein kinase AtCPK31 regulates arsenite absorption by binding to AtNIP1; 1. Furthermore, a mutant of AtCPK31 has better arsenite resistance in comparison with the wild type (Ji et al. 2017). Plants tend to use a variety of strategies to control metal transporters. Metal absorption through soil or mobilisation to other plant organs is involved by a variety of carriers located by the plasma membrane as well as envelope membranes of cell organelles including the vacuole, mitochondria, and plastids. Plants have a metal homeostasis sensing system in which transporters act as both receptors and transporters, or transceptors (Cointry and Vert 2019; Jogawat et al. 2021; Narayan et al. 2020; Yadav et al. 2021). Metal stress-induced ROS, particularly hydrogen peroxide (H2 O2 ), serves as a signalling compound involved in the control of metal carriers as well as alternative plant defence mechanisms including antioxidant system activities (Nazir et al. 2020). Plants also use energy-driven metal transport, namely ATP-binding cassettes (ABC) transporters and heavy metal ATPases, to facilitate metal efflux or extrusion (HMAs). The metals are normally effluxed from the root cells to the external environment or other areas of the plant, where they can accumulate safely. The importance of ABC transporters in metal transport and relocalisation has been demonstrated in several studies. Cd treatment stimulated the G-type ABC transporter ABCG36 in rice, and the loss-of-function mutant had higher Cd levels in roots, implying that ABCG36 is involved in Cd translocation from root to shoot (Fu et al. 2019). Heavy metal stress tolerance is provided by the Arabidopsis ABC transporter pleiotropic drug resistance 8 (AtPDR8), which functions as a plasma

8 Heavy Metal Toxicity and Phytoremediation by the Plants …

243

membrane-localised Cd efflux pump that extrudes Cd from the cytosol to the exterior of the cell (Kim et al. 2007).

8.5 Mechanism of Phytoremediation The type of pollutant, bioavailability, and soil conditions all influence the mechanisms and efficiency of phytoremediation (Cunningham and Ow 1996). Plants can clean up or remediate contaminated environments in a variety of ways (Fig. 8.2). Contaminants enter plants predominantly through the root system, which also contains the primary mechanisms for toxicity prevention. Water, nutrients, and other non-essential contaminants are collected and stored by the root system, which has a huge surface area (Rajendran et al. 2022; Raskin and Ensley 2000). a. Phytoextraction The uptake and transport of metal pollutants of the soil via plant roots into the shoot of the plants are referred to as phytoextraction, also known as phytoaccumulation. Phytoextraction is most commonly used to treat polluted soils (Laboratory

Fig. 8.2 Different types of phytoremediation mechanisms

244

K. Ball et al.

2000). Both water and soil ecosystems can benefit from phytoextraction. Phytoextraction is the process of removing toxins from plants’ roots, particularly heavy metals and metalloids, and transporting them to aerial plant organs. The focus of research and development is on two fields of study: (1) contaminants such as lead, arsenic, cadmium, chromium, mercury, and radioisotopes must be removed from the environment and (2) mining, or recovery of inorganic nuclides compounds, primarily Ni and Cu. Contaminants deposited in the aerial parts of plants are gathered as well as eliminated from the location using accumulating plants. Phytoextraction is classified into two types: induced and continuous. Continuous phytoextraction necessitates the use of plants that accumulate significant quantities of harmful pollutants throughout their lives. By adding accelerants or chelators to the soil, induced phytoextraction methods increase toxin accumulation at a single time point (Ali et al. 2021; Anderson et al. 1993; Bosiacki et al. 2014). b. Phytodegradation/phytotransformation The process of breaking down organic pollutants sequestered by plants is known as phytotransformation or phytodegradation (Pivetz 2001). It involves the degradation of complex contaminants into a simple molecule, which happens either inside the plant during metabolism or adjacent to the plant through phyllosphere and rhizosphere symbiotic relationships (McGrath and Zhao 2003). Rhizodegradation occurs in the rhizosphere and is carried out by soil organisms such as bacteria, fungus, or enzymes secreted by plants or microorganisms. Plants can produce enzymes such as nitroreductases, dehalogenases, and laccases that catalyse and accelerate degradation (Lee et al. 2020; Morikawa and Erkin 2003). Plants release sugars, amino acids, and enzymes that stimulate bacterial growth in the soil which help microbes, i.e. bacteria and fungi, to degrade the pollutants by releasing exudates/enzymes into the rhizosphere. Rhizodegradation is termed as plant-based bioremediation. As a result, organic contaminants are degraded into smaller molecular forms and absorbed within plant cells to enhance plant growth and development (Ma et al. 2016; Nigam and Sinha 2021; Pilon-Smits and LeDuc 2009). c. Phytovolatilisation The process in which plants collect inorganic and organic pollutants that are degraded and then released into the atmosphere via stomata. The pollutants that are emitted through stomata are destroyed in the atmosphere by hydroxyl radicals and remain as air pollutants, although with reduced toxicity (Limmer and Burken 2016). Phytovolatilisation is a technique that works for metals that are volatile (Hg and Se). The main advantage of this technique is that it converts the contaminants into a less toxic form. d. Rhizofiltration Rhizofiltration is a technique of phytoremediation in which contaminants are absorbed, concentrated, and precipitated by the use of hydroponically produced plant roots to remediate polluted water (Abdullahi 2015). The technique is used for cleaning up contaminated groundwater, surrounding the root zone upon plant roots,

8 Heavy Metal Toxicity and Phytoremediation by the Plants …

245

and uptake of pollutants within plant roots (rhizosphere). Heavy metals including lead, cadmium, cobalt, copper, uranium, and arsenic are way too low to be removed efficiently using conventional procedures but they can be removed effectively with this technology (Srivastava et al. 2021). Rhizofiltration is comparable to phytoextraction, except it focuses on the treatment of polluted groundwater instead of soil (Kaur et al. 2020). Metal pollutants such as copper, lead, cadmium, zinc, chromium, and nickel can be absorbed into the root tissues through the root surface. This approach makes use of both aquatic and terrestrial plants. e. Phytostabilisation Phytostabilisation is the process of setting a plant cover on the surface of polluted areas to minimise pollutants’ movement inside the vadose zone by accumulating them in the roots or immobilising them in the rhizosphere, reducing off-site pollution (Bolan et al. 2011). Phytostabilisation involves the trapping of edaphic pollutants (heavy metals) in soil. They are adsorbed on the root surface and precipitated within the root zone. In phytostabilisation, the entire plant is used for the inhibition of pollutants from spreading or migrating by wind and water erosion, soil scattering, as well as leakage. This process reduces the mobility of the pollutant as well as inhibits its movement into groundwater as well as diminishes the HMs bioavailability in the food chain. The technique is beneficial in remediating HMs such as lead (Pb), arsenic (As), cadmium (Cd), chromium (Cr), copper (Cu), and zinc (Zn) (Li et al. 2021; Yan et al. 2020) (Table 8.1).

8.6 Physiological Damage The harm caused by toxic levels of HMs has been linked to a variety of factors that usually act in concerts, such as direct metal damage and indirect oxidative stress (Viehweger 2014). Reduced chlorophyll (due to reduced synthesis or greater breakdown), changed water balance, lower activity of numerous enzymes, stomatal closure, photosynthetic rate slowdown, and reduced uptake of critical mineral nutrients are all commonly observed impacts (Angulo-Bejarano et al. 2021; Nagajyoti et al. 2010). Several investigations with heavy metals have found a drop in water content in metal-stressed plants, suggesting that the toxic effect of metals may be induced indirectly by a reduction in water intake (Ali et al. 2015). For example, the amount of water dramatically falls in B. juncea when exposed to Pb toxicity, even in this species that is considered tolerant (Mourato et al. 2015; Zaier et al. 2010). Heavy metal poisoning commonly shows up as growth retardation, but it can also show up in a multitude of ways. Root growth was inhibited, and root morphology was altered (Feigl et al. 2013; Jaishankar et al. 2014). Roots are usually more impacted than leaves since they are the organs that come into close touch with the harmful substance. Under different heavy metals, most studies of Brassica species find lower root development (Ebbs and Kochian 1997; John et al. 2009). Cu was found to have a stronger influence on lateral root formation than Zn (Ebbs and Kochian 1997). Under

246

K. Ball et al.

Table 8.1 Some plants of the Brassicaceae family with phytoremediation properties and their metal transporters Plants

Cell organelles involved in metal transport

Genes or transporters

Transported metal/metalloid

References

Arabidopsis thaliana

Vacuole

COPT1, COPT5

Cu and Fe

Carrió-Seguí et al. (2019), Liu et al. (2019), Zhang et al. (2020)

Plasma membrane

OsLCT1, OsHMA2 and OsZIP3

Zn and Cd

Tian et al. (2019)

Chloroplast

CMT1

Mn

Eisenhut et al. (2018)

Mitochondria

FRO3

Fe

Kim et al. (2021)

Golgi apparatus

AtNRAMP6

Fe

Li et al. (2019)

RAN1

Cu

Li et al. (2017)

AtIRT2

Fe

Vert et al. (2009)

ZTP29

Zn

Wang et al. (2010) Kupper et al. (1999)

Endoplasmic reticulum Arabidopsis halleri

Brassica chinensis

Mesophyll

?

Zn

Trichome

?

Zn, Cd

Vacuole

AhZIP6)

Cd

Spielmann et al. (2020)

Vacuole

BcIRT1, BcABCC1 and BcABCC2

Cd

Huang et al. (2021)

Brassica napus

Plasma membrane

NRAMP

Zn, Mn, Cd, Pb

Meng et al. (2017)

Golgi apparatus

BnMTP3

Mn and Zn

Gu et al. (2021)

Alyssum murale

Epidermal cell vacuoles

?

Ni

Smart et al. (2007)

Alyssum lesbiacum

Trichome, epidermis

?

Ni

Kramer et al. (1997)

A. inflatum

Trichome

?

Ni

Ghasemi et al. (2009)

Noccaea japonica

Vacuole

IREG2

Ni

Nishida et al. (2020)

Brassica juncea

Trichome

?

Cd

Salt et al. (1995)

Noccaea caerulescens

Epidermis

?

Zn

Vázquez et al. (1994)

Vacuole

?

Zn

Kupper et al. (1999) (continued)

8 Heavy Metal Toxicity and Phytoremediation by the Plants …

247

Table 8.1 (continued) Plants

Cell organelles involved in metal transport

Genes or transporters

Transported metal/metalloid

References

Noccaea goesingensis

Cell wall

?

Ni

Kramer et al. (2000)

? = Not reported

Cd stress, both root and shoot growth were reduced in B. juncea and B. napus, and it was thought that this was due to a restriction in the uptake of Fe and Mn to the shoots, but there was no evidence to support this hypothesis (Ahmad et al. 2021; Nouairi et al. 2006). Because Zn, like other heavy metals, usually accumulates in the roots, it has been found that Zn toxicity (500 μM) reduced root biomass but had no effect on foliar biomass in B. oleracea plants (Barrameda-Medina et al. 2014). Except for one of the four cultivars studied, there is a reduction in biomass in B. napus plants under Zn and Cd stress, however at greater concentrations (2000 and 250 μ-M, respectively) (Ghnaya et al. 2009). At a concentration of 500 μ-M, a similar impact was observed in B. rapa plants growing under Zn toxicity (Blasco et al. 2015). A considerable decrease in root biomass was seen in research on the toxic effects of Cu on B. juncea at Cu at a meagre level of 4 μ-M (Wang et al. 2004). Plant biomass was observed to be reduced at Pb concentrations of 200 μ-M and higher in a study on the same species (Zaier et al. 2010). Lead concentrations of 50 and 100 μ-M have been found to have a substantial impact on B. napus plants in hydroponic solution (Shakoor et al. 2014). Growth indicators, chlorophyll, and carotenoid content were all impaired, and levels of hydrogen peroxide and malondialdehyde increased dramatically, indicating oxidative stress. Although Cd is highly poisonous to plants (Cuypers et al. 2010), early growth metrics of B. juncea plants grown in Cd-polluted soil and hydroponics were recorded. The scientists ascribe it to a deleterious impact, which they believe is related to a plant’s “overcompensation” response to a break in equilibrium (Armas et al. 2015; Seth et al. 2008).

8.7 Micronutrient Status Excessive levels of heavy metals (essential or non-essential) can alter the intake of other important elements, although the outcomes are extremely variable, and there is no obvious trend to be seen. When B. napus and B. rapa plants were exposed to Cu, Zn, and Cu + Zn toxicity, there was an overall decrease in Mn and Fe (with less clear effects for B. juncea) (Ebbs and Kochian 1997). It has been found that more tolerant plants can preferentially uptake important nutrients and retain appropriate nutrition for their organs and that B. juncea under Pb stress has a large decline in nutrient concentration (Zaier et al. 2010). Outstanding decreases in Fe absorption

248

K. Ball et al.

were observed in a research on the toxicity of Cd in B. juncea plants grown in Cdcontaminated soil (Sikka and Nayyar 2012). Cu and Zn are also present but to a lower extent. Under Cd stress, primarily Zn contents in B. napus leaves were considerably decreased (Baryla et al. 2001), although not below the deficiency threshold. There was a considerable decline in Zn, Fe, Mn, and Co concentrations in a hydroponic experiment with B. juncea and B. napus plants with excess Cu, although the effect was not dose dependent (Feigl et al. 2013). Aside from the above-mentioned differences in heavy metal toxicity’s impact on essential element uptake, the interplay between these elements further exacerbates the issue. According to certain research, adding an essential element can minimise the hazardous effects of other heavy metals (Kaur et al. 2011). An excess amount of Zn was found to inhibit Cd absorption in B. juncea plants growing in Cd-contaminated soil when contrasted to a reference with regular quantities of the important element (Podar et al. 2004).

8.8 Enzymatic Defence Mechanism Heavy metals cause oxidative stress in plants and interfere with a variety of metabolic pathological processes (Dutta et al. 2018; Fryzova et al. 2017; Mittler 2002). Even though the precise methods through which various heavy metals cause plant toxicity are still unknown. Plants have a variety of defence mechanisms to diminish heavy metal toxicity, and each plant’s tolerance capacity is determined by the coordinated function of all of these systems, which include the induction of both enzymatic and non-enzymatic compounds (Emamverdian et al. 2015; Mourato et al. 2012). Several enzymes coordinate to prevent the harmful effects of reactive oxygen species (ROS) and other hazardous species. Ascorbate peroxidase (APX, EC 1.11.1.11), catalase (CAT, EC 1.11.1.6), and guaiacol peroxidase (GPOD, EC 1.11.1.7) catalyse the disintegration of H2 O2 to water. However at varying rates, with varied preferences, and in different organelles, their actions have been investigated in multiple trials using Brassica species and with various heavy metals (Emamverdian et al. 2015; Hasanuzzaman et al. 2020; Mittler 2002). Cu stress causes an increase in APX and GPOD, as well as a decrease in CAT in B. juncea (Małecka et al. 2019; Wang et al. 2004). While there was an increase in SOD and APX and a decrease in CAT in the same species, there was also an increase in Cd and Pb toxicity (John et al. 2009). The induced toxicity in this last experiment lasted for a long time (up to 60 days), and there was a general decrease in enzyme activity for the longer periods and higher dosages (300 mg/kg of Cd and 500 mg/kg of Pb). Even though the enzyme activity was not directly assessed, an increase in the transcript quantity of the catalase 3 gene (CAT3) was identified in B. juncea (Minglin et al. 2005). In B. juncea plants, higher Cd concentration increased CAT activity, but the effect in B. napus was the absolute opposite (Nouairi et al. 2009). Plant antioxidant defence also includes ascorbate and glutathione, which are both components of the ascorbate–glutathione cycle, which is a key metabolic route for the

8 Heavy Metal Toxicity and Phytoremediation by the Plants …

249

elimination of reactive oxygen species (ROS). Glutathione and ascorbate are potent antioxidants in and of themselves, and glutathione is required for the formation of phytochelatins, a family of essential heavy metal sequesters (Lallement et al. 2016; Potters et al. 2002). Increased ascorbate levels in plants, including Brassica species, are a frequent response to induced heavy metal stress, and this could point to its role as an antioxidant in the plant defence system (Feigl et al. 2013). When subjected to heavy metals, the interaction of many enzymes associated with the ascorbate– glutathione cycle (such as APX and glutathione reductase, GR, EC 1.6.4.2) increased in B. juncea plants, emphasising the role of this metabolism in providing resistance to this type of abiotic stress (Ahmad et al. 2015; Ali et al. 2015; Mobin and Khan 2007). GR has a role in the regeneration of reduced glutathione and reduced ascorbate that has been oxidised by H2 O2 (Mourato et al. 2012). The majority of research on metal poisoning offer analytical findings for antioxidative enzymes, with scanty research reporting highly specific gene expression measurements (Bernard et al. 2015). Although overexpression of a gene may not always result in increased enzyme activity, enzyme activity measurements are not always as precise as they are when measuring global enzyme activities. SOD, for example, has three isoforms: FeSOD (found in chloroplasts), MnSOD (found in mitochondria and peroxisomes), and Cu/ZnSOD (found in chloroplasts and cytoplasm), all of which are expressed by a large number of genes (Alscher et al. 2002).

8.9 Heavy Metal Chelating and Other Effects Plants use a variety of transporters for trapping metal ions into organelles, either chelated or unchelated. Surplus metals could be stored in neutral chelated forms in the vacuoles of plants. Long-distance transportation is also feasible with chelated metal forms. Metal chelators include metal-binding proteins as well as amino acids, amino acid derivatives, and organic acids, which aids in the reduction of metallic toxicity (Clemens 2001; Hall 2002; Morrissey and Guerinot 2009; Polle and Schützendübel 2003; Singh et al. 2016; Yadav 2010). Phytochelatins (PCs) are one of the most important plant metal chelators. These are glutathione polymers, which are small versions of the antioxidant chemical glutathione. Plant cells primarily use PCs as metal chelators. The enzyme phytochelatin synthase catalyses (PCS) the synthesis of PCs. Heavy metal clean-up necessitates the use of PCs (Yadav 2010). The Fechelator nicotianamine (NA) is another essential metal chelator. HMs are carried and accumulated in the roots and leaves of tomato plants due to NA which help to reduce metal stress (Pich and Scholz 1996). The Fe-NA transporters YSL1 and YSL3 play an important role in Fe-long-distance sensing by regulating Fe levels in the phloem. If the Fe level in the phloem of the shoot is normal, it indicates to the root that Fe is sufficient. Furthermore, when Fe was depleted, the YSL1 YSL3 double mutant was unable to trigger the Fe transporters iron regulated transporter 1 (IRT1) and ferric reduction oxidase 2 (FRO2) in roots, as well as other Fe-sensitive genes (Jogawat et al. 2021; Waters et al. 2006). In transgenic Arabidopsis, overexpression

250

K. Ball et al.

of MT2 from Brassica juncea (BjMT2) improved Cd and Cu tolerance (Zhigang et al. 2006). When the phytochelatin synthase (AtPCS1) is directed into chloroplasts, it improves Cd stress vulnerability, but it boosts Cd stress resistance when directed to the cytoplasm (Picault et al. 2006).

8.10 Biotechnological Process A perfect phytoremediator might have a great pollutant tolerance, the potential to break down or accumulate contamination at elevated amounts within the biomass, broad root networks, the ability to process significant quantities of water from the soil, and quick growth rates and high biomass levels (Cherian and Oliveira 2005; Nedjimi 2021). As a consequence, traditional plants do not meet the requirements for successful phytoremediation (Gratão et al. 2005). Genetic manipulation and plant transformation technologies can considerably boost plants’ restorative capacity (Krämer 2005). The establishment of enhanced phytoremediators is proven to be a viable technique for introducing innovative features for the absorption as well as bioaccumulation of contaminants into high biomass plants (Martínez et al. 2006). After physiological and biochemical tests have revealed potential rate-limiting stages, the particular membrane transporters or enzymes liable can be identified for overexpression. If the genes encoding these characteristics are found in any organism, they can be introduced into the plant, and transgenics can be compared to wild-type (non-transgenic) plants in terms of pollution remediation (Pilon-Smits and Freeman 2006; Sharma et al. 2022). Human activities including industry, mining, motorised traffic, agriculture, lagging, and military acts encourage inorganic pollution discharge and accumulation in the environment, resulting in toxicity. Metals/metalloids (e.g. As, Cd, Cu, Hg, Mn, Se, Zn), radionuclides (e.g. Cs, P, U), and plant fertilisers are examples of inorganic pollutants (e.g. nitrate, phosphate). Immobilisation (phytostabilisation), confinement in extractable plant bodies (phytoextraction or rhizofiltration), and, in rare situations, phytovolatilisation are some of the inorganic phytoremediation methodologies (Sharma et al. 2022). While evaluating the most effective and appropriate method to successfully treat a contaminated environment, geological attributes of the contaminated location(s), including the type of soil, pollutant complexity as well as type, site location concerning human habitation, and functional properties of each bioremediation strategy, should all be considered (Azubuike et al. 2016). Plant tolerance and accumulation have been the focus of biotechnological techniques that have successfully improved plant capacity for inorganic phytoremediation (Pilon-Smits et al. 1999; Yan et al. 2020). Metal transporter genes, and genes that contribute to the chelator synthesis, are among the genes of the target. Genes that aid in the conversion of elements to volatile forms were also overexpressed in the case of volatile elements (Dhankher et al. 2012). Arsenic species are non-biodegradable and can be found in agricultural soils’ surface and subsurface. AsV, as a phosphate analogue, is absorbed by plants through phosphate absorption mechanisms, according to several

8 Heavy Metal Toxicity and Phytoremediation by the Plants …

251

studies (Abedi and Mojiri 2020; Finnegan and Chen 2012). In Arabidopsis thaliana, the phosphate transporter PHT1;1 has been linked to AsV absorption. AsV also represses genes implicated in the phosphate starvation response, implying that AsV disrupts phosphate sensing and changes the phosphate signalling system. There are nine high-affinity phosphate transporters (PHT) in A. thaliana, each with a different affinity for arsenate. For improved As tolerance and accumulation, several transgenic plants have been developed. Overexpression of genes involved in the manufacture of PCs or their precursor GSH, improved As tolerance greatly but did not improve As tolerance significantly (Catarecha et al. 2007; Młodzi´nska and Zboi´nska 2016; Okumura et al. 1998; Singh et al. 2021b). The first method of manipulating plants genes associated in sulphur/selenium assimilation as well as volatilisation was overexpressed in Se tolerance, build-up, and/or volatilisation. B. juncea plants overexpressing ATP sulphurylase (APS), a selenite-to-selenite conversion enzyme, showed increased selenate reduction, as evidenced by the fact that transgenic APS plants given selenate gathered as an organic type of Se, whereas wild-type plants formed selenate (de Souza et al. 2000; Pilon-Smits et al. 1999; White 2016). The APS transgenic absorbed 2–3 times higher Se as well as 1.5 times additional sulphur compared to wild type. The APS plants survived the absorbed Se well over wild-type plants due to the organic type of Se. In the APS transgenics, the rate of selenium volatilisation was unaffected. When compared to untransformed plants, Indian mustard overexpressing cystathionine gamma synthase (CgS, the first enzyme in the conversion of SeCys to SeMet) demonstrated two to threefold higher volatilisation rates, A. thaliana, for example, is a diverse plant species. Tobacco, yellow poplar, cottonwood, and rice that were genetically modified to express modified merA were resistant to at least 10 times higher levels of Hg (II) than non-transgenic controls (Raina et al. 2021; Rugh et al. 1996; Van Huysen et al. 2003; Zhu et al. 2009). In comparison with controls, these transgenic plants had much higher amounts of Hg (0) volatilisation. The chloroplast and endoplasmic reticulum (ER) has been identified as Hg poisoning targets (Bizily et al. 2003; Ruiz and Daniell 2009). As a result, designing Hg elimination mechanisms into chloroplasts or ER could provide increased levels of Hg tolerance and removal. The merA and merB genes were integrated into the chloroplast genome for Hg detoxification. Transgenic tobacco plants showed significant tolerance to the organomercurial chemical phenylmercuric acetate (PMA) and deposited 100- and four folds more Hg in the shoot when exposed to PMA or HgCl2 , respectively, than untransformed plants (Ponce-Hernández et al. 2022; Ruiz et al. 2003; Singh et al. 2021a). Plant biotechnological methods have undoubtedly played a significant key role in the advancement of phytoremediation. While biotechnology is being utilised to generate transgenic plants with greater potential, effective, clean, economical, and long-lasting bioremediation systems are still needed, and there are a few barriers to overcome.

252

K. Ball et al.

8.11 New Insights and Innovative Technologies for Improving Phytoremediation 8.11.1 Microbial-Assisted Phytoremediation (PGPR) Plant growth-promoting bacteria (PGPB) that can colonise the rhizospheric system and encourage plant growth and mineral nutrition are used in phytoremediation. These microorganisms can break down or transform dangerous substances into less damaging forms (Ullah et al. 2015). Several PGPBs have been shown to improve plant phytoremediation capacity by allowing HMs to be taken up by the roots. Such bacteria are important in HM remediation because they secrete a variety of chemicals, including siderophores (chelators) and organic acids, that increase HM bioavailability by lowering soil pH (Chen et al. 2017). Some PGPR has a significant part in phytoremediation processes in a variety of ways, including (a) increasing plant detoxification rates, (b) increasing enzyme root secretion, which leads to faster pollutant breakdown, and (c) altering soil pH (Liu et al. 2020). As a result, various bacterial strains have been discovered to boost plant HM tolerance.

8.11.2 AMF Inoculation-Assisted Phytoremediation Arbuscular mycorrhizal fungi (AMF) are symbiotic fungi that form a symbiotic relationship with root host plants to increase phosphorus phytoavailability (Zhang et al. 2015). AMF used two strategies to decontaminate HMs: (a) immobilisation of HMs through the synthesis of chelating chemicals as well as adherence to fungal cell walls and (b) phytoextraction of HMs through improved plant growth and increased HMs uptake in the rhizosphere through changing the chemical constitution of root secretion and/or lowering the soil pH (Cabral et al. 2015).

8.11.3 Earthworm-Assisted Phytoremediation The primary category of soil macro-invertebrates is earthworms, also known as “ecosystem engineers”. They are essential for organic matter decomposition, nitrogen cycling, and soil improvement (Sharma et al. 2020). Earthworms help to lower the pH of soil by secreting organic acids like fulvic and humic acids through their gut microflora, which improves nutrition and HM bioavailability in the rhizosphere (Lemtiri et al. 2016; Wang et al. 2020).

8 Heavy Metal Toxicity and Phytoremediation by the Plants …

253

8.11.4 Phytohormone-Assisted Phytoremediation Plant growth regulators (PGR)-assisted phytoremediation is a technique for enhancing HMs accumulation in plant tissues. Phytohormones such as auxins (IAA), cytokinins, gibberellins, and abscisic acid could be advantageous in this approach. Many reports have demonstrated that these phytohormones boost HMs accumulation and plant development and tolerance to HMs in a favourable way. Exogenous phytohormone treatment at the early phases of plant growth has been shown to aid plants in avoiding toxicity while subjected to HMs. For instance, in A. thaliana application of exogenous auxin (0.5 M) is a viable strategy to improve Cd tolerance (Zhu et al. 2013).

8.11.5 Nanoparticles-Assisted Phytoremediation The inclusion of nanoparticles (NPs) is a unique strategy for improving the clearance effectiveness of HMs (Zhu et al. 2019); these particles can boost phytoremediation capability in a variety of ways, including (a) facilitating HMs phytoremediation, (b) plant growth stimulation, or (c) adsorption/redox interactions with HMs (Song et al. 2019). Nanoparticles can assist plants to stabilise HMs by electrostatic adsorption, according to the chemical interaction. The use of exogenous salicylic acid nanoparticles (SANPs) during the early stages of growth can increase Isatis cappadocica belonging to the family Brassicaceae phytoremediation against arsenic (As) (Souri et al. 2017).

8.11.6 Transgenic Approaches Transgenic plants are plants that have been genetically modified (by DNA editing and genome transformation) to incorporate additional genes that do not present naturally in the species to improve HM uptake and translocation (Rai et al. 2020). Overexpression of genes was used to alleviate the stress caused by HMs and improve plants’ phytoremediation abilities (Liu et al. 2020).

8.12 Future Prospects Phytoremediation is among the most effective strategies for the eco-rehabilitation of polluted places. However, more research and analysis are needed to improve our understanding of effective phytoremediation of HMs. To avoid failure during field

254

K. Ball et al.

cultures, it has become crucial to look for new ways to elucidate processes, metabolites, and genes employing omic methods. These techniques can help to identify new metabolites and pathways involved in the extraction of HMs by hyper-accumulator plants. Through overexpressing foreign genes in non-tolerant plants, it is feasible to remediate soil contaminated with HMs. Although numerous plants and shrubs have been genetically modified to clean up HMs, no perfect model for HMs detoxification can be built until the availability of whole-genome data is confirmed. Urgent research into the impact of plant hormones such as IAA, GA and cytokine in increasing the potential of HMs detoxification plants is also required. Plant–microorganism interaction (bacteria, fungi) was also found to be a successful method for HM absorption as well as transport in plants. These methods can aid in the discovery of novel metabolites and pathways that contribute to the degradation of pollutants via plant–microbe interactions (Mishra and Arora 2019). The analysis of the hologenome of microorganisms is another advanced technology that could be used to manipulate microbial niches to boost resistance to HMs contamination (Mueller and Sachs 2015). Nanoremediation is a new technology that uses the integration of microbial cells to make the reclamation system further effective at eliminating HMs from heavily polluted soils (Song et al. 2019; Zhu et al. 2019). To improve the chances of polluted soil remediation, the relationship between phytoremediation molecular techniques and nanoparticles must be clarified.

8.13 Conclusion Due to increased industrialisation, population growth, and agricultural practices, xenobiotics are becoming more prevalent in the earth’s biosphere. To ensure the longterm viability of natural ecosystems, rapid and effective environmental clean-up of contaminants is indispensable. Several plant species can tolerate toxic HMs along with normal growth and development. Plant species with high absorption capacity are ideal for restoring damaged soils and ecosystems. Therefore, phytoremediation is an efficient strategy for cleaning toxic and polluted environments. There are several species of plants belonging to the Brassicaceae family which can hyper-accumulate toxic heavy metals. At present, approximately 25% of members of this family, which includes about 90 species, have already been found globally and are showing to be prospective contenders for efficient phytoremediation. Despite phytoremediation with metal hyper-accumulators being an inexpensive and environmentally benign alternate to chemical remediation procedures, it has its drawbacks.

8 Heavy Metal Toxicity and Phytoremediation by the Plants …

255

References Abdullahi M (2015) Soil contamination, remediation and plants: prospects and challenges. In: Khalid RH, Muhammad S, Munir O, Ahmet RM (eds) Soil remediation and plants, 525 Abedi T, Mojiri A (2020) Arsenic uptake and accumulation mechanisms in rice species. Plants 9(2):129 Ahmad A, Shahzadi I, Mubeen S, Yasin NA, Akram W, Khan WU, Wu T (2021) Karrikinolide alleviates BDE-28, heat and Cd stressors in Brassica alboglabra by correlating and modulating biochemical attributes, antioxidative machinery and osmoregulators. Ecotoxicol Environ Saf 213:112047 Ahmad P, Sarwat M, Bhat NA, Wani MR, Kazi AG, Tran L-SP (2015) Alleviation of cadmium toxicity in Brassica juncea L.(Czern. & Coss.) by calcium application involves various physiological and biochemical strategies. PloS One 10(1):e0114571 Ali B, Gill RA, Yang S, Gill MB, Farooq MA, Liu D, …, Zhou W (2015) Regulation of cadmiuminduced proteomic and metabolic changes by 5-aminolevulinic acid in leaves of Brassica napus L. PLoS ONE 10(4):e0123328 Ali H, Khan E, Sajad MA (2013) Phytoremediation of heavy metals—concepts and applications. Chemosphere 91(7):869–881 Ali S, Shahid MJ, Hussain A, Rizwan M, Ahmad A, Adrees M (2021) Metals phytoextraction by Brassica species. In: Approaches to the remediation of inorganic pollutants, pp 361–384 Alloway BJ (2013) Sources of heavy metals and metalloids in soils. In: Heavy metals in soils. Springer, pp 11–50 Alscher RG, Erturk N, Heath LS (2002) Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J Exp Bot 53(372):1331–1341 Anderson TA, Guthrie EA, Walton BT (1993) Bioremediation in the rhizosphere. Environ Sci Technol 27(13):2630–2636 Angulo-Bejarano PI, Puente-Rivera J, Cruz-Ortega R (2021) Metal and metalloid toxicity in plants: an overview on molecular aspects. Plants 10(4):635 Arif N, Yadav V, Singh S, Singh S, Ahmad P, Mishra RK, …, Chauhan DK (2016) Influence of high and low levels of plant-beneficial heavy metal ions on plant growth and development. Front Environ Sci 4:69 Armas T, Pinto AP, de Varennes A, Mourato MP, Martins LL, Gonçalves MLS, Mota AM (2015) Comparison of cadmium-induced oxidative stress in Brassica juncea in soil and hydroponic cultures. Plant Soil 388(1):297–305 Ashraf S, Ali Q, Zahir ZA, Ashraf S, Asghar HN (2019) Phytoremediation: environmentally sustainable way for reclamation of heavy metal polluted soils. Ecotoxicol Environ Saf 174:714–727 Azubuike CC, Chikere CB, Okpokwasili GC (2016) Bioremediation techniques–classification based on site of application: principles, advantages, limitations and prospects. World J Microbiol Biotechnol 32(11):1–18 Baker A, McGrath S, Sidoli C, Reeves R (1994) The possibility of in situ heavy metal decontamination of polluted soils using crops of metal-accumulating plants. Resour Conserv Recycl 11(1–4):41–49 Baker AJ, McGrath S, Reeves RD, Smith J (2020) Metal hyperaccumulator plants: a review of the ecology and physiology of a biological resource for phytoremediation of metal-polluted soils. In: Phytoremediation of contaminated soil and water, pp 85–107 Barrameda-Medina Y, Montesinos-Pereira D, Romero L, Ruiz JM, Blasco B (2014) Comparative study of the toxic effect of Zn in Lactuca sativa and Brassica oleracea plants: I. Growth, distribution, and accumulation of Zn, and metabolism of carboxylates. Environ Exp Bot 107:98–104 Baryla A, Carrier P, Franck F, Coulomb C, Sahut C, Havaux M (2001) Leaf chlorosis in oilseed rape plants (Brassica napus) grown on cadmium-polluted soil: causes and consequences for photosynthesis and growth. Planta 212(5):696–709

256

K. Ball et al.

Bernard F, Brulle F, Dumez S, Lemiere S, Platel A, Nesslany F, …, Vandenbulcke F (2015)Antioxidant responses of Annelids, Brassicaceae and Fabaceae to pollutants: a review.Ecotoxicol Environ Saf 114:273–303 Bizily SP, Kim T, Kandasamy MK, Meagher RB (2003) Subcellular targeting of methylmercury lyase enhances its specific activity for organic mercury detoxification in plants. Plant Physiol 131(2):463–471 Blasco B, Graham NS, Broadley MR (2015) Antioxidant response and carboxylate metabolism in Brassica rapa exposed to different external Zn, Ca, and Mg supply. J Plant Physiol 176:16–24 Bolan NS, Park JH, Robinson B, Naidu R, Huh KY (2011) Phytostabilization: a green approach to contaminant containment. Adv Agron 112:145–204 Bosiacki M, Kleiber T, Markiewicz B (2014) Continuous and induced phytoextraction—plant-based methods to remove heavy metals from contaminated soil. In: Environmental risk assessment of soil contamination. IntechOpen Boye K (2002) Phytoextraction of Cu, Pb and Zn: a greenhouse study. Sveriges lantbruksuniv Broadley MR, White PJ, Hammond JP, Zelko I, Lux A (2007) Zinc in plants. New Phytol 173(4):677–702 Broadley MR, Willey NJ, Wilkins JC, Baker AJ, Mead A, White PJ (2001) Phylogenetic variation in heavy metal accumulation in angiosperms. New Phytol 152(1):9–27 Brooks RR, Lee J, Reeves RD, Jaffré T (1977) Detection of nickeliferous rocks by analysis of herbarium specimens of indicator plants. J Geochem Explor 7:49–57 Cabral L, Soares CRFS, Giachini AJ, Siqueira JO (2015) Arbuscular mycorrhizal fungi in phytoremediation of contaminated areas by trace elements: mechanisms and major benefits of their applications. World J Microbiol Biotechnol 31(11):1655–1664 Carrió-Seguí À, Romero P, Curie C, Mari S, Peñarrubia L (2019) Copper transporter COPT5 participates in the crosstalk between vacuolar copper and iron pools mobilisation. Sci Rep 9(1):1– 14 Catarecha P, Segura MD, Franco-Zorrilla JM, García-Ponce B, Lanza M, Solano R, …, Leyva A (2007) A mutant of the Arabidopsis phosphate transporter PHT1; 1 displays enhanced arsenic accumulation. Plant Cell 19(3):1123–1133 Cempel M, Nikel G (2006) Nickel: a review of its sources and environmental toxicology. Pol J Environ Stud 15(3) Chen Y, Yang W, Chao Y. Wang S, Tang Y-T, Qiu R-L (2017) Metal-tolerant Enterobacter sp. strain EG16 enhanced phytoremediation using Hibiscus cannabinus via siderophore-mediated plant growth promotion under metal contamination. Plant Soil 413(1–2):203–216 Cherian S, Oliveira MM (2005) Transgenic plants in phytoremediation: recent advances and new possibilities. Environ Sci Technol 39(24):9377–9390 Clemens S (2001) Molecular mechanisms of plant metal tolerance and homeostasis. Planta 212(4):475–486 Clemens S (2006) Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie 88(11):1707–1719 Cointry V, Vert G (2019) The bifunctional transporter-receptor IRT 1 at the heart of metal sensing and signalling. New Phytol 223(3):1173–1178 Cunningham SD, Ow DW (1996) Promises and prospects of phytoremediation. Plant Physiol 110(3):715 Cuypers A, Plusquin M, Remans T, Jozefczak M, Keunen E, Gielen H, …, Artois TJ (2010) Cadmium stress: an oxidative challenge. Biometals 23(5):927–940 DalCorso G, Fasani E, Manara A, Visioli G, Furini A (2019) Heavy metal pollutions: state of the art and innovation in phytoremediation. Int J Mol Sci 20(14):3412 Dar MI, Khan FA, Rehman F, Masoodi A, Ansari AA, Varshney D, …, Naikoo MI (2015) Roles of Brassicaceae in phytoremediation of metals and metalloids. Phytoremediation 201–215 de Souza MP, Lytle CM, Mulholland MM, Otte ML, Terry N (2000) Selenium assimilation and volatilization from dimethylselenoniopropionate by Indian mustard. Plant Physiol 122(4):1281– 1288. https://doi.org/10.1104/pp.122.4.1281

8 Heavy Metal Toxicity and Phytoremediation by the Plants …

257

Dhankher OP, Pilon-Smits EA, Meagher RB, Doty S (2012) Biotechnological approaches for phytoremediation. In: Plant biotechnology and agriculture. Elsevier, pp 309–328 Dushenkov V, Kumar PN, Motto H, Raskin I (1995) Rhizofiltration: the use of plants to remove heavy metals from aqueous streams. Environ Sci Technol 29(5):1239–1245 Dutta S, Mitra M, Agarwal P, Mahapatra K, De S, Sett U, Roy S (2018) Oxidative and genotoxic damages in plants in response to heavy metal stress and maintenance of genome stability. Plant Signal Behav 13(8):e1460048 Ebbs SD, Kochian LV (1997) Toxicity of zinc and copper to Brassica species: implications for phytoremediation (0047-2425) Eisenhut M, Hoecker N, Schmidt SB, Basgaran RM, Flachbart S, Jahns P, …, Weber AP (2018) The plastid envelope chloroplast Manganese transporter1 is essential for manganese homeostasis in Arabidopsis. Mol Plant 11(7):955–969 Emamverdian A, Ding Y, Mokhberdoran F, Xie Y (2015) Heavy metal stress and some mechanisms of plant defense response. Sci World J 2015:756120. https://doi.org/10.1155/2015/756120 Erakhrumen AA, Agbontalor A (2007) Phytoremediation: an environmentally sound technology for pollution prevention, control and remediation in developing countries. Educ Res Rev 2(7):151– 156 Fasani E, Manara A, Martini F, Furini A, DalCorso G (2018) The potential of genetic engineering of plants for the remediation of soils contaminated with heavy metals. Plant Cell Environ 41(5):1201–1232 Feigl G, Kumar D, Lehotai N, Tugyi N, Molnár Á, Ördög A, …, Erdei L (2013) Physiological and morphological responses of the root system of Indian mustard (Brassica juncea L. Czern.) and rapeseed (Brassica napus L.) to copper stress. Ecotoxicol Environ Saf 94179–189 Finnegan P, Chen W (2012) Arsenic toxicity: the effects on plant metabolism. Front Physiol 3:182 Fryzova R, Pohanka M, Martinkova P, Cihlarova H, Brtnicky M, Hladky J, Kynicky J (2017) Oxidative stress and heavy metals in plants. Rev Environ Contam Toxicol 245:129–156 Fu S, Lu Y, Zhang X, Yang G, Chao D, Wang Z, …, Li R (2019) The ABC transporter ABCG36 is required for cadmium tolerance in rice. J Exp Bot 70(20):5909–5918 Gerhardt KE, Gerwing PD, Greenberg BM (2017) Opinion: taking phytoremediation from proven technology to accepted practice. Plant Sci 256:170–185 Ghasemi R, Ghaderian SM, Krämer U (2009) Accumulation of nickel in trichomes of a nickel hyperaccumulator plant Alyssum Inflatum. Northeast Nat 16(sp5):81–92 Ghnaya AB, Charles G, Hourmant A, Hamida JB, Branchard M (2009) Physiological behaviour of four rapeseed cultivar (Brassica napus L.) submitted to metal stress. C R Biol 332(4):363–370 Gratão PL, Prasad MNV, Cardoso PF, Lea PJ, Azevedo RA (2005) Phytoremediation: green technology for the clean up of toxic metals in the environment. Braz J Plant Physiol 17(1):53–64 Gu D, Zhou X, Ma Y, Xu E, Yu Y, Liu Y, …, Zhang W (2021) Expression of a Brassica napus metal transport protein (BnMTP3) in Arabidopsis thaliana confers tolerance to Zn and Mn. Plant Sci 304:110754 Haider FU, Liqun C, Coulter JA, Cheema SA, Wu J, Zhang R, …, Farooq M (2021) Cadmium toxicity in plants: impacts and remediation strategies. Ecotoxicol Environ Saf 211:111887 Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53(366):1–11 Hamzah A, Hapsari RI, Wisnubroto EI (2016) Phytoremediation of cadmium-contaminated agricultural land using indigenous plants. Int J Environ Agric Res 2(1):8–14 Hasan M, Uddin M, Ara-Sharmeen I, Alharby HF, Alzahrani Y, Hakeem KR, Zhang L (2019)Assisting phytoremediation of heavy metals using chemical amendments.Plants 8(9):295 Hasanuzzaman M, Bhuyan M, Zulfiqar F, Raza A, Mohsin SM, Mahmud JA, …, Fotopoulos V (2020) Reactive oxygen species and antioxidant defense in plants under abiotic stress: revisiting the crucial role of a universal defense regulator. Antioxidants 9(8):681 Huang Y, Chen J, Zhang D, Fang B, YangJin T, Zou J, …, Cui J (2021) Enhanced vacuole compartmentalization of cadmium in root cells contributes to glutathione-induced reduction of cadmium

258

K. Ball et al.

translocation from roots to shoots in pakchoi (Brassica chinensis L.). Ecotoxicol Environ Saf 208:111616 Iqbal M, Iqbal N, Bhatti IA, Ahmad N, Zahid M (2016) Response surface methodology application in optimization of cadmium adsorption by shoe waste: a good option of waste mitigation by waste. Ecol Eng 88:265–275 Jaishankar M, Tseten T, Anbalagan N, Mathew BB, Beeregowda KN (2014) Toxicity, mechanism and health effects of some heavy metals. Interdiscip Toxicol 7(2):60 Ji R, Zhou L, Liu J, Wang Y, Yang L, Zheng Q, …, Yang Y (2017) Calcium-dependent protein kinase CPK31 interacts with arsenic transporter AtNIP1; 1 and regulates arsenite uptake in Arabidopsis thaliana. PLoS ONE 12(3):e0173681 Jogawat A, Yadav B, Narayan OP (2021) Metal transporters in organelles and their roles in heavy metal transportation and sequestration mechanisms in plants. Physiol Plant John R, Ahmad P, Gadgil K, Sharma S (2009) Cadmium and lead-induced changes in lipid peroxidation, antioxidative enzymes and metal accumulation in Brassica juncea L. at three different growth stages. Arch Agron Soil Sci 55(4):395–405 Jonak C, Nakagami H, Hirt H (2004) Heavy metal stress. Activation of distinct mitogen-activated protein kinase pathways by copper and cadmium. Plant Physiol 136(2):3276–3283 Kaur D, Singh A, Kumar A, Gupta S (2020) Genetic engineering approaches and applicability for the bioremediation of metalloids. In: Plant life under changing environment. Elsevier, pp 207–235 Kaur R, Bhardwaj R, Thukral AK, Narang U (2011) Interactive effects of binary combinations of manganese with other heavy metals on metal uptake and antioxidative enzymes in Brassica juncea L. seedlings. J Plant Interact 6(1):25–34 Kaur R, Sharma S, Kaur H (2019) Heavy metals toxicity and the environment. J Pharmacognosy Phytochem SP1:247–249 Kim DY, Bovet L, Maeshima M, Martinoia E, Lee Y (2007) The ABC transporter AtPDR8 is a cadmium extrusion pump conferring heavy metal resistance. Plant J 50(2):207–218 Kim LJ, Tsuyuki KM, Hu F, Park EY, Zhang J, Iraheta JG, …, Clyne M (2021) Ferroportin 3 is a dualtargeted mitochondrial/chloroplast iron exporter necessary for iron homeostasis in Arabidopsis. Plant J 107(1):215–236 Krämer U (2005) Phytoremediation: novel approaches to cleaning up polluted soils. Curr Opin Biotechnol 16(2):133–141. https://doi.org/10.1016/j.copbio.2005.02.006 Krämer U (2010) Metal hyperaccumulation in plants. Annu Rev Plant Biol 61:517–534 Kramer U, Pickering IJ, Prince RC, Raskin I, Salt DE (2000) Subcellular localization and speciation of nickel in hyperaccumulator and non-accumulator Thlaspi species. Plant Physiol 122(4):1343– 1354 Kramer U, Smith RD, Wenzel WW, Raskin I, Salt DE (1997) The role of metal transport and tolerance in nickel hyperaccumulation by Thlaspi goesingense Halacsy. Plant Physiol 115(4):1641–1650 Kumar PN, Dushenkov V, Motto H, Raskin I (1995) Phytoextraction: the use of plants to remove heavy metals from soils. Environ Sci Technol 29(5):1232–1238 Kumar S, Dubey RS, Tripathi RD, Chakrabarty D, Trivedi PK (2015) Omics and biotechnology of arsenic stress and detoxification in plants: current updates and prospective. Environ Int 74:221– 230 Kumar S, Trivedi PK (2016) Heavy metal stress signaling in plants. In: Plant metal interaction. Elsevier, pp 585–603 Kupper H, Jie Zhao F, McGrath SP (1999) Cellular compartmentation of zinc in leaves of the hyperaccumulator Thlaspi caerulescens. Plant Physiol 119(1):305–312 Laboratory NRMR (2000) Introduction to phytoremediation. National Risk Management Research Laboratory, Office of Research and Development Lallement P-A, Roret T, Tsan P, Gualberto JM, Girardet J-M, Didierjean C, …, Hecker A (2016) Insights into ascorbate regeneration in plants: investigating the redox and structural properties of dehydroascorbate reductases from Populus trichocarpa. Biochem J 473(6):717–731

8 Heavy Metal Toxicity and Phytoremediation by the Plants …

259

Lee BXY, Hadibarata T, Yuniarto A (2020) Phytoremediation mechanisms in air pollution control: a review. Water Air Soil Pollut 231(8):1–13 Lemtiri A, Liénard A, Alabi T, Brostaux Y, Cluzeau D, Francis F, Colinet G (2016) Earthworms Eisenia fetida affect the uptake of heavy metals by plants Vicia faba and Zea mays in metalcontaminated soils. Appl Soil Ecol 104:67–78 Li J, Chang Y, Al-Huqail AA, Ding Z, Al-Harbi MS, Ali EF, …, Ghoneim AM (2021) Effect of manure and compost on the phytostabilization potential of heavy metals by the halophytic plant wavy-leaved saltbush. Plants 10(10):2176 Li J, Wang Y, Zheng L, Li Y, Zhou X, Li J, …, Chen X (2019) The intracellular transporter AtNRAMP6 is involved in Fe homeostasis in Arabidopsis. Front Plant Sci 10:1124 Li W, Lacey RF, Ye Y, Lu J, Yeh K-C, Xiao Y, …, Zhao Y (2017) Triplin, a small molecule, reveals copper ion transport in ethylene signaling from ATX1 to RAN1. PLoS Genet 13(4):e1006703 Limmer M, Burken J (2016) Phytovolatilization of organic contaminants. Environ Sci Technol 50(13):6632–6643 Liu J, Wang J, Lee S, Wen R (2018) Copper-caused oxidative stress triggers the activation of antioxidant enzymes via ZmMPK3 in maize leaves. PLoS ONE 13(9):e0203612 Liu S, Yang B, Liang Y, Xiao Y, Fang J (2020) Prospect of phytoremediation combined with other approaches for remediation of heavy metal-polluted soils. Environ Sci Pollut Res 27(14):16069– 16085 Liu XS, Feng SJ, Zhang BQ, Wang MQ, Cao HW, Rono JK, …, Yang ZM (2019) OsZIP1 functions as a metal efflux transporter limiting excess zinc, copper and cadmium accumulation in rice. BMC Plant Biol 19(1):1–16 Luo J-S, Zhang Z (2021) Mechanisms of cadmium phytoremediation and detoxification in plants. Crop J Ma J, Yamaji N (2008) Functions and transport of silicon in plants. Cell Mol Life Sci 65(19):3049– 3057 Ma Y, Oliveira RS, Freitas H, Zhang C (2016) Biochemical and molecular mechanisms of plantmicrobe-metal interactions: relevance for phytoremediation. Front Plant Sci 7:918 Martínez M, Bernal P, Almela C, Vélez D, García-Agustín P, Serrano R, Navarro-Aviñó J (2006) An engineered plant that accumulates higher levels of heavy metals than Thlaspi caerulescens, with yields of 100 times more biomass in mine soils. Chemosphere 64(3):478–485 Małecka A, Konkolewska A, Han´c A, Barałkiewicz D, Ciszewska L, Ratajczak E, …, Jarmuszkiewicz W (2019) Insight into the phytoremediation capability of Brassica juncea (v. Malopolska): metal accumulation and antioxidant enzyme activity. Int J Mol Sci 20(18) McGrath SP, Zhao F-J (2003) Phytoextraction of metals and metalloids from contaminated soils. Curr Opin Biotechnol 14(3):277–282 Mellem JJ, Baijnath H, Odhav B (2012) Bioaccumulation of Cr, Hg, As, Pb, Cu and Ni with the ability for hyperaccumulation by Amaranthus dubius. Afr J Agric Res 7(4):591–596 Meng JG, Zhang XD, Tan SK, Zhao KX, Yang ZM (2017) Genome-wide identification of Cdresponsive NRAMP transporter genes and analyzing expression of NRAMP 1 mediated by miR167 in Brassica napus. Biometals 30(6):917–931 Minglin L, Yuxiu Z, Tuanyao C (2005) Identification of genes up-regulated in response to Cd exposure in Brassica juncea L. Gene 363:151–158 Mishra I, Arora NK (2019) Rhizoremediation: a sustainable approach to improve the quality and productivity of polluted soils. In: Phyto and rhizo remediation. Springer, pp 33–66 Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7(9):405–410 Mobin M, Khan NA (2007) Photosynthetic activity, pigment composition and antioxidative response of two mustard (Brassica juncea) cultivars differing in photosynthetic capacity subjected to cadmium stress. J Plant Physiol 164(5):601–610 Morikawa H, Erkin ÖC (2003) Basic processes in phytoremediation and some applications to air pollution control. Chemosphere 52(9):1553–1558 Morrissey J, Guerinot ML (2009) Iron uptake and transport in plants: the good, the bad, and the ionome. Chem Rev 109(10):4553–4567. https://doi.org/10.1021/cr900112r

260

K. Ball et al.

Mourato M, Reis R, Martins LL (2012) Characterization of plant antioxidative system in response to abiotic stresses: a focus on heavy metal toxicity. Adv Sel Plant Physiol Aspects 12:1–17 Mourato MP, Moreira IN, Leitão I, Pinto FR, Sales JR, Martins LL (2015) Effect of Heavy Metals in Plants of the Genus Brassica. Int J Mol Sci 16(8):17975–17998. https://doi.org/10.3390/ijm s160817975 Mueller UG, Sachs JL (2015) Engineering microbiomes to improve plant and animal health. Trends Microbiol 23(10):606–617 Muradoglu F, Gundogdu M, Ercisli S, Encu T, Balta F, Jaafar HZ, Zia-Ul-Haq M (2015) Cadmium toxicity affects chlorophyll a and b content, antioxidant enzyme activities and mineral nutrient accumulation in strawberry. Biol Res 48:1–7 Młodzi´nska E, Zboi´nska M (2016) Phosphate uptake and allocation—a closer look at Arabidopsis thaliana L. and Oryza sativa L. Front Plant Sci 7:1198 Nagajyoti PC, Lee KD, Sreekanth T (2010) Heavy metals, occurrence and toxicity for plants: a review. Environ Chem Lett 8(3):199–216 Narayan OP, Verma N, Jogawat A, Dua M, Johri AK (2020) Role of sulphate transporter (PiSulT) of endophytic fungus Serendipita indica in plant growth and development. BioRxiv Nazir F, Fariduddin Q, Khan TA (2020) Hydrogen peroxide as a signalling molecule in plants and its crosstalk with other plant growth regulators under heavy metal stress. Chemosphere 252:126486 Nedjimi B (2021) Phytoremediation: a sustainable environmental technology for heavy metals decontamination. SN Appl Sci 3(3):1–19 Neff J, Lee K, DeBlois EM (2011) Produced water: overview of composition, fates, and effects. Produced Water 3–54 Nigam S, Sinha S (2021) Phytoremediation: an eco-friendly and sustainable approach for the removal of toxic heavy metals. In: Removal of refractory pollutants from wastewater treatment plants. CRC Press, pp 417–432 Nishida S, Tanikawa R, Ishida S, Yoshida J, Mizuno T, Nakanishi H, Furuta N (2020) Elevated expression of vacuolar nickel transporter gene IREG2 is associated with reduced root-to-shoot nickel translocation in Noccaea japonica. Front Plant Sci 11:610 Nouairi I, Ammar WB, Youssef NB, Daoud DBM, Ghorbal MH, Zarrouk M (2006) Comparative study of cadmium effects on membrane lipid composition of Brassica juncea and Brassica napus leaves. Plant Sci 170(3):511–519 Nouairi I, Ammar WB, Youssef NB, Miled DDB, Ghorbal MH, Zarrouk M (2009) Antioxidant defense system in leaves of Indian mustard (Brassica juncea) and rape (Brassica napus) under cadmium stress. Acta Physiol Plant 31(2):237–247 Okumura S, Mitsukawa N, Shirano Y, Shibata D (1998) Phosphate transporter gene family of Arabidopsis thaliana. DNA Res 5(5):261–269 Opdenakker K, Remans T, Vangronsveld J, Cuypers A (2012) Mitogen-activated protein (MAP) kinases in plant metal stress: regulation and responses in comparison to other biotic and abiotic stresses. Int J Mol Sci 13(6):7828–7853. https://doi.org/10.3390/ijms13067828 O’Lexy R, Kasai K, Clark N, Fujiwara T, Sozzani R, Gallagher KL (2018) Exposure to heavy metal stress triggers changes in plasmodesmatal permeability via deposition and breakdown of callose. J Exp Bot 69(15):3715–3728 Palmer CE, Warwick S, Keller W (2001) Brassicaceae (Cruciferae) family, plant biotechnology, and phytoremediation. Int J Phytorem 3(3):245–287 Picault N, Cazalé A, Beyly A, Cuiné S, Carrier P, Luu D, …, Peltier G (2006) Chloroplast targeting of phytochelatin synthase in Arabidopsis: effects on heavy metal tolerance and accumulation. Biochimie 88(11):1743–1750 Pich A, Scholz G (1996) Translocation of copper and other micronutrients in tomato plants (Lycopersicon esculentum Mill.): nicotianamine-stimulated copper transport in the xylem. J Exp Bot 47(1):41–47 Pichtel J (2016) Oil and gas production wastewater: soil contamination and pollution prevention. Appl Environ Soil Sci 2016

8 Heavy Metal Toxicity and Phytoremediation by the Plants …

261

Pilon-Smits EA, Freeman JL (2006) Environmental cleanup using plants: biotechnological advances and ecological considerations. Front Ecol Environ 4(4):203–210 Pilon-Smits EA, Hwang S, Mel Lytle C, Zhu Y, Tai JC, Bravo RC, …, Terry N (1999) Overexpression of ATP sulfurylase in Indian mustard leads to increased selenate uptake, reduction, and tolerance. Plant Physiol 119(1):123–132. https://doi.org/10.1104/pp.119.1.123 Pilon-Smits EA, LeDuc DL (2009) Phytoremediation of selenium using transgenic plants. Curr Opin Biotechnol 20(2):207–212 Pivetz BE (2001) Phytoremediation of contaminated soil and ground water at hazardous waste sites. US Environmental Protection Agency, Office of Research and Development Podar D, Ramsey MH, Hutchings MJ (2004) Effect of cadmium, zinc and substrate heterogeneity on yield, shoot metal concentration and metal uptake by Brassica juncea: implications for human health risk assessment and phytoremediation. New Phytol 163(2):313–324 Polle A, Schützendübel A (2003) Heavy metal signalling in plants: linking cellular and organismic responses. In: Plant responses to abiotic stress. Springer, pp 187–215 Ponce-Hernández A, Alonso-Castro AJ, García-De La Cruz RF, Carranza-Alvarez C (2022) Engineering plants for metal tolerance and accumulation. In: Phytoremediation. Elsevier, pp 455–480 Potters G, De Gara L, Asard H, Horemans N (2002) Ascorbate and glutathione: guardians of the cell cycle, partners in crime? Plant Physiol Biochem 40(6–8):537–548 Rafique N, Tariq SR (2016) Distribution and source apportionment studies of heavy metals in soil of cotton/wheat fields. Environ Monit Assess 188(5):309 Rai PK, Kim K-H, Lee SS, Lee J-H (2020) Molecular mechanisms in phytoremediation of environmental contaminants and prospects of engineered transgenic plants/microbes. Sci Total Environ 705:135858 Rai PK, Lee SS, Zhang M, Tsang YF, Kim K-H (2019) Heavy metals in food crops: health risks, fate, mechanisms, and management. Environ Int 125:365–385 Raina M, Sharma A, Nazir M, Kumari P, Rustagi A, Hami A, …, Kumar D (2021)Exploring the new dimensions of selenium research to understand the underlying mechanism of its uptake, translocation, and accumulation. Physiol Plant 171(4):882–895 Rajendran S, Priya T, Khoo KS, Hoang TK, Ng H-S, Munawaroh HSH, …, Show PL (2022) A critical review on various remediation approaches for heavy metal contaminants removal from contaminated soils. Chemosphere 287:132369 Raskin I, Ensley B (2000) Recent developments for in situ treatment of metal contaminated soils. In: Phytoremediation of toxic metals: using plants to clean up the environment. John Wiley & Sons Inc., New York. Available at: http//clu-n.org/techfocus Rugh CL, Wilde HD, Stack NM, Thompson DM, Summers AO, Meagher RB (1996) Mercuric ion reduction and resistance in transgenic Arabidopsis thaliana plants expressing a modified bacterial merA gene. Proc Natl Acad Sci 93(8):3182–3187 Ruiz ON, Daniell H (2009) Genetic engineering to enhance mercury phytoremediation. Curr Opin Biotechnol 20(2):213–219. https://doi.org/10.1016/j.copbio.2009.02.010 Ruiz ON, Hussein HS, Terry N, Daniell H (2003) Phytoremediation of organomercurial compounds via chloroplast genetic engineering. Plant Physiol 132(3):1344–1352 Salt DE, Prince RC, Pickering IJ, Raskin I (1995) Mechanisms of cadmium mobility and accumulation in Indian mustard. Plant Physiol 109(4):1427–1433 Sarma H (2011) Metal hyperaccumulation in plants: a review focusing on phytoremediation technology. J Environ Sci Technol 4(2):118–138 Sarwar N, Malhi SS, Zia MH, Naeem A, Bibi S, Farid G (2010) Role of mineral nutrition in minimizing cadmium accumulation by plants. J Sci Food Agric 90(6):925–937 Seth CS, Chaturvedi PK, Misra V (2008) The role of phytochelatins and antioxidants in tolerance to Cd accumulation in Brassica juncea L. Ecotoxicol Environ Saf 71(1):76–85 Shakoor MB, Ali S, Hameed A, Farid M, Hussain S, Yasmeen T, …, Abbasi GH (2014) Citric acid improves lead (Pb) phytoextraction in Brassica napus L. by mitigating Pb-induced morphological and biochemical damages. Ecotoxicol Environ Saf 109:38–47

262

K. Ball et al.

Sharma P, Bakshi P, Kour J, Singh AD, Dhiman S, Kumar P, …, Bhardwaj R (2020) PGPR and earthworm-assisted phytoremediation of heavy metals. In: Earthworm assisted remediation of effluents and wastes. Springer, pp 227–245 Sharma P, Jha A, Bauddh K, Korstad J, Dubey R (2021) Efficient utilization of plant biomass after harvesting the phytoremediator plants. In: Phytorestoration of abandoned mining and oil drilling sites. Elsevier, pp 57–84 Sharma R, Kumar R, Hajam YA, Rani R (2022) Role of biotechnology in phytoremediation. In: Phytoremediation. Elsevier, pp 437–454 Sheoran V, Sheoran A, Poonia P (2010) Role of hyperaccumulators in phytoextraction of metals from contaminated mining sites: a review. Crit Rev Environ Sci Technol 41(2):168–214 Sidhu GS (2016) Heavy metal toxicity in soils: sources, remediation technologies and challenges. Adv Plants Agric Res 5(1):445–446 Sikka R, Nayyar V (2012) Cadmium accumulation and its effects on uptake of micronutrients in Indian mustard [Brassica juncea (L.) czern.] grown in a loamy sand soil artificially contaminated with cadmium. Commun Soil Sci Plant Anal 43(4):672–688 Singh K, Sharmila P, Kumar PA, Pardha-Saradhi P (2021a) Successful expression of the synthetic merBps gene in tobacco. Plant Physiol Biochem 167:874–883 Singh R, Misra AN, Sharma P (2021b). Safe, efficient, and economically beneficial remediation of arsenic-contaminated soil: possible strategies for increasing arsenic tolerance and accumulation in non-edible economically important native plants. Environ Sci Pollut Res 1–17 Singh S, Parihar P, Singh R, Singh VP, Prasad SM (2016) Heavy metal tolerance in plants: role of transcriptomics, proteomics, metabolomics, and ionomics. Front Plant Sci 6:1143 Smart K, Kilburn M, Salter C, Smith J, Grovenor C (2007) NanoSIMS and EPMA analysis of nickel localisation in leaves of the hyperaccumulator plant Alyssum lesbiacum. Int J Mass Spectrom 260(2–3):107–114 Song B, Xu P, Chen M, Tang W, Zeng G, Gong J, …, Ye S (2019) Using nanomaterials to facilitate the phytoremediation of contaminated soil. Crit Rev Environ Sci Technol 49(9):791–824 Souri Z, Karimi N, Sarmadi M, Rostami E (2017) Salicylic acid nanoparticles (SANPs) improve growth and phytoremediation efficiency of Isatis cappadocica Desv., under As stress. IET Nanobiotechnol 11(6):650–655 Spielmann J, Ahmadi H, Scheepers M, Weber M, Nitsche S, Carnol M, …, Clemens S (2020) The two copies of the zinc and cadmium ZIP6 transporter of Arabidopsis halleri have distinct effects on cadmium tolerance. Plant Cell Environ 43(9): 2143–2157 Srivastava S, Anand V, Singh P, Roy A, Pallavi S, Bist V, …, Srivastava S (2021) Microbial systems as a source of novel genes for enhanced phytoremediation of contaminated soils. In: Microbe mediated remediation of environmental contaminants, pp 177–198 Suman J, Uhlik O, Viktorova J, Macek T (2018) Phytoextraction of heavy metals: a promising tool for clean-up of polluted environment? Front Plant Sci 9:1476 Tangahu BV, Sheikh Abdullah SR, Basri H, Idris M, Anuar N, Mukhlisin M (2011) A review on heavy metals (As, Pb, and Hg) uptake by plants through phytoremediation. Int J Chem Eng 2011 Tchounwou PB, Yedjou CG, Patlolla AK, Sutton DJ (2012) Heavy metal toxicity and the environment. Exp Suppl 101:133–164. https://doi.org/10.1007/978-3-7643-8340-4_6 Tian S, Liang S, Qiao K, Wang F, Zhang Y, Chai T (2019) Co-expression of multiple heavy metal transporters changes the translocation, accumulation, and potential oxidative stress of Cd and Zn in rice (Oryza sativa). J Hazard Mater 380:120853 Ullah A, Heng S, Munis MFH, Fahad S, Yang X (2015) Phytoremediation of heavy metals assisted by plant growth promoting (PGP) bacteria: a review. Environ Exp Bot 117:28–40 ur Rehman MZ, Rizwan M, Ali S, Ok YS, Ishaque W, Nawaz MF, …, Waqar M (2017) Remediation of heavy metal contaminated soils by using Solanum nigrum: a review. Ecotoxicol Environ Saf 143:236–248 Van Huysen T, Abdel-Ghany S, Hale KL, LeDuc D, Terry N, Pilon-Smits EA (2003) Overexpression of cystathionine-gamma-synthase enhances selenium volatilization in Brassica juncea. Planta 218(1):71–78. https://doi.org/10.1007/s00425-003-1070-z

8 Heavy Metal Toxicity and Phytoremediation by the Plants …

263

Vara Prasad MN, de Oliveira Freitas HM (2003) Metal hyperaccumulation in plants: biodiversity prospecting for phytoremediation technology. Electron J Biotechnol 6(3):285–321 Vert G, Barberon M, Zelazny E, Séguéla M, Briat J-F, Curie C (2009) Arabidopsis IRT2 cooperates with the high-affinity iron uptake system to maintain iron homeostasis in root epidermal cells. Planta 229(6):1171–1179 Viehweger K (2014) How plants cope with heavy metals. Bot Stud 55(1):1–12 Vives-Peris V, de Ollas C, Gómez-Cadenas A, Pérez-Clemente RM (2020) Root exudates: from plant to rhizosphere and beyond. Plant Cell Rep 39(1):3–17 Vázquez M, Poschenrieder C, Barceló J, Baker A, Hatton P, Cope G (1994) Compartmentation of zinc in roots and leaves of the zinc hyperaccumulator Thlaspi caerulescens J & C Presl. Bot Acta 107(4):243–250 Wang G, Wang L, Ma F, You Y, Wang Y, Yang D (2020) Integration of earthworms and arbuscular mycorrhizal fungi into phytoremediation of cadmium-contaminated soil by Solanum nigrum L. J Hazard Mater 389:121873 Wang M, Xu Q, Yu J, Yuan M (2010) The putative Arabidopsis zinc transporter ZTP29 is involved in the response to salt stress. Plant Mol Biol 73(4):467–479 Wang S-H, Yang Z-M, Yang H, Lu B, Li S-Q, Lu Y-P (2004) Copper-induced stress and antioxidative responses in roots of Brassica juncea L. Bot Bull Acad Sinica 45 Waters BM, Chu H-H, DiDonato RJ, Roberts LA, Eisley RB, Lahner B, …, Walker EL (2006) Mutations in Arabidopsis yellow stripe-like1 and yellow stripe-like3 reveal their roles in metal ion homeostasis and loading of metal ions in seeds. Plant Physiol 141(4):1446–1458 White PJ (2016) Selenium accumulation by plants. Ann Bot 117(2):217–235. https://doi.org/10. 1093/aob/mcv180 Wuana RA, Okieimen FE (2011) Heavy metals in contaminated soils: a review of sources, chemistry, risks and best available strategies for remediation. Int Sch Res Not 2011 Yadav B, Jogawat A, LalNITRATE SK, Lakra N, Mehta S, Shabek N, Narayan OP (2021) Plant mineral transport systems and the potential for crop improvement. Planta 253(2):1–30 Yadav S (2010) Heavy metals toxicity in plants: an overview on the role of glutathione and phytochelatins in heavy metal stress tolerance of plants. S Afr J Bot 76(2):167–179 Yamaguchi N, Ishikawa S, Abe T, Baba K, Arao T, Terada Y (2012) Role of the node in controlling traffic of cadmium, zinc, and manganese in rice. J Exp Bot 63(7):2729–2737 Yan A, Wang Y, Tan SN, Mohd Yusof ML, Ghosh S, Chen Z (2020) Phytoremediation: a promising approach for revegetation of heavy metal-polluted land. Front Plant Sci 11:359 Zaier H, Mudarra A, Kutscher D, De La Campa MF, Abdelly C, Sanz-Medel A (2010) Induced lead binding phytochelatins in Brassica juncea and Sesuvium portulacastrum investigated by orthogonal chromatography inductively coupled plasma-mass spectrometry and matrix assisted laser desorption ionization-time of flight-mass spectrometry. Anal Chim Acta 671(1–2):48–54 Zhang X, Chen B, Ohtomo R (2015) Mycorrhizal effects on growth, P uptake and Cd tolerance of the host plant vary among different AM fungal species. Soil Sci Plant Nutr 61(2):359–368 Zhang X, Li Q, Xu W, Zhao H, Guo F, Wang P, …, Wei C (2020) Identification of MTP gene family in tea plant (Camellia sinensis L.) and characterization of CsMTP8. 2 in manganese toxicity. Ecotoxicol Environ Saf 202:110904 Zhigang A, Cuijie L, Yuangang Z, Yejie D, Wachter A, Gromes R, Rausch T (2006) Expression of BjMT2, a metallothionein 2 from Brassica juncea, increases copper and cadmium tolerance in Escherichia coli and Arabidopsis thaliana, but inhibits root elongation in Arabidopsis thaliana seedlings. J Exp Bot 57(14):3575–3582 Zhu XF, Wang ZW, Dong F, Lei GJ, Shi YZ, Li GX, Zheng SJ (2013) Exogenous auxin alleviates cadmium toxicity in Arabidopsis thaliana by stimulating synthesis of hemicellulose 1 and increasing the cadmium fixation capacity of root cell walls. J Hazard Mater 263:398–403

264

K. Ball et al.

Zhu Y, Xu F, Liu Q, Chen M, Liu X, Wang Y, …, Zhang L (2019) Nanomaterials and plants: positive effects, toxicity and the remediation of metal and metalloid pollution in soil. Sci Total Environ 662:414–421 Zhu Y-G, Pilon-Smits EA, Zhao F-J, Williams PN, Meharg AA (2009) Selenium in higher plants: understanding mechanisms for biofortification and phytoremediation. Trends Plant Sci 14(8):436–442

Chapter 9

Combating Nanotoxicity in Plants: Green Nanotechnology Perspective for a Sustainable Future Pooja Singh and Krishna Kumar Choudhary

Abstract Nanoparticles have immensely contributed toward agriculture sector, due to their unique physical and chemical properties, thus enhancing the plant growth through eradication of pathogens, nutrient availability, and soil fertility enhancement. Synthesis of nanoparticles occurs by physical, chemical, and biological methods. Physical methods including mechanical grinding, ball milling method, laser ablation synthesis, and ion sputtering are energy consuming and expensive, whereas chemical methods involving co-precipitation, sol–gel, pyrolysis, hydrothermal synthesis, microemulsion, microwave irradiation, and chemical vapor depositions are expensive and contain toxic substances like thiophenol, thiocarbamide, hydrazine, hydroxylamine, and sodium borohydride. However, several toxic by-products are generated via these techniques along with the requirement of non-biodegradable capping agents for the stabilization of nanoparticles. Plants growing under ambient conditions observe various biotic and abiotic stresses. Nanoparticles play an important role for alleviating stress-induced alterations in plants. Uptake of nanoparticles by the plants is size dependent and concentration specific. They have the potential to alter the physiology of plants by modulating the physiological, biochemical responses in the plant. Therefore, role of nanoparticles in growth and development of plant is ambiguous and controversial. Recently, it has been observed that different nanoparticles affect several crop species in both positive and detrimental ways, i.e., reduced chlorophyll content and photosynthesis, enlargement of roots along with the impact on yield and germination rate of soybean, mung bean, tobacco, cucumber, onion, and spinach. Considering the above facts, scientists are paying attention to biological methods since it is eco-friendly and economically relevant technique. Therefore, present chapter will focus on the interaction of nanoparticles with the plants, mechanism of nanotoxicity in plants, and further enlists the preventive strategies such as green nanotechnology for a sustainable future. Keywords Nanoparticles · Nanotoxicity · Green nanotechnology · Stress · Sustainability P. Singh · K. K. Choudhary (B) Botany Section, MMV, Banaras Hindu University, Varanasi 221005, India e-mail: [email protected] © The Author(s), under exclusive license to Springer Nature Switzerland AG 2022 T. Aftab (ed.), Sustainable Management of Environmental Contaminants, Environmental Contamination Remediation and Management, https://doi.org/10.1007/978-3-031-08446-1_9

265

266

P. Singh and K. K. Choudhary

9.1 Introduction Nanoparticles (NPs) are extremely small materials with a diameter of less than 100 nm. Because of their substantially greater surface area to volume ratio, NPs have distinctive physio-chemical properties, i.e., highly reactive and dynamic (Mauter et al. 2018), due to which they are distinguished from their bulk counterparts (Dasgupta et al. 2017). Due to the multifaceted nature of NPs, it is potentially utilized in various sectors like agriculture, medical, cosmetics, textiles, and chemical industries (Srivastava et al. 2018; Yata et al. 2018). Synthesis of NPs occurs via physical and chemical methods. The physical methods include laser ablation, electron beam evaporation, and evaporation–condensation in top-down synthesis process. The major challenge behind these methods includes agglomeration of NPs, as capping agents are not used (Lee and Jun 2019). Also, it consumes lot of energy around the source material that raises its temperature and takes a long time to attain thermal stability (Landage et al. 2014; Jung et al. 2006; Iravani et al. 2013). However, chemical synthesis of NPs involves microwave-assisted synthesis, electrochemical synthesis, chemical reduction, polyol method, radiolytic process, and microemulsion process (Gudikandula and Maringanti et al. 2016). Demerits of these synthetic techniques have already been addressed (Refer paper: Biswas et al. 2012). The implication of nanotechnology research in agriculture has become vital and perhaps critical aspect for sustainable development. The pertinent use of nanoenabled/nano-engineered items (Villaseor and Ros 2018), nanofertilizers (Adisa et al. 2019), nanoinsecticides (Wibowo et al. 2014), and nanofungicides (Arruda et al. 2015; Saharan et al. 2015) is expected to increase the burden of NPs on the environment via diverse mechanisms, with unknown implications on biota, water, and soil (Eduok and Coulon 2017). Excessive utilization of NPs in agricultural sector should be monitored in the view of futuristic scenarios, as we are still unaware of its harmful consequences on living organisms and their environment (Tripathi et al. 2017). Generation of reactive oxygen species (ROS) in plants through NPs depends upon the shape, size, and surface area of NPs (Dayem et al. 2017). For example, in Allium cepa cells, interaction of gold NPs (variable sizes) with root hairs generates ROS in a dose (0.1, 1, and 10 μgmL−1 ) and size-dependent manner (15, 30, and 40 mm) that promotes lipid peroxidation and chromosomal aberrations (Rajeshwari et al. 2016). In Arabidopsis thaliana, on exposure of AgNPs, alteration in conductance of plasma membrane as well as root elongation and leaf expansion were significantly inhibited (Sosan et al. 2016). Similarly, barley plants grew longer roots and shoots when exposed to