Role of Microbial Communities for Sustainability (Microorganisms for Sustainability, 29) 9811599114, 9789811599118

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Microorganisms for Sustainability 29 Series Editor: Naveen Kumar Arora

Gamini Seneviratne Junaida Shezmin Zavahir  Editors

Role of Microbial Communities for Sustainability

Microorganisms for Sustainability Volume 29

Series Editor Naveen Kumar Arora, Environmental Microbiology, School for Environmental Science, Babasaheb Bhimrao Ambedkar University, Lucknow, Uttar Pradesh, India

More information about this series at http://www.springer.com/series/14379

Gamini Seneviratne • Junaida Shezmin Zavahir Editors

Role of Microbial Communities for Sustainability

Editors Gamini Seneviratne Microbial Biotechnology National Institute of Fundamental Studies Kandy, Sri Lanka

Junaida Shezmin Zavahir Faculty of Science School of Chemistry, Monash University Melbourne VIC, Australia

ISSN 2512-1901 ISSN 2512-1898 (electronic) Microorganisms for Sustainability ISBN 978-981-15-9911-8 ISBN 978-981-15-9912-5 (eBook) https://doi.org/10.1007/978-981-15-9912-5 © The Editor(s) (if applicable) and The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2021 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 Singapore Pte Ltd. The registered company address is: 152 Beach Road, #21-01/04 Gateway East, Singapore 189721, Singapore

Preface

The omnipresence of microbes makes their pivotal role in nature hard to ignore. They co-exist in various ecosystems as well as support growth and sustenance to plants in their vicinity. Microbes applied as inoculants play an important role in sustainable soil management in agriculture and the environment. Here, the conventional approach is the use of single species or ad hoc mixed cultures as plant growthpromoting agents. However, the importance of naturally existing complex microbial communities in the soil or developed microbial communities as growth-promoting agents has not been adequately studied and reported in scientific literature. Their potential to efficiently solve agricultural problems, combat environmental stress conditions, and thereby support resources to feed the world’s growing population, is often not fully harnessed. Thus, the main objective of this book is to gather knowledge for filling this gap with an adequate understanding of complex processes occurring in the microbial community-soil-plant system in order to reduce the heavy use of harmful chemicals in agriculture, and also to establish a sound basis for researchers to enhance studies on this line leading to the development of new products. The first chapter of this book deals with an overview of the role of microbial communities in plant–microbe interactions, metabolic cooperation and selfsufficiency, which are important to sustainability of agriculture. Then, most of the subsequent chapters discuss different facets of the microbial communities in terms of their significance in agricultural sustainability. Amongst these the understanding of agriculturally essential bacterial biofilms, and their effective use as biofilm-based biofertilizers in sustainable production of rice and rubber are described with examples of field applications. Potential contribution of microbial communities in global food security and crop protection are also overviewed. Further, the integrated use of microbes like arbuscular mycorrhizal fungi, and natural and constructed cyanobacteria-based consortia in sustainable crop production and soil fertility are explored. Another interesting chapter of this book describes in detail the potential use of microbiome towards sustainable crop production.

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A few other chapters elaborate on engineering symbiotic microbial consortia for biotechnological applications, and also for soil carbon sequestration. Further, application of microbial siderophores for integrated plant disease management and alleviation of metal stress in contaminated soils are also reported. The importance and application of microbial communities in sustainable, low-cost bioremediation of pig effluent waste is also delved into. These chapters provide a comprehensive overview of the various existing approaches as well as the new trends and technologies which can be used together to achieve agro-ecological sustainability. The capability of microbial consortia to benefit the ecosystems they are in is also amply highlighted. In this manner, this timely book will be equally useful to advanced students and academia for renewing their knowledge on the use of natural and engineered microbial communities in agriculture, industry, and the environment. Kandy, Sri Lanka Melbourne, VIC, Australia

Gamini Seneviratne Junaida Shezmin Zavahir

Contents

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Role of Microbial Communities in Plant–Microbe Interactions, Metabolic Cooperation, and Self-Sufficiency Leading to Sustainable Agriculture . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Junaida Shezmin Zavahir, Piyumi C. Wijepala, and Gamini Seneviratne

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Symbiotic Interactions of Phototrophic Microbes: Engineering Synthetic Consortia for Biotechnology . . . . . . . . . . . . . . . . . . . . . . Derek T. Fedeson and Daniel C. Ducat

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Understanding Agriculturally Indispensable Bacterial Biofilms in Sustainable Agriculture . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Firoz Ahmad Ansari, John Pichtel, and Iqbal Ahmad

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Global Food Demand and the Roles of Microbial Communities in Sustainable Crop Protection and Food Security: An Overview . . . Ahmadu Tijjani and Ahmad Khairulmazmi

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Sustaining Productivity Through Integrated Use of Microbes in Agriculture . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 109 Rakesh Kumar, Kirti Saurabh, Narendra Kumawat, Prem K. Sundaram, Janki Sharan Mishra, Dhiraj K. Singh, Hansraj Hans, Bal Krishna, and Bhagwati Prasad Bhatt

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Arbuscular Mycorrhizal Fungi for Sustainable Crop Protection and Production . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 147 Thangavelu Muthukumar

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Role of Microbial Communities in Sustainable Rice Cultivation . . . 189 Thilini A. Perera and Shamala Tirimanne

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Applications of Soil Bacterial Community in Carbon Sequestration: An Accost Towards Advanced Eco-sustainability . . . . . . . . . . . . . . 225 Ved Prakash, Rishi Kumar Verma, Kanchan Vishwakarma, Padmaja Rai, Mohd Younus Khan, Vivek Kumar, Durgesh Kumar Tripathi, and Shivesh Sharma

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Approach Towards Sustainable Crop Production by Utilizing Potential Microbiome . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 239 Usha Rani, Manoj Kumar, and Vivek Kumar

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Diversity, Function, and Application of Fungal Iron Chelators (Siderophores) for Integrated Disease Management . . . . . . . . . . . . 259 Umesh Dhuldhaj and Urja Pandya

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Role of Microbial Communities in the Low-Cost, Sustainable Treatment of Pig Effluent Waste . . . . . . . . . . . . . . . . . . . . . . . . . . . 289 Sasha N. Jenkins, M. L. M. Anjani W. Weerasekara, and Junaida Shezmin Zavahir

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Metal Stress Impacting Plant Growth in Contaminated Soil Is Alleviated by Microbial Siderophores . . . . . . . . . . . . . . . . . . 317 Lalitha Sundaram, Santhakumari Rajendran, and Nithyapriya Subramanian

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Natural and Constructed Cyanobacteria-Based Consortia for Enhancing Crop Growth and Soil Fertility . . . . . . . . . . . . . . . . 333 Radha Prasanna, Nirmal Renuka, Lata Nain, and B. Ramakrishnan

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Microbial Communities Based Biofilmed Biofertilizers Enhance Soil Fertility and Plant Growth in Hevea Ecosystem: Evidences from Seedlings and Immature Plants . . . . . . . . . . . . . . . 363 Rasika Priyani Hettiarachchi, Gamini Seneviratne, Ananda Nawarathna Jayakody, Kiththangodage Eranga De Silva, P. D. Thushara Gunathilake, and Vishani U. Edirimanna

Editors and Contributors

About the Series Editor Naveen Kumar Arora, PhD in Microbiology Fellow of International Society of Environmental Botanists (FISEB), is Professor and Head, Department of Environmental Science at Babasaheb Bhimrao Ambedkar University (A Central University), Lucknow, Uttar Pradesh, India. He is a renowned researcher in the field of environmental microbiology and biotechnology. His specific area of research is plant-microbe interactions, particularly plant growth promoting rhizobacteria. He has more than 75 research articles published in premium international journals and several articles published in magazines and dailies. He is an editor of 25 books, published by Springer. He is a member of several national and international societies, Secretary General of Society for Environmental Sustainability, in editorial board of 4 journals, and reviewer of several international journals. He is also the editor in chief of the journal “Environmental Sustainability” published by Springer Nature. He has delivered lectures in conferences and seminars around the globe. He has a long-standing interest in teaching at the PG level and is involved in taking courses in bacteriology, microbial physiology, environmental microbiology, agriculture microbiology, and industrial microbiology. He has been advisor to 134 postgraduate and 11 doctoral students. He has been awarded for excellence in research by several societies and national and international bodies/ organizations. Although an academician and researcher by ix

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profession he has a huge obsession for the wildlife and its conservation and has authored a book, Splendid Wilds. He is the President of Society for Conservation of Wildlife and has a dedicated website www. naveenarora.co.in for the cause of wildlife and environment conservation.

About the Editors Gamini Seneviratne received his PhD from the University of Peradeniya, Sri Lanka, followed by postdoctoral fellowships in Katholieke Universiteit Leuven, Belgium, and the University of Sydney, Australia, where he is also a visiting professor. Currently, he is a senior research professor at the National Institute of Fundamental Studies (NIFS), Sri Lanka. He directs a novel field of research where microbial biofilms are developed for various biotechnological applications, including the world-first biofilm-based biofertilizer biotechnology. He is a member of Soil Science Society of America, American Society for Microbiology, and a former editor, Agriculture, Ecosystems & Environment (Elsevier). He is a fellow of the National Academy of Sciences in Sri Lanka. Junaida Shezmin Zavahir received a BSc (microbiology) and MSc (biotechnology), from the Bangalore University, India. She is a PhD researcher in analytical chemistry at Monash University, Melbourne, Australia, and a teaching associate at its Faculty of Science. Her current research interests include gas chromatographic and infrared analysis of biofuels and essential oils, preceded by research on fungal–bacterial biofilm-based biofertilizers. She also has extensive experience as a formulation and analytical chemist of alternate fuels. A science communicator on various platforms and the recipient of numerous international and national awards, she is a member of the Monash Chemicals and Plastics Manufacturing Innovation Network Industry Partnership, Australian Centre for Research on Separation Science, and the Royal Australian Chemical Institute.

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Contributors Iqbal Ahmad Biofilm Research Lab, Department of Agricultural Microbiology, Faculty of Agriculture Sciences, Aligarh Muslim University, Aligarh, India Firoz Ahmad Ansari Biofilm Research Lab, Department of Agricultural Microbiology, Faculty of Agriculture Sciences, Aligarh Muslim University, Aligarh, India Bhagwati Prasad Bhatt ICAR Research Complex for Eastern Region, Patna, Bihar, India Kiththangodage Eranga De Silva Soils and Plant Nutrition Department, Rubber Research Institute, Dartonfield, Agalawatte, Sri Lanka Umesh Dhuldhaj School of Life Sciences, Swami Ramanand Teerth Marathwada University, Nanded, Maharashtra, India Daniel C. Ducat MSU-DOE Plant Research Laboratories, Biochemistry and Molecular Biology Department, Michigan State University, East Lansing, MI, USA Vishani U. Edirimanna Soils and Plant Nutrition Department, Rubber Research Institute, Dartonfield, Agalawatte, Sri Lanka Derek T. Fedeson Charles River Laboratories (CR-MWN), Mattawan, MI, USA P. D. Thushara C. Gunathilake Soils and Plant Nutrition Department, Rubber Research Institute, Dartonfield, Agalawatte, Sri Lanka Hansraj Hans Division of Crop Research, ICAR Research Complex for Eastern Region, Patna, Bihar, India Rasika Priyani Hettiarachchi Soils and Plant Nutrition Department, Rubber Research Institute, Dartonfield, Agalawatte, Sri Lanka Ananda Nawarathna Jayakody Department of Soil Science, Faculty of Agriculture, University of Peradeniya, Peradeniya, Sri Lanka Sasha N. Jenkins UWA School of Earth and Environment, Faculty of Science, The University of Western Australia, Perth, WA, Australia Ahmad Khairulmazmi Department of Plant Protection, Faculty of Agriculture, Universiti Putra Malaysia, Serdang, Selangor Darul Ehsan, Malaysia Mohd Y. Khan Department of Biotechnology, Motilal Nehru National Institute of Technology Allahabad, Prayagraj, India Bal Krishna Division of Plant Breeding and Genetics, Bihar Agricultural University, Sabour, Bihar, India Manoj Kumar Center for Life Sciences, School of Natural Sciences, Central University of Jharkhand, Ranchi, India

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Rakesh Kumar Division of Crop Research, ICAR Research Complex for Eastern Region, Patna, Bihar, India Vivek Kumar Himalayan School of Biosciences, Swami Rama Himalayan University, Jolly Grant, Dehradun, India Narendra Kumawat AICRP on Management of Salt Affected Soil and Use of Saline in Agriculture, College of Agriculture, RVSKVV, Gwalior, Indore, Madhya Pradesh, India Lalitha Sundaram Department of Botany, School of Life Sciences, Periyar University, Salem, Tamil Nadu, India Janki Saran Mishra Division of Crop Research, ICAR Research Complex for Eastern Region, Patna, Bihar, India Thangavelu Muthukumar Root and Soil Biology Laboratory, Department of Botany, Bharathiar University, Coimbatore, Tamil Nadu, India Lata Nain Division of Microbiology, ICAR-Indian Agricultural Research Institute, New Delhi, India Urja Pandya Department of Microbiology, Gujarat Vidyapith, Sadra, Gandhinagar, Gujarat, India Thilini A. Perera Department of Plant Sciences, Faculty of Science, University of Colombo, Colombo, Sri Lanka John Pichtel Department of Environment, Geology and Natural Resources, Ball State University, Muncie, IN, USA Ved Prakash Department of Biotechnology, Motilal Nehru National Institute of Technology Allahabad, Prayagraj, India Radha Prasanna Division of Microbiology, ICAR-Indian Agricultural Research Institute, New Delhi, India Padmaja Rai Department of Biotechnology, Motilal Nehru National Institute of Technology Allahabad, Prayagraj, India Santhakumari Rajendran Department of Botany, School of Life Sciences, Periyar University, Salem, Tamil Nadu, India B. Ramakrishnan Division of Microbiology, ICAR-Indian Agricultural Research Institute, New Delhi, India Usha Rani Himalayan School of Biosciences, Swami Rama Himalayan University, Jolly Grant, Dehradun, India Nirmal Renuka Institute for Water and Wastewater Technology, Durban University of Technology, Durban, South Africa

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Kirti Saurabh Division of Crop Research, ICAR Research Complex for Eastern Region, Patna, Bihar, India Gamini Seneviratne National Institute of Fundamental Studies, Kandy, Sri Lanka Shivesh Sharma Amity Institute of Organic Agriculture (AIOA), Amity University, Noida, Noida, Uttar Pradesh, India Dhiraj K. Singh Division of Socio-Economics and Extension, ICAR Research Complex for Eastern Region, Patna, Bihar, India Nithyapriya Subramanian Department of Botany, School of Life Sciences, Periyar University, Salem, Tamil Nadu, India Prem K. Sundaram Division of Land and Water Management, ICAR Research Complex for Eastern Region, Patna, Bihar, India Ahmadu Tijjani Department of Crop Production, Faculty of Agriculture and Agricultural Technology, Abubakar Tafawa Balewa University, Bauchi, Bauchi State, Nigeria Shamala Tirimanne Department of Plant Sciences, Faculty of Science, University of Colombo, Colombo, Sri Lanka Durgesh Kumar Tripathi Amity Institute of Organic Agriculture (AIOA), Amity University, Noida, Noida, Uttar Pradesh, India Rishi Kumar Verma Department of Biotechnology, Motilal Nehru National Institute of Technology Allahabad, Prayagraj, India Kanchan Vishwakarma Department of Biotechnology, Motilal Nehru National Institute of Technology Allahabad, Prayagraj, India M. L. M. Anjani W. Weerasekara Advanced Water Management Centre (AWMC), Level 4, Gehrmann Bldg, Research Rd, The University of Queensland, Brisbane, QLD, Australia Piyumi C. Wijepala Faculty of Science, Monash University, Clayton, VIC, Australia Junaida Shezmin Zavahir Faculty of Science, School of Chemistry, Monash University, Melbourne, VIC, Australia

Chapter 1

Role of Microbial Communities in Plant– Microbe Interactions, Metabolic Cooperation, and Self-Sufficiency Leading to Sustainable Agriculture Junaida Shezmin Zavahir

, Piyumi C. Wijepala, and Gamini Seneviratne

Abstract Microbes in nature exist as mixed microbial consortia rather than pure isolated cultures. These consortia show differentiation of function and division of labor. Microbes involved in the rhizosphere, phyllosphere, and in planta (endophytes) play a vital role in determining the various plant–microbe interactions in an ecosystem, a factor which has much importance in agricultural sustainability. Soil fertility and crop production are largely determined by the resident microbial community. The capability of plant–microbe interactions to carry out biofertilization, bioremediation, and biocontrol is used amply to enhance agricultural productivity. Plants and microbes can also release a multitude of compounds which bring about nutrient exchange, molecular signaling, exchange of information, and metabolic cooperation. Metabolites released by microbial consortia can help both the microbes involved as well as the plants in its vicinity. Also, the fungal/bacterial ratio in such settings contributes to the carbon content of soil and its self-sufficiency. It is imperative to have an in-depth and integrated study of the various factors affecting such relationships prior to their application to larger agricultural areas. Before scaling-up any organism to field applications, their long-term consequences need to be assessed. Use of microbial communities to bring about sustainability in agriculture is the need of the hour.

J. S. Zavahir Faculty of Science, School of Chemistry, Monash University, Melbourne, VIC, Australia P. C. Wijepala (*) Faculty of Science, Monash University, Clayton, VIC, Australia e-mail: [email protected] G. Seneviratne National Institute of Fundamental Studies, Kandy, Sri Lanka e-mail: [email protected] © The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2021 G. Seneviratne, J. S. Zavahir (eds.), Role of Microbial Communities for Sustainability, Microorganisms for Sustainability 29, https://doi.org/10.1007/978-981-15-9912-5_1

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Keywords Microbial communities · Functionalities · Metabolic cooperation · Plant–microbe interactions · Sustainability

1.1

Introduction

The ubiquitous presence of microbes in nature has made their in-depth study indispensable. They do not exist in isolation or as pure cultures in nature, but rather in mixed microbial consortia which interact with each other. Their existence in such communities is accompanied by divisions of labor as well as marked differences in their behavior as single cultures. Researchers over the world have continued to stretch their efforts in trying to gain an understanding of such microbial communities. With the world’s steadily increasing population and declining arable land extent due to pollution and urbanization, it is imperative to have the best practices and technologies to maximize the provision of food sources from such arable lands to feed the growing population. This swelling need constantly challenges agricultural methods to meet the obstacles of coping with the escalating number. Such needs have over time led to simple agricultural practices being substituted or complemented with methods of achieving higher crop yields with reduced disease susceptibility. This widely includes the use of agrochemicals, pesticides, and fertilizers of various forms and sources. The control of pests and pathogens (weeds, fungal pathogens, and insects) in this regard is brought about by a variety of herbicides, fungicides, and insecticides which cause the contamination of soils as a major side effect, where pesticide residues affect non-target organisms thus creating an inequality in the natural ecological balance of the ecosystem. This in turn could also affect protected environmental resources. It is here that the omnipresence of microbial communities plays perhaps the largest role in affecting human existence. A variety of processes involved in modern-day farming practices have led to a steady decline in the fertility of soils as well as the amount of cultivatable land available for farming. These include, but are not limited to, land mismanagement, reducing arability of lands, salinization, extensive constructions, deforestation both in legal and illegal manners, etc. This calls for methods of managing farming processes in a sustainable manner, commonly referred to by the term sustainable agriculture. Such an approach attempts to meet the growing society’s present food and textile needs without compromising the ability of future generations to meet these same needs. It is imperative that this is carried out based on a thorough study of the multitude of relationships between the environment in question and the organisms therein as well as the various ecosystem balances. Despite being a multifaceted and complex concept, agricultural sustainability has been a focal point within many disciplines including agriculture, socioeconomics, conservation, ecology, and demography. It addresses many current issues including the more commonly found ones such as fertility loss, climate change, soil erosion, pest control, loss of biodiversity, and disparity in food distribution among poor and

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richer nations. Although no standardized unit or dimension exists to measure it, various parameters and indicators attempt to present the level of sustainability on farm as well as at national levels. The knowledge obtained from studying both the individual components as well as their interactions creates a portrait of the level of agricultural sustainability. One of the greatest needs and challenges of the current era is to resourcefully harness high crop yields in an eco-friendly manner to meet the ever-increasing needs of a growing population, in which soil plays a central role. Soil humus, a complex, stable, microbe-rich composition, has been considered one of the best measures of soil health and the “gold standard” for determining and directing agricultural sustainability. Humus assists mainly by chelating and holding fertilizer in the root zone for plant use, maintaining the soil aerobic content and increasing soil water holding capacity. Yet its greatest benefit is that it provides the “home” for soil microbes, which in turn are responsible for a vast array of activities. A decrease in soil organic matter would therefore inevitably lead to a decline of its physical, chemical, and biological activity and a concomitant drop in soil fertility. Of all the various microbial communities present in this environment, none takes precedence over the importance of those associated with the rhizosphere—the zone immediately surrounding the plant root with immense microbial activity where microbial communities and/or their activities are either inhibited or stimulated by root exudates. A more appropriate definition in today’s understanding of the zone would present as the “field of action or influence of a root” (Brimecombe et al. 2007). The root surface referred to as the rhizoplane also contributes as a nutrient base for many microbial species. The rhizosphere and rhizoplane together—referred to as the soil-plant interface—work together to make this region a highly active zone. Despite its astonishing spatial and temporal heterogeneity, the rhizosphere has immense biophysical, biochemical, and ecological relevance to life on earth (Hinsinger et al. 2009). This region, which harbors maximum activity compared to its surrounding regions, is also responsible for the numerous plant–microbe interactions in both agricultural and non-agricultural settings. These interactions, which can present themselves as complex relationships, can have beneficial as well as negative impacts on both the plant and microbes involved (Jones and Hinsinger 2008). Exploring the metabolism of microbes in the community rather than an individual context is advantageous for reasons which include (1) revealing new phenotypes, (2) designing of new synthetic communities for biotechnology, (3) assisting in cultivating the “uncultivatable”, (4) understanding metabolic cross feeding, and (5) making way for metabolic modeling (Ponomarova and Patil 2015). The microbes which appear in various environments have been classified and aid in interpretation of taxonomic and biological studies relating to the specific environment or ecosystem. Classification of bacteria (and other microbial forms) which traditionally was based largely on metabolic, morphological, biochemical and physiological traits, determined mainly through the cultivation of individual species under controlled conditions, is now gradually being replaced by a polyphasic taxonomy approach. This polyphasic approach additionally integrates all available phenotypic, phylogenetic and genotypic data to better define and

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categorise species (Vandamme et al. 1996). Despite such studies rendering an understanding of various microbial traits, they may fail to be fully representative of the abundance, diversity, and inter-microbial associations existing in natural environments. Oren and Garrity (2014) presented a review of the changes in prokaryote systematics over time, including nomenclature and requirements for describing new species, as well as the presence of genomics and metagenomics in systematics. This gives an in-depth understanding of the ongoing methods and emerging trends to achieve a polyphasic approach to taxonomy, and more importantly, sheds light on the fact that taxonomy alone cannot fully classify the behavior and classification of microbes in natural settings. This chapter focuses on the various plant–microbial interactions at the community level, their metabolic cooperative roles, and their unison to create selfsufficiency in agricultural settings in a sustainable manner.

1.2

Microbial Communities in Plant–Microbe Interactions

The evolution of plant varieties in any ecosystem does not happen independent to the evolution and development of its associated microbial community. The various microorganisms both within the different parts of a plant as well as in areas surrounding a plant hold importance in also contributing to its health. Extensive studies have been carried out by researchers through the decades since this plantassociated microbial role has been recognized. Such efforts continue to throw light on the various dynamics and structure of these relationships as well as the complex and important functions of its microbiome. Of these, the role of the rhizospheric microorganisms in characterizing a plant’s root zone cannot be overlooked. The complex interactions in this rhizosphere zone occur in a more complicated and diverse manner than those existing in non-rhizospheric soil or the above-soil surface. The type and number of microbes that occupy the rhizosphere depend on both the soil as well as the plant itself. This highly active zone, the most diverse microbial reservoir, produces a plethora of compounds which directly and indirectly affect the plant roots. The process of releasing various organic compounds by the plant into the rhizosphere is known as rhizodeposition, and this has a profound influence over the chemical, biological, and physical properties of the rhizosphere soil (Paterson 2003). While these components can be either water-soluble (sugars, amino acids, hormones, and vitamins) or water-insoluble (cell walls, root debris, sloughed-off root material, mucilage, etc.), the amount and type of such components vary depending on the plant type, species, metabolic activity, and its developmental stage. Rhizodeposition provides organic substrates for soil microbial growth and has a strong influence on the rhizosphere’s soil carbon turnover (Hütsch et al. 2002). Until a few decades ago, it was thought that microbes in a rhizospheric region contributed to the plant in an independent manner. But it has since been proven that microbes interact between themselves as complex communities while interacting with plants and that individual members have specific and disproportionate roles in

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Fig. 1.1 Schematic diagram of roles of microbial interactions in maintaining homeostasis in microbial communities (Adapted from Yung-Hua Li et al. 2017)

maintaining the stability and composition of a microbiome. This was demonstrated in 2017 in a study of the Maize (Zea mays) plant’s root microbiome (Niu et al. 2017). It was seen that of the seven microbial strains identified and chosen by sequencing surveys used in the study (Enterobacter cloacae, Stenotrophomonas maltophilia, Ochrobactrum pituitosum, Herbaspirillum frisingense, Pseudomonas putida, Curtobacterium pusillum, and Chryseobacterium indologenes), removal of one strain affected the population. Here removal of E. cloacae led to the disappearance of five strains thus making C. pusillum the dominant remaining strain. This regulatory role carried out by E. cloacae was not seen in a similar substrate without the maize seedlings thus confirming the role the plant had in maintaining the community composition. This also confirms that understanding microbial interspeciesinteractions within a plant–microbial interaction may not seem as straightforward as thought before. This complexity places a greater weight on finding ways of balancing plant–microbe interactions and in engineering microbes to behave in various environments. Microbial interactions can have an effect on the balance of the microbial community it is hosted by and is known as its homeostasis which is maintained by various positive interactions (+ feedback) and negative interactions ( feedback). The positive interactions, which aid in increasing productivity, include co-adhesions, metabolic cooperation, nutritional synergy, cross feeding within food chains, commensalism or mutualism, and quorum sensing. Likewise, the negative interactions aid in enhancing the stability of the biofilm by creating competition for binding sites and nutrients, antagonism, metabolic inhibition, detachment, etc. Any adverse effect by means of antimicrobial agents, foreign invasions, physiological factors, and dietary changes can tip this balance between

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the (+) and ( ) feedbacks thus disturbing the stability of a microbial community (Li et al. 2017). This balance is depicted in Fig. 1.1. The four main ways microbes interact with plants are as symbionts, pathogens, epiphytes, or endophytes all of which may have one or more members of the bacteria, virus, fungi, and nematodes groups. The definition of these are interaction types that are outlined as follows and readers are directed to the extensive in-depth literature available on these relationships. 1. Symbionts—an organism with a close and long-term association with another, living in a state of symbiosis, usually with benefits to both organisms 2. Pathogens—a biological agent which causes illness or disease to its host disrupting the physiology of its host 3. Epiphytes—an organism which grows on another plant (merely for physical support) while deriving its nutrients from the atmosphere 4. Endophytes—an organism living inside another plant for at least part of its life cycle without causing apparent disease to its host Microbes form certain important relationships within these four plant–microbe interaction domains, the most common of which are highlighted and discussed below for their uniqueness of action.

1.2.1

Biofilms: A Wonder World of Microbial Interactions

The highly cooperative nature of microbes can even form organized structures, a lot like multicellular tissues. A significant example of this is the formation of biofilms. Biofilms, often composed of multicellular communities, are three-dimensional, surface-associated entities which are found on both biotic as well as abiotic surfaces. With the ability of being formed by either one species or a conglomeration of many species (multi-species biofilms), they can be found in various environments including human and animal bodies as well as various ecosystems (Costerton 1999; Seneviratne 2003). Individual cells within a biofilm are bound by an extracellular polymeric substance (EPS) layer which confers differences in physiology and action in comparison to planktonic (free-living) cells. A special circumstance where the formation of bacterial biofilms occurs on biotic fungal surfaces—commonly referred to as fungal-bacterial biofilms (FBB)—is also seen to give enhanced metabolic activities to the biofilm in comparison to multi-species biofilms on abiotic surfaces (Seneviratne et al. 2008). Microbes found in nature in different environments and every level of biological organization are known to carry out the division of labor (Zhang et al. 2016)—a trait seen in biofilms as well. For example, in Bacillus subtilis biofilms, two cell types within the same biofilm were seen to conduct flagellum-independent migration. These were the (1) surfactin-producing cells which produced the lubricant surfactin and (2) the matrix-producing cells which produced the EPS matrix that bind the biofilm (van Gestel et al. 2015). In biofilms, it is imperative to have clarity of

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the overall activities and relationships each organism has with other microbes within the biofilm. In some instances, the initiation periods of biofilms are accompanied by microbes undergoing severe abiotic stresses. This is generally followed by external stress in the mature period leading to competition for the decreased resources available (Mueller et al. 2011; Seneviratne et al. 2013). With their ability to carry out biofertilization, bioremediation, bioprocessing, and a host of other applications, their potential to develop novel biotechnological applications can be tapped to bring beneficial results in agricultural settings and sustainability (Seneviratne et al. 2008). As with other microbial communities, microbial interactions in multi-species biofilms can have both positive as well as negative effects discussed above and outlined in Fig. 1.1.

1.2.2

Plant Growth Promoting Rhizobacteria (PGPR)

Root exudates such as polysaccharides and proteins—the type and secretion of which depend on the plant itself—encourage and assist in rhizospheric organisms, mainly bacteria, to competitively and effectively colonize plant roots. Of the numerous bacterial strains which have the ability to do so, a group of bacteria associated with the roots of higher plants, commonly referred to as plant growth promoting rhizobacteria (PGPR), stand out in their ability to exert a positive impact on the plant as well as soil fertility. These free-living bacterial strains, with their metabolically and functionally diverse features, have been studied over the years to utilize them for gaining optimistic results on plant growth and development. The various bacterial genera used as PGPR may exist either in the rhizosphere or within root cells in specialized structures called nodules. Those which exist in the rhizosphere are referred to as extracellular PGPR (ePGPR) and include genera such as Arthrobactor, Agrobacterium, Azotobactor, Azospirillum, Pseudomonas, Bacillus, Burkholderia, Alcaligenes, and Serratia. Intracellular PGPR (iPGPR), which exist within root cells mainly consist of Rhizobium, Bradyrhizobium, Mesorhizobium, Allorhizobium, Azorhizobium, and members of the order Rhizobiales (MercadoBlanco 2015). Recent studies have also included Delftia sp. for their versatility in plant growth promotion (Ubalde et al. 2012). The effect of PGPR on plant growth and development may occur in a direct or indirect manner. This includes, but is not limited to, the release of plant growth regulators, uptake of necessary nutrients through mobilization or fixation, production of biologically active substances, rhizoremediation, induction of systemic resistance plant stress control, root growth stimulation, antibiosis, and reduction of the harmful effects of pathogenic microbes (Nadeem et al. 2013). These processes occur through a multitude of mechanisms employed by the PGPR to suit the need and/or plant in concern (Lugtenberg and Kamilova 2009; Jeyanthi and Kanimozhi 2018; Kumar et al. 2019). Biofilms have also been seen to aid largely in supporting Rhizobium-legume symbiosis in instances PGPR colonize nitrogen-fixing legume nodules (Seneviratne et al. 2010).

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Many studies have been conducted to evaluate and understand the competence of PGPR in biological control (Bach et al. 2016). The recognition of PGPR’s beneficial role has led to an increasing annual market demand accompanied by the search for novel microbial bioinoculants to render higher yields. With deep screening of microbes in the search for novelty in this field, several PGPRs which can be unsafe for human and animal health have emerged. Despite most strains used as PGPR, biofertilizers have been reported as low risk level microbes. Some studies have revealed side effects of the use of PGPR despite their benefits to the plant and can include human health associated conditions such as skin wounds, peritonitis, septicemia, gastrointestinal infections, respiratory conditions, urinary tract infections, etc., with most being opportunistic human pathogens (OHPs) (Berg et al. 2013; Fernández et al. 2015). Hence, it is imperative that there is a thorough study of pathogenicity and side effects as well as precise identification of useful strains of PGPR before production and application are scaled up to a mass field application (Keswani et al. 2019).

1.2.3

Endophytes

First proposed by De Bary in 1866, the term endophytes (Greek: endon-within; phyton-plant) refers to the microbes which reside within plant tissues for all or part of their life cycles causing no disease symptoms or apparent infections (Lacava and Azevedo 2013). Their relationship with plants may be pathogenic or symbiotic and are mainly categorized as clavicipitaceous (able to infect only some species of grasses) and non-clavicipitaceous (found in tissues of higher plants). The endophytic species are diverse in their symbiotic and ecological functions and play a significant role in the evolution, community structure, and biogeography of plants (Rodriguez et al. 2009). They have been isolated from different plant species (Sturz et al. 2000) and can stimulate plant growth through mechanisms which include biological control, production of growth regulating compounds, nitrogen fixation, mineral or nutrient uptake, high metal tolerance, uptake of water, induction of systemic resistance to pathogens, etc. (Lacava and Azevedo 2013). Endophytic species have been observed to be present in both fungal as well as bacterial groups. The volatile organic carbons (VOCs) emitted by endophytic fungi are reported as high-value agents in sustainable agricultural approaches—especially in their use as antimicrobial agents (Kaddes et al. 2019; Segaran and Sathiavelu 2019). The diversity and population of endophytic fungi greatly depend on the location, physiology of the wide variety of host plants they are found in/on. As outlined by Segaran and Sathiavelu (2019), those belonging to the genera of Phyllosticta, Phoma, Colletotrichum, and Phomopsis are found more commonly whereas some others are found on specific hosts. Though not as widely popular as their fungal counterparts, endophytic bacteria—belonging to both Gram-positive and Gram-negative bacterial groups—have been reported and mainly include the

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classes Alpha-, Beta-, and Gammaproteobacteria, Actinobacteria, Firmicutes, and Bacteroidetes (Lacava and Azevedo 2013). With their beneficial role in biological control of plant pathogens as well as plant growth promotion in a wide variety of crops, they can be used efficiently in agronomic production (Hallmann et al. 1997; Sturz et al. 2000). Many questions still remain unanswered regarding how these endophytes communicate with hosts to confer host fitness, the evolutionary dynamics of their habitat-adapted symbiosis, their evolutionary origins, the ability to predict plant–fungal interactions based on the differences of their functional classes, etc. (Rodriguez et al. 2009). It is not the scope of this chapter to extensively cover the roles and characteristics of biofilms, PGPR, and endophytes in-depth, and hence readers are directed to the extensive literature available on these valuable topics. Yet their importance will be taken into account when discussing the following sections.

1.2.4

Microbial Communities in Plant–Microbe Interactions

In all ecosystems, plants are constantly challenged with various abiotic and biotic factors which exert beneficial, harmful, or neutral effects on the plant. Of these factors, microorganisms in the plant’s vicinity—more importantly in its rhizosphere—play a crucial role. Plant infections by bacterial, viral, or fungal pathogens can lead to diseases or even death of plants and thus elicit negative effects on the plant. In response to such infections, most plants have developed ways of protecting themselves by producing various metabolites to either destroy such microbes or minimize the extent of damage caused by them. The interactions between plants and the microbial communities in their vicinity could provoke benefits or damage to the plant. There are also instances when various microbial species harbor themselves on plants for their mutual benefit where they obtain nutrition and support from the plant. This close proximity of microbial species to the plant makes available a concoction of microbial exudates which would not be available to the plant otherwise, and reciprocally the variety of plant released compounds/plant dead material which nourish the associated microbes. In many instances, such beneficial microbial species have been reported to defend the host plant against pathogenic forms of microorganisms. Such a defence mechanism relies on a strong interaction between the plant and the microbe(s) as well as a highly efficient and well-developed communication pathway based on various molecular mechanisms (Babar et al. 2016). Such plant–microbe interactions have great value in agricultural spheres to reduce the dependence on destructive technologies and to enhance sustainability. These interactions are multidimensional and intermingled with no exact demarcation of their function as they all act together to maintain these relationships in a balanced manner. Yet for ease of discussion and study, they can be divided into a few specific functions portrayed below.

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1.2.4.1

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Biofertilization

Despite its ability to act as fast solution to meet the world’s food production demands, the deleterious effects of the ongoing use of chemical fertilizers are well known. This can include the degradation of soil fertility as well as health and environmental hazards including water contamination, soil erosion pesticide poisoning, biodiversity depletion, decreasing groundwater table, etc. (Suhag 2016). In addition, it has been seen that a tripartite symbiosis can exist among the plant, fungal hosts, and endofungal bacteria that exist within fungal spores and hyphae. Despite being in its early stages of study, such tripartite relationships are known to contribute to plant growth and disease resistance of pathogenic microbes (Alabid et al. 2019). The use of formulations of beneficial living microorganisms to bring about fertilization in plants has been a sought-after trend to minimize the harmful effects of chemical fertilizers. Commonly referred to as biofertilizers, they can be classified based on their symbiotic nature, organism involved, or the biological activity which brings about fertilization. These microbes can be found within the plant or in the rhizosphere and bring about growth by a variety of mechanisms including nitrogen fixation, phosphate solubilization, ion sequestration, siderophore synthesis, depleted soil regeneration, increasing ecosystem functioning, sustainability, etc. (Jayasinghearachchi and Seneviratne 2006; Zakeel and Safeena 2019). Many cyanobacterial species have also been known to enhance plant growth by their ability to fix atmospheric nitrogen and thereby increase soil fertility. While having the ability to exist independently they also occur symbiotically with microbial, animal, and plant hosts (Rai et al. 2000). They play a pivotal role in soil microbiota with their high photosynthetic activity, mass development ability, soil humic compound formation, and as producers of organic compounds which benefit other microbes and plants. These features make them ideal candidates to be used in microbial consortia, especially in instances such consortia are to be developed as biofertilizers. In some instances, certain microbial species can be added to the consortia to maintain the pH for purposes of intensifying the nitrogen fixation. In one such example, naturally occurring cyanobacteria and Azotobactor species were isolated from a rice (Oryza sativa) paddy field in Khazakstan and new microbial consortia were developed (Zaiadan et al. 2014). Here the ZOB-1 consortium was made up of Anabaena variabilis, Chlorella vulgaris, and Azotobactor sp. and ZOB-2 was made of Nostoc calsicola, Chlorella vulgaris, and Azotobactor sp., in which C. vulgaris was added to adjust the pH in these consortia. Of all plant hormones present in nature, indole-3-acetic acid (IAA) belonging to the auxins group takes precedent as the most commonly occurring and has been studied intensely and extensively by plant physiologists. Its ability to bring about plant growth and development by effects such as cell elongation and cell division, and hence its increased presence in biofertilizer environments is advantageous. A study on Pigeon pea (Cajanus cajan) using the rhizospheric bacterial consortium of Burkholderia sp. MSSP and Sinorhizobium meliloti PP3 strain proved that an increased IAA production and

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subsequent growth can be driven by mixed-species inoculations compared to monospecies entities (Pandey and Maheshwari 2007). A special group of biofertilizers are the biofilmed biofertilizers (BFBFs) in which the microbes have been developed to exist in the biofilm mode. Such BFBFs are instrumental in reinstating ecosystems which have been depleted due to conventional agronomic practices (Seneviratne et al. 2011). Their action is via increasing biodiversity by breaking dormancy of the inactive soil microbial seed bank that developed due to various environmental stresses. Therefore, the BFBFs are considered as developed biofilm-based microbial ameliorators rather than just biofertilizers (Seneviratne et al. 2017a, b). BFBFs are used in many countries and have also been commercialized for different crops. For example, Biofilm-T™ has been developed for tea plantations in Sri Lanka with BFBFs being developed for rice, maize, coconut, rubber, and vegetables. A study using hydroponically grown strawberry, tomato, and rice with the BFBF of the rhizospheric Enterobacter sp. as the bacteria and Aspergillus sp. as the fungus showed a marked ability to improve crop growth when compared to monoculture bacterial and fungal biofetilizer applications (Singhalage et al. 2019). Cyanobacteria also possess this ability to form biofilms with other microbes which can be useful in various crop systems. However, the full potential of combining cyanobacteria with PGPRs has not been fully exploited as inoculants in agricultural crops. In an evaluation of such systems, it was seen that the cyanobacterium Anabaena torulosa based biofilms with Azotobacter chroococcum, Mesorhizobium ciceri, Serratia marcescens, and Pseudomonas striata demonstrated an enhanced nitrogen fixing ability and viability than their single cultures when applied to wheat (Triticum aestivum) (Swarnalakshmi et al. 2013). These studies also confirmed the ability of mixed species of microbes to better provide increase in growth when compared to the presence of single species.

1.2.4.2

Bioremediation

Modern biotechnological advances have made it possible to engineer microbial communities to remove or reduce contaminants from various environments. The use of such microbes—either naturally occurring or deliberately introduced—to clean contaminated sites by breaking down or consuming environmental pollutants is referred to as bioremediation. This can be done in water, soil, or subsurface environments and is generally more sustainable than other remediation techniques. How these microbial consortia coexist in nature needs to be understood to fully take advantage of their potential applications. By division of labor achieved through splitting the function among the different populations, fitness and system performance of the individual populations can be earned to thus achieve a higher yield compared to single populations (Tsoi et al. 2019). The presence of microbes in almost all environments and their high adaptability makes it possible to use them in bioremediation processes as long as their main requirements of an energy source and carbon source are fulfilled. They can be

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subdivided into the groups aerobic, anaerobic, ligninolytic, or methylotrophic (Vidali 2001) based on their requirements and mode of action. Bioremediation can refer to the use of all biological entities (plants, microbes, enzymes, etc.) for removing pollutants. Of these, phytoremediation refers to the strict use of plants in such remediation. The five main types of phytoremediation are (1) Phytoaccumulation—contaminant accumulation in roots or shoots, (2) phytotransformation—transforming soil organic contaminants to less harmful forms, (3) phytostabilization—reducing the mobility of contaminated soil, (4) rhizofiltration—contaminant uptake by roots in water environments, and (5) rhizodegradation—contaminant breakdown through rhizospheric activity. Of these, rhizodegradation or rhizoremediation is of interest in this chapter due to its direct relevance to plant–microbe interaction. Often the plant root exudates indirectly participate in the rhizodegradation as they affect the microbial biomass and metabolic activity which in turn enhances the remediation process (Turkovskaya and Muratova 2019). Plants support efficient rhizospheric-bacterial-pollutant degradation in two main ways; (1) releasing plant exudates which enhance the survival and action of rhizospheric bacteria and (2) spreading of bacteria through the soil to help penetrate impermeable soil layers (Kuiper et al. 2004). The beneficial effects of rhizodegradation can be applied to a variety of crops and situations. For example, recent studies have shown that the root exudates of alfalfa (Medicago sativa L.) actively participated in rhizodegradation of phenanthrene—a polycyclic aromatic hydrocarbon (PAH)—when coupled to the PAH degrading bacteria Ensifer meliloti (Muratova et al. 2015). The plant Sorghum bicolor is known to be useful in remediating oil hydrocarbon-contaminated soil. Also, the rhizobacterium Sinorhizobium meliloti P221 is able to produce indole-3-acetic-acid (IAA) and degrade PAHs such as phenanthrenes. This knowledge has been used to successfully study the plant–pollutant–microbe interaction in the S. bicolor– phenanthrene–S. meliloti relationship (Golubev et al. 2011). Another interesting approach studied the biodegradation of soil contaminated by pentachlorophenol (PCP). Here the Gram-negative bacterium Sphingobium chlorophenolicum ATCC 39723 which is capable of completely mineralizing PCP through its PCP degradative pathway was used. It was seen that PCP removal by the bacteria was more effective in soils planted with Triticum aestivum (Winter wheat) over the uninoculated soils where the plant acted as a vector to facilitate the inoculum reaching the target compound PCP thus highlighting the importance of the plant–microbe relationship in remediating the contaminated soil (Dams et al. 2007). While this has been seen as a sustainable means of remediating contaminated environments, in the use of microbial communities for bioremediation a few major factors which affect the process need to be considered. These factors mainly include microbial, environmental, substrate, biological (aerobic vs anaerobic), mass transfer limitations, physicochemical bioavailability, type of pollutants, etc.

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Biocontrol and Antibiosis

Plants are under constant threat of diseases and destruction caused by pathogenic microorganisms and pests. The control of such pests (insects, mites, weeds, etc.) and disease-causing organisms using other living organisms is referred to as biological control or biocontrol. This approach, which has been used for more than half a century, relies on mechanisms such as parasitism, predation, herbivory, natural approaches and human management, and uses natural enemies to control the invasive organism in its native setting. Its success has been seen in developed, developing, and emerging nations and has transitioned from a trial and error method to a more predictive approach based on population dynamics and predator–prey interactions (Heimpel and Mills 2017). When challenged by nonhost pathogens, plants have the ability to produce certain chemical compounds which provides it with the defence from these threats. Microbial biological control agents (MBCAs) have been used with increasing popularity as they can be applied on crops to control plant pathogens via a range of actions. This is achieved either by inducing resistance or by nutrient/space competition which modulates the pathogen’s growth conditions (Köhl et al. 2019). Antibiosis is a major fraction of biological control and is an interaction between two or more organisms which is detrimental to at least one of them, and is thus useful in controlling harmful organisms. Antibiosis is brought about by antimicrobial metabolites or antibiotics which are low-molecular weight, heterogeneous, organic compounds produced by one organism which is deleterious to the metabolism or growth of another. They are produced and released to the environment in small quantities. Although huge numbers of such antibiotics are known to be produced by bacteria (2900), fungi (4900), and actinomycetes (8700), their total numbers are still unknown as those are produced in situ by bacteria which have no cultured representative (Berdy 2005; Raaijmakers and Mazzola 2012). Although microbe-mediated plant disease control has been amply studied and applied and examples of this approach are widely found in literature, recent interests are focused on instances when microbial consortia rather than single microbes are used to achieve biocontrol. Here it has been seen that under biotic stress conditions or pathogen invasion, beneficial microbial communities have a profoundly enhanced host defence response over that provided by single microbes. This has been mainly through the better activation of phenylpropanoid pathways, antioxidants, and systemic resistance when microbes are in a community (Sarma et al. 2015). It is vital to study the compatibility between the microbes in developing such consortia for field applications. This has led to the current trend of mixing biocontrol agents (BCAs) of different microbial species to attain the required outcome. For example, use of the two PGPR species Pseudomonas fluorescens Aur 6 strain and Chryseobacterium balustinum Aur 9 was used in rice (Oryza sativa) in the integrated management of rice blast disease (Lucas et al. 2009). In another example, systemic resistance against Botrytis cinerea was induced in cucumber (Cucumis sativus) plants and model Arabidopsis thaliana plants when the two cucumber rhizospheric organisms

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Trichoderma harzianum Tr6 and Pseudomonas sp. Ps14 were used in combination (Alizadeh et al. 2013). Oxalic acid is known to be an important pathogenic factor and can work by reducing hydrogen peroxide production leading to oxalic-acid induced cell death, which was studied in the pathogenic invasion of Sclerotinia sclerotiorum on Pea (Pisum sativum). A consortium of the three BCA agent strains Pseudomonas aeruginosa PJHU15, Bacillus subtilis BHHU100, and Trichoderma harzianum TNH U27 when applied together were seen to acting on Sclerotinia sclerotiorum (Jain et al. 2015). Biocontrol being a natural approach reduces the reliance on harmful chemicals which could have an adverse effect on the environment. There are instances it is disadvantageous in the required long (5–10 years) timescale, and because it lacks total predictability in some cases. However, given its permanency, reduced danger to human health and reduced ongoing costs, it is also seen as a sustainable option in this era of non-native species arriving in countries due to increased trade and travel. Both plants and microbes have evolved over time to develop specific mechanisms to survive in the ecosystem as well as food chain while maintaining associations and interactions with each other. They thus have mutual benefits through various forms of relationships via a plethora of molecular mechanisms. Molecular basis of plant– microbe interactions is usually elucidated by various means which include but are certainly not limited to genome sequencing, transcriptomics, mutagenesis, metabolomics, proteomics, secretomics, comparative genomic information, etc. The results of these can be deciphered by commonly used techniques such as pyrosequencing, phylochipping, third-generation sequencing, molecular markers, metatranscriptomic studies, polymerase chain reaction (PCR) with molecular fingerprinting, qRT-PCR, phospholipid derived fatty acid (PLFA) studies, etc. (Babar et al. 2016) (Table 1.1).

1.2.5

Factors Affecting Plant–Microbe Interactions

A plethora of chemical, mechanical, and environmental factors have been observed to affect the interactions between plants and microbes. An understanding and management of these factors are imperative to ensure the best outcome of using the benefits of plant–microbe interactions in agricultural settings.

1.2.5.1

Chemical Signals

With all living beings thriving on various chemical reactions, it is inevitable that exposure to microbes would change the chemical balance of a plant leading to the formation of new chemical compounds in the plant. This mainly occurs in response to various metabolites released by the microbe as well as enzyme-activated reactions (Babar et al. 2016). Of all chemical reactions, redox reactions and generations of oxygen species have seen to be the most commonly observed.

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Table 1.1 Examples of plant–microbe interactions in sustainable agriculture Interaction type Biofertilization Biofertilization

Biofertilization

Rhizoremediation

Rhizoremediation

Rhizoremediation

Biocontrol Biocontrol

Biocontrol

1.2.5.2

Plant species Rice (Oryza sativa) Pigeon pea (Cajanus cajan) Wheat (Triticum aestivum) Alfalfa (Medicago sativa L.) Sorghum (Sorghum bicolor) Winter wheat (Triticum aestivum) Rice (Oryza sativa) Cucumber (Cucumis sativus) Pea (Pisum sativum)

Microbial species Anabaena variabilis, Chlorella vulgaris, Azotobacter sp., and Nostoc calsicola Burkholderia sp. MSSP and Sinorhizobium meliloti PP3 Anabaena torulosa-based biofilms with Azotobacter chroococcum, Mesorhizobium ciceri, Serratia marcescens, and Pseudomonas striata Ensifer meliloti

Ref. Zaiadan et al. (2014) Pandey and Maheshwari (2007) Swarnalakshmi et al. (2013)

Muratova et al. (2015)

Sinorhizobium meliloti

Golubev et al. (2011)

Sphingobium chlorophenolicum ATCC 39723

Dams et al. (2007)

Pseudomonas fluorescens Aur 6 strain and Chryseobacterium balustinum Aur 9 Trichoderma harzianum Tr6 and Pseudomonas sp. Ps14

Lucas et al. (2009) Alizadeh et al. (2013)

Pseudomonas aeruginosa PJHU15, Bacillus subtilis BHHU100, and Trichoderma harzianum TNH U27 acting on the fungus Sclerotinia sclerotiorum

Jain et al. (2015)

Mechanical Signals

Plants have been known to respond to various mechanical stimuli from either the environment or microbes in their vicinity, immediately or with a delayed response. Such stimuli could include factors such as wind, turgor, gravity, touch, pathogens, and wounding and may have a profound effect on plant functions such as growth, development, morphogenesis, reproduction, and survival (Scippa et al. 2008). A review of the various factors and responses involved in mechanical signals affecting plant–microbe interactions has been looked into by Jayaraman and coworkers (Jayaraman et al. 2014).

1.2.5.3

Environmental Factors

In addition to the abovementioned factors, a collection of environmental factors plays a role in directing the way in which plants and microbes interact with each

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other. Variations in the time of exposure to these factors could occur depending on the environmental stimuli which may be biotic or abiotic. Such factors largely include physical and nutritional characteristics of the soil (e.g., carbon, nitrogen, and essential element availability), agricultural practices, cropping systems, variation in atmospheric temperature and soil humidity, exposure to sunlight, etc. (Babar et al. 2016).

1.3

Microbial Communities and Metabolic Cooperation

The existence of microbes as a conglomeration of different microbial species would inevitably lead to a variety of interactions between these species. As opposed to the viewing of the function of microbes as individuals, understanding them in a community context sheds light upon a broad range of metabolic interactions. The proximity of such cells and their arrangement enables a variety of components to be interchanged in specific manners. Thus, the phenomenon of low-molecular weight compounds (e.g., nucleotides, ions) transferring from one cell to another through permeable junctions located between adjacent cell membranes is broadly defined as metabolic cooperation. This phenomenon, which plays a vital role in the transmission of a plethora of intercellular signals, though mainly observed in vitro is also prevalent in vivo (Hooper and Subak-Sharpe 1981). In the latter instances, it is assumed that there is a buffering of the levels of metabolites and ions of other molecules by means of the cell linkages within a particular tissue. Multispecies microbes have been characterized in cocultures in recent times where they exhibit complementary metabolism naturally (Kim et al. 2008) or can be engineered to carry out specific interactions (Zavahir and Seneviratne 2007; Kenny and Balskus 2018). The ability of such microbial groups to participate in metabolic cooperation enables them to carry out activities and utilize environmental resources which they are unable to in their individual cell state. In certain instances, this cooperation does not involve the entire cell colony of a microbial community but rather takes place between specialized cells within the colony. The phenomenon of metabolic cooperation is also seen in biofilms where the signaling molecules secreted by the biofilm’s cells can recruit adjacent cells thus causing the biofilm colony to grow. Channels within the biofilm allow the steady exchange of nutrients, metabolites, and enzymes as well as the expulsion of waste products (Sutherland 2001). The metabolites released by the biofilm also enhance the EPS growth and thus the adhesion of the cells to the substrate and one another. Despite the ubiquitous nature of metabolic exchanges in such communities, its complexity and dynamic nature make it hard to detect metabolite cross feeding and characterization (Ponomarova and Patil 2015). Various alternative approaches to predict interactions among species and to further understand their metabolic networks in their natural habitats are emerging. Of these, the field of Reverse Ecology which emerged around 2007 attempts to gain an understanding of an organism’s ecology directly from its genomic information, while also emphasizing on its

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microbial ecology. This has been seen to be greatly useful in gaining insights into both poorly characterized as well as complex microbial systems (Levy and Borenstein 2012).

1.3.1

Nutrient Exchange in Microbial Communities

Microbial communities rely on the various nutritional interactions among community members to ensure their stability and efficiency of function. The liberation of additional nutrients which result from metabolite cooperation maintains the characteristic diversity of various participants of the cooperation. Often the metabolites released by one species get used as building blocks or energy sources by another species and this can lead to metabolite cross feeding. For example, unique cell-tocell interactions leading to metabolite exchange and gene expression altering of both organisms was seen in a synthetic coculture of Clostridium acetobutylicum and Clostridium ljungdahlii. Here the CO2 and H2 released by C. acetobutylicum are used by the latter for survival and growth (Charubin and Papoutsakis 2019). In addition to bacterial species, reciprocal growth promotion between fungal and bacterial species has also been recorded. Deveau et al. proved this using the fungus Laccaria bicolor S238N which accumulated the disaccharide trehalose in its hyphae which chemoattracted and led to growth promotion in the bacterium Pseudomonas fluorescens BBc6R8 while thiamine produced by the latter enhanced fungal growth (Deveau et al. 2010). The study of nutrient exchange and metabolic cooperation in ecosystems can be carried out by metabolomics-based studies. An investigation in 2011 was carried out cultivating Bacillus megaterium and Ketogulonicigenium vulgare (Zhou et al. 2011). Use of gas chromatography with time-of-flight mass spectrometry (GC–TOF–MS) was used for a metabolomics study of determining the interaction between the two microbes and the exchange of numerous metabolites were observed. Amounts of components such as amino acids, 2-keto-gulonic acids (2KGA), erythrose, guanine, erythritol, and inositol remarkably increased when the two bacteria were cocultured rather than in their single culture stage. Here, it was observed that a mechanism of symbiotic interaction via metabolites in the ecosystem was established. It was also confirmed that the cell–cell communication via metabolic cooperation and intracellular metabolism played a role in determining the population dynamics. It was long thought that metabolite exchange between bacteria occurred by diffusion mainly through the extracellular environment. But recent studies show that nutrient exchange can occur directly by cell–cell connections facilitated by nanotubes. It was confirmed by electron and fluorescence microscopy studies of two distant bacterial species—Acinetobacter baylyi and Escherichia coli—which were seen to reciprocally exchange amino acids and distribute metabolic functions within the microbial community (Samay et al. 2015). Such cross feeding as well as auxotrophy (an organism showing total dependence on the environment for compounds needed for its growth) can take place in

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microbial communities which enable them to survive in resource-poor environments. Often the exchange of such metabolites is costly for the producer and can render a reduction in fitness or growth rate. Those metabolites which do not cause a decrease in fitness—costless metabolites—are reported to be drivers of intermicrobial interactions and stable cooperation. These interactive patterns which can be investigated using genome-scale metabolic models can help design synthetic microbial consortia for agriculture (Pacheco et al. 2019).

1.3.2

Metabolic Cooperation and Signaling Compounds

The microbe–microbe and plant–microbe interactions successfully occur within ecosystems based on a collection of signaling molecules which are involved in a range of inter-microbial and plant–microbe interactions. These components, some of which are produced and released by microbial communities while others are plantderived, can orchestrate various defence associations and symbiotic relationships (Seneviratne et al. 2017a, b). Microbial signaling can also affect factors such as biodegradation, faster growth, increased virulence, avoiding biochemical conflict, etc. and can occur in single or multispecies bacterial communities (Miller and Bassler 2001). Chemical signals released by bacteria (at sufficient concentrations) can also be a result of quorum sensing (QS) or cell-to-cell communication, where the gene expression is regulated in response to the cell-population’s density fluctuations. Such chemical signals which are called autoinducers, the most common of which is acyl homoserine lactones (AHLs), can be produced by Gram-positive as well as Gram-negative bacteria and can help these bacteria communicate or coordinate activities (Badri et al. 2009). The QS phenomenon can regulate a range of physiological activities which include symbiosis, virulence competence, antibiosis, sporulity, biofilm formation, conjugation, etc. (Miller and Bassler 2001). These chemical “dialogs” between plants and microbes occur via a plethora of diffusible molecules produced by both counterparts. Unlike humans who depend on visual and auditory cues, plants rely on the secretion and detection of informationexchanging-chemicals or infochemicals for their communication (Rowe et al. 2018). In the context of plant–microbe interactions both the plants and microbes can act as either the sender or the receiver. This is carried out by a myriad of encoding metabolic pathways instructed by their various genes. The extensive communication which arises from the signaling molecules of plants and microbes play a pivotal role during the different stages of plant growth and development. For example, bacterial and fungal species have the ability to detect plant hosts and produce plant growth regulating substances or phytohormones such as auxins and cytokinins. These have been known to affect cell proliferation, increase water and nutrient uptake by increasing the number of lateral roots and root hairs (Ortíz-Castro et al. 2009). Conversely, plants are able to detect such microbe-derived components and adjust their growth and defence according to the

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microbe encountered. Such communication strategies determine the range of plant– microbe relationship from pathogenesis to symbiosis (Bais et al. 2004; Ortíz-Castro et al. 2009). Such low-molecular weight and volatile organic compounds released by microbes, referred to as microbial volatile compounds (MVCs), can be generated by different biosynthetic pathways. The diffusion of such molecules across membranes enables short- or long-term intercellular connections and can thus act as signaling molecules in a variety of microbial species. As a result, they can also have impacts on the plants in their vicinity either directly or indirectly to trigger plant immunity, growth regulation, or morphogenesis (Seneviratne et al. 2017a, b; Tyagi et al. 2018). One of the early studies on this showed a growth promotion in Arabidopsis thaliana plants triggered by the MVCs 2,3-butanediol and acetoin released by Bacillus subtilis GB03 and Bacillus amyloliquefaciens IN937a (Ryu et al. 2003). In another classic study showing the plant growth promotion as well as biocontrol ability of such signaling molecules, it was seen that the MVCs released by the bacterial strains Bacillus amyloliquefaciens UQ154, Bacillus velezensis UQ156, and Acinetobacter sp. UQ202 successfully inhibited the pathogen Phytophthora capsici and promoted the growth of Arabidopsis thaliana and Capsicum annuum (Syed-Ab-Rahman et al. 2019). Plant root released secondary plant metabolites such as flavonoids and strigolactones have also been seen as important signaling molecules (Steinkellner et al. 2007). Growth responses in lettuce plants (Lactuca sativa L.) were also mediated by cytokinins produced by Bacillus subtilis which also had an antagonistic activity towards Fusarium fungi (Arkhipova et al. 2005). Similarly, auxins such as indole-3-acetic acid (IAA), phenylacetic acid, indole-3-butyric acid (IBA), 4-chlorindole-3-acetic acid, or their precursors are key regulators of plant– microbe interactions (Spaepen et al. 2007). The most commonly occurring of these, IAA, is also able to carry out reciprocal signaling (Lambrecht et al. 2000) as seen in the inoculation and nodule formation of white clover (Trifolium repens) roots by Rhizobium leguminosarum (Mathesius et al. 1998). These and other select examples of low-molecular weight components acting as signaling molecules in metabolic cooperation activities are seen in Table 1.2. Understanding the myriad of molecular associations and the signals they transduce provides a deeper understanding of the underlying mechanisms occurring in the rhizosphere and can contribute to improvements in crop productivity and agricultural sustainability. Further, the progress in molecular signaling research to give an understanding of such plant–microbe interactions occurs in leaps and bounds with its associated developments (Morel and Castro-Sowinski 2013). The current knowledge in microbial signaling, their mechanisms, and the role they play in ecosystem stability has been reviewed by Seneviratne et al. (2017a, b).

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Table 1.2 Examples of role of signaling molecules in plant–microbe interactions

Plant species Centaurea maculosa (spotted knapweed) and Senecio inaequidens (narrow-leaved ragwort) Arabidopsis thaliana

Microbial species Multiple rhizospheric organisms

Bacillus subtilis GB03 and Bacillus amyloliquefaciens IN937a

Arabidopsis thaliana and Capsicum annuum (Capsicum)

Bacillus amyloliquefaciens UQ154, Bacillus velezensis UQ156, and Acinetobacter sp. UQ202

Lactuca sativa (lettuce)

Bacillus subtilis

Trifolium repens (white clover)

Rhizobium leguminosarum

Vigna mungo (black gram)

Rhizobium sp. VMA301

1.3.3

Metabolic cooperation phenomenon Polyploidy leading to change in bacterial diversity Release of MVCs as signaling molecules and growth promotion Release of MVCs as signaling molecules Inhibition of Phytophthora capsici Cytokinin production leading to increased leaf and root fresh weight IAA production in reverse signaling of nodule formation Stimulation of phenolic acid and IAA production

Reference Thébault et al. (2010) Ryu et al. (2003)

Syed-AbRahman et al. (2019) Arkhipova et al. (2005) Mathesius et al. (1998) Mandal et al. (2009)

Microbial Metabolic Cooperation in Agriculture

Despite the universal abundance of metabolic cooperation in microbial communities, their stabilization depends on vital contributing factors. The absence of these supporting mechanisms would lead to an inevitable instability of the relationships and pathways required for efficient intra- and intercellular cooperation. Such factors mainly include (1) ecological and evolutionary forces at work, (2) structure of the microbial environment, (3) horizontal gene transfer, and (4) cellular regulatory mechanisms. These factors play a key role in determining the microbes involved in the cooperation as well as the resulting phenomena with great importance to agriculture. These can result in benefits to crop plants which include but are not limited to biodegradation capability, faster growth and development, increased virulence by a range of antibiotic secondary metabolites (bactericidal and fungicidal activity), and avoiding biochemical conflicts. Outsourcing metabolic functions to fellow members embed each pathway in a specialized microenvironment thus avoiding biochemical conflict (Johnson et al. 2012). One such is the production of phytohormones which

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modulate plant growth and protect them from external or soil-derived pests and pathogens. Plants are diverse beings with many factors affecting their evolution to the current state and further. A fundamental mechanism which brings about this diversification is whole-genome duplication (WGD) or polyploidy which refers to the state of having two sets of chromosomes (Segraves 2017) which can thus lead to the presence of many cytotypes (Thébault et al. 2010). Since genomes direct the phenotype and genotype of living organisms, WGD directly influences the ecology of polyploid lineages (Levin 2002). The increased DNA content in polyploid plants render many genetic effects which shape interacting communities in the plant’s vicinity. Arbuscular mycorrhizal fungi (AMF), fungal pathogens, and bacteria are microbes affected directly by plant genotypes (Hartnett et al. 1993; Lamit et al. 2014). In a study which looked at the effects of such polyploid plants and their various cytotypes on the rhizobacterial community was carried out using the plants Centaurea maculosa (spotted knapweed) and Senecio inaequidens (narrow-leaved ragwort). Here, although microbial biomass carbon content did not significantly change, changes were recorded in bacterial community composition (Thébault et al. 2010). It has been found that bacteria form close cooperative loops within their natural communities, thus benefitting all species involved in a natural community (Freilich et al. 2011). The chemical communication between adjacent organisms assists in interactions which serve many purposes to both the microbes themselves as well as those living within host-associated microbial communities (microbiotas). Having a solid understanding of the various chemical interactions that partake in metabolic cooperation activities can direct engineering of microbes to participate in chemical signaling activities to suit the need (Kenny and Balskus 2018). With the need to understand metabolic corporation and cellular signaling comes the vital need to obtain information on the various interactions between proteins and other small molecules within cells. Such information is increasingly being stored in databases which focus on genomes, phenotypic observations, biochemical interactions, protein binding constants, biological pathways, and biological action of drugs, etc. (Kuhn et al. 2007). Monitoring the metabolic cooperation activities and interrelationships in bacterial communities can be carried out by various direct or indirect methods and modern technological advances. These techniques can assist in employing strategies to improve microbial diversity, soil quality, and thereby crop productivity and fall into four main categories; (1) structural profiling, (2) catabolic profiling, (3) genetic profiling, and (4) comprehensive structural and functional community profiling (Sharma et al. 2011). Various detection methods have been developed and utilized for the analysis of compounds found in relation to microbial communities. Such methods include comprehensive two-dimensional gas chromatography with mass spectrometry component profiling, DNA-based methods, monoclonal antibodies, enzyme-linked immunosorbent assay (ELISA), protein fragment complementation assay (PCA), etc. (Subramaniam et al. 2001; Lévesque 2001; van Elsas and Boersma 2011; Zeng et al. 2013).

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Role of Microbial Communities in Self-Sufficiency

Microorganisms play a vital role in balancing the ecosystem functions and structure, within which their role in plant growth and survival takes a significant position. The relationships between plants and microbes date back to the very origin of these two entities, where soil microbial communities have been reported to determine plant species diversity in natural ecosystems (Mangan et al. 2010). As amply discussed, in an agricultural system, soil fertility and crop production are highly dependent on its resident microbial communities. Immediate or lasting alterations on ecosystem structure and functioning may occur as a result of changes in the composition and activity of such microbial communities. Essentially, the microbial community present in the plant’s vicinity and soil provides nutrients, hormones, and drought and disease tolerance among other benefits for the plant. In addition, microbial communities are capable of adapting to environmental changes such as adaptation to variations in temperature, precipitation regimes, and redox fluctuations (Wallenstein and Hall 2010). These characteristics make microbial communities play an important role in self-sufficiency of agricultural system.

1.4.1

Soil Fertility and Crop Productivity

Soil is a highly complex medium; an ecosystem with multiple abiotic and biotic components. It is not merely a single habitat, but more of a conglomeration of a myriad of minute and microscopic habitats and microenvironments. This biotic complexity and the fact that we cannot look very far into the soil without disturbing it makes soil one of the most difficult ecosystems to study in situ. Disturbances caused due to human activities—especially cultivation, erosion, pollution, and contamination—affect soil habitats, and thus have an impact on the diversity of the soil biota (Mujtar et al. 2019). Sustainable land management methods such as land sharing/sparing, organic agriculture, crop rotation, etc., have been proposed as a unifying theme for current global efforts on combating the desertification, loss of biodiversity, and climate change. However, there are certain limits to those management practices due to the ever-increasing global food demand, particularly in the tropics. Therefore, a domineering need of the hour is the search for methods that sustain the productivity of large-scale conventional croplands even with continuous monocropping (Seneviratne and Kulasooriya 2013). It has been shown that the collapse of microbial communities, specially nitrogen fixers, (mainly due to chemical inputs) leads to reduced plant diversity; mainly because soil microbes play a crucial role in determining plant species diversity (Seneviratne and Kulasooriya 2013). Reduction of soil microbial communities due to chemical inputs and agricultural practices leads to a number of issues which greatly influence sustainable productivity.

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In order to maintain biodiversity, productivity, and sustainability of agroecosystems, developed microbial communities can be directly applied to the soil rather than manipulating relatively less effective plant and animal components to reinitiate sustainability (Seneviratne and Kulasooriya 2013). It is hence important to introduce developed microbial communities into the ecosystem rather than introducing monocultures or multiple cultures of microbial communities. Direct application of developed microbial communities in biofilm mode—the aforementioned BFBFs—has been proved to restore depleted tropical cropland soils, soon after their application, perhaps within 1–2 months, with better yields (Seneviratne et al. 2011). Direct plant growth mediated by endophytes is mostly based on providing essential nutrients to plants and the production and/or regulation of phytohormones (Vinayarani and Prakash 2018). This mostly includes phosphate solubilization activity, indole-3-acetic-acid production, and the production of siderophores. Endophytic organisms can also supply essential vitamins to plants. Furthermore, osmotic adjustment, stomatal regulation, improved uptake of minerals, and modification of root morphology can be listed as other significant effects of endophytes on plant growth (Ryan et al. 2008). Endophytes can also accelerate seedling emergence, promote plant establishment under adverse conditions, and enhance plant growth. Bacterial endophytes have been shown to prevent disease development through endophyte-mediated de novo synthesis of novel compounds and antifungal metabolites. Some of them have the ability to resist antimicrobial compounds. Further, they degrade organic compounds which can have adverse effects on the plant. This natural ability to degrade these xenobiotics is being investigated with regard to improving phytoremediation (Ryan et al. 2008). Similarly, endophytic bacteria available within non-leguminous crops show the ability of biological nitrogen fixation, especially in rice (Vinayarani and Prakash 2018). Such endophytic bacterial genera are well known for their diverse range of secondary metabolic products including antibiotics, anticancer compounds, volatile organic compounds, and antifungal, antiviral, insecticidal, and immunosuppressant agents (Ryan et al. 2008). Such biological molecules can be extracted and utilized for beneficial uses (Selim et al. 2012). Bacterial endophytes colonize an ecological niche similar to that of phytopathogens, which makes them suitable as biocontrol agents. Endophytic microorganisms can have the capacity to control plant pathogens (Ryan et al. 2008; Vinayarani and Prakash 2018). While the biocontrol effect of endophytic bacteria is well known, the mechanisms of biocontrol mediated by endophytes are less well elucidated. Exploitation of endophytic plant interactions can result in the promotion of plant health and can play a significant role in low-input sustainable agriculture applications for both food and non-food crops (Ryan et al. 2008). It is apparent that plant inhabited endophytic microorganisms—either bacteria or fungi—play a valuable role by means of plant productivity. As discussed in previous sections, with the impact of chemical fertilizers and agricultural practices, the diversity of endophytic microbes and their functionality is destroyed. For this reason,

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it is essential to rehabilitate beneficial plant endophytes rather than finding ways to improve crop productivity with the various modern unnatural approaches available.

1.4.2

The Fungal–Bacterial Ratio

Long-term storage of organic carbon in soil is governed by the transformations carried out by fungi and bacteria (Bailey et al. 2002). However, the organic matter degradation pathways preferred by these two major microbial groups differ from each other. Here, a more persistent nature to fungal-mediated carbon storage is prevalent as opposed to the labile nature of that mediated by bacterial biomass. Fungi can use organic substrates more efficiently than bacteria (Schindlbacher et al. 2011) and they are dominating degraders of plant components and generally, fungal biomass is found to be greater than bacterial biomass in agricultural soils (Zelles et al. 1995). The fungal diversity usually reaches the highest level near organic material such as roots (Powlson et al. 2012). Thus, with increased fungal abundance, the availability of organic matter to the crops is increased than with bacterial communities. It is frequently assumed that high soil fungal–bacterial (F/B) ratios are indicative of a more sustainable agroecosystem and can also be applied to determine the organism group more active in plant residue degradation. For example, increased F/B ratios have been recorded in extensively managed grasslands (Vries et al. 2006). Therefore, a solid understanding of the F/B ratio and soil dynamics with respect to changes in environmental factors enable prediction of the carbon storage potential of the soil, longevity of stored carbon in soil, and the results of added carbon to soil. In addition, F/B ratio may also be affected by other factors such as presence of toxic metals (Tobor-Kaplon et al. 2006). But, most of these factors are related to nutrient availability. Plants and soil shape soil microbial communities through a complex sequence of interactions. Plants, through their exudates, and soil, through its chemical and physical characteristics, can be considered to be the main determinants of soil microbial community structure (Garbeva et al. 2004). Bittman et al. (2005) observed a decreasing fungal biomass as a consequence of the application of manure and fertilizer. Inorganic nitrogen fertilization has been reported to reduce the F/B biomass ratio, while organic matter with a high C/N ratio stimulates fungal growth and thus increases the F/B ratio (Vinten et al. 2002). Therefore, higher F/B biomass ratios are indicatives of a more sustainable agroecosystem with a lower impact on the environment, in which organic matter decomposition and N mineralization dominate the supply of plant nutrients for crop growth (Vries et al. 2006), promoting self-sufficiency of agricultural ecosystems.

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Response to Changing Climate

It is a well-established fact that changes in climatic conditions, such as increasing temperature, occurrence of heat waves, etc., can have a detrimental effect on crop production and hence threaten the food security of people worldwide. Over the decades, changes in climatic conditions have been accelerated mainly due to anthropogenic activities. Not surprisingly, some agricultural practices also contribute to this alteration of environmental conditions. Use of agrochemicals to increase crop production is one way of adding unwanted substances to the environment, which eventually contributes to the emission of greenhouse gases. These harmful practices can be reduced if microbial communities are used wisely in agricultural activities for vital approaches of improving soil fertility and crop production. There are evidences which prove that nitrogen and carbon emission and leaching from soil can be reduced with the effective use of mutualistic microbial communities (Bakker et al. 2012). As discussed in the previous sections, microbial communities are capable of increasing soil and plant health by increasing the efficiency of plant resource uptake as well as plant tolerance of abiotic (salinity) and biotic stress (pathogens). Thereby, the use of microbial ameliorates in the agricultural field has the potential for significantly decreasing synthetic fertilizer application. Moreover, in microbial communities the performance of cell-to-cell communication via quorum sensing allows resuscitating cells to break the dormancy of other dormant cells (Lennon and Jones 2011). Some beneficial microorganisms get dormant to avoid stressed environmental conditions. Breaking of cell dormancy of the dormant microorganisms helps to improve the diversity of the system. Eventually, these processes contribute to strengthening the relationship between agrobiodiversity and ecosystem functioning (Langenheder et al. 2010), which eventually leads to ecosystem sustainability (Seneviratne and Kulasooriya 2013). Therefore, it is evident that microbial communities can play a major role in maintaining the self-sufficiency of agricultural systems. Use of novel technologies in the field of microbial biotechnology may also be capable of increasing the efficiency of microbial activity, in order to enhance the soil and plant health.

1.5

Challenges Faced in Sustainable Agriculture and Future Prospects

As amply highlighted in the preceding sections, microbial communities have an enormous potential to be used in agricultural settings in a sustainable manner with minimal harm or deleterious effects on the environment. Yet the use of any approach would not maximize its beneficial effects if it were not to be used in a well-studied manner.

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Measurement of Agricultural Sustainability

With its multifaceted dimensions, sustainability in agriculture is a complex concept with varied viewpoints on its measurement of success by different scholars. Often the decision if an approach or result is sustainable depends on the analyst because it is a dynamic concept which depends on the location and situation. Despite the inability to precisely measure sustainable agriculture, the selection of specific parameters or criteria makes it possible to ascertain whether a certain trend is rising, declining, or remaining steady (Hayati et al. 2010). It has long been known that changes in macroorganism composition of an ecosystem determine its rate of change. However, it has not been easy to ignore the contributing role played by the same ecosystem’s microbial community in shaping its existence. Both macroorganisms and microorganisms are primarily responsible for the biodiversity of an ecosystem—may it be genetic, functional, or taxonomic biodiversity—and help understand the ecological importance of species in a community (Zak et al. 1994; Laureto et al. 2015). With perturbations to an ecosystem, most microbial groups are sensitive but not immediately resilient (rate at which microbial composition returns to its original composition following a disturbance) or resistant (degree of remaining unchanged after a disturbance) to changes. Certain communities can also display functional redundancy where they display different functional abilities under different conditions. Such resilience, resistance, or redundancy occurs with the exception of rapid evolutionary adaptation which occurs due to horizontal gene transfer, where sensitive microbes gain the ability to return the ecosystem to its original condition despite disturbance. The compositional variations of microbial communities thus directly affect ecosystem processes and can be used as an indicator to predict such changes (Allison and Martiny 2008). In agricultural settings, practices such as crop rotation, organic amendments, microbial inoculants, and tillage can create a shift in the structure and diversity of its microbial populations which consequently can alter its soil quality. Since the quality of the soil determines the environmental quality, food security, and economic viability of an environment it can be justly identified as a potential indicator in monitoring sustainable land management (Sharma et al. 2011). Soils are rich ecosystems harboring a multitude of living organisms. Thus, its inherent microbial community’s characteristics, diversity, function, and structure as well as the various interrelationships they hold play a crucial role in determining the soil quality, which in turn shapes its respective ecosystem. The study of soil quality can be carried out quantitatively or qualitatively yet possess a challenge as it depends on land management in a particular agroecosystem or agroclimatic condition (Sharma et al. 2011). For example, cover cropping—a beneficial approach to ensure soil health in agricultural ecosystems—is known for sustaining agricultural productivity and is recommended as a technique which should be integrated into modern agricultural practices. Although the impacts of such cover crops can be evaluated quantitatively, it largely depends on site-specific factors, the crop species, and tillage practices (Daryanto et al. 2018).

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Challenges Faced and Future Prospects

As well-documented, the use of any technology for agricultural productivity needs to be thoroughly studied with respect to the environment it is applied to. A blanket rule would by no means answer questions relating to all forms of crop and ecosystems. A comprehensive evaluation of the microbes existing in an ecosystem and a risk assessment of its effects on the soil microbiota is a necessity. But this alone may not be sufficient when the assessment of pesticide ecotoxicology is done by one or few methods. This need for standardized methods has also been recognized by the European Food Safety Authority (EFSA). One such way of overcoming this problem could be the development and use of innovative microbial markers—biomarkers which highlight the effect a particular pesticide has on a microbe/microbial population (Thiour-Mauprivez et al. 2019). Often the challenge is the translation of an approach from its theoretical aspects to putting it into practice. It has been proposed that goal-oriented concepts based on agronomy and management models can bridge this gap (von Wirén-Lehr 2001). Studies have been conducted in comparing synthetic community approaches in modeling dynamics to the species interactions which occur in natural communities. Here it was seen that while some community dynamics between two communities for some species had common trends, there can be discrepancies among other communities between the synthetic and natural environments (Yu et al. 2016). The dynamic nature of microbial consortia limits the ability to simultaneously control the composition and function of microbial communities. The use of microbes to solve problems in agricultural settings has thus initiated a focus on synthetic biology approaches which facilitates coordination on a population level to control the stability and dynamics of ecosystems. The screening and prediction of community behavior in such instances can be further enhanced by novel experimental and computational tools as well as metabolic models. Such partnerships of synthetic biology and metabolic engineering have seen success in bioprocessing applications (Shong et al. 2012). These approaches lead the way to synthetic microbial consortia being used in agricultural settings in a well-suited manner. Most biotechnological applications used currently rely on genetically engineered monocultures or mixedcultures whose composition is partially known. Thus, the massive potential of the “microbial ecological power” should not be overlooked and hence propositions have been made to capitalize on spatially linked microbial consortia (SLMC) to expand the range of possible microbial combinations, their applications, and productivity (Ben Said and Or 2017). While many age-old agricultural practices are incorporated into modern agriculture with improvements, there are also many novel technologies entering this sphere. Of use here is the growing branch of agriculture referred to as agrigenomics which combines the aspects of genomics, traditional plant breeding, and phenotypic markers. Soil and crop management strategies (SCMs) as well as some innovative approaches such as nanotechnology have the added benefit of combating challenges of environmental security and sustainability (Shah and Wu 2019; Pandey 2018).

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Such multi-omic approaches derive extensive amounts of data, and hence a more multivariate approach is required to derive a complete picture of biological interactions, a clear image which often fails to emerge (Meng et al. 2014; Bersanelli et al. 2016; Vilanova and Porcar 2016). Studying the complexities of microbial communities in this context is hence shifting the paradigm of sustainable agriculture.

1.6

Concluding Remarks

Microbial communities have been the stronghold of plant–microbe interactions in all ecosystems irrespective of the fact of them being under human influence. Their role in agricultural settings cannot be overlooked. The varied plant–microbe interactions in such settings can be spread over a spectrum of relationships which range from pathogenicity to symbiosis to mutualism and other direct and indirect relationships. Such relationships bring about multiple metabolic cooperative strategies and connections which can benefit one, both, or all members involved in the relationship where these members may belong to microbial groups as well as plants. Recent research which has exposed the human and animal health risks associated with some bioinocula highlight the fact that microbial strains need to be chosen for the optimum result. Renewed interests with technological modifications on age-old technologies have brought in a fresher insight into agricultural sustainability. Agricultural microbiology is constantly being developed bringing together the fundamental knowledge from the fields of general microbiology, microbial ecology, agricultural biotechnology, genetics, molecular biology, evolution of symbiotic interactions, etc., and thus builds a strong basis of microbe-based sustainable agriculture (Tikhonovich and Provorov 2011). In addition, green approaches such as harnessing valuable bioactive chemicals from fruit processing wastes contribute to this (Banerjee et al. 2017). Amongst such current technologies, reinstating the lost biodiversity in an ecosystem using developed microbial biofilms in a more natural manner (Seneviratne and Kulasooriya 2013) has gained much attention, because synthetic microbial communities may adversely affect the soil environment. Biofilm technology has further proven extensive applicability with improved performance in sustainable agriculture through a variety of approaches such as biofertlization, drought tolerance, biocontrol, etc. It is hence apt to focus on efforts to develop newer varieties of biofilmed inocula, in particular BFBFs, and to also enable their commercialization. This will no doubt make it more convenient to transfer the benefits of this technology from the laboratory to the farmer as an end-user. An added benefit would be products with qualities of long shelf life and ease-of-use which can act as saviors in rural communities as well as agricultural settings affected by environmental adversities. Use of more modern approaches such as metabolomic studies of microbial interactions will enable the study of interactions previously unknown and will help determine microbial populations which together with other populations can render an outcome more efficiently than when they are alone. This can be done in unison

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with microbial modeling of synthetic and natural microbial consortia. Such efforts should also be focussed on bioprocessing applications and metabolic engineering to enhance and increase the use of new technologies in achieving increased crop yields with minimal harm to the environment. There is unfortunately a great disparity in the standardization of methods used and quality aspects between developed nations and developing nations. This also gives rise to adulteration, low-quality products, dearth of technological advancements, delays in finding solutions to combat a problem, etc. Approaching the sustainability aspect on a more international scale with a knowledge transfer between countries in close proximity and/or similar environments will enable combatting adverse effects in a more efficient manner. Bringing together experts in scientific, agronomic, management, finance, computer-modeling, legal, etc. fields in a goal-oriented manner can help achieve needed outcomes more successfully. This will also assist in changing or adapting existing approaches when and as needed to give long-term viability. As with any new technology used, one cannot underestimate the need for careful screening and evaluation of microbes before application on a mass scale in the field. The complexities of chemicals are further deepened by the different roles they play in biological systems. Their numerous interactions as well as their phenotypic effects, both known and yet unknown to humans, lead to a better understanding of their purpose of presence. Thus, a major challenge to overcome is finding the gentle balance between controlled culturing of microorganisms, multi-omic approaches, and other emerging newer techniques. The novel, environmental-friendly solutions constantly being explored will no doubt continue to propose alternative solutions to current agricultural issues. The integrated approaches required to arrive at these points of success will constantly need to be reviewed and adapted to suit the need of the hour and issue prevalent. Irrespective of the field of study, a solid commitment to working towards agricultural sustainability will continue to be the responsibility of all alike.

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Chapter 2

Symbiotic Interactions of Phototrophic Microbes: Engineering Synthetic Consortia for Biotechnology Derek T. Fedeson and Daniel C. Ducat

Abstract Natural microbial communities consist of assemblies of species possessing distinct metabolic capacities. Diversification within the consortia leads to the division of labor between species, whereby the global population exhibits functional capabilities that are possessed by only a fraction of its members. Furthermore, community diversity is also associated with higher bioproductivities and robustness compared to microbial “monocultures”. In this review, we highlight both natural and engineered interactions between photosynthetic microbes and other organisms, with an emphasis on learning design principles of microbial communities through the process of building them from the “bottom up”. Rational design of relatively simple microbial communities is likely to substantially improve our understanding of much more complex natural consortia that have important ecological significance. Furthermore, a deeper understanding of effective design principles of microbial communities could enable the application of light-driven microbial cultures for a variety of environmental and biotechnological goals. Keywords Photosynthetic microbes · Consortia · Cocultures · Ecology

2.1

Introduction

Microbial communities comprise a substantial proportion of the biomass on Earth (Bar-On et al. 2018) and underlie the health and functioning of many different ecosystems. Complex microbial communities contribute to turnover of a number of critical global biogeochemical cycles, including nitrogen, oxygen, carbon, sulfur, D. T. Fedeson Charles River Laboratories (CR-MWN), Mattawan, MI, USA D. C. Ducat (*) MSU-DOE Plant Research Laboratories, Biochemistry and Molecular Biology Department, Michigan State University, East Lansing, MI, USA e-mail: [email protected] © The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2021 G. Seneviratne, J. S. Zavahir (eds.), Role of Microbial Communities for Sustainability, Microorganisms for Sustainability 29, https://doi.org/10.1007/978-981-15-9912-5_2

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and phosphorous (De Roy et al. 2014). Furthermore, the composition of local microbiomes is increasingly recognized to have direct and substantial impacts on the health of multicellular plants and animals (Mueller and Sachs 2015). Indeed, the vast majority of microorganisms live within multispecies communities, yet we have relatively limited knowledge about microbial interactions within these networks and how these interactions shape community properties and ecosystem functions (Chodkowski and Shade 2017). The majority of microbiology research conducted in the twentieth century focused upon axenic (single species) cultures (Jessup et al. 2005). Reductionist microbiology has led to a number of scientific breakthroughs and valuable outcomes, but has also necessarily isolated microorganisms from their natural context, instead emphasizing their behaviors within a test tube (Little et al. 2008). A deeper understanding of the complex interplay of interspecies microbial interactions and how they contribute to properties of productivity and robustness will be necessary if we are to leverage consortia advantages towards new sustainable biotechnologies. Within the past two decades, powerful new methodologies have emerged that facilitate systems-level approaches to study microbial community ecology. These methods include improved genomic and transcriptomic sequencing, mass spectrometry-based metabolomics, and proteomics (Franzosa et al. 2015). The development of such technologies has paved the way to approach some of the most ecologically and bioindustrially relevant microbial communities that are involved in everything from human health to agriculture (Tringe and Rubin 2005). Yet, while these technologies have greatly expanded our capacity to inventorize the total species and reactions within microbial consortia, the complex datasets they generate do not illuminate the structure of these communities. These deficiencies highlight the need to distill generalizable principles that describe fundamental organization of disparate communities. Identification of common themes of microbial interaction that translate across numerous consortia is needed in order to more fully understand consortia behaviors. Furthermore, this knowledge can provide the basis of design principles that may inform the engineering of artificial multispecies consortia. The ability to customize microbial communities or redesign existing microbiomes represents a new horizon in medicine, agriculture, and bioindustry (Costello et al. 2012; Rollié et al. 2012; Gopal et al. 2013; Song et al. 2014b; Lindemann et al. 2016). For example, extensive efforts are currently being directed to design microbial supplements for amending soils, with the goal of influencing consortia composition and improving plant growth and resilience to stress (Busby et al. 2017). In this chapter, we summarize different approaches that have been used to study microbial communities and interspecies interactions. To productively constrain our discussion within this broad field, we will focus upon natural communities dominated by phototrophic microbes (especially cyanobacteria), and emphasize biotechnological applications relying on these microbes. We first briefly summarize a couple of representative natural photosynthetic microbial consortia of ecological significance. This includes interactions between photosynthetic microbes within the open ocean that contribute a large proportion to global biogeochemical cycles and

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plant-cyanobacterial symbioses that can influence agricultural productivity. A discussion of these natural communities will also highlight features evident within natural microbial consortia (e.g., high productivity, robustness to environmental perturbations, resistance to invasive species) that are lacking in many current bioindustrial technologies. Yet, the difficulty of dissecting the interaction networks within these natural communities also illustrates current limitations in our ability to uncover fundamental design principles that underlie desirable traits within these communities. As an alternative approach for understanding microbial consortia, we will then review the emerging field of synthetic microbial ecology, which advocates the use of a “bottom-up” approach for understanding microbial consortia. Synthetic microbial ecology is a term that broadly describes all rationally designed ecosystems created by assembling two or more defined microbial populations in a well-characterized and controlled environment. By organizing a relatively small number of defined microbes into a consortium, synthetic ecology allows for the creation of greatly simplified interaction networks relative to the highly complex and integrated interactomes of natural communities (Jessup et al. 2004). Furthermore, because the communities are built from the bottom up, member species with established molecular toolkits can be selected. This enables the use of genetic manipulation to systematically dissect the functions of a given microbe within a larger community. In this way, synthetic microbial ecologists are attempting to distill complex interaction networks into broadly applicable theoretic principles useful for constructing predictive models for microbial communities (Prosser et al. 2007). We will discuss some applications for synthetic consortia, summarize their current limitations, and provide perspectives on the progression of this field.

2.2

Natural Photosynthetic Microbial Communities of Ecological and Technological Relevance

Photosynthetic microbes are found in many symbiotic interactions across most ecosystems, and cyanobacteria appear especially prolific in their capacity to form symbiotic associations with a wide variety of both prokaryotic and eukaryotic partners. Indeed, cyanobacteria have well-documented mutualisms across many kingdoms, including plants, mosses, fungi, sponges, dinoflagellates, diatoms, and other bacteria (Adams 2000; Usher et al. 2007). Such symbiotic interactions can be with a single other species, or, as is more common in most environments, a collective of other organisms. Cyanobacterial symbiotic interactions can be largely categorized around their capacity to fix atmospheric carbon (CO2) or nitrogen (N2) and provide them in bioavailable forms to associated species within their communities. Below, we discuss two representative symbiotic relationships involving cyanobacteria that revolve around their capacity to either provide fixed carbon or fixed nitrogen for partner species.

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Cyanobacterially Driven Marine Ecosystems

Marine microbial communities are responsible for as much as half of the global cycling of carbon, nitrogen, sulfur, phosphorus, as well as many important micronutrients (Fuhrman et al. 2015). Such communities can be composed of bacteria, archaea, protists, fungi, and their respective viruses, which form the foundation of the food webs comprising larger marine lifeforms (Sherr and Sherr 2002). In many marine environments, primary production is mainly attributable to prokaryotic phototrophs, which in turn are dominated by the large cyanobacterial groups, Synechococcus and Prochlorococcus (see Table 2.1 for a list of all organisms discussed). In much of the surface waters of the open ocean, free-living Prochlorococcus are the most abundant organisms in both number and total biomass. Due to the large area of this environment, these cyanobacteria are estimated to be the most abundant photosynthetic cell type on Earth (Partensky et al. 1999). As such, it has been estimated that Prochlorococcus accounts for ~4 gigatons of fixed carbon annually, a number equivalent to the primary productivity of all croplands (Biller et al. 2015). Prochlorococcus is a broad bacterial group that descends from the marine lineage of Synechococcus and is classified partially by some unique features that distinguish it from other cyanobacteria. Prochlorococcus is unusually small for a photosynthetic prokaryote (typically 300 heterotrophic bacteria isolated from marine environments indicated that the majority of these heterotrophs positively influenced cyanobacterial growth, suggesting that mutualisms may dominate autotroph/heterotroph relationships in these environments (Sher et al. 2011). Prochlorococcus/SAR11 interactions may occur against a background of other oceanic microbes, yet some estimates suggest that as few as 0.01–0.1% of these marine species can be cultured in the lab with conventional approaches (Connon and Giovannoni 2002). These complex networks defy current metagenomics and bioinformatics approaches to disentangle and assign roles to individual members within the community (Temperton and Giovannoni 2012; Zengler and Palsson 2012), demanding the development of new approaches to understand such communities at a systems level (Kazamia et al. 2016).

2.2.2

Plant-Cyanobacterial Symbioses

Cyanobacteria have a rich history of symbiotic interactions with many plants, and are particularly notable for their mutualistic relationships with an evolutionarily wide

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range of plants in the green lineage, from Bryophytes (e.g., hornworts, mosses), to ferns, to more recently evolved angiosperms (Usher et al. 2007; Bergman et al. 2008). Many of the most tightly integrated symbiotic interactions are formed between the widespread, terrestrial cyanobacterial genera, Nostoc and Anabaena. Species within these genera are often capable of nitrogen fixation and form differentiated cellular structures called heterocysts that protect nitrogenases from inactivation by oxygen (Zhang et al. 2006). These traits are important because the capacity to provide a source of fixed nitrogen is a core feature of most cyanobacterial symbioses with plants. In addition to providing nitrogen, cyanobacteria can perform a number of other functions that promote plant health and productivity, including secretion of antibiotics that discourage plant pathogens and improvement of soil fertility (Dodds et al. 1995; Adams 2000). As plant–bacterial interactions are a focal topic of other chapters of this book, we do not focus upon this topic at length here, (interested readers are directed to excellent reviews; Adams 2000; Adams et al. 2013; Bergman et al. 2008; Rai et al. 2000), but instead provide a brief discussion in the broader context of the study of microbial communities. Unlike the symbiotic interactions between cyanobacteria and heterotrophic bacteria within marine habitats, some of the best-studied examples of plant– cyanobacterial interactions have a high degree of structural definition. Such mutualistic interactions are often initiated by the release of diffusible signals (e.g., hormogonia inducing factor, HIF) from nitrogen-starved plants, where these signals stimulate differentiation of nearby cyanobacteria into infective stages (i.e., hormogonia; Meeks and Elhai 2002). Hormogonia development involves structural changes and the expression of motility genes that allow cyanobacterial filaments to migrate towards the plant, often leading to invasion and colonization of predefined plant cavities, open stomata, or uptake as intracellular endophytes (Rai et al. 2002). Following colonization, interspecies signaling pathways direct further differentiation of cyanobacteria, often leading to enhanced heterocyst formation and improved nitrogen fixation capabilities. In this way, the cyanobiont becomes capable of increased secretion of ammonium or other nitrogen-containing compounds for the benefit of the host plant. “Loose associations” between plants and cyanobacteria are also widespread, where cyanobacteria play important roles in the broader microbial community in rhizosphere surrounding plant roots, or where cyanobacteria grow epiphytically on plant leaves or other surfaces. In return, the plant provides several benefits for cyanobacterial partners. In most cases, the plant host can become the primary source of carbon for the cyanobiont, secreting carbohydrates into a localized space, or by general secretion of diffusible organic carbon compounds in the broader vicinity of plant structures. For example, it is estimated that many plants secrete a substantial proportion (up to 20%) of the total carbon they fix through the roots, where it can support the growth of nearby microbes (Bais et al. 2006). Cyanobacteria tightly associated with plants can gain other advantages due to the environment that is provisioned by the plant, including supply of additional nutrients (Rai et al. 2000), and protection from external environmental stresses, such as desiccation (Adams 2000). For example, in one of the better studied interactions between the cyanobacteria Nostoc azollae and the

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free-floating aquatic fern Azolla, the cyanobacterium is housed in a dorsal leaf cavity where it is fed carbohydrates and other nutrients. Nostoc azollae in turn provides the host plant with sufficient nitrogen to promote its rapid growth even in relatively nitrogen depleted waters (Adams et al. 2013). This symbiotic interaction is of major agronomic significance, particularly in the cultivation of rice, as Azolla is widely used as a traditional “green manure” for fertilization of crop species (Vaishampayan et al. 2001). Despite a more detailed understanding of some molecular mechanisms of cyanobacteria–plant interactions, these relationships remain difficult to study and relatively poorly understood. In many cases, the coevolution of the cyanobiont and host has been extensive, leading to the development of complex networks of metabolic exchange and signaling molecules. Many plant-derived HIF factors are unknown, while cyanobacteria also employ a range of anti-hormongonia factors (Liaimer et al. 2015) that also are relatively poorly understood. Once in an established mutualistic interaction, the network of signals exchanged is likely extensive but largely uncharacterized. Efforts to disentangle these networks are sometimes complicated by the limited ability to culture partner species independently, and underdeveloped molecular toolkits. As an example, cyanobionts are vertically transmitted in the Nostoc-Azolla mutualism. This means that the association between partners is extremely long-lived and stable across generations, to the extent that it is debatable if de novo infection occurs in a natural context, and if freeliving cyanobacteria can grow independently (Adams et al. 2013). While this level of stability would be desirable to replicate in engineered microbial interactions, it renders natural mutualisms with this level of interdependency difficult to dissect.

2.3 2.3.1

Promise and Current Limitations of the Application of Synthetic Microbial Communities Synthetic Microbial Ecology and Microbial Ecology Theory

Synthetic microbial ecology offers an alternative approach to study fundamental questions concerning microbial interactions and to examine how local interactions between microbes can lead to complex higher order patterns at the population level. Synthetic microbial ecology uses simple artificial communities that retain features of natural microbial communities, but which display greatly reduced network complexity in terms of the number of interacting species and the degree of connectivity between species (Momeni et al. 2011). Synthetic microbial communities are typically established between experimentally tractable organisms that can be selected or engineered to interact through defined pathways. The ability to construct ecologies composed of model organisms can be beneficial for a variety of reasons including the short generation times, small genomes, advanced genetic toolkits, and capacity to

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freeze populations for evolution studies. There are, of course, inherent tradeoffs between the level of control over such artificial systems and the realism of these platforms to natural microbial communities (Fig. 2.1). Yet, it is recognized that the field of microbial ecology currently has limited theories that can be used to predict the behavior of populations (Prosser et al. 2007; Widder et al. 2016), and artificial communities are increasingly regarded as an important bridge between abstract mathematical models and the complexity of natural consortia. For some of these reasons, the last decades have seen a steady rise in the use of synthetic microbial communities as a method to study fundamental questions related to the structure and function of ecological networks (Jessup et al. 2005). In recent years, the study of synthetic microbial ecologies has provided a number of useful platforms for the study of a variety of variables known to influence natural microbial consortia (De Roy et al. 2014; Jessup et al. 2004; Prosser et al. 2007; Fig. 2.1). Natural consortia can be composed of hundreds to thousands of species that interact through the exchange of (often unknown) metabolites and signaling molecules, yet despite these intricate features, such communities display a surprising persistence and resilience in the face of environmental perturbations. This trait is commonly referred to as robustness, or the ability of a community to maintain its functional and structural integrity in the face of fluctuating environmental and biotic conditions. In previously discussed examples, the Azolla-Nostoc mutualism can persist through numerous generations (Adams et al. 2013), while Prochlorococcus-dominated communities in the open ocean display a surprising degree of regularity in composition from year-to-year, even cycling through predictable, seasonally driven states that maintain key features at the population level (Malmstrom et al. 2010). One core ecological theory is that higher diversity contributes to increased community stability; robustness is derived in part by diversity and by redundancy of functions divided among multiple community members (Ives and Carpenter 2007; McCann 2000). These theories are supported by studies that used a recombinatorial approach to assemble microbial communities with a variable number of phototrophs, heterotrophic bacteria, and predators, finding that community-level features (such as total CO2 flux or biomass production) became more reliable with increased species diversity (McGrady-Steed et al. 1997; Naeem and Li 1997). Other studies have emphasized the role of spatial structuring in promoting community stability. For example, multiple synthetic microbial systems for studying predator-prey interactions have been developed and examined for conditions that influence the rate of extinction of one or more partners (Bohannan and Lenski 2000; Kerr et al. 2002). In one notable example, artificial communities of protists were examined for stability under homogenous environments, or under conditions where the same total population size could become subdivided into connected, but locally differentiated microcosms (Holyoak and Lawler 1996). The results indicated that the heterogeneous environment could substantially stabilize the artificial microbial community, providing evidence in support of metapopulation theories that had primarily been examined in mathematical models (Hanski and Hanski 1998). Similarly, a spatially structured environment can also increase the resilience of

Fig. 2.1 Study of microbial ecology at different levels of abstraction. Natural microbial communities are frequently composed of dozens to hundreds of different microbial species, many of which may have coevolved in the given ecosystem over many generations. Direct (solid lines) and indirect (dotted lines) interactions comprise a complex network between species. Natural environments also display highly irregular physical and chemical properties, which dynamically shift over time. Different degrees of reductionism have been used to disentangle the complexities of natural systems. Mathematical theories and

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computational models represent the most abstracted field of research; including low-resolution population-based models, metabolic network models, and individual-based simulations (Song et al. 2014a). Synthetic microbial consortia are more complex than pure monocultures, consisting of two or more microbes that interact through defined pathways. Although other emergent interactions (red dotted lines) are likely to arise between species, the networks are regarded to be much less tightly integrated, and the nature of such interactions can be probed through genetic approaches generally not available during the study of natural ecologies

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cooperative behaviors in microenvironments that contain noncooperating individuals (Doebeli and Hauert 2005). In a homogenous environment, cooperative behaviors that benefit neighboring species but which incur a fitness cost upon the individual (e.g., secretion of a metabolite that requires investment of biochemical resources) are often counter-selected, since non-cooperating community members can reap public benefits without the costs of contributing. Both theoretical and experimental evidence using synthetic microbial consortia have demonstrated that structuring microbial partners into localized communities can stabilize cooperative behavior (Kim et al. 2008; Chuang et al. 2009; Waite and Shou 2012; Allen et al. 2013; Momeni et al. 2013; Kelsic et al. 2015; Pande et al. 2016). Briefly, when the exchange of goods between partners is partially restricted to localized environments (e.g., within flocs or isolated colonies), isolated populations dominated by non-cooperative individuals have weak positive feedback loops, while nearby micro-communities dominated by cooperators can have robust positive feedback and relatively high total growth rates. The above examples serve to demonstrate how the simplified composition and increased molecular tools of synthetic microbial consortia enable testing of fundamental theories of microbial ecology. Interested readers are directed to several excellent reviews for additional information on synthetic microbial ecology (Jessup et al. 2004; Prosser et al. 2007; Kazamia et al. 2012a; De Roy et al. 2014; Widder et al. 2016).

2.3.2

The Biotechnological Potential of Synthetic Consortia

As with the academic literature in microbiology, the majority of current bioindustrial technologies rely on microbial monocultures, although polyculture offers several potential benefits. In particular, if the high metabolic efficiencies and robustness commonly observed in natural consortia could be replicated in synthetic microbial communities, it would have considerable implications for a wide array of industrial, medical, and environmental applications (Goers et al. 2014). Although one common conception in synthetic biology is that improved genetic tools will allow us to reprogram a target biological chassis (e.g., E. coli) for any desired output, many ecological examples argue that mixed communities should typically outperform a single species (no matter how extensively engineered) in terms of total bioproductivity and robustness. The concept of biological division of labor is chief among the reasons that increased bioproductivity can be observed in consortia (Brenner et al. 2008; Werner et al. 2014; Hays et al. 2015; Lindemann et al. 2016). Individual members in a complex community adopt specialized roles, allowing niche differentiation and functional complementarity that can enable more efficient resource utilization (Savage et al. 2007). This is reflected in higher bioproductivity yields (e.g., total biomass) from communities compared to populations containing one species, an observation that also applies in rationally designed systems (Eiteman et al. 2008;

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Shong et al. 2012). Indeed, the improved efficiency of networks containing specialists is a core tenant of biological systems at other scales, including intracellular compartmentalization (Chaijarasphong and Savage 2018), tissue differentiation in multicellular organisms (Ispolatov et al. 2012), and even within social economic theories (Werner et al. 2014). Furthermore, compartmentalization of metabolic reactions across distinct species can mitigate constraints imposed by trade-offs between different objectives, where increased efficiency in one objective (e.g., metabolic reaction), comes at the cost of another. For example, different enzymes may compete for a common pool of biomolecules (e.g., ATP, NADH, or other precursors and cofactors) and inter-enzyme competition (even between enzymes within a simple, linear metabolic pathway) can result in the accumulation of intermediates and/or constraints in the total flux through desired metabolic steps (Lindemann et al. 2016). In other instances, incompatibilities between one metabolic pathway and another can essentially preclude their simultaneous operation. One example of this is represented by attempts to produce hydrogen gas by using reductant from oxygenic photosynthesis: hydrogenase enzymes are highly oxygensensitive, generating many complications when both processes are confined within the same cell (Ghirardi 2015; Posewitz 2018). Similarly, incompatibilities in metabolic regulation have made it difficult to engineer a single heterotrophic microbe that can efficiently utilize all major sugars released from the hydrolysis of lignocellulosic materials (Eiteman et al. 2008; Minty et al. 2013). Robustness of natural systems is another feature that is particularly important for biotechnological applications where environmental conditions cannot be strictly controlled. One application where this is the case is in the scaled cultivation of algae and cyanobacteria for the production of fuels, polymers, and other biologics. Algal farming requires areal scaling of the surface area to expand the available input light, which complicates the design of economically feasible enclosed photobioreactors, especially for the production of commodity goods (Ducat et al. 2011; Chisti 2013). By contrast, the open systems that are deemed more realistic (Sheehan et al. 1998; Chisti 2007) make algal cultures vulnerable to invasive species and largely preclude the possibility of tight environmental control (e.g., temperature; Gupta et al. 2015). Any other biotechnological applications that require release into natural environments (e.g., the application of soil microbes to improve crop yields; Chaparro et al. 2012), will also face the challenge of obtaining a predictable output under highly variable biotic and abiotic conditions. Most microbial species are not sufficiently robust to be used in a monoculture approach for applications that are exposed to natural environmental fluctuations. Among the largest problems of scaled cultivation of algae and cyanobacteria is the high rate of “pond crashes” caused by invasion of a foreign microbe or virus (Smith et al. 2010; Wang et al. 2013; Carney and Lane 2014). By contrast, natural ecosystems with diverse members can be described as reaching a “climax” steady state, where multiple stable equilibria can be reached following a perturbation, helping to minimize variation and invasion by foreign species (May 1977; Law and Daniel Morton 1996). If effective ecological principles can be identified and applied to

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synthetic consortia, higher productivities and “self-regulating” behaviors should be theoretically possible to engineer for biotechnological applications.

2.3.3

Synthetic Cocultures for Photosynthesis-Driven Bioindustry

Given the improbability of maintaining axenic ponds of cyanobacteria or algae, increasing focus is being placed on identifying suitable partner species that will improve the productivity or stability of the culture. Many of the current efforts involve prospecting for heterotrophic bacteria which increase total culture yields. As an example, co-inoculation of a bacterial species (Brevundimonas sp.) that was isolated as a contaminant of algal cultures, with Chlorella ellipsoidea resulted in up to three times greater algal growth than that of C. ellipsoidea alone (Park et al. 2008). There are many similar examples (Amin et al. 2009; Natrah et al. 2014; Cho et al. 2015), and microbial species that promote growth of cyanobacteria and algae need not be isolated from environments where they grow in proximity to these phototrophs (Hays et al. 2017; Tandon and Jin 2017). The fact that species that do not naturally coexist with a given phototrophic microbe can also enhance growth in coculture suggests that there may be generalizable pathways by which heterotrophs perform beneficial functions for algae and cyanobacteria. These pathways may include: mitigation of ROS, increasing dissolved CO2, cross-feeding of TCA cycle intermediates, increasing accessibility of essential metal ions (i.e., via siderophore secretion), or secretion of soluble vitamins (Natrah et al. 2014; Cooper and Smith 2015; Hays et al. 2017). Identifying a more complete list of common synergistic interactions between autotroph/heterotroph pairs could benefit from the use of synthetic communities where each partner species has a developed genetic toolkit and robust metabolic models. Deeper understanding of naturally occurring interactions at the species level could assist in the rational design of partner microbes that could optimize an artificial system (e.g., production in a race-way pond) towards target goals. One systematic way to explore the design space of synthetic microbial communities is through the development of modular consortia (Fig. 2.2). In synthetic biology, a biological module is defined as a unit of function that can be separated from its native context and repurposed in new networks while retaining fidelity of core functions (Andrianantoandro et al. 2006). While it is a common practice of synthetic biology to conceptualize biological units as “modular” on the molecular scale (e.g., protein domains, genes, promoter elements), these concepts are increasingly being applied at the level of whole cells, tissues in multicellular organisms, or species within ecosystems (Ortiz-Marquez et al. 2013; Cameron et al. 2014; Ducat 2018). In this context, a given strain within a microbial community would serve a defined set of functions but could be substituted in a “plug-and-play” fashion with a different species that fulfill those roles. One advantage of developing modular

Fig. 2.2 Modularity in microbial consortia. Synthetic microbial consortia can be designed in a modular fashion, where each “module” contributes one or more key functions towards the overall capabilities of the community. Compatible modules may be recombined with one another in a flexible, “Plug-and-Play” approach to generate a range of related communities with distinct outputs. By contrast, natural microbial communities are composed of hundreds to thousands of species and there is a high degree of functional redundancy for many individual species. Furthermore, because members of these communities have coevolved

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microbial communities is that it streamlines design of new multispecies consortia, and facilitates the identification of common themes of interaction between related communities. Some recent examples of modular microbial platforms are based on cyanobacteria that have been engineered to secrete soluble carbohydrates. These engineered strains can behave as a “carbon fixation module” (Fig. 2.2) within synthetic communities that is analogous to natural cyanobacterial symbionts that secrete organic carbon for the community, as Prochlorococcus does in marine ecosystems (see above). One example that has been utilized in numerous synthetic cocultures is a strain of Synechococcus elongatus sp. PCC 7942 that has been modified to express the sucrose/proton symporter, cscB (Ducat et al. 2012). This strain stably exports a large proportion of photosynthetically fixed carbon as the easily metabolized disaccharide, sucrose (Ducat et al. 2012; Abramson et al. 2016). Multiple labs have shown that photosynthate from these cyanobacteria is sufficient as the sole source of carbon for metabolism and growth of cocultured heterotrophic microbes. In this design, the heterotroph can be conceptualized as a “conversion module” to transform the fixed carbon into more valuable bioproducts, including the bioplastic precursors polyhydroxyalkanoate (paired microbe: Psuedomonas putida; Löwe et al. 2017), polyhydroxybuterate (Halomonas bolieviensis; Weiss and Ducat 2017, E. coli; Hays et al. 2017, or Azotobacter vinelandii; Smith and Francis 2016), fatty acids (Saccharomyces cerevisiae or Rhodotorula glutinis; Li et al. 2017), or secreted enzymes (Bacillus subtilis; Hays et al. 2017). Of note, in a recent report utilizing synthetic cocultures of sucrose-secreting S. elongatus and H. bolieviensis, the designed community was able to continuously produce PHB over the course of more than 5 months while also resisting invasion by a common laboratory contaminant (Weiss and Ducat 2017). Collectively, these results highlight the flexibility and utility of adopting a modular approach to synthetic consortia design (Fig. 2.2). A number of other cyanobacterial strains have been engineered to export carbohydrates, permitting substitution of the “photosynthetic module” in the aforementioned synthetic consortia. For example, cscB has been expressed to improve carbohydrate secretion in numerous other model cyanobacteria (Du et al. 2013; Duan et al. 2016; Song et al. 2016). Alternatively, cyanobacteria have been engineered to secrete a variety of other carbohydrates (Niederholtmeyer et al. 2010; Xu et al. 2012; Aikens and Turner 2013; McEwen et al. 2013; Hays and Ducat 2015), whereas some microalgal strains have been engineered to secrete glycerol (Demmig-Adams et al. 2014). Additionally, many cyanobacterial mutants that are deficient in storing carbohydrates through glycogen synthesis instead secrete

Fig. 2.2 (continued) over many generations, interspecies interactions are more likely to be contextspecific. This can complicate the ability to define discrete roles or identify predictable interaction patterns for individual species. As the field of synthetic microbial ecology matures, construction of modular communities that more closely mimic natural systems (e.g., composed of species with specialized metabolic modes) may assist in the identification of generalizable design principles

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a wide array of carbon compounds as overflow metabolism products (Carrieri et al. 2012; Gründel et al. 2012; Xu et al. 2012; Hickman et al. 2013). Other modular synthetic microbial communities have been generated using strains engineered to fix atmospheric nitrogen and provide it to neighboring species. Some such experiments were originally performed with the diazatrophic cyanobacteria, Anabaena variabilis, specifically utilizing mutants where the nitrogenase genes are constitutively derepressed (Spiller et al. 1986). Consequently, these strains maintain nitrogenase activity even after fulfilling their own needs, resulting in the secretion of excess ammonia (Singh and Tiwari 1998). When such mutants were cocultivated with wheat or rice, they supplemented the nitrogen requirements of the plant and increased crop yields (Latorre et al. 1986; Spiller and Gunasekaran 1990). More recently, a heterotrophic diazotrophic species, A. vinelandii, was modified to continuously express nitrogenase and secrete ammonia, and these strains have been used in coculture with cyanobacteria, algae, and with plants (Ortiz-Marquez et al. 2012, 2014; Smith and Francis 2016; Ambrosio et al. 2017). In each case, the partner species effectively gained the benefit of nitrogen-fixing capabilities through the association, leading to enhanced coculture productivity. Experiments in development seek to combine both the carbon- and nitrogen-fixing modules into a single species by heterologously expressing cscB within Anabaena strains that also secrete ammonia: such cyanobacterial strains are regarded as promising for supporting microbial transformations during long-range space flights (Verseux et al. 2015, 2016). A final class of rationally designed interactions between a phototroph and a heterotroph involves the exchange of vitamins or other cofactors. Again, codependencies can be programmed into selected partners that mimic exchanges that are routinely found in natural environments. In cocultures of the green alga Lobomonas rostrata with the rhizobial bacterium Mesorhizobium loti, algae could secrete sufficient carbon to support the growth of the prokaryote, while receiving sufficient cobalamin (vitamin B12) for its own needs (Kazamia et al. 2012b). In each of the above consortia, the mixed autotroph/heterotroph populations exhibited improved bioproduction and/or metabolic functionality not achievable by the individual species alone. Furthermore, many of these platforms function as simplified systems to study key exchanges that are found in natural communities in a more methodical fashion.

2.3.4

Limitations in Synthetic Coculture Approaches and Future Perspectives

Despite a number of recent advances, the use of synthetic consortia for both academic and applied research is still in its infancy and must overcome a number of limitations to realize their potential. Ironically, while natural consortia display a high degree of robustness, the simplified microbial communities built to mirror them

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are often highly unstable even under controlled conditions. Furthermore, the majority of published examples of synthetic consortia are composed of only two heterotrophic strains, often that are same species but which have been slightly modified with different genetic constructs (e.g., Basu et al. 2005; Danino et al. 2010; Goers et al. 2014; Wintermute and Silver 2010). Natural communities are composed of individuals from many species and with distinct trophic modes (i.e., chemoheterotrophs, methylotrophs, photoautotrophs, photomixotrophs, and chemoautotrophs). The presence of metabolic specialists can be anticipated to have profound effects on community stability in the face of environmental perturbations. Indeed, a cornerstone ecological principle is that species coexistence in the long-term is impossible if they share the same resources and niches (MacArthur and Levins 1964; Kazamia et al. 2012a). Thus, increasing the number of synthetic microbial platforms that are composed of more than one trophic mode may partially alleviate the problem of instability. Providing a structured environment is another approach that may be used to increase the robustness of synthetic consortia. As discussed above, there are a number of theoretical and experimental studies that demonstrate the physical structure and spatial arrangement between microbial partners can increase the long-term stability of interactions that are otherwise prone to collapse (Kim et al. 2008; Chuang et al. 2009; Waite and Shou 2012; Allen et al. 2013; Momeni et al. 2013; Kelsic et al. 2015; Pande et al. 2016). For example, a tripartite heterotrophic community that was unstable when cultivated in well-mixed homogenous environments could be stabilized over long time periods by sequestration of each species into distinct wells of a microfluidic device that were connected by channels allowing exchange of small molecules (Kim et al. 2008). Microfluidic devices also may greatly increase the capacity to test many microbial consortia through recombinatorial approaches by miniaturizing growth chambers (Nai and Meyer 2018). Yet, for some large-scale applications (such as the microalgal ponds discussed above) cultivation in such carefully manufactured conditions may not be economically realistic. An alternative approach to providing structure within microbial communities would be to engineer the cells to self-organize into higher order patterns. One avenue worth additional exploration in this regard is the refinement of cell-cell attachment systems (Fedeson and Ducat 2017; Zhang et al. 2017; Glass and Riedel-Kruse 2018). Programmable cell adhesion between partner species could allow biologists to better define the spatial positioning and architecture of the community (e.g., programming cells to flocculate or form structured biofilms), gaining the benefits of a structured environment even in an otherwise homogenized environment. Finally, the instability of many synthetic microbial communities limits the time scales these consortia have been observed to only a few hours or days (Goers et al. 2014). Increasing the period of observation for stable synthetic communities would offer a new window into the early evolution of symbiotic interactions. While we have learned a great deal from “top down” dissection of specific natural mutualisms (e.g., the chloroplast), the prehistoric origins of these relationships can only be inferred. By contrast, because the partner species in synthetic microbial communities are naïve with regard to one another, stable synthetic ecologies offer a “bottom-up”

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approach to study the early stages of evolution of a symbiosis (Hom and Murray 2014). For example, Shou et al. have studied the evolution of synthetic yeast consortia in the early generations to determine what adaptive traits underlie the observed capacity of these populations to evolve towards higher population density limits (Shou et al. 2007). Long-term study of the coevolution of species within synthetic autotroph/heterotroph consortia could provide new insights into common themes of the early stages of the formation of cyanobacterial and algal mutualisms that are abundant in nature.

2.4

Concluding Remarks

Synthetic microbial consortia are increasingly being used to disentangle the complex networks of natural microbial communities and program consortia to efficiently perform valuable services. Synthetic microbial consortia offer a biological platform for probing the mechanisms of microbial interactions that is both much simpler and more readily controlled than natural microbial ecologies. The earliest examples of synthetic microbial consortia have already provided a wealth of information useful for the development of generalizable theories of microbial ecology. Yet, these early examples are often overly simplistic, with limited numbers of metabolic specialists and poor stability. Improvement upon early examples may help to determine effective design rules that increase the robustness and bioproductivity of engineered consortia. When challenges related to designing more complex consortia and the fragility of these synthetic consortia can be overcome, many additional real-world applications will become possible. In particular, such advanced artificial consortia would be much better suited for a number of sustainability initiatives. This is due in part to the fact that scaling many “green” biotechnologies require large expansions in surface area (e.g., to capture more solar energy in cyanobacterial bioreactors) precluding the ability to fully shield cultures from environmental fluctuations and stressors. Only when engineered consortia can maintain function in the face of dynamic conditions and competing species will they become viable for applications such as bioremediation, improving soil quality, or bioproduction of commodity goods from solar energy. Yet, the ability to confer designer traits on engineered consortia would expand the viability of many other applications including those in human medicine and living therapies. Acknowledgments This work was supported by the Office of Science of the U.S. Department of Energy DE-FG02-91ER2002, and NSF Grant CBET #1437657.

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Chapter 3

Understanding Agriculturally Indispensable Bacterial Biofilms in Sustainable Agriculture Firoz Ahmad Ansari, John Pichtel, and Iqbal Ahmad

Abstract Microbial biofilms have emerged as a compelling research and development topic due to their significance in agriculture, industry, health care, and management of environmental stressors. Innovative approaches using biochemical and molecular tools have advanced our understanding of biofilm development and its structural analysis. Research on microbial biofilms had primarily been focused on medical and industrial aspects. Recently, however, biofilms in agricultural systems have gained consideration due to their enormous potential for crop protection and production. Biofilms perform crucial roles in surface colonization of soil colloids and plant surfaces and facilitate proliferation in desired niches, while also improving fertility of soil. Numerous reports are available which address the general properties and functions of microbial biofilms; however, the role of agriculturally important biofilms and their interactions in the soil system have been inadequately explored. Our understanding of biofilms in relation to climate change, plant nutrition, plant protection, soil quality, and bioremediation has been enhanced in recent years. Both biotic and abiotic factors are known to influence biofilm development. Biochemical and genetics exploration of different biofilms and their interaction will hopefully provide effective strategies to improve crop productivity in a sustainable manner. This chapter addresses the fundamental features of biofilms in relation to their development, involvement in gene transfer, regulatory mechanisms, and importance to plant growth and metabolism. Special attention is given to biofilms of agriculturally important microorganisms and their role in alleviation of plant environmental stressors like drought and excess salinity.

F. A. Ansari · I. Ahmad (*) Biofilm Research Lab, Department of Agricultural Microbiology, Faculty of Agriculture Sciences, Aligarh Muslim University, Aligarh, India e-mail: [email protected] J. Pichtel Department of Environment, Geology and Natural Resources, Ball State University, Muncie, IN, USA e-mail: [email protected] © The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2021 G. Seneviratne, J. S. Zavahir (eds.), Role of Microbial Communities for Sustainability, Microorganisms for Sustainability 29, https://doi.org/10.1007/978-981-15-9912-5_3

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Keywords Biofilms · Gene regulation · PGPR · Rhizosphere · Root colonization · Stress alleviation

3.1

Introduction

Biofilms consist of microbial consortia which are enclosed within self-produced extracellular polymeric substances comprising a meshwork-like structure of carbohydrates, proteins, and DNA. In natural environments, biofilms create a protected environment that permits microbes to survive and exist in hostile surroundings (Rinaudi and Giordano 2010). Such a cellular configuration enhances factors regulating surface attachment, virulence, and nutrient utilization, and furnishes microorganisms with an arsenal of properties that enable existence in stressful environmental situations (Oliveira et al. 1994). The characteristics of the biotic and abiotic factors, nature of medium, microbial consortia involved, and their interactions play a major role in development of biofilms (Petrova and Sauer 2012; Ansari et al. 2017). Microorganisms (bacteria and fungi) employ universal traits for biofilm development when growing and attaching to biotic and abiotic surfaces. For example, bacterial cellular constituents such as flagella, fimbriae, lipopolysaccharides, pili, and membrane proteins are involved in the formation of biofilms (Hinsa et al. 2003; Belas 2013). Microorganisms employ biofilms as a strategy to overcome stresses which include fluctuations in pH, presence of oxygen radicals, nutrient depletion, and presence of disinfectants and antibiotics in the local environment (Karatan and Watnick 2009). Reproductive fitness in terms of physiological heterogeneity and steady growth is an advantage conferred by biofilms when compared with the planktonic mode of growth (Jefferson 2004). In biofilm-associated cells, the transfer rate of genetic material among bacteria is rapid compared to that of planktonic cells due to cell-to-cell contact (Hausner and Wuertz 1999). The frequencies of genetic transformation in biofilms are 6–100 times greater than that of the planktonic mode. Biofilm cells vary both phenotypically and metabolically due to changes in gene expression and regulation as compared with planktonic cells (Kuchma and O’Toole 2000). Abiotic and biotic factors such as salinity and drought are known to drastically reduce crop productivity (Ansari and Ahmad 2018a, b; Ansari et al. 2019). Microbial strategies are proposed to help solve many aspects of plant stress management. The increase in global population and the concomittant demand for higher crop productivity is a key challenge of the twenty-first century. Agriculturally important biofilms are expected to provide innovative approaches to combat plant stress. A brief review on the various aspects of biofilms and their significance is provided in this chapter.

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3.2

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Agriculturally Indispensable Microorganisms (AIMs)

Microorganisms present in the rhizosphere and rhizoplane play an essential role in plant growth and plant health via production of numerous secondary metabolites; these compounds serve as growth regulators and biocontrol compounds for plants (Bais et al. 2004; Lareen et al. 2016). Interactions between plants and microbes in the rhizosphere are responsible for proper ecosystem functioning as well as for various chemical transformations such as carbon sequestration and cycling of nutrients (Rinaudi and Giordano 2010). In recent years many workers have emphasized that microbial interactions with plants are essential to plants in terms of growth promotion, optimizing nutrition, disease suppression, and response to stress (e.g., salinity, drought, heavy metal) alleviation (Qurashi and Sabri 2011; Bogino et al. 2013). Additionally, soil chemical and physical properties are influenced by plant–soil and plant–microbe interactions through biogeochemical cycling and facilitating optimal nutrient balance in soil. Interactions between plants and microbes can be either beneficial or harmful. Beneficial interactions such as symbiotic, associative, free-living, mycorrhizae, biocontrol agents, endophytes, and plant growth promoting rhizobacteria (PGPR) direct plant growth as well as determine plant health in stressful environments. Harmful associations between microbes and plants include infection caused by disease-causing bacteria, viruses, and fungi. The major components of biofilms are microbial cells, which are covered by self-produced exopolymeric substances (EPS) which play an important role as a barrier against diffusion of antibiotics and other compounds from the host (Sutherland 2001). Protection for plants against environmental stress factors such as pH fluctuation, elevated temperature, UV radiation, dessication, and osmotic stress by rhizobacteria colonizing the plant surfaces is well documented. In the context of biocontrol, bacteria in the biofilm mode produce an enormous number of antimicrobial compounds (antibacterial and antifungal) and suppress the growth of plant pathogens (Matthysse et al. 2005; Mansfield et al. 2012). Biofilm-forming PGPR are able to colonize the rhizosphere as well as plant root surfaces and may lead to enhanced plant growth by various mechanisms, such as secretion of plant growth stimulating substances. They also maintain the fertility and health of a soil by nutrient mineralization as well as solubilization, soil aggregation, and remediation of certain contaminants (Sorroche et al. 2010, 2012). An outline of the importance of bacterial biofilms in plant and soil health is presented in Fig. 3.1.

3.3

Agriculturally Indispensable Bacterial Biofilms

Biofilm development on root surfaces is an important capability of rhizospheric microbes for preventing cells from being detached from the root during root elongation and other processes. Interactions such as neutral, symbiotic, or pathogenic

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Fig. 3.1 An overview of biofilm significance in plant and soil health

associations between rhizobacteria and root influence EPS synthesis and establishment of the biofilm. EPS act to block those protection mechanisms applied by plants and provide an environment which is conducive for proliferation of bacteria within the plant system (Janczarek et al. 2010). Plant surface colonization by epiphytic bacterial populations is observed by EPS-mediated pathways; this phenomenon has been widely studied (Bogino et al. 2013). EPS create an environment for plant pathogens to survive and exist in the interior region of the host plant by acting as a barrier against the defense machinery of plants (Leigh and Coplin 1992). Most plant growth stimulating bacteria having biofilm forming capabilities enhance growth and provide protection against abiotic and biotic stress factors by several mechanisms such as production of multifunctional plant growth promoting (PGP) traits, nitrogen fixation, alleviation of salinity and drought, and biocontrol activity. Biofilm development by several genera of agriculturally indispensable bacteria and their plant growth promotion and stress amelioration traits are presented in Table 3.1.

3.4

Factors Influencing Biofilm Development

Associations between plants and microbes depend primarily on physical interactions in the host plant with relevant microorganisms. Physical interactions comprise electrostatic attraction and adherence of bacteria to surfaces. Interactions among the bacterial cell wall and plant cell surfaces are influenced primarily by attraction (interfacial electrostatic), van der Waals forces, and repulsion. Many nonspecific forces also influence cell attachment including hydration, hydrophobic interactions, and steric effects. Several reports have illustrated multicellular diverse assemblies of

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Table 3.1 Biofilm development among agriculturally indispensable microorganisms Microorganisms Anabaena-Azotobacter chroococcum; Trichoderma-Azotobacter chroococcum Azospirillum brasilense

Herbaspirillum seropedicae

Traits N fixer, plant growth promotion N fixer, plant growth promotion Plant growth promotion and biocontrol Plant growth promotion and salinity alleviation Bioremediation, biocontrol N fixer Endophyte, N fixer, plant growth promotion Endophyte, N fixer

Mesorhizobium tianshanense

N fixer

Paenibacillus polymyxa

N fixer and biocontrol

Pseudomonas entomophila

Plant growth promotion

Pseudomonas fluorescens

Rhizobium leguminosarum

Plant growth promotion and biocontrol Bioremediation Bioremediation and biocontrol N fixer

Sinorhizobium meliloti

N fixer

Bacillus subtilis Brevibacterium halotolerans Burkholderia cepacia Bradyrhizobium japonicum Gluconacetobacter diazotrophicus

Pseudomonas aeruginosa Pseudomonas putida

References Prasanna et al. (2014); Prasanna et al. (2015) Jofré et al. (2004); Lerner et al. (2009) Vlamakis et al. (2013); Beauregard et al. (2013) Ansari and Ahmad (2018b) Conway et al. (2004) Lee et al. (2014) Wang et al. (2008) Balsanelli et al. (2010, 2014) Yegorenkova et al. (2011); Das et al. (2017) Koutsoudis et al. (2006); Quinn et al. (2012) Ansari and Ahmad (2018a) Lugtenberg et al. (2002); Hinsa et al. (2003) Rizvi and Khan (2018) Kang and Kondo (2002) Ausmees et al. (2001); Skorupska et al. (2006) Torres et al. (2007); Sorroche et al. (2012)

microbial populations on the plant surface, which differ in morphological form such as microcolonies, clusters and aggregates (Morris and Monier 2003; Parsek and Fuqua 2004). Several abiotic factors such as temperature, pH, nutrient levels, oxygen level, metal ion concentrations, and nature of surfaces also influence biofilm formation (Renner and Weibel 2011; Toyofuku et al. 2016). In response to surface properties, eDNA, proteins, lipopolysaccharides and lipids are secreted by the cells that form the EPS (extracellular polymeric substances) and influence the stiffness/ elasticity of biofilms (Jayathilake et al. 2017). Biotic factors such as presence of antimicrobials, biocides, and EPS and plant volatiles also influence biofilm formation (Beauregard et al. 2013; Ansari et al. 2017). A summary of mechanisms involved in regulation and factors encouraging biofilm development are depicted in Fig. 3.2. The details of their mechanisms have been published in many research

Nutrient level in surrounding

• • • • •

• • • Biocides Antibiotics Chemicals

Antimicrobials

Cell surface interaction

Mechanical signalling

EPS biosynthesis/inhibition

Biofilm forming gene regulation

EPS degrading enzymes

Enzymes

Fig. 3.2 Regulatory mechanisms and factors affecting biofilm development

pH Metals Temperature Osmolarity Extracellular DNA

Nutritional factors

Environmental factors

Factors

Biofilm development / dispersal

• • • •

• • AHLs Autoinducing peptides nitric oxide Adhesins Amino acids volatiles

Quorum sensing

Gene expression

Host derived signals

Mechanisms

Regulation of gene expression

c di-GMP modulation

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papers (Zhang et al. 2014; Ansari et al. 2017; Singh et al. 2017; Padmavathi et al. 2017). Herein we briefly review various factors influencing biofilm development.

3.4.1

Environmental Factors Influencing Biofilms

Various environmental factors such as temperature, pH, and availability of oxygen influence biofilm development. Solution pH is considered among the most important factors for growth, survival, and activity of microorganisms (Dang and Lovell 2016). Biofilm formation among bacteria are affected by deviations in pH and temperature; this phenomenon has been observed, for example, in biofilm development in Haemophilus influenza (Ishak et al. 2014) and Sinorhizobium meliloti. Many bacteria can, however, counter fluctuations in pH by adjusting cellular functions such as degradation of amino acids and proton translocation (Olsen 1993). Production of EPS by bacterial cells during biofilm development assists in response to environmental fluctuations, e.g., pH changes. The quality and quantity of EPS secreted by microorganisms also influence biofilm development. Several components of EPS (xanthan, alginate, and gellan) are recognized to form more hydrated viscoelastic gels as well as a thick polymeric layer which provides mechanical support to the biofilm for overcoming various stresses (Laus et al. 2005; Ansari et al. 2017, 2019; Ansari and Ahmad 2018a, b). Biofilm formation is affected by temperature variations, as optimum temperatures support normal activities and metabolism, nutrient acquisition, and subsequent biofilm development. Adhesive properties in bacterial polymers are impaired upon reduction in temperature. Viscosity or stickiness of polysaccharides of the EPS is enhanced upon temperature increase which may directly influence attachment of biofilms to surfaces. In biofilms of Pseudomonas aeruginosa, the hydration capability of alginate increased due to formation and release of acetylated uronic acids in the EPS matrix (Stoodley et al. 2002; Klapper et al. 2002). Temperature fluctuations affect the formation as well as functions of bacterial appendages. Since appendages play an important role in adhesion and biofilm development, it follows that fluctuations in exterior temperature will influence biofilm development (Nisbet et al. 1984). Most microbially secreted polysaccharides are stable at lower temperatures; hence, lower temperatures favor establishment of biofilms as compared to elevated temperatures (Nisbet et al. 1984). Oxygen availability in the local media modulates biofilm development in microorganisms. Similarly, water content affects biofilm development and structures by modulating the EPS matrix (Thormann et al. 2005; An et al. 2010).

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Nutritional Factors Influencing Biofilms

The nutritional composition of root exudates markedly influences its associations with the biofilm mode. Variations in root exudation and nutrient-releasing patterns in different plant components impart significant effects on biofilm growth and structure (Ramey et al. 2004). An environment having greater nutrient content as well as moisture supports aggregation of bacteria and biofilm development. The quantities of carbon and nitrogen in the medium influence the production of EPS quantitatively as well as qualitatively, thus regulating biofilm formation (Chai et al. 2012; Zhang et al. 2014). Excess quantities of available iron suppressed genes responsible for biofilm development in Pseudomonas aeruginosa (Musk et al. 2005; Glick et al. 2010). The availability of inorganic phosphates (Pi) influenced biofilm development in Pseudomonas fluorescens Pf0-1 (Newell et al. 2011). At low levels of inorganic phosphate (Pi), a c-di-GMP (cyclic diguanylate GMP) phosphodiesterase (PDE) RapA gene is expressed and depletes c-di-GMP of the cells, consequently triggering a loss in adhesin LapA of the outer membrane of the cell. This, in turn, leads to a reduction in adhesion and biofilm development among bacteria. Amino acids play an important role as both a nitrogen and carbon source for root colonizing microorganisms. The role of amino acids in biofilm development among rhizosphere bacteria, especially as associated with assembly as well as disassembly, has been intensely deliberated (Valle et al. 2008; Kolodkin-Gal et al. 2010). The presence of several amino acids originating from root exudates and from biosynthesis in the rhizosphere support growth and biofilm development in bacteria (Vlamakis et al. 2013). Certain amino acids occurring in substantial quantities were detected in the biofilm mode of lifestyle in most Gram-negative bacteria; these amino acids were absent in the planktonic growth mode. Casamino acids regulate the chemotaxis and biofilm development in rhizosphere-dwelling P. fluorescens WCS365. Amino acids in P. aeruginosa altered the bacterial phenotypes (structural changes in lipopolysaccharides, colony morphology and expression, and modification of membrane porins) (Sriramulu et al. 2005). Agriculturally indispensable microorganisms such as P. fluorescens and Bacillus subtilis exhibited chemotactic movement towards proteinogenic amino acids (Ordal and Gibson 1977). Alterations of amino acids, which are involved in chemotaxis movement in P. fluorescens Pf0-1, led to declined rhizoplane colonization (Oku et al. 2012). In B. subtilis subjected to a scarcity of serine, the serine amino acids were used as an alternative which led to growth and triggered development of biofilms (Subramaniam et al. 2013). During the exponential growth phase, serine is exhausted rapidly. Exchange of serine codons (TCN) with AGC or AGT reduced expression of the gene and subsequently biofilm formation in B. subtilis. In contrast, switching of AGC or AGT to TCN codons is upregulated for biofilm development (Subramaniam et al. 2013).

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Signals Generated by Host Plants and Microbes

Root exudates secreted by the plant play a crucial role as chemoattractants for rhizosphere microorganisms during rhizosphere colonization (de Weert et al. 2002). Chemotaxis and the associated motility (swimming and swarming) are active mechanisms for establishing biofilms on surfaces of crop plants (Vande Broek and Venderleyden 1995). Root exudates which promote rapid rhizosphere colonization mediated by chemotaxis and consequent stable biofilm development by Pseudomonas putida was described earlier (Espinosa-Urgel et al. 2002). For the pseudomonads, biofilm development as well as competitive root colonization is regulated by type IV pili or flagella for chemotaxis (Lugtenberg et al. 2002). Flagella serve a dual character as organs for motility as well as a sensing element in microorganisms for early cell adhesion and succeeding biofilm development (Belas 2013). Microorganisms (bacteria and fungi) secrete various secondary metabolites which possess heterogeneous chemical properties and roles. Most of these metabolites in the diffusible form play an important role as signal molecules in fungal–bacterial interactions (Frey-Klett et al. 2011; Haq et al. 2014). Fungi produce several classes of volatile organic compounds (VOCs) including benzenoides, aldehydes, alcohols, esters, alkenes, acids, and ketones (Morath et al. 2012; Piechulla and Degenhardt 2014), which have crucial ecological roles in communication or interactions between microorganisms. Davies et al. (1998) described the interference of quorum sensing (QS) in the development of biofilm using a lasI–mutant of P. aeruginosa. QS, which is simply the process of regulating gene expression in response to variations in a microbial populations, is an important diffusible metabolic signal which acts as an essential regulator for production of EPS as well as biofilm development (Abisado et al. 2018). QS is facilitated by tiny diffusible signal molecules known as autoinducers which regulate gene expression of bacterial communities in response to their density or mass in the environment. Two such routes, known as autoinducer-1 and autoinducer-2 (AI-1 and AI-2), regulated by the QS, have been described in bacteria. While autoinducer-1 plays an important role in intraspecies interactions, autoinducer-2 is involved in cross-talk as well as interspecies communication and interaction. The AHL (N-acyl homoserine lactones) is a small diffusible signaling molecule in Gram-negative bacteria which controls the density of the bacterial population (Waters and Bassler 2005; Abisado et al. 2018), whereas on the alteration in oligopeptides, which produce signals from membrane-bound sensor histidine kinases, act as receptors molecules. Studies on most bacterial species show that exopolysaccharides (i.e., surface components) and flagella with the QS signal play a chief role in development of biofilms. Nitric oxide (NO) is a widely known intercellular and intracellular signaling molecule that controls myriad interactions between bacteria and plants (Chen et al. 2015). It was observed that NO levels in microorganisms influence development and dispersal of biofilm-mediating c-di-GMP through the signal network (Plate and Marletta 2012). A significant production of NO by Azospirillum brasilense under

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oxygenic conditions was noted, which is important for induction of lateral root development in plants (Creus et al. 2005). Di Palma et al. (2013) showed that NO can act as an initial signal during the attachment or adherence process of biofilm development in A. brasilense. Several polyphenolic compounds such as ellagic acid, tannic acid, and epigallocatechin gallate (EGCG) are commonly found in plants which interfere with AHL-mediated signaling (quorum sensing) and consequently with biofilm development. A number of compounds secreted by plants imitate bacterial AHL molecules in affecting signals in quorum sensing in plant-associated bacteria (Teplitski et al. 2000). Interference of bacterial volatile compounds in cross-species interactions (bacterium–host and bacterium–bacterium) has also been examined. Roots secrete a large number of volatile compounds which are involved in initial stages of biofilm development on the plant surface. Chen et al. (2015) demonstrated that acetic acid acts as a volatile or quorum sensing signal by B. subtilis for selecting the timing of biofilm development. Organic acids secreted as root exudates, and polysaccharides of the cell wall were also reported as host signals which trigger biofilm development.

3.6

Genetic Factors Influencing Biofilms

Various genetic factors are involved in different stages of biofilm development and play a vital role in regulation of adherence or attachment as well as dispersal of biofilms. The processes involved in bacterial adherence to the plant surface and consequently development of the biofilm are highly regulated events. Multidimensional pathways involved in regulating expression of genes in biofilm formation. A c-di-GMP (cyclic diguanylate GMP) is a secondary messenger which plays a crucial role and determines the fate of the bacterium, i.e., whether to remain in the planktonic state or switch to biofilm mode (Valentini and Filloux 2016; Hsieh et al. 2018). The c-di-GMP also plays an important role in binding to effector protein molecules and carries out transcription of adhesins, and subsequently the localization of protein in biofilm cells (Duerig et al. 2009). This c-di-GMP also has an essential role in the regulation of motility, flagellar function, and production of extra polymeric substances (Merighi et al. 2007; Hsieh et al. 2018). The histidine kinase (KinD) sensor affects biofilm development via sensing of small molecules. The involvement of sRNAs (small noncoding RNAs) in biofilm development has been reported earlier (Chambers and Sauer 2013). Density of the initial cell populations determines the pattern of development during biofilm formation. Regulation of gene expression (up and downregulation) in microbes serves key roles in formation of the biofilm. Genes involved in regulation of EPS synthesis and formation of fimbriae are downregulated during the biofilm disassembly process and halt sessile cell development, while genes involved in proteins responsible for chemotaxis and development of flagella are upregulated to enhance motility of the cell (Rollet et al. 2009).

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Mixed-Species or Multispecies Biofilms

Advancements in microscopic techniques, molecular tools, and methods of cultureindependent studies of bacterial populations has facilitated an improved understanding of the dynamics of bacterial biofilms. In natural settings, most microbes form biofilms in monoculture; however, microorganisms are also reported to interact with different microbial populations for survival in harsh ecological niches to form complex communities and mixed-species biofilms. In recent years there has been increased attention in the study of mixed or multispecies biofilms (Burmølle et al. 2014), mainly focusing on interactions among bacteria and fungi (Nazir et al. 2010; Scherlach et al. 2013). Multispecies biofilms are essential in sustaining the ecological stability in soil systems. Mixed or multispecies biofilms are more resistant to antimicrobial (antibacterial and antifungal) compounds in comparison to their monospecies counterparts. Multispecies biofilms confer increased protection against protozoan predation as well as from desiccation. Horizontal gene transfer is also enhanced. The need exists, therefore, for research directed towards understanding the interactions among fungi and bacteria. Interactions in multispecies biofilm development result in the production of new types of polysaccharides which differ in composition in comparison to those found in monospecies biofilms (Andersson et al. 2011). This demonstrates the synergistic interactions of microbial partners in biofilm development. Diverse interactions can arise in the biofilm of multispecies or mixed-species, which may impart significant effects on their metabolic pathways as well as physiology. In a mixed-species biofilm, bacteria experienced greater resistance to antimicrobial compounds (Lee et al. 2014). Synergistic interactions are found among the partners in mixed-species biofilms and due to this interaction, biomass production is greater in comparison to monospecies biofilms. Antibiosis (competition) leading to cell damage in P. aeruginosa for survival was established as an important indication of biofilm development (Oliveira et al. 2015). In multispecies biofilms, individual species develop their own unique biofilms which metabolically complement each other and exist for longer periods (Elias and Banin 2012). The production of metabolites by one species in the community is used by another species, thus increasing resistance to unfavorable environments.

3.8

Environmental Stress (Salinity and Drought) Amelioration by AIM

Salinity is considered to be the most severe abiotic stress to plants, which significantly limits productivity and growth. Unfortunately, the area of land affected by excess salinity continues to increase. For many important agricultural crops worldwide, average yields are estimated to be between 20 and 50% of optimal yields; these losses in productivity are due to elevated drought and excess soil salinity, situations

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which are expected to worsen in many areas as a consequence of global climate change. Various methods of mitigation as well as adaptation approaches are necessary to manage such influences (Ansari and Ahmad 2018a, b). Several technologies and approaches have been established to reduce the toxic effects caused by elevated salinity and excess drought on plant health and growth, including genetic engineering of the plant (Wang et al. 2008), and application of plant growth promoting bacteria (PGPB) to protect plants against environmental stress (Ansari and Ahmad 2018a, b). Microorganisms play an essential role in plant growth promotion, disease control, and nutrient management as well as enhancement of soil fertility. Beneficial rhizospheric microorganisms colonize the rhizosphere and the rhizoplane, as well as the cortical region of the root, and enhance plant growth via a number of mechanisms, both direct and indirect. Earlier investigations proposed that the use of PGPB may offer a promising alternative for alleviating stresses to plants affected by salinity (Yao et al. 2015). Understanding the role of microbes in abiotic and biotic stress management is gaining importance. The subject of environmental abiotic stress tolerance by PGPR and its alleviation has been reviewed (Yang et al. 2011; Dodd and Pérez-Alfocea 2012). Microorganisms impart some grade of tolerance to plants against environmental stresses like salinity, drought, metal toxicity, chilling injury, and elevated temperature. In the past, different bacterial genera including Bacillus, Pseudomonas, Burkholderia, Pantoea, Paenibacillus, Achromobacter, Azospirillum, Microbacterium, Enterobacter, Methylobacterium, and Variovorax have been described to provide tolerance under various environmental stresses to host plants (Grover et al. 2011). Stress tolerance in the plants elicited by microbes may be due to various mechanisms. The correct application of these microbes can ameliorate environmental stresses in agriculture sectors thus opening novel applications for plant cultivation. Most PGPR survive and colonize the root surface and thrive in-between rhizodermal layers and root hairs, whereas some are not in contact with the root surface (Gray and Smith 2005). Root exudates are secreted in the rhizosphere and have a role in signaling systems and in regulating communication between microbe and plant. Organic acids, phenols, and flavonoids are among the components of root exudates and act as chemical signals which regulate several processes such as exopolysaccharide production, bacterial chemotaxis, quorum sensing, and biofilm development during colonization of the rhizosphere (De-la-Peña and Loyola-Vargas 2014; Ma et al. 2016).

3.9

Conclusion

Biofilm development by bacteria serves as a highly effective strategy to overcome both biotic and abiotic stresses and to support microbial establishment within a favorable niche. It is now well recognized that biofilms offer diverse and practical applications in many fields including agriculture, food production, and

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bioremediation. Their beneficial aspects can be applied to a multitude of crops and climate conditions, given the diversity of traits microorganisms demonstrate in biofilm mode. The well-planned use of such biofilms can greatly assist in enhancing agricultural sustainability the world over.

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Chapter 4

Global Food Demand and the Roles of Microbial Communities in Sustainable Crop Protection and Food Security: An Overview Ahmadu Tijjani and Ahmad Khairulmazmi

Abstract For sustainable food security, food supplies must keep pace with increasing population and urbanization which can partially be achieved by reducing the yield losses caused by the destructive pests and disease activities to the harvestable parts of the crops. A doubling in global demand for food projected by 2050 or beyond imposes a number of challenges for agricultural sustainability. Today, plant growth to meet human demands for food is enhanced by the increasing input of agrochemicals, which act as plant nutrients as well as plant growth regulators (PGRs). Apart from increasing the cost of production, excessive use of chemicals increases the possibilities of land degradation and deteriorating environmental quality. To overcome this problem and enhance crop production, utilization of microorganisms for sustainability is one of the most ideal and compatible approaches while maximizing profits and keeping people and the planet safe. Numerous microorganisms including fungi, actinomycetes, bacteria, and plant growth promoting rhizobacteria (PGPR) posess mechanisms of plant growth promotion. These microorganisms help in the recycling of materials to increase nutrient uptake and improve plant health by providing plants with protection against attack by phytopathogens in the form of biocontrol agents and toxic effects of nutrient hyper-accumulation. The use of these microbes should not be overemphasized. Hence in this chapter we aim to highlight the roles of such microorganisms in sustainable crop protection and food production for global food security. Keywords Crop protection · Food security · Microbes · Nutrients · Sustainability

A. Tijjani Department of Crop Production, Faculty of Agriculture and Agricultural Technology, Abubakar Tafawa Balewa University, Bauchi, Bauchi State, Nigeria A. Khairulmazmi (*) Institute of Plantation Studies (IKP), Universiti Putra Malaysia, Serdang, Selangor Darul Ehsan, Malaysia e-mail: [email protected] © The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2021 G. Seneviratne, J. S. Zavahir (eds.), Role of Microbial Communities for Sustainability, Microorganisms for Sustainability 29, https://doi.org/10.1007/978-981-15-9912-5_4

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Introduction

Agricultural sustainability is the development that meets the needs of the present generation without compromising the ability of future generations to meet their own needs (Brundtland 1987). The growing global population needs to be satisfied with food supply through an intensive agricultural production system which signifies the need for various green revolutions. At present, our practices that involve indiscriminate use of synthetic chemicals, chemical fertilizers, and high utilization of nonrenewable energy source have led to a large threat to environmental sustainability. The world is now facing a great challenge to adopt sustainable measures, green technologies, sustainable science, and cleaner production such that the generations to come may be able to benefit from the earth’s ecology at its conserved form (Akinsemolu 2018). Conservation of the planet becomes necessary as “We don’t have a Plan B, since there is no Planet B” (Ki-moon 2016). All key processes in the biosphere and related human activities are quite interdependent, interconnected, and hence should be steered through a mutual systems approach (United Nations 2015). One cannot deny nature because microbial populations are an important and integral part of biogeochemical cycles which are useful for our sustenance. Life is possible without higher organisms, but life is not possible in the absence of microbes (Kuhad 2012). Food security is one of the three most pressing super challenges of the twenty-first century, after climate change and overdependence on petroleum importation, and microbes are good enough in meeting out these challenges (Mishra et al. 2016). There is quite a possibility that land use and climate changes can be compensated by the homeostatic activities of the microbial populations. The urgent need for the world’s food security and generations to come is sustainable food production (Meena et al. 2017; Ahmad et al. 2016; Jat et al. 2015; Kumar et al. 2015a, b). This, therefore, necessitates the search for compatible ways for sustainability in food production without depleting soil fertility and destroying the quality of the environment. A suitable system that can maintain agricultural productivity at a higher level without causing problem to the agroecosystem is the need of the hour (Meena and Meena 2017; Nath et al. 2017). By the year 2050, agricultural production is expected to increase by 70% and good agricultural practices are the fundamentals to meet this target (Barea 2015). Different technological packages or inventions are being carried out to intensify crop productivity but still we are not in a position to fulfill the global demand for food. Microbial populations associated with plants might be used to overcome the problems related to soil fertility, salinity, habitat loss, and degradation in order to increase crop productivity. Microbial populations are unique since they are directly associated with promotion of plant growth, soil fertility enhancement, and lowering abiotic and biotic stresses via several mechanisms. The soil matrix contains different microorganisms such as fungi, bacteria, insects, algae, annelids, and other diverse invertebrates which show an intimate relation to each other and with plants (Akinsemolu 2018; Glick 2010). People, Planet, Profit (Prosperity), Peace, and Partnerships (Fig. 4.1) are the main goals of the sustainable development (Costanza et al. 2016)

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Fig. 4.1 The five goals of sustainable development

and if microbes are utilized judiciously they can make a significant contribution in the achievement of these goals (Akinsemolu 2018; Kuhad 2012). Microorganisms are much of our past and our future, pivotal agents of ecosystem and planet’s functioning hence are key parts of the stewards committee of planetary health and sustainability.

4.2

Global Demand for Food Security

The major concern of the world today is the alarming rise in the human population and the fulfillment of their food requirements (Meena et al. 2017; Meena and Meena 2017). As per estimates obtained in the records of the United Nations Food and Agriculture Organization (FAO 2014), about 11% of the world’s land surface (1.5 billion ha) is utilized for the production of crops. Despite this fact, many countries cannot further expand the land for agricultural production due to population pressure. As a result, global agriculture is facing serious problems of meeting or providing adequate food for more than seven billion people and the generations to

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come (FAO 2012). By the year 2050, the planet is expected to be inhabited by ten billion people, mostly in developing countries (Barea 2015). Such a rise in population leads farmers to intensify agriculture by injudicious application of agrochemicals like fertilizers and pesticides to boost agriculture, and this has implications on the environment and the biodiversity. Balanced utilization of improved technologies and agricultural inputs provided in the past few years are now reaching a diminishing returns point (Dawe et al. 2000). It can rightly be said that a goldmine—microbes—could widely be used by farmers for sustainable crop production to provide abundant fiber, food, and bioenergy while managing the biosphere. As a recommended and proposed approach, microbial communities present in the soil could be exploited for a healthy and sustainable crop production, whereas preserving the biosphere is the best of our hour. In an agricultural context, the roles of microbes (microbial services) in improving agriculture sustainability and environmental management should not be overemphasized (Lugtenberg 2015; Barea et al. 2013). However, different techniques used to effectively exploit the services of microbial populations, as a low input biotechnology, to help in environmental sustainability via simple agrotechnologies have been, and are being, proposed with the final aim of optimizing the role of microbes in plant protection and nutrient supply (Raaijmakers and Lugtenberg 2013).

4.3 4.3.1

Roles of Microbes in Sustainable Food Production The Microbes and Plants

The association of plants with eukaryotic fungi and the prokaryotic bacteria have resulted in a broad diversity of living habits whose symbiotic or saprophytic relationships with the plants might be beneficial or detrimental. Most microorganisms live in the rhizoplane or rhizospheric soil, but a little or minute subpopulations of them, termed as “endophytes”, are able to penetrate and live within plant tissues (MercadoBlanco 2015; Brader et al. 2014; Malfanova et al. 2013). As a result of their interaction with the plant, such microbes do escape from immunity responses of the plant and colonize their tissues, causing no disease symptoms, in different morphological parts of the plant (i.e., fruits, leaves, roots, or shoots), or in various apoplast regions of the plant (i.e., phloem and xylem vessels) and sometimes within the cells of the plant. Some affect plant growth, its responses to environmental changes, to pathogens, or production of important secondary metabolites (Barea 2015). Other groups of microbes such as rhizobia, mycorrhizal fungi, and some other pathogens that colonize the plant tissues are also endophytes but separated from the “endophytes” core group, that are involved in causing disease to their host plant or transfer of nutrient from sources outside the root, such as atmosphere or soil. According to Barea (2015) and Barea et al. (2013), managing these interactions that involve selected Plant Growth Promoting Rhizobacteria (PGPR) and fungi is

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considered as feasible approach in agricultural sustainability. A number of co-inoculation trials with selected rhizosphere microorganisms have been reported. They include interactions related to: (a) phosphate mobilization, (b) symbiotic N2-fixation, (c) bioremediation of heavy metals in plants (Table 4.1), (d) improvement of soil quality, and (e) biological control of root pathogens (Mishra et al. 2016; Barea et al. 2013). The tool for the application of microbial biotechnology is not in sustainable agriculture but included also in other ecosystem issues such as restoration of ecosystem, enhancing resilience of plant communities, recovering of endangered flora, etc. (Barea et al. 2013). In this chapter, the management of beneficial microbial activities is focused on the manipulation of naturally existing microbial populations on sustainable agriculture. It is important to note that microbial communities and their interactions with the crops are affected by different agronomic managements and ecological factors, and thus the impact of biotic and abiotic factors have to be taken into consideration, especially in the present time of global change (Zolla et al. 2013). Advances in detailed knowledge of the mode of actions underlying the interactions between plant and microbial population in the rhizoplane have been constrained by lack of appropriate methodologies. However, molecular-based technologies are currently being used to open the molecular basis of the interactions between plants and microbiome or to decipher the hidden diversity of microorganisms inhabiting soil and rhizosphere habitats (Mishra et al. 2016; Barea 2015), as shown in Fig. 4.2. These approaches, based on molecular techniques, also gave the basis to assess the effects of perturbations led by abiotic and biotic factors on plant–microbe interactions and on soil microbiome diversity, in the present global change scenario. The processes of using molecular techniques begin with the collection of the environmental samples, followed by the extraction of RNA/DNA, and then application of different biochemical markers. As it is well understood, the genes that are expressed in a given situation are referred to as RNA, while the functional capability and phylogenetic identity of the microbes are determined by DNA (Barea 2015). The ribosomal DNA (rDNA) obtained from samples could be subjected to various molecular methods such as polymerase chain reaction (PCR) amplification, cloning, hybridization, or high throughput sequencing. For example, application of the polymerase chain reaction methods, and its derivative qPCR approach, to analyze rDNA obtained from microbial samples have led to a major break-through for deciphering diversity among microorganisms. The small subunit of ribosomal sequences exemplified by 16S and 18S genes for bacteria and fungi respectively are the molecular markers targeted on microbial identification. The 16S and 18S rRNA gene analysis which requires comparison is the molecular technique used frequently for microbial delineation. The amplicons (PCR products) having variable or identical regions are taking consideration as OTUs (operational taxonomic units). Variation in PCR amplicons could be assessed by using different molecular tools such as next generation sequencing, thirdgeneration sequencing, single-molecule real-time sequencing (SMRT), and the gene microarray-based PhytoChip and GeoChip techniques. Other sequencing methodologies utilized in the identification of microbial communities at all levels of

Bacillus megaterium

Bradyrhizobium japonicum CB1809

Staphylococcus, Bacillus, and Aerococcus

Arsenic

Cadmium, Chromium, Copper, Zinc and Lead

PGPR Alcaligenes faecalis, Brevundimonas diminuta Microbacterium sp., Rhizobium sp.

Lead

Chromium (VI)

Metals Mercury

Table 4.1 Phytoremediation of heavy metals by PGPR

Lolium multiflorum, Prosopis juliflora

Helianthus annuus and Tricuma estivum

Brassica napus

Pisum sativum

Plants Scripus mucronatus

Greenhouse conditions

Pot studies

Field conditions

Trials Greenhouse conditions Glasshouse conditions

Results – Decrease toxicity in soil – Increase phytoremediation – Decreased chromium toxicity – Improved the nitrogen (54%) concentration in the plants – Decreased in soil pollution – Increased in total dry-matter yield of plants – Growth in high arsenic concentration – Excess of plant biomass – Tolerate high concentration of Chromium (up to 3000 mg/L) – Improve the efficiency of phytoremediation

Wani and Khan (2012)

Yavar et al. (2014)

Reichman (2014)

References Soni et al. (2014)

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Fig. 4.2 System-based molecular approaches presently utilized to open up the diversity of microorganisms inhabiting soil and rhizoplane. Sources: Barea (2015)

taxonomy in different biomes and soils are pyrosequencing of 16S/18S rDNA amplicons and qRT-PCR.

4.3.1.1

Nutrient Recycling and Acquisition: A Key to Sustainability

Globally, soil infertility is the major factor limiting crop yield and this can be alleviated through better management of microbiomes present in the soil and the implementation of better cultivation practices. In the context of sustainability, the most important thing is to maintain the quality of the soil through better environmental functions some of which are generated from soil microorganisms (Zancarini et al. 2013). According to Zolla et al. (2013), finding effective methodologies for recycling nutrients, alleviating the negative effect of abiotic stress factors, controlling pests and diseases, and the sustainability of global ecosystems is the target for sustainability. The abovementioned activities are typical microbial services obtainable if beneficial microbes and their functions are managed appropriately (Mishra et al. 2016; Barea 2015; Zolla et al. 2013). Microbial populations in the rhizosphere mediate the cycling of nutrients, enhance their mobilization, and above all facilitate their uptake, leading to increased root growth, biomass, and yield of plants (Manjunath et al. 2016) and confer resistance to the host plant from pathogens causing diseases by customized and specialized secretions of antibiotics (Bonfante and Genre 2015; Gourion et al. 2015).

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Living together in the biological world is the most famous phenomena and mycorrhization is one such interesting interaction (Varma et al. 2002). Apart from secondary metabolite production such as enzymes, hormones, and antibiotics; and organic material decomposing, nutrient recycling plays a major role in increasing bioavailability of various nutrients that helps in microbial growth such as bacteria and in turn these bacteria play an important role in enhancement plant growth (Dhuldhaj and Pandya 2017). Today, exploitation of microbes offers environmentally friendly plant growth promotion for intensive agricultural ecosystems which have gradual increase in demand worldwide (Kumar et al. 2016a, b; Jat et al. 2015).

4.3.1.2

Nitrogen Fixation

Nitrogen, Phosphorus, and Potassium (NPK) are the most important and essential minerals for vegetative growth and development of plants (Meena et al. 2017). Application of chemical fertilizers in intensive agricultural system especially application of high N fertilizer results in environmental pollution with subsequent global N cycle imbalance, nonrenewable resources depletion, and nitrogen oxides volatilization of nitrogen into the atmosphere leading to climate changes and global warming (Saha et al. 2017; Singh and Ryan 2015). Accordingly, continuous increase in the human population which almost expand exponentially requires urgent novel approaches of lifting food supply that go together with sustainability and sparing the environmental features (Ahmad et al. 2016; Kumar et al. 2015a, b, 2016a, b; Jat et al. 2015; Bahadur et al. 2014). In nature a symbiotic relationship known as biological nitrogen fixation (BNF) takes place among most of the legume plants and beneficial microbes, in which bacteria are able to convert N2 from the atmosphere and make it available to the associating plant for sustainable agriculture (Bahadur et al. 2016; Meena et al. 2016; Yadav and Sidhu 2016; Saha et al. 2016; Verma et al. 2015). Beijerinck (1901) discovered BNF by some prokaryotes that include aquatic organisms such as freeliving soil bacteria, cyanobacteria, Azotobacter, Azospirillum (Saha et al. 2017), and most importantly Bradyrhizobium and Rhizobium, forming symbiotic association with mostly leguminous plants (Wagner 2011). These microorganisms use nitrogenase enzyme that catalyzes the conversion of nitrogen (N2) from the atmosphere to ammonia (NH3) which can be readily assimilated by plants to produce aforementioned nitrogenous biomolecules. N2 þ 8e þ 8Hþ þ 16 ATP $ 2NH3 þ H2 þ 16 ADP þ 16Pi Biological nitrogen fixation (BNF) is catalyzed by an enzyme known as nitrogenase which via reduction process mediated the breakdown of covalent bond of free N2. The enzyme has redox potential centers in multiple due to the presence of two proteins. A reductase is the first part which provides the electrons, whereas nitrogenase is the second part that uses these electrons to turn nitrogen into ammonia. The

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Fig. 4.3 Organogram of the N-fixer microbes isolated from natural systems and agricultural land. Source: Wagner (2011)

electrons are transferred from reductase to nitrogenase via a process that is coupled with the hydrolysis of ATP by the reductase (Brill 1980). The ATP molecules that supported the process of nitrogen fixation are either derived from organic compounds decomposition in nitrogen-fixing heterotrophs, supported indirectly from the processes of photosynthesis or directly from photosynthetic processes in N2-fixing photoautotrophs. Two or more electrons are required by the reduction process of free atmospheric N2 by nitrogenase enzyme; since the BNF reaction needs to be repeated many times for conversion of nitrogen (N2) into ammonia (NH3), and during the electron transfer, it reacts with H+ and produces hydrogen. In addition to nitrogen and hydrogen, several low molecular weight compounds are also reduced to ammonium (Swain and Abhijita 2013). The processes of BNF and the microorganisms involved are summarized in Fig. 4.3.

4.3.2

The Microbes and Soil

The soil is the physical covering of the earth surface that represents the interface of three states of materials: solids (dead biological and geological materials), liquids (H2O), and gases (air in soil pore spaces) and is also regarded as the fundamental of all terrestrial ecosystems (Aislabie and Deslippe 2013). In the soil captivity or matrix, a number of microbes such as fungi, bacteria, and archaea are engaged critically with one other and involved in mutualistic functioning of the ecosystem. According to Blackwell (2011), 1 g of soil may approximately contain up to 200 m

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fungal hyphae and 6000–50,000 species of bacteria most of which are considered beneficial to the plants as well as soils (Mishra et al. 2015). Their direct relationship or association with root of plant leads to mineral uptake from the soil, decomposition of organic matter, nutrient acquisition, and also help in phytopathogen suppression as well as plant growth promotion (Nihorimbere et al. 2011). As a naturally occurring entity, soil also contains harmful microorganisms that parasitize or invade plants and reduce productivity. Soil fungi having 1.5 million fungal species typically make up the highest percentage of the soil communities (Robertson and Groffman 2007), but only 5–10% have been described formally (Laughlin and Stevens 2012) and are considered as major contributors to the processes of soil nutrient recycling that includes nitrogen mineralization, immobilization, and transformation (Selim et al. 2012). The soil bacteria known as PGPR are potential microbes that facilitate plant growth either directly or indirectly by colonizing the plant root (Goswami et al. 2016; Ahemad and Kibret 2014; Mishra and Arora 2012; Lugtenberg and Kamilova 2009). There is well-documented literature that describes the effectiveness of PGPR in sustainable agriculture (Arora et al. 2016; Ahemad and Kibret 2014). Their indirect role has been noticed in their growth inhibition activity on phytopathogens through one of their various mechanisms such as production of antibiotic, antimicrobial or antifungal metabolite(s), induced systemic resistance (ISR), iron depletion from the rhizosphere, competition for binding site(s) on the roots, and production of fungal cell wall lytic enzymes (Vejan et al. 2016). Additionally, PGPR are also recognized as potential microbial communities that can protect the plant from various normal environmental stresses as well as artificially stressed environments (Khare and Arora 2011; Kang et al. 2014).

4.3.2.1

Biofertilizer

The term “biofertilizer” is a contraction of biological fertilizer, which differs from the term “organic fertilizer”. Biofertilizers consist of microorganisms that add to the nutrient status of the host (plant) via their symbiotic relationship, while organic fertilizers consist of compounds, organic in nature, that increase fertility of the soil either directly or indirectly (Padda et al. 2017). The biofertilizer is a substance that contains living organisms that, when applied as seed treatments or on surfaces of plants, colonizes the interior or the rhizosphere of the plant and serve as growth promoters by enhancing the supply or availability of micronutrients needed for growth by the host plant (Padda et al. 2017; Kumar et al. 2016a, b; Jat et al. 2015; Maurya et al. 2014; Bahadur et al. 2014). Again, Bhattacharjee and Dey (2014) define biofertilizers as substances containing living microbes which colonize the rhizosphere of the plants leading to an increase in the availability or supply of primary nutrients and/or growth stimulus to the target plant. Biofertilizers are applied in the greenhouses or agricultural fields as replacement to chemical fertilizers. They are gaining acceptance due to the maintenance of soil quality, health, minimizing environmental pollution, and cut down on the use of synthetic chemicals

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in agriculture (Saeed et al. 2015). Different beneficial soil microbes have been used as biofertilizers for various crops as shown in Table 4.2. For example, PGPR applied as biofertilizer provides macro- and micronutrients; help in enhancing defense mechanisms and tolerance of the host against plant pathogens (Hafeez et al. 2013). In addition to the fact that they are cost-effective and inspire plant growth, biofertilizers are environmentally friendly method compatible with the beneficial microorganisms like PGPR, mycorrhiza, actinomycetes, and cyanobacteria instead of harmful pesticide and artificial fertilizer (Gupta et al. 2015). Cyanobacteria are naturally ubiquitous and photosynthetic prokaryotes commonly found in ponds, lakes, springs, streams, wetlands, and rivers that are also important component of soils (Singh et al. 2016a, b). Their abundance was first noticed by Fritsch (1907) in the rice fields and De (1939) further described their importance in the maintenance of rice-field fertility due to N2 fixation and considered them as a natural biofertilizer (Sahu et al. 2012). The algal-based biofertilizer is another easily usable input perpetually yielding a self-generating system that enhances soil nutrient status. In addition to contributing 20–25 kg N per hectare in one season, they also excrete growth-promoting substances, add organic matter to the soil, and also enhance the efficiency of fertilizer utilization of the crops (Meena et al. 2017).

4.3.2.2

Arbuscular Mycorrhizal Symbiosis

The most primitive living beings on the earth planet are the microorganisms, whose origin dates back ~3.5 billion years (Burchell 2010). Apart from the PGPR known to partake in numerous essential processes of the ecosystem, such as the nutrient cycling and biocontrol of phytopathogens, the well-known microbial symbionts are the arbuscular mycorrhizal (AM) fungi belonging to the phylum Glomeromycota (Schubler et al. 2001), which are known to form mycorrhizal relationships (associations) with the roots of most species of plant (van der Heijden et al. 2015). The AM fungi already acquired such adaptations and features for mutual coexistence with other divers living entities throughout their evolutionary process thus establishing different interaction in functions (Taylor et al. 2012). Among the various ongoing biological associations existing among all life forms, mycorrhizal symbiosis—is the most prevalent and best-known interaction between the plant roots and soil (Zuccaro et al. 2014). They possess the ability to form mutual, symbiotic, and beneficial interactions with the roots of most important plants (Munyanziza et al. 1997). During this association, they form extensive extraradical hyphal networks in the roots that enhance the nutrient absorption ability of the roots in the plant (George 2000). The advantage of AM fungi particularly in restoring problematic soils and in improving plant growth and plant resistance to diseases is known very well (Rillig 2004). Different researchers have discovered that certain species of plants are generally more responsive to mycorrhizal colonization than others (Bonfante and Genre 2008), and this response could be both AMF-specific and crop-specific. According to Smith and Read (2008), mycorrhizal symbiosis takes place in about 250,000 species of plants globally, including the major arable crops. Based on the

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Table 4.2 Description of some beneficial soil microbes-based (BSM) biofertilizers Biofertilizer type Phytohormones producers

Nitrogen fixers

Microbes used Bacillus, Mycorrhiza, Rhizobium, Pseudomonas, and Burkholderia

Rhizobium spp.

Azotobacter spp.

Azospirillum spp.

Azolla spp.

Cyanobacteria

Phosphate solubilizers

Potassium solubilizers

Bacillus spp., Mycorrhiza spp., Rhizobium spp., Pseudomonas spp., and Burkholderia Bacillus spp., Pseudomonas spp., and Burkholderia

Zinc solubilizers

Pseudomonas spp. and Bacillus spp.

Source: Modified from Mishra et al. (2017)

Description Produce phytohormones such as cytokinins, auxins, ethylene, and gibberellins that can affect cell proliferation in the root through overproduction of lateral roots and root hairs with a subsequent increase in nutrient and water uptake. The enzyme 1-aminocyclopropane-1 carboxylic acid (ACC) is a pre-requisite for ethylene production, catalyzed by ACC oxidase Known for their ability to fix atmospheric N2 via symbiotic association with plants forming nodules in roots Fixes high N2 level leading to rapid growth in different agricultural soils Azospirillum is a free-living and nonsymbiotic N2 fixer, beneficial to a wide array of crops including vegetables, cereals, sugarcane, and cotton It is a water fern that has asymbiotic relation with green, blue algae and can help in rice or other crops cultivation Some cyanobacteria have terminally differentiated, specialized structures called heterocyst and considered as photodiazotrophs. Their presence in rice fields provided aid in nitrogen fixation PSB and Mycorrhiza can help in improving uptake of an insoluble form of phosphate to plants in different ways Solubilise potassium present in the insoluble form of rocks and silicate minerals Solubilize zinc compounds like zinc carbonate (ZnCO3), zinc oxide, (ZnO) and zinc sulfide (ZnS) and may reduce the rate of costly zinc sulfate

References Ahemad and Kibret (2014)

Baset Mia and Shamsuddin (2010) Siddiqui et al. (2014) Bashan (1993)

Carrapico et al. (2000)

Kaushik (2014)

Duarah et al. (2011)

Shanware et al. (2014) Ahemad and Kibret (2014)

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taxonomy of the mycorrhizal symbiosis, divergent groups have been accepted with distinct morphological forms in relation to the presence of various hyphal network structures (Filho et al. 2017; Bonfante and Desirò 2015; Bonfante and Perotto 2000). Three distinct forms of mycorrhizal associations are recognized depending on the mycelium colonization of the root, and they include endomycorrhizas, ectomycorrhizas, and pseudomycorrhizas (ectendomycorrhizas) (Smith and Read 2008). The arbuscular mycorrhizal fungi represented the most studied mycorrhizal interaction among the endomycorrhizas (Balestrini et al. 2015; Smith et al. 2009). Symbiosis in AM fungi occurred in distinct steps, depicted by the extent of hyphae progression at the time of root colonization (Gutjahr and Parniske 2013). The first step is “presymbiotic” which means the mutual recognition, and the second step is “symbiotic” which means the appressorium and arbuscule formation (Zahedi 2016; Raghavendra et al. 2016; Dotaniya et al. 2016; Yu et al. 2014; Favre et al. 2014). The next step is known as “root colonization” which leads to alterations in the physiology of the plant (Hause et al. 2007), that cover the alterations from the transcriptional profile and hormonal balance to alterations in metabolism (both primary and secondary), which most of them are associated with defense mechanisms, likely contributing to the plant maintaining control over the symbiotic relationship (Pozo et al. 2015; Martín-Rodríguez et al. 2015; Fernández et al. 2014; Torres-Vera et al. 2014; Gutjahr 2014), and lastly mycorrhizal network formation (Walder et al. 2016; Gutjahr and Parniske 2013). After, all these stages are established, the plant now has to mediate the level of invasion by the fungus within the roots in order to avoid hyper-colonization and carbon drainage thus regulating relationship at mutualistic levels (Jung et al. 2012). Finally, a mycorrhizosphere is formed with a specific plant– microbe association (Barea 2015). Arbuscular mycorrhizal symbiosis plays an important function in enabling the plant to produce under stress conditions (Barea 2015). Parts of the attributes noted by researchers from AM fungi is their function in the phytostabilization of toxic element that polluted the soils by the mechanism of sequestration which help plant in mycorrhizal plants survive in polluted soils. Production of glomalin, which is a glycoprotein, is one of the components produced by the hyphae of AM fungi (Driver et al. 2005). This efficient mechanism has implications in minimizing the exposure of plant to toxic compounds with use of mycorrhiza remediation technology in sustainable soil–plant systems (Fig. 4.4). Other attributes of AM fungi (mycorrhizal symbiosis) includes that which confer resistance or tolerance of mycorrhizal plants to different types of abiotic stress (Miransari 2010), among which are reported recently in different papers on water stress (Pagano 2014), salinity (Abdel Latef and Miransari 2014; Hameed et al. 2014; Hajiboland 2013), metal stress (Manchanda and Garg 2011), toxicity (Cicatelli et al. 2014), and soil acidification (Muthukumar et al. 2014). At present, there is no available information concerning the mode of action implemented by arbuscular mycorrhizal fungi themselves to tolerate the harmful effects stimulated by stresses despite their potentials to provide protection to plants against several adverse climatic and edaphic conditions (Singh et al. 2016a, b; Lenoir et al. 2016).

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Fig. 4.4 Symbiotic association of arbuscular mycorrhizal fungi and the plant root system observed under the rhizosphere: An overview. Source: Meena et al. (2017)

4.4 4.4.1

Roles of Microbes in Sustainable Crop Protection for Food Security Role of Biocontrol Agents in Pest Management

It has been observed recently that in the course of production and storage of agricultural products, pests (invertebrates, plant pathogens, and weeds) caused about 40% of the potential global crop yield loss which results in cost increment and another 20% is destroyed by postharvest pests and diseases (Bailey et al. 2010). The challenges facing pest control are so many that old methods are not enough and therefore need improvement. Pest control should give emphasis to ensure food security through enhancement of crop productivity, decreasing food contamination by toxins produced by microbes, and supply of different and reasonable food prices (Ahmad et al. 2016; Jat et al. 2015; Parewa et al. 2014). However, for sustainable environment and agriculture, utilization of chemical-based pesticides should be regulated due to their negative effects on the environment. The use of biofertilizers, phytostimulators, and BCAs with proper crop management practices together is a welcome choice in agricultural sustainable practices due to their compatibility nature or efficiency to reduce overdependence on the intensive applications of agrochemicals (Adesemoye et al. 2009). The term “biocontrol” is a contraction of the synonym “biological control” which means purposeful and artificial use of resident or introduced microorganisms, to deter or suppress pest populations as well as their activities (Pal and McSpadden

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Gardener 2006). The term “biocontrol agent” is the organism that suppresses the pathogens or pest populations. Biological control agents (BCAs) or biocontrol agents are also known as microbial pesticides (biopesticides). Biopesticides are substances derived from natural materials including plants, animals, and minerals (Mishra et al. 2016). Microbes used as biocontrol agents are grouped into three major categories, namely fungal, bacterial, and viral. Out of the microbial-based pesticides for crops, bacterial incorporated biopesticides claim about 74%, followed by fungalbased biopesticides with 10%, biopesticides from viruses with about 5–8% for predator-based biopesticides, and 3% for “other” biopesticides (Thakore 2006). Among the bacterial pesticides, the genus Bacillus and Pseudomonas are the most widely used organisms. Chattopadhyay et al. (2004) reported that in the USA, Bacillus thuringiensis (Bt) accounts for about 90% of the biopesticide in the market, just as Arora (2015) reported that biopesticides containing Pseudomonas syringae and Pseudomonas fluorescens are now in use at large scale. Trichoderma harzianum is included in most of the fungal biopesticides and, used against phytopathogens. It is reported by Hartmann et al. (2008) as an important antagonist of various soil-borne fungi like Pythium, Rhizoctonia, Fusarium, and other phytopathogens. Other examples of fungi considered as good BCAs Baevuria bassiana and Metarhizium anisopliae which are naturally occurring entomopathogenic fungi that are infectsucking pests including Creontiades sp. (green and brown mirids) and Nezara viridula L. (green vegetable bug) (Sosa-Gomez and Moscardi 1998). The main viral BCA is baculovirus which is commercially utilized for designing phage pesticides and over 24 baculovirus species have been reported to be registered for use in insect–pest management throughout the world (Kabaluk et al. 2010). Table 4.3 shows some of the major biopesticides utilized in agroecosystems.

4.4.1.1

Mechanism of Control by Strains Biocontrol Agents (BCAs)

In recent times, numerous research attempts have been conducted to reveal the modes of actions of plant and microbial interactions (Beneduzi et al. 2012). The earliest mechanism of biological control studied are associated with the indirect role of the biocontrol agents such as iron depletion from the rhizosphere by secreting compound-like siderophores (synthesizing iron chelators) that effectively sequester iron and neglect the pathogen from the element, induced systemic resistance (ISR), production of fungal cell wall lytic enzymes such as β-1,3-glucanase and chitinase, production of biosurfactants, toxins and antifungal or antibiotic metabolites, and competition for binding site(s) of minerals in the roots (Vejan et al. 2016; Haas and Defago 2005; Raaijmakers et al. 2002) (Fig. 4.5). The genus Pseudomonas is one of the best and most widely used bacteria, which serve the role of BCAs in various species of plants. Examples of the Pseudomonas species known to produce various antibiotics like 2,4-diacetylphloroglucinol (2,4-DAPG), phenazine-1-carboxylic acid (PCA), pyoluteorin (Plt), pyrrolnitrin (Prn), and oomycin and considered as potential BCAs are P. syringae, P. fluorescens, P. aeruginosa, and P. putida, etc. (Ligon et al. 2000; Raaijmakers and Weller 2001). Genetic analysis shows that

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Table 4.3 Some microbial-based biopesticides used in agroecosystems Group PGPR

PGPF

Biocontrol agents Pantoea agglomerans Agrobacterium radiobacter Pseudomonas syringae Pseudomonas aureofaciens Pseudomonas fluorescens Pseudomonas syringae Pseudomonas chlororaphis Pseudomonas resinovorans Pseudomonas alcaligenes Bacillus pumilus Bacillus licheniformis Bacillus amyloliquefaciens

Trade name BlightBan C9-1 NoGall AgriPhage Spot-Less Esvin, Biomonas Bio-Save 10LP At-Eze Agriphage Not known Sonata EcoGuard Taegro

Bacillus subtilis

Kodiak

Bacillus popilliae

Milky spore powder Dipel WP, Batik

B. thuringiensis subsp. kurstaki B. thuringiensis subsp. israelensis B. thuringiensis subsp. aizawai Aspergillus flavus Candida oleophila Trichoderma harzianum Trichoderma viride Trichoderma gamsii Trichoderma polysporum Pythium oligandrum Alternaria destruens Beauveria bassiana Paecilomyces fumosoroseus Verticillium lecanii Metarhizium anisopliae

Target pest Fire blight Crown gall disease Bacterial speck Turf fungal diseases Bacterial wilt, root rot Postharvest diseases Seed-borne fungi Insect pest control Locusts, grasshoppers Seedling diseases Downy mildew, Fusarium wilt Fusarium and Rhizoctonia wilt diseases Fusarium, Pythium, and Rhizoctonia Japanese beetle grubs Lepidoptera pests

VectoBa

Lepidoptera pests

Turex

Lepidoptera pests

Afla-guard

Aspergillus flavus producing aflatoxin Postharvest disease Soil-borne pathogens

NEXY Biozim, Phalada 105 Monitor, Trichoguard Remedier, Bioten Binab T Polyversum Smolder Naturalis L, Botanigard Preferal WG ABTEC, Ecocil Biomagic, Biomet

Soil-borne pathogens Soil-borne pathogens Soil and foliar diseases Root rots Herbicide—dodder Thrips, whitefly, and mites Greenhouse whiteflies Whitefly, coffee green bug Coleoptera and lepidopteran insect

a PGPR Plant Growth Promoting Rhizobacteria, PGPF Plant Growth Promoting Fungi. Source: Modified from Mishra et al. (2017)

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Fig. 4.5 Schematic overview for mode of actions by Pseudomonas on disease management and plant growth promotions. Source: Kumar et al. (2017)

production of 2,4-diacetylphloroglucinol (2,4-DAPG) antibiotic by Pseudomonas indicated a positive correlation between disease separation and antibiotic production as in the disease of wheat caused by fungus Gaeumannomyces graminis var. tritici that act as a BCA that suppress the disease. Another genetically modified strain of Pseudomonas known as Pseudomonas syringae strain 01 CE prevents different crops from cold frost. Pseudomonas is an important biocontrol agent that combats phytopathogens in different crops such as tomato, chickpea, and wheat (PérezMontano et al. 2014; Dashti et al. 2012). In case of tomato plants, P. fluorescens showed strong chemoattractants towards some amino acids such as Gly, Cys, Ile, Met, Lys, Phe, Ser, and Pro which lead to effective root colonization and plant disease management (Oku et al. 2012). Duffy and Defago (1999) reported that the addition of glucose enhanced DAPG production in Pseudomonas strains, while phosphate fertilizer supplementation suppressed the DPAG production in P. fluorescens. Another important microbe considered as a potential biocontrol agent for sustainable crop protection is Paenibacillus polymyxa formerly known as Bacillus polymyxa (Jaiswal et al. 2016; Raghavendra et al. 2016; Dotaniya et al. 2016; Zahedi 2016). The genus Paenibacillus belong to the family Paenibacilliaceae (Yasin et al. 2016; Yadav and Sidhu 2016; Dominguez-Nunez et al. 2016; Das and Pradhan 2016) as it was reclassified into the family Paenibacilliaceae by Ash et al. (1991) and officially announced and approved by the International Committee on Systematic Bacteriology (1994) through their official journal. Beatty and Jensen (2002) reported that the two categories of antibiotics produced by P. polymyxa are effective against some fungi at one hand and effective against some bacteria at the other hand. Again P. polymyxa (B5 and B6) strains show antagonistic effect against Aspergillus niger (Haggag and Timmusk 2008). Similarly, strains B5 and B6 viewed under scanning electron microscopy (SEM) colonized the roots of peanut and decrease the disease-causing potentiality of A. niger thereby reducing the development of the disease (crown rot). It was also reported that these strains increase the activity of plant defense enzymes including β-1,3-glucanase and chitinase, which might be the reason behind the suppression of pathogen activity (Haggag and Timmusk 2008; Haggag 2007). Another strain of P. polymyxa (WR-2) showed a similar antagonistic effect against Fusarium oxysporum f. sp. niveum (Raza et al. 2015). Strain WR-2 inhibited the growth of fungal pathogen by ~40% in three different media (natural

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soil, sterilized soil, and agar), and this inhibitory effect was increased to about 60% with the addition of organic fertilizer. Raza et al. (2015) also reported that the growth of F. oxysporum was inhibited by strain WR-2 through the production of seven different volatile organic compounds, including benzaldehyde, benzothiazole, undecanal, hexadecanal, dodecanal, 2-tridecanone, and phenol. In another study, P. polymyxa strain CF05 showed in vitro antagonism against F. oxysporum f. sp. lycopersici that causes Fusarium wilt of tomato.

4.5

Challenges and Future Prospects

Currently, we know that there is a probability that the global population will exceed the quota of nine billion by 2050 (Shelden and Roessner 2013; Godfray et al. 2010; FAO 2009), just as the United Nations (2015) reported that the world’s population is set to reach ~9.7 billion by 2050, which is fourfold of the 1950 population. By 2025, the world’s production of agricultural produce should be improved by over 40% in order to satisfy the increasing demands (Pennisi 2008), as well as to provide food security for over 870 million people presently under hunger, according to the Organization for Economic Co-operation and Development (OECD) and the Food and Agriculture Organization of the United Nations (FAO) (2012). The excessive use of inorganic fertilizers, chemical pesticides, and various other anthropogenic activities in intensive agriculture are destroying the agroecosystems deliberately and the balance of our planet. As a consequence, crop productivity and loss of soil fertility have generated concern among agriculturists, and their awareness of using beneficial microbes in the agroecosystems has gained acceptance for enhancing crop productivity and improving soil quality in its natural form. These microbes are endowed with diverse mechanisms to work as efficient and potential candidates in the sector of sustainable agriculture and environmental management. It has been shown that in properly managed-agriculture systems, microbial communities act as biofertilizers, soil improvers, and biocontrol agents. Beneficial microbes used as biocontrol agents tend to be specific in their actions and are eco-friendly. Their role in agricultural sustainability and crop protection can easily be expanded if we successfully find some unrevealed concepts related to their population dynamics, ecology, and their functionality over different environments. In the near future, the agricultural sector will depend on beneficial microbes to increase crop production in an eco-friendly manner to meet the global demand for food security for the doubling increase in the human population.

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Concluding Remarks

The role of microbial communities in environmental management and sustainable agriculture should not be overemphasized as it offers countless benefits. Their application in the form of biopesticides and biofertilizers is gaining popularity and providing substantial aid to the ecosystems. Their ability to survive under harsh environmental conditions makes them potential candidates in various types of stress management. Additionally, their catabolic efficacy and diversity can be used in the removal of recalcitrant pollutants. Our understanding of the beneficial microbes response in the agroecosystems is increasing, and their potential significant effects on the restoration of environment are also strengthening and collectively helping to obtain the goal of sustainable development. As a consequence, the impact of climate change particularly in the agricultural sector can also be minimized by the application of these microbes. However, considering the perspective of climate change, effective utilization of beneficial microbes requires more investigations and it has been realized that elucidation of different mechanisms involved in their association with plants in extreme conditions may also provide better chance of their vast application in environmental as well as agricultural sustainability.

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Chapter 5

Sustaining Productivity Through Integrated Use of Microbes in Agriculture Rakesh Kumar, Kirti Saurabh, Narendra Kumawat, Prem K. Sundaram, Janki Sharan Mishra, Dhiraj K. Singh, Hansraj Hans, Bal Krishna, and Bhagwati Prasad Bhatt

Abstract In intensive agriculture, integrated plant nutrient management takes care of both crop nutritional needs as well as soil fertility considerations leading to increased crop yields through judicious consumption of inorganic nutrients in cropping systems. There is an urgent need to reduce the usage of chemical fertilizers and in turn increase application of microbes along with organic manures, which are known to improve the physicochemical properties of the soil and supply of nutrients in an available form to plants. Therefore, integrated use of microbes for nutrient and disease management, along with organic manures and inorganic fertilizers simultaneously has been suggested as the most effective method to maintain a healthy and sustainable soil, while increasing crop productivity. Inoculation with these methods was found to increase crop yields by ~10–15% under farm conditions. In many situations, this association also leaves substantial amounts of residual nitrogen fixation for subsequent cropping systems. Use of biofertilizers requires special skills and therefore farmers need to be equipped with the knowledge and skills of using

R. Kumar (*) · K. Saurabh · J. S. Mishra · H. Hans Division of Crop Research, ICAR Research Complex for Eastern Region, Patna, Bihar, India e-mail: [email protected] N. Kumawat AICRP on Management of Salt Affected Soils and Use of Saline Water in Agriculture, College of Agriculture, RVSKVV, Gwalior, Indore, Madhya Pradesh, India P. K. Sundaram Division of Land and Water Management, ICAR Research Complex for Eastern Region, Patna, Bihar, India D. K. Singh Division of Socio-Economics and Extension, ICAR Research Complex for Eastern Region, Patna, Bihar, India B. Krishna Division of Plant Breeding and Genetics, Bihar Agricultural University, Sabour, Bihar, India B. P. Bhatt ICAR Research Complex for Eastern Region, Patna, Bihar, India © The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2021 G. Seneviratne, J. S. Zavahir (eds.), Role of Microbial Communities for Sustainability, Microorganisms for Sustainability 29, https://doi.org/10.1007/978-981-15-9912-5_5

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various biofertilizers in order to promote sustainability. Hence, this chapter enlightens the reader on the effect of different microbes [Rhizobium, phosphate solubilizing bacteria (PSB), and plant growth promoting Rhizobacteria (PGPR)] alone as well as in combinations with organic and inorganic additives on crop productivity and soil health. Keywords Crop yields · Nutrient solubilizing microbes · Nutrient dynamics · Soil health

Abbreviations AEC/CEC AFM AgNPs AIMs AM AMF BMPs CA EDX FAO GA GHG IAA INM ISFM KSMs LUM MBC MT NPs NT NUE PBRMs PGP PGPMs PGPR PSA PSB SEM SOC SOM TEM WSAs WUE Zn

Anion and cation exchange capacity Atomic force microscope Silver nanoparticles Agriculturally important microorganisms Arbuscular mycorrhiza Arbuscular mycorrhizal fungi Best management practices Conservation agriculture Energy dispersive X-ray spectroscopy Food and Agriculture Organization Gibberellic acid Greenhouse gas Indole acetic acid Integrated nutrient management Integrated soil fertility management Potassium solubilizing microorganisms Land use management Microbial biomass carbon Minimum tillage Nanoparticle No tillage Nutrient use efficiency Plant beneficial rhizospheric microbes Plant growth promotion Plant growth promoting microorganisms Plant growth promoting Rhizobacteria Particle size analyzer Phosphate solubilizing bacteria Scanning electron microscopy Soil organic carbon Soil organic matter Transmission electron microscopy Water-stable aggregates Water use efficiency Zinc

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Introduction

The world consumption of nitrogen, phosphorous, potassium (NPK) fertilizers during 2010–2011 was reported to be ~104, 41, and 28 MT, respectively and forecast figures for these fertilizers during 2016–2017 are ~115, 46, and 33 MT, respectively. However, the demand of NPK nutrients during 2011–2015 was estimated to increase by 1.5, 2.3, and 3.7% annum, respectively. Furthermore, of nutrients supplied externally, only a small proportion of fertilizer applied to soil is actually utilized by plants. Consequently, ~40–70% N, ~80–90% P, and ~50–70% K of total applied conventional fertilizers are lost to the environment due to different soil dynamics (Fageria 2014). This level of loss in agricultural nutrients not only leads to yield reduction and loss of valuable resources but also severely pollutes ecological sustainability. Hence, it is essential to improve the use of applied fertilizers to achieve the optimum crop yield and higher nutrient use efficiency (NUE) (Rakshit et al. 2015). Improvement in NUE and agricultural production with reduction of inorganic fertilization for economic as well as environmental reasons will require new technologies (Dobermann 2005). Over the last three decades, agronomy has been playing an important role in increasing NUE and crop productivity via better crop management, proper selection of fertilizer sources, amount, time, and method of application, introduction of new varieties, etc. (Bashan et al. 2016; Kumar et al. 2017a, b). Moreover, acknowledging critical contribution of agronomy to improve efficient nutrient use, genetic improvement becomes essential for further improvement (Samal et al. 2017; Singh et al. 2017d). This may be achieved by marker-assisted breeding in which genetic information is derived from basic plant science, and utilization of this information is used to produce genetically modified crops which utilize nutrient efficiently (Yin et al. 2016; Kumawat et al. 2017a). However, some limitations are associated with this breeding technique including requirement for long-term and variable responses in heterogeneous environment. Hence, there are quick techniques needed to increase NUE in order to increase crop yields to fulfill food requirements of ever-increasing populations (Kumar et al. 2013a, b, c; Kumar and Kumawat 2014). Integration of new generation technologies like ecological and molecular approaches is being utilized by the world agriculture community to achieve more yield while minimizing negative impact on environment (Meena et al. 2010a, b, c; Huang et al. 2017). Microorganisms that sustain soil fertility, resulting in improved plant nutrition have continued to magnetize attention because of the increasing cost of agricultural inputs and some of their negative impacts on environmental sustainability (Kumar et al. 2014a, 2016b). Continuous increase in the world population at an alarming rate requires more food for nutritional security (Kumar et al. 2015a). A doubling in global food demand projected for the next 50 years poses huge challenges for agricultural sustainability. Nowadays, plant growth is enhanced by increasing input of agrochemical, which acts as plant growth regulators (PGRs) and as nutrients (Kumar et al. 2008, 2013a, b, c; Kumari et al. 2014; Kumar 2015a, b). Excessive or injudicious use of chemicals increases the chances of deteriorating soil and

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environmental quality. Rhizospheric plant growth promoting microorganisms (PGPMs) are increasingly and promisingly being distributed in world agriculture. Meanwhile, the current use of these efficient PGPMs may offer agronomic, pathogenic, environmental benefits for intensive agricultural production systems. PGPMs are exhibiting a gradual increase in demand on the world market as sustainable and eco-friendly tools (Kumar et al. 2019; Prasad et al. 2019; Mishra et al. 2019). Possible mechanisms for effectiveness of biofertilizers are mobilization of scarcely available plant nutrients N-fixer P, K, and Zn solubilizers; production of plant growth promoting substances; enhanced or induced resistance to environmental multi-stress factors; and direct or indirect suppression of harmful microbes (Thirugnanavel et al. 2019; Mondal et al. 2019; Kumawat et al. 2019a). Research activities are currently limited by lack of the standards for production and quality control of different commercially used biofertilizers. Plant growth promoting rhizobacteria (PGPR) are a heterogeneous group of soil bacteria that inhabit rhizosphere, around/on root surfaces, which improve plant growth directly or indirectly via production and secretion of various regulatory substances. PGPR affect plant growth and development either by releasing phytohormones or other biologically active substances, altering endogenous levels of plant growth regulators (PGR), enhancing availability and uptake of nutrients through fixation and mobilization, reducing harmful effects of pathogenic microorganisms on plants, or employing multiple mechanisms of action. In recent times, PGPR have received more attention for its use as a biofertilizer for sustainability of agroecosystems. Numerous studies have suggested that PGPR in an integrated nutrient management (INM) system could be used as effective supplements to chemical fertilizers for promoting crop yields and soil health on sustainable basis. In prospect of healthy and sustainable agriculture, PGPR approaches are revealed as one of the best alternatives. The agricultural sector plays a key role as a backbone in process of economic development of a country. According to estimates from the FAO of the United Nations (2014), ~11% (1.5 billion ha) of global land surface (~13.4 billion ha) is used in crop production. This area represents slightly over one-third (~36%) of land estimated to be, to some degree, suitable for crop production (Singh et al. 2017a, b, c). To fulfill the demand for food requirements, agricultural farmers have used injudicious application of agrochemicals, i.e., fertilizers and pesticides, for crop production (Kumari et al. 2010; Kumawat et al. 2013). However, in most countries, there is no scope to further increase the availability of agricultural land. Nowadays, global agriculture is faced with the serious challenge of providing adequate and sustainable food production for over ~7 billion people and next generation (FAO 2012). Such an increase in population growth will intensify pressure on a global resources base to achieve sustainable food production by intensifying cropping intensity to improve productivity (Kumar et al. 2018b, c, d). On other hand, there is an increasing demand for land to build new homes, public institutions, roadways, railways, and other developments to accommodate growing populations. This in turn decreases the availability of agricultural land for the next generation (Kumari et al. 2012; Kumar et al. 2014b, 2015b; Bahadur et al. 2017). Sustainable management of soil health, crop residue management (CRM), water

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dynamics, soil loss, and C-sequestration are all dependent on sustainable crop production system (Kumar et al. 2013a, 2016c, 2017a, b, c). Sustaining food production is an urgent need for global food security for future generations (Kumar et al. 2015a, b, c, d, e). However, there is an urgent need to search for possible ways of sustaining food production without deteriorating soil and environmental quality (Kumawat et al. 2017b, c, d). Balanced use of agricultural input and improved technologies introduced over the past few decades are now almost reaching a point of diminishing returns (Dawe et al. 2000; Singh et al. 2010, 2014, 2017d). The possibilities of converting marginal lands into productive land as an option for productivity improvement are now becoming increasingly limited (Karforma et al. 2012; Kumar et al. 2017a, 2018a). Genetically engineered plants also may not be major factors in increasing food grain production in the near future. A sustainable system that can maintain agricultural productivity at a higher level without causing deterioration of ecosystems is thus the need of hour (Nath et al. 2017; Saurabh et al. 2020).

5.2

Current Status of Soil Fertility

Soil is a critical component of earth’s systems, sustaining the whole biomes, functioning for production of food grains and assisting in maintenance of global environmental quality (Pathak 2010). Increased farming produced through introduction of high yielding varieties (HYVs), intensive use of chemical fertilizers and pesticides, and extensive tillage are first choice methods for most farmers. There are now concerns whether dramatic increase in production of food crops following the success of the Green Revolution is sustainable in the long-term and whether it is worthy of sustainable evergreen agricultural production system (Table 5.1). Soils rated as high can show significant responses to applied N, P, K, S, and Zn in certain soils, crops, and climatic situations. Thus, soil test methods for categorizing soils into low, medium, and high nutrient values need further refinement for better soil test/crop response correlation.

Table 5.1 Present status of nutrient use efficiency (NUE) of agricultural ecosystem

Nutrients Nitrogen (N) Phosphorus (P) Potassium (K) Sulfur (S) Zinc (Zn) Iron (Fe) Copper (Cu) Manganese (Mn)

Nutrients use efficiency (NUE %) 30–50 10–20 >80 8–12 2–5 1–2 1–2 1–2

Adopted from Meena et al. (2017)

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375

400 350 284

NPK (kg ha-1)

300 250 200

204.9 156.1

188.3 122.1

150

101

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107

100 50 0 India

Pakistan Bangladesh

China

Korean Republic

Egypt

Sri Lanka

Indonesia

U.S.A

World Average

Country

Fig. 5.1 The worldwide fertilizers (NPK) used by the farmers (Meena et al. 2017)

A serious attitude towards fertilization is still lacking among farmers and extension workers. There is an urgent need to educate farming communities about the importance of balanced fertilization in worldwide agricultural systems (Fig. 5.1) for nutrient balance and efficiency, top crop yields, quality, and farmer profitability. Lack of farmer awareness about the importance of balanced fertilization indicates the need for extra consciousness (Kumawat et al. 2009a, 2017b, c; Shivran et al. 2013; Kuotsuo et al. 2014). For example, farmers may not realize the effect of applied NPK on size, shape, and quality of produce at maturity, so its need may be overlooked (Kumawat et al. 2010). In contrast, benefits from N and P are more readily apparent from initial stages of crop growth (Meena et al. 2010a, b, c, 2011). However, significant responses to applied NPK may be noted in high fertility status of agricultural soils. In most tropical countries, organic carbon (OC) content of agricultural soils is very low (100 years and passive pool of C has a turnover time in the order of >103 years (Trumbore 1997). Carbon input, magnitude of SOC pools, and finally C mineralization depends on many factors. However, changing patterns of land use types and land use management (LUM) practices had significant direct and indirect effects on SOC pool, while impact of land use type changes on SOC pools in mineral soil depends also on long-term, site-specific factors and is often overridden by high spatial heterogeneity of SOC in soil–plant systems.

5.6

Soil–Microbe System

SOM formed from dead plants—containing carbon (C), oxygen (O), and hydrogen (H)—is the basic food and energy source for soil/rhizospheric microorganisms. The essential minerals required for growth of rhizospheric microorganisms are similar to needs of plants (Kumar et al. 2014a, b, c, 2016a). Most macro-and micronutrients are needed in small amounts and are mainly found in protein and nucleic acids of microbes. Therefore, an adequate supply of N is needed for the rapid decomposition of SOM. The optimum C to N ratio is 30:1. However, straw and similar mulches have a high C to N ratio (100:1), and when soil is covered with dense straw mulch plant growth is retarded because of N deficiency. These efficient microbes growing on straw consume most of the available forms of N and as a result small plants suffer from N deficiency. Optimum P content in a soil system for decomposition is 100:1. Root exudates provide many nutrients stimulating microbial growth in the rhizosphere surrounding the root tip. These microbes break down SOM, converting nutrients into soluble forms, which are able to be absorbed by the plant roots. Soil system is one of the most complex systems in an ecosystem that comprises a diversity of microhabitats with different physicochemical gradients and

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discontinuous environmental conditions. Microorganisms in such soil systems adapt to their microhabitats and live mutually in consortia with more or less sharp boundaries, interacting with each other and with other parts of soil-biota. A number of long-term investigations have emphasized the impact of soil structure and spatial isolation on microbial diversity and community structure (Das and Pradhan 2016). Results from different analyses of spatial distribution of bacteria/rhizobacteria at microhabitat levels showed that in soils subjected to different fertilization treatment, ~80% of rhizobacteria were located in micropores of stable soil micro-aggregates of 2–20 μm/water-stable aggregates (WSAs). Such microbes offer the most favorable conditions for microbial growth with respect to water and substrate availability, gas diffusion, and protection against predation. Here, soil aggregation and size distribution of different aggregates in soil systems had a greater impact on microbial diversity and community structure than did factors such as soil reaction (pH) and type and amount of organic compound input. Results showed that a biodiversity infraction with small soil particles was higher than that in a fraction of WSAs. A great diversity of rhizobacteria belonging to Holophaga/Acidobacterium division and Prosthecobacter were present in small particles (silt and clay). Large-sized particles (sand) harbored few members of Holophaga/Acidobacterium division and were dominated by rhizobacteria belonging to Alphaproteobacteria (Sarkar et al. 2017). The interaction of numerous physical, chemical, and biological properties in soils control plant nutrient availability in soil–plant systems. Understanding these processes and how they are influenced by environmental conditions enables us to optimize NUE, WUE, and plant productivity. This knowledge is essential for decisions regarding the management of nutrients to optimize plant growth and health, and to minimize nutrient application impacts on environment. Nutrient supply to plant roots is a very dynamic process (Bahadur et al. 2017). Plant nutrients are absorbed from soil solutions by plant roots, and as plant roots absorb nutrients, nutrient concentration in the soil solution decreases. As a result, several chemical and biological reactions occur to buffer or resupply these nutrients to soil solution. Microbial availability, as well as other properties, is related to soil productivity and sustainability. Soil quality of soil–plant system depends not only on its chemical composition but also on quantitative nature of microorganisms inhabiting it.

5.7

Application of PGPR in Agriculture and Soil Health

PGPR are mostly used as seed, soil, or foliar applications for improving yield of agricultural crop. They represent a component of biofertilizer technology, which is used to improve the productivity of agricultural crops in the long-term (Naiman et al. 2009). Various PGPR have shown great promise as potential inoculants for agriculture uses and environmental protection, and may consequently play very vital roles in maintaining sustainability of agroecosystems (Khalid et al. 2009). Selection of an effective PGPR strain is very critical, and plant responses are often variable depending upon PGPR strain, plant genotypes, and experimental locations. It has

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also been claimed that PGPR isolated from a particular crop or ecological zone are more effective in producing consistent results if reapplied to the same crop and reused in the same ecological zone (Nowak 1998). This might be due to a greater adaptability of introduced PGPR in a given rhizosphere, while inconsistency in responses of same crop to same PGPR could be attributed to (1) poor quality of inocula, (2) short shelf life of PGPR, (3) lack of standard delivery systems, and/or (4) failure in maintaining a required density of PGPR on seeds or roots. Moreover, nature and composition of material used as a carrier for a PGPR also play a significant role in producing its impact on inoculated plants (Khalid et al. 2009). However, current use of PGPR in agriculture is poor due to location-specific response, despite numerous reports on their fair performance under laboratory and field conditions. In this context, significant effects of PGPR have been observed on various agricultural crops including cereals, legumes, oilseed crops and horticultural crops, and other environmentally important plant species. Furthermore, impact of PGPR in an integrated manner increased soil fertility, microbial activity, and WUE (Arshad et al. 2008). Potential uses and benefits of PGPR in improvement of overall performance of agricultural crops and soil health are discussed herewith in the following sections.

5.7.1

Field Crops

Increasing demand for food and improving environmental quality have focused on the importance of PGPR in agriculture. PGPR have the ability to increase germination, seedling emergence, growth, vigor, and establishment and therefore yield of various cereals and non-cereal crops (Gravel et al. 2007) by enhancing availability of N (Anjum et al. 2007), Fe (Masalha et al. 2000), and P (Villegas and Fortin 2002) to agricultural crops. They improve plant growth and yield by a variety of ways, i.e., production of phytohormones, nitrogen fixation, phosphate solubilization, improvement in root morphology and are also useful in cutting down the cost of chemical fertilizers (Shrivastava et al. 2016). A plant’s root system is mainly characterized by its total length which is influenced by a number of factors like soil fertility, soil moisture, physicochemical properties of the soil, and occurrence of numerous PGPR. An enormous number of PGPR are known to promote plant growth, crop yield, seed emergence thus promoting agriculture (Parewa and Yadav 2014). Various studies have shown the effect of PGPR on plants. Plant properties like leaf area, chlorophyll content, total biomass were enhanced by inoculation of PGPR (Baset Mia et al. 2010). Enhanced mineral uptake in inoculated cereal plant was proposed as a possible mechanism of plant growth enhancement by PGPR. Inoculation effect of Azospirillum sp. on development of agriculturally important plants was assessed (Dobbelaere et al. 2001) and noted with a noteworthy boost in dry weight of both the root system and aerial parts of the PGPR-inoculated plants, resulting in better progress and flowering.

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Field experiment was conducted at Banaras Hindu University (BHU), Varanasi, India to study the response of fertility levels, farm yard manure (FYM), and bio-inoculants on yield attributes and yield and quality of wheat during 2009–2011. Seed bacterization with composite PGPR including (Azotobactor chroococum W5 + Azospirillum brasilense Cd + Pseudomonas fluorescens BHUPSB06 + Bacillus megaterium BHU PSB14) + Glomus fasciculatum (soil application) significantly increased yields of wheat than that to uninoculated control and other treatment (Parewa and Yadav 2014). Similarly, seed inoculation with Azotobacter (strain AZO-8) significantly increased yield attributes of wheat. Seed bacterization with Azotobacter (strain AZO-8) along with 60 kg N ha 1 (urea) and 40 kg N ha 1 (FYM) was most responsive treatment in respect of ~23 and 36% increase in shoot fresh and dry weight, ~26 and 38% increase in root fresh and dry weight, ~39% increase in test weight of seed, and ~27% increase in yield compared to control. Results clearly indicated that there was a saving of ~20 kg N ha 1, when Azotobacter (strain AZO-8) culture was used along with 60 kg N ha 1 (urea) and 40 kg N ha 1 (FYM) (Singh et al. 2013). Lavakusha et al. (2014) conducted a pot experiment at BHU, Varanasi, to study the effect of PGPR and different phosphorus levels on yield and nutrient content of rice (Oryza sativa). PGPR strains, e.g., Pseudomonas aeruginosa BHUJY16, P. aeruginosa BHUJY20, P. putida BHUJY13, P. putida BHUJY23, and P. fluorescens BHUJY29 were known as combined Pseudomonas culture (CPC). Treatment combination of (CPC + Azotobacter chroococcum + Azospirillum brasilense + 60 kg ha 1 P2O5) and (CPC + A. Chroococcum + A. Brasilense + 30 kg ha 1 P2O5) showed greater significant grain yield of rice compared to control. Combination of (CPC + A. Chroococcum + A. Brasilense + 30 kg ha 1 P2O5) gave at par results of yield and nutrient contents in grain of rice compared to PGPR combination with 60 kg ha 1 P2O5. Pulse crops are an important source of protein in Indian diets. But cultivation of pulses is confined to poor and marginal lands resulting in low productivity. Besides this, minimal application of chemical fertilizers and cultivation as rainfed crops could be attributed to poor yield or productivity of pulses in India. Since legume crops could fix atmospheric N by root nodulating Rhizobium sp., augmentation of symbiotic N-fixing bacteria along with PSB will result in increased biomass production and economic yield of many legume crops. Hence, applications of a combination of PGPR bacteria consisting of symbiotic nitrogen-fixing bacteria, P-solubilizers, and biocontrol agents to legume crop would result not only in increased yields but in reduced incidence of important diseases like root-rot and wilt (Velazquez et al. 2016). Combined inoculation of Bradyrhizobium, P. fluorescens, P. Striata, and Glomus mosseae significantly enhanced root nodulation, biological nitrogen fixation, and yield of soybean (Shabayey et al. 1996). Some PGPR strains enhanced legume growth, nodulation and nitrogen fixation, root and shoot biomass, nodule dry weight, and grain yield in chickpea (Parmar and Dadarwal 1999) and pigeon pea (Tilak et al. 2006). Combined inoculation of PGPR in pulses enhanced yields of Vigna mungo (Selvakumar et al. 2009); dry matter, grain yield, and P uptake in Cicer arietinum (Elkoca et al. 2008); yields, nutrient

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uptake, and net returns (Singh and Singh 2012), dry matter, grain yield, and macroand micronutrient uptake significantly over uninoculated control in legumes (Selvakumar et al. 2009); germination percentage of Cyamopsis tetragonoloba; and catalase, peroxidase enzyme activity, and yields of Vigna radiata. Thus, a number of studies have been conducted in various crops found that application of composite PGPR to these legume crops resulted positively. In semi-arid tropics, production levels of oilseed crops are hampered due to foliar and soil-borne diseases incited by fungal pathogens. Present management of these oilseed diseases using chemical fungicides has environment-related concern. Moreover, labeled fungicides are very expensive and are not affordable by small and marginal farmers, with utilization of these efficient PGPR as a viable alternative to enhance crop production. A synergistic effect in sunflower (Helianthus annuus) with triple inoculation of Azotobacter chroococcum, Penicillium glaucum, and Glomus fasciculatum has been observed (Gururaj and Mallikarjunaiah 1995). Seed inoculation of mustard with Azotobacter or Azospirillum significantly increased yields (Chauhan et al. 1995). Similarly, combined inoculation of Rhizobia with Azospirillum and phosphobacteria significantly enhanced higher pod yield in groundnut compared to individual inoculations (Balamurugan and Gunasekaran 1996). Ekin (2010) reported positive effect of combined inoculation with PGPR on grain yield, oil content, and nutrient uptake by oilseed crops. Application of PGPR enhanced pod yield, haulm yield, nodule dry weight and root length, as well as inhibited fungal pathogens like Aspergillus niger and Sclerotium rolfsii, causing collar and stem rot in Arachis hypogaea (Mathivanan et al. 2014); increased yields, oil and protein content in sunflower and soybean (Zarei et al. 2012).

5.7.2

Spice and Vegetables

Spice crops contribute a major portion of agricultural exports to the Indian economy. Major production constraints of spice crops are low soil fertility, poor-germination, poor-input management, slow initial growth, competition from weeds, and high susceptibility to diseases, insect, pest, and frost (Agarwal et al. 2001). Various spices crops, i.e., black pepper (Piper nigrum), fenugreek (Trigonella foenum-graecum L.), cumin (Cuminum cyminum L.), coriander (Coriandrum sativum L.), and fennel (Foeniculum vulgare L.) are cultivated in different agroclimatic zones in India. These crops require more input than other agricultural crops and sustainability maintenance is quite significant. For these reasons, there is a need for different techniques to increase input efficiency, of which PGPR have proved to be a major tool (Singh et al. 2016). PGPR can affect plant growth by production and release of secondary metabolites, preventing deleterious effects of phytopathogenic organisms in the rhizosphere and/or facilitating availability and uptake of N, P, and Fe from root environment. Application of N-fixers and P-solubilizers along with biocontrol agents for many economically important pests and diseases resulted in increased productivity, reduced input cost, and improvement in the quality of product. Since

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spice crops are cultivated in an intensive cropping manner, PGPR organisms were studied mainly in relation to their disease control/resistance mechanism and growth promotion by production of plant growth regulators in spices. Several researchers have reported that root and soil inoculation and/or foliar application of PGPR increased number of roots, biomass production, disease-free rooted cuttings, uptake of N, P, K, Mg, Fe, and Mn, and yield of spice crops. It is well documented that PGPR are used for different purposes in spice crop to improve plant growth and yields (Sumathi et al. 2011) and uptake of N and K, enhance nutrient mobilization in black pepper (Paul et al. 2001), produce robust disease-free rooted cutting of black pepper (Sarma 2000), suppress soil-borne fungal pathogens (Jisha et al. 2002). PGPR increase not only macro-and microelement composition but yields of vegetable crops by secreting plant growth promoting substances, i.e., growth hormones and enzymes. Nowadays, use of PGPR in production plays an important role as a supplement to improve the yield of several agricultural, horticultural, and medicinal plants (Rao 2008). There are several reports that PGPR promoted growth of cereals, ornamentals, vegetables and medicinal plants (Radha and Rao 2014). Potential of PGPR increased germination percentage, seedling vigor, emergence, root/shoot growth, biomass, seed weight, early flowering, grain fodder, and fruit yields of chilli (Ramamoorthy and Samiyappan 2001); root/shoot fresh weight, root dry weight, and total root length of tomato; and K uptake (Ordookhani et al. 2010) and higher oil, seed, and fruit yield of pumpkin (Habibi et al. 2011). Combined use of PGPR with N and P fertilizers significantly increased number of non-wrapper leaves, curd diameter, curd depth, and curd weight of cauliflower and induced indole acetic acid (IAA) production and P solubilization (Kaushal et al. 2011). Similarly, yield, quality, root length, and dry root weight of bitter gourd are enhanced by application of PGPR (Kumar et al. 2012).

5.7.3

Fruit Crops

Soil-plant-PGPR associations are mediated through an exchange of chemical metabolites. Root exudates provide energy-rich organic acids, sugars, and amino acids that are metabolized within a short time by soil microorganisms, while specialized microorganisms generate an array of biologically active compounds that elicit plant growth promotion. PGPR enhance growth and nutrient uptake of fruit crops in a number of ways. In recent years, use of PGPR in fruit crops enhances plant growth, development, and yield in various parts of the world. Several researchers have reported that root inoculation and/or foliar spray with PGPR can result in increased germination, seedling emergence, modified root architecture, and yield of various fruit crops. PGPR can be used for various purposes, i.e., rooting/cutting, grafting union, fruit setting and thinning, lateral root formation, and increasing tolerance against biotic stress as well as growth, development, and biological control with root inoculation and/or spraying. In addition, PGPR have been used for different purposes in horticultural crops like improving grafting union in grape

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(Kose et al. 2005), fruit setting (Esitken et al. 2006), and fruit thinning (Esitken et al. 2009). Jeeva (1987) reported that total soluble solids (TSS), total sugar, and sugarto-acid ratios were positively influenced by inoculation of Azospirillum to banana over uninoculated control.

5.7.4

Medicinal Plants

The World Health Organization (WHO) has estimated that ~80% of the global population relies on traditional medicines, mostly plant drugs, for their primary health-care. Moreover, modern medicines contain ~25% of drugs derived from plants. Medicinal plants are known to be rich in secondary metabolites and are potentially useful to produce natural drugs (Pouryosef et al. 2007). Medicinal plants are very important in modern civilization in order to obtain natural active substances known as secondary metabolites. An introduction of PGPR and arbuscular mycorrhizal fungi (AMF) is known to increase the growth of many plant species including medicinal plants. Leaves of Begonia malabarica are used for treatment of respiratory tract infections, diarrhea, blood cancer, and skin diseases (Kiritkar and Basu 1975). Yield, essential oil and secondary metabolites in many medicinal plants, i.e., Phyllanthus amarus, Withania somnifera, Mentha piperita, Solanum viarum, and Ocimum basilicum, increased by application of PGPR (Abdullah et al. 2012). Hence, use of microbial association for medicinal plants provides a sustainable approach to improving crop yields. Application of seed bio-priming as seed treatment delivers efficient microorganisms directly to plant rhizosphere (Philippot et al. 2013). Most of the beneficial rhizospheric microorganisms of agricultural importance are rhizosphere-colonizing species, with the ability to increase plant growth promotion (PGP) via a range of mechanisms (Babalola 2010). However, utilization of these efficient and beneficial soil microorganisms as agricultural input for improved crop productivity requires the selection of rhizosphere-competent microorganisms with PGP traits (Hynes et al. 2008). Beneficial PGP rhizobacteria are disease-suppressive rhizospheric microorganisms, which enhance soil–plant system sustainability. Results from previous long-term experiments and documentation abound, and all point towards the need to commercially exploit PGPR as biofertilizers for their agricultural benefits. From a general perspective, however, problems of variability in colonization efficiency, NUE, and rhizosphere competence are controversial issues (Bahadur et al. 2016). Efficient utilization of various bio-inoculants under field culture as well as pot-culture is seen as being very attractive, since it would substantially reduce the use of mineral fertilizations, and as a result there are now an increasing number of inoculants being commercialized for agricultural crops (Berg 2009). These efficient microorganisms play a key role in agricultural systems, particularly PGPMs with various mechanisms which include:

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• PGPMs acting as biofertilizers (N-fixing bacteria/rhizobacteria, P, K, Zn-solubilizing rhizobacteria) assist plant nutrient uptake by providing fixed N and other elements (Kennedy and Islam 2001). • Phyto-stimulators (microbes expressing phytohormones such as Azospirillum) can directly promote growth of plants (Glick et al. 2007). • Biological control agent (Trichoderma/Pseudomonas) protects plants against phytopathogenic organisms (Dawar et al. 2010). These efficient PGP rhizobacteria enhance availability, uptake of plant nutrients, enhancing NUE. Unlike adverse effects of continuous use of mineral fertilization, combinations of PGP rhizobacteria when applied to soil, improve soil structure, leaving no toxic effects. PGP rhizobacteria are known to fix atmospheric molecular N through symbiotic and asymbiotic/associative N-fixing processes (Anjum et al. 2007). With more and more emphasis being placed on organic farming, PGP rhizobacteria are finding increasing applications today as biofertilizers. These efficient PGP rhizobacterial bioactive factors are substances that impact growth of agricultural/horticultural crops. Since efficient inoculation consists of supplying high densities of viable and efficient microbes for rapid colonization of host rhizosphere, it induces at least a transient perturbation of equilibrium of soil microbial communities/biodiversity. The changes in soil microbial composition may be undesirable if important native species/unculturable species are lost thus affecting subsequent crops. Loss of certain rhizobacterial species may, however, not change functioning of the system, because of rhizobacterial redundancy, due to different rhizobacterial species which may carry out same functions (Nannipieri et al. 2003). Judicious utilization of commercial AMF inoculants is increasing in horticultural and land reclamation industries (Gianinazzi and Vosátka 2004), and is an emerging technology in field crop production worldwide. AM fungi are able to colonize and establish symbiotic, mutually beneficial associations with roots of most agricultural crops and increase effective absorptive area of roots by formation of an extensive extra radical hyphal network, which enhances efficiency of absorption of nutrients (George 2000). Importance of AM fungi in improving plant growth and plant resistance to soil-borne diseases, and in restoring problematic soils, is well known (Rillig 2004). Many researchers have noted that certain plant species are generally more responsive to mycorrhizal colonization than others (Bonfante and Genre 2008), and responses may be both host plant and AMF specific. Thus, there is a need to investigate response of target field crops to AMF inoculants (Gonzalez-Chavez et al. 2004). These efficient AM fungi play a significant ecological role in phytostabilization of potentially toxic trace element-polluted soils by sequestration and, in turn, help mycorrhizal plants survive in polluted soils. One of these components is glomalin, a glycoprotein produced by hyphae of AM fungi (Driver et al. 2005). Extra radical mycelium of AM fungi, in addition to its crucial role in enhancing NUE/WUE of host plants, also plays a role in soil particle aggregation and soil stability, mainly of WSAs (Dodd et al. 2000). All of these efficient mechanisms have implications in reducing plant exposure to potentially toxic

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elements with use of mycorrhiza remediation technology in sustainable soil–plant systems. Soil sustainability and productivity are considered important factors for the success of agricultural production rather than soil health. The status of nutrients present in soil–plant systems and their ability to supply nutrients determines soil fertility, whereas ability of soil to produce higher yields is soil productivity or productivity of the system. Production of agricultural crops depends upon many properties of soil, i.e., its textural class, structure, acidity, alkalinity, water-holding capacity (WHC), and cation/anion and cation exchange capacity (AEC/CEC) (Brady and Weil 2002). Agriculturally beneficial microbial populations are PGP N-fixing cyanobacteria, rhizobacteria, mycorrhiza, plant disease-suppressive beneficial rhizobacteria, stresstolerance endophytes, and bio-degrading microbes. Counts of rhizospheric microbes, i.e., Azotobacter, Azospirillum, Rhizobium, cyanobacteria, PSMs, K-solubilizing microorganisms (KSMs), and mycorrhizae are high under NT or minimum tillage (MT). These are some of PGP rhizobacteria (Bhardwaj et al. 2014). Bacteria/rhizobacteria are important soil microorganisms responsible for many enzymatic transformations, i.e., nitrification, ammonification, Azospirillum is a microaerobic bacterium, which fixes N in association with roots of grasses. Inoculation of grass crops with Azospirillum has positive hormonal effects on roots and plant growth. Nonsymbiotic associations of Azotobacter and Clostridium fix ~5–20 kg N ha 1 year 1 and various species of BGA fix ~10–50 kg N ha 1 year 1 (Dastager et al. 2010). Nitrifying bacteria/rhizobacteria of genus Nitrosomonas produce nitrite ions from oxidation of ammonia. Efficient rhizobacterium genus Nitrobacter and a few other genera can oxidize nitrites to nitrates. N-fixers, i.e., Clostridium pasteurianum and Desulfovibrio desulfuricans are obligate anaerobes (Dastager et al. 2010). Acid products of rhizobacterial fermentation convert insoluble P into soluble phosphates, which are then utilized by plants for growth and development. Some rhizobacteria, i.e., Thiobacillus ferrooxidans and iron rhizobacteria of genus Gallionella are capable of oxidizing ferrous ion (Fe2+) into ferric iron (Fe3+) (Heritage et al. 1999). Thus, it may be concluded that presence of microorganisms in soil is beneficial for soil productivity and better yields. Therefore, effective rhizospheric microorganisms will remain effective only if we manage our pastures with them in mind too. It can enhance soil quality, yield, and quality of crops. It helps in decomposition of SOM and during fermentation produces several normally unavailable organic acids—lactic acid, acetic acid, amino acid, and malic acid—and various other bioactive substances and vitamins. It has an antioxidant effect, which improves the immune systems of plants.

5.7.5

Soil Health

PGPR communities directly or indirectly affect plant physiology, nutritional, and physicochemical properties of rhizospheric soils through their metabolic activities.

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PGPR are important components of integrated farming, which help to nourish crops through required nutrients. These PGPR help to fix atmospheric N; solubilize and mobilize phosphorus; translocate minor elements like Mo, Zn, Cu to plants; produce plant growth promoting hormones like IAA and gibberellic acid (GA); and improve soil structure by production of polysaccharides thus helping to improve soil health and increase crop production. They are reported to increase uptake of Ca, K, Fe, Cu, Mn, and Zn through proton pump ATPase (Mantelin and Touraine 2004). Importance of PGPR in maintaining soil fertility is well studied by many scientists (Das and Singh 2014). Inoculation of seeds with PGPR significantly increased available P, microbial population, acid phosphatase, alkaline phosphatase, dehydrogenase activity in soil, and yields over uninoculated seeds (Hemashenpagam and Selvaraj 2011). Singh et al. (2012) who studied the effect of INM on pigeon pea-based intercropping system and soil properties, results revealed that application of different treatments did not affect bulk density and particle density, but porosity significantly increased after harvest of pigeon pea in both years. Inoculation of seeds with PSB (Bacillus polymyxa) recorded significantly higher values of available P, microbial population, dehydrogenase activity in soil, and yield over uninoculated seeds. Application of FYM at 5.0 t ha 1 increased SOC; available N, P, and K content; biological properties of soil, viz., microbial population and dehydrogenase activity; and yield component of crops and pigeon pea equivalent over no application of FYM. Das and Singh (2014) have undertaken a field experiment in an organic farming plot of BHU, Varanasi, to study the effects of manures and PGPR on soil properties. Organic manures, i.e., farm yard manure (FYM), cereal compost, legume compost, and combination of all manures with or without PGPR (Rhizobium + Azotobacter + Pseudomonas + Trichoderma) were applied at 5 t ha 1 in each plot. Combined application of cereal compost/legume compost and FYM along with PGPR significantly increased SOC, available N, P2O5, and K2O and S compared to control or individual application. The positive impact of biological and organic manure application has been recorded with an additional advantage of the reduction of chemical fertilizer use.

5.8 5.8.1

Nanotechnology in Agriculture Significance of Biosynthesized Nanoparticles for Agriculture Sustainability

Nanotechnology is one of the most important and recent tools in modern science yet only a few attempts have been made to apply these advances for increasing crop productivity (Chen et al. 2014). With ever enhancement in global populace and demand for food, nanotechnology techniques may be one of the most hopeful and reassuring ways to improve overall agricultural production. Potential applications of nanoparticles in agriculture sector include biosensors; gradual, time-consuming, and

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controlled delivery of chemical fertilizers and pesticides; detection and control of plant diseases; soil and water remediation. At present, however, use and employment of nanotechnology in agricultural field is at an infant stage; however, if discovered gradually and used in a sustainable way, this technology can help in orientation of agriculture today to new heights in future.

5.8.2

Biosynthesis of Nanoparticles

Preparation of nanoparticles can be done by using physical, chemical, and biological methods (Raliya et al. 2015). Chemical method of synthesis is more useful as it takes short time for the synthesis of bulk amounts of nanoparticles. However, in this method capping agents are required for size stabilization of nanoparticles. Moreover, chemical reagents used in chemical methods are toxic and lead to synthesis of by-products, which are not environment friendly. Therefore, there is the need for the development of a procedure which is eco-friendly and does not require any toxic material for the synthesis of nanoparticles. Tarafdar and Rathore (2016) explained a methodology for nanoparticle synthesis from microorganisms (Fig. 5.3). First microorganisms were forced to grow on respective salt solution to check their compatibility. Then well-growing organisms were selected for fungal ball preparation which was then allowed to release for enzymes to breakdown the salt into a nano-form. In this way biosynthesized nanoparticles are more stable due to natural encapsulation Isolation of organisms from soil by serial dilution technique ↓ Culturing of selected microorganisms to obtain microbial ball for 72 h and separated from broth by centrifugation (500 rpm) at 4°C for 10 min ↓ Isolation of extracellular microbial proteins for the use of nano-particle synthesis ↓ Addition to the solid/suspended test compounds in a flask at room temperature for a period of 48 h ↓ Nano-particles synthesized ↓ Characterization by TEM, SEM, PSA, AFM, EDS Fig. 5.3 Methodology for nanoparticle synthesis from microorganisms (Tarafdar and Rathore 2016)

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by mother protein. A variety of natural sources are there for metal nanoparticle synthesis including plants, fungi, yeast, actinomycetes, and bacteria (Pantidos and Horsfall 2014). The unicellular and multicellular organisms can produce intracellular and extracellular inorganic nanoparticles. Synthesis and applications of nanoparticles from/with microorganisms have been shown in the following flow chart. Bacteria have been most extensively researched for synthesis of nanoparticles because of their fast growth and relative ease of genetic manipulation (Shivaji et al. 2011). Cell-free culture supernatants of five psychrophilic bacteria, P. meridiana, P. proteolytica, P. antactica, A. kerguelensis, and A. gangotriensis and two mesophilic bacteria B. indicus and B. cecembensis have been used by Shivaji et al. (2011) to synthesize silver nanoparticles (AgNPs). Raliya et al. (2015) developed a low cost, eco-friendly approach using fungi Aspergillus flavus TFR 7 for biosynthesis of TiO2 nanoparticle (NPs).

5.8.3

Use of Biosynthesized Nanoparticles in Agriculture

Intense problems confronting productivity in agriculture, i.e., several abiotic and biotic stress factors, require more precise and effective solutions, and products with higher efficacy are further required to mitigate stress. Nanotechnology can improve our understanding and also deliver better products. It can contribute to the development of improved systems for monitoring environmental conditions and delivering nutrients or appropriate pesticides, and thus potentially enhance yields or nutritional values. Thus, nanotechnology can be an important part of further agriculture, food systems, and industry (Fig. 5.4). This frontier area of technology has potential to revolutionize in every sector of agricultural and food industry after providing nanosensors for contaminant detection, water flow detection, disease diagnosis, and tracking use of elite lines, breeds and cultivars; nanomembranes for purification, desalination, and detoxification; nanoparticles for preparation of nano-fertilizers (Saurabh et al. 2015, 2019b; Saurabh 2016), robust water tanks to prevent seepage, liquid and gaseous fuel-based lighting, cooking materials, pesticides, hormones, vaccines, solar cell panel; nano-catalysts for hydrogen generation; nano-zeolites for efficient release of water, slow release of fertilizer particles; nanomagnets for soil health testing, removal of soil contaminants; nano-emulsions for enhancing shelf life; quantum dots for diagnosis; nanoscale formulations of different food products for flavoring, refining catalytic devices in oil, dairy, meat, poultry products; nanocomposite particles in packaging materials; nano-capsules for better nutrient delivery, bioavailability. Nanotechnology gives strong impact on food preparation and conservation. It has great promise of sustainable development in long-term and second green revolution. Tarafdar and Rathore (2016) reported several merits of biosynthesized nanoparticles as they are eco-friendly in nature, can increase threefold NUE, 80–100 times less requirement than chemical fertilizer, 10 times more stress tolerance by crops, 30% more nutrient mobilization in rhizosphere, 17–54%

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Fig. 5.4 Nanotechnology in agriculture

Fig. 5.5 Phenology of mungbean plant under varying treatment; Control; OTiO2: ordinary titanium dioxide; n TiO2: nano titanium dioxide (Raliya et al. 2015)

improvement in crop yield and improvement in soil aggregation (33–82%), moisture retention (10–14%), and C buildup (2–5%) in soil. There are several other applications of these nanoparticles in agriculture. Raliya et al. (2015) determined suitability of these nanoparticles as nutrient by evaluating their influence on mungbean with spray of 10 mg L 1 concentration of TiO2 NPs on the leaves of 14 days old plant (Fig. 5.5). They also noticed an increase in microbial population by 21.4–48.1% and

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activity of acid phosphatase (67.3%), alkaline phosphatase (72%), phytase (64%), and dehydrogenase (108.7%) enzyme with NPs spray. A study conducted by Tarafdar et al. (2012) reported that ZnO nanoparticles induced synthesis of enzyme phosphatases by Aspergillus fungi, which was involved in mobilizing P for plant nutrition from unavailable organic P sources. Application of these biosynthesized zinc nanoparticles as fertilizer enhanced pearl millet (Pennisetum americanum L.) yield by 37.7%, enzyme activities of acid phosphatase (76.9%), alkaline phosphatase (61.7%), phytase (322.2%), and dehydrogenase by 21% (Tarafdar et al. 2014). These nano-fertilizers (Zn) penetrates into plants either through stomata and natural nano-pore which may enhance plant metabolic activities that lead to higher crop production. Gopinath and Velusamy (2013) biosynthesized AgNPs using Bacillus sp. GP-23 and evaluated antifungal activity towards Fusarium oxysporum, responsible for fusarium wilt disease of tomato, tobacco, legumes, cucurbits, sweet potatoes, and banana. Effect of application of different concentrations of AgNPs on hyphal growth of F. oxysporum was done by potato dextrose agar (PDA) plate assay. They observed that culture supernatant with 8 μg mL 1 resulted in much inhibition of the pathogen as compared to the control treatment (culture supernatant without AgNO3). Table 5.2 presents a cross-section of examples for the synthesis and applications of nanoparticles from microorganisms.

5.9

Conclusion

Rhizospheric microorganisms contribute significantly to fixation of atmospheric N and solubilization of P, K, Fe, and Zn from insoluble forms to plant-available forms. Inoculation of crops with rhizospheric microorganisms has been shown to improve fertility status of agricultural soils. Apart from their nutrient-solubilizing abilities, rhizospheric microorganisms have the ability to produce plant growth hormones, ammonia, and siderophores. Although rhizospheric microorganisms are abundant in many soils, they have not yet been successfully commercialized, and thus their application under large-scale field conditions is still limited. This communication highlights contribution of rhizospheric microbes in enhancing soil–plant system productivity. This type of noble-microbial consortium is cost-effective and eco-friendly in nature for enhancing evergreen agricultural food production systems. Use of biosynthesized nanoparticles in the agriculture sector is in its early stage but has incredible prospective. Attention towards improvement of synthesis efficiency and control of particle size is needed as synthesis processes by biological sources is relatively slow, compared to physical and chemical methods. Reduction of synthesis time will make this biosynthesis process much more attractive. By varying parameters like microorganism type, growth phase of microbial cells, growth medium, synthesis conditions, pH, substrate concentration, source compound of target nanoparticle, temperature, reaction time, and addition of nontarget ions; it might be possible to obtain desired quality and quantity of NPs. With a better understanding

TiO2

Zinc

Silver

Extracellular

Extracellular

Extracellular

Extracellular

Bipolaris tetramera

Rhizoctonia bataticola TFR-6 Trichoderma viride

Intracellular

Actinomycetes Rhodococcus sp.

Extracellular

Extracellular

Yeast Yeast strain MKY3

Thermomonospora sp.

Silver

Extracellular

Gold

Gold

Silver

Silver

Extracellular

Bacteria Spirulina platensis (AJ401120) Bacillus sp. GP-23

Silver and gold

Types of nanoparticle

Extracellular/ intracellular

Microorganism Fungi Aspergillus flavus

Spherical

Spherical

Hexagonal

Spherical

Spherical

Spherical and occasionally rod like

Spherical

9–10 nm

5–15 nm

2–5 nm

7–21 nm

50 nm

5–40 nm

Silver (54.78–73.49 nm) Gold (58.4 and 261.73 nm) 50 nm

12–15 nm

– Silver (irregular) Gold (spherical or hexagonal)

Size (nm)

Shapes

Table 5.2 Synthesis and applications of nanoparticles from microorganisms

–

–

–

Antimicrobial activity against Pseudomonas solanocearum, Pseudomonas syringae Antifungal activity against plant pathogenic fungus, Fusarium oxysporum

As nano-fertilizer to enhance crop production in pearl millet cv. HHB 67 Nanoparticles incorporated into sodium alginate for vegetable/fruit preservation

Antimicrobial, cytotoxic, and immunomodulatory activity

Influence on mung bean as nutrient

Applications

Jaipur Ahmad et al. (2003) Jaipur Ahmad et al. (2003)

Kowshik et al. (2002)

Mala et al. (2012) Gopinath and Velusamy (2013)

Tarafdar et al. (2014) Fayaz et al. (2009)

Raliya et al. (2015) Fatima et al. (2015)

References

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of synthesis mechanisms on a cellular and molecular level, including isolation and identification of compounds responsible for reduction of nanoparticles, it is expected that short reaction time and high efficiency can be obtained. With recent progress and ongoing efforts in improving particle synthesis efficiency and exploring their biomedical and agricultural applications, it is hoped that implementation of these approaches on a large scale and their commercial application will take place in coming years. As evidenced by various research studies, farmers are still not well equipped with the knowledge and skill required for using biofertilizers and biopesticides. This calls for organization of awareness campaign, demonstration of biofertilizers, and capacity building of farmers and other stakeholders which are involved in promotion, production, distribution, and use of these compounds. The existing gap in demand and supply of biofertilizers needs to be bridged. Use of biofertilizers and biological control measures for disease and pest control will become a necessity in near future in order to save our depleting land and water resources as well as reducing the residual effect of chemicals in agricultural produce.

5.10

Future Prospects

Keeping in mind all these beneficial roles of plant beneficial rhizospheric microbes (PBRMs) present in the soil rhizosphere, it can be concluded that in integrated nutrient management (INM) system integration of microbial inoculants with less fertilizer should be considered in many situations as it promises high crop productivity and agricultural sustainability. Commercial use of PBRMs must await the development of coating technology to improve methods of storing and applying bacteria without loss of viability. Novel, genetically modified soil and regionspecific microbial intervention and technologies for their ultimate transfer to fields have to be developed, pilot-tested, and transferred to farmers in a relatively short time. And last but not the least, search for new strains of beneficial microbes for biofertilizer and development of microbial diversity map for any region just like nutrient mapping may be helpful too. Advance simulation models related to the nature of microbes and their behavioral patterns under changing edapho-climatic conditions may be developed with suitable technical calibrations and testing for better development and maintenance of agricultural sustainability and microbial diversity in the near future. PBRMS are potential tools for sustainable agriculture and trend for future. For this reason, there is an urgent need for research to have a clear definition of what bacterial traits are useful and necessary for different environmental conditions and plants so that optimal microbial strains can either be selected and/or improved. Combinations of PBRMs strains that interact synergistically are currently being devised and numerous recent studies show a promising trend in the field of inoculation technology. Developing suitable alternate formulations, viz., liquid inoculants/granular, PBRMs selected for biocontrol against multiple plant pathogens in bioassays are prerequisite for the advancement of the agriculture industry.

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Chapter 6

Arbuscular Mycorrhizal Fungi for Sustainable Crop Protection and Production Thangavelu Muthukumar

Abstract Modern agriculture is confounded by many challenges like reduced fertility and sustainability of agricultural soils resulting from decades of irrational use of chemical fertilizers and biocides to scale up crop productivity. Currently, alternative means of crop nutrition and protection are being widely explored which also include soil microorganisms and plant–microbe interactions that could benefit crop growth. Arbuscular mycorrhizal (AM) fungi are an integral part of plant development as they play a pivotal role in satisfying the nutrient demand of plants in several ecosystems including the agroecosystems. Besides, AM fungi also safeguard plants against various biotic and abiotic stresses, ameliorate soil structure, and influence soil microbial communities. There is clear evidence that AM fungi can reduce the use of synthetic chemicals in crop production systems. Nevertheless, several practices of conventional agriculture like the development of crop varieties that are less dependent on AM symbiosis, application of synthetic chemicals, and tillage affect AM fungi. In this chapter, the role of AM fungi in improving crop production and protection are explored. Further, this chapter also highlights the significance of AM fungi in sustainable crop production systems and emphasizes the need to develop cultivation practices for effective utilization of these useful soil fungi. Keywords Arbuscules · Diversity · Glomeromycota · Microbial interaction · Mycorrhizal symbiosis · Mycorrhizosphere · Phosphorus · Stress · Sustainable agriculture

T. Muthukumar (*) Root and Soil Biology Laboratory, Department of Botany, Bharathiar University, Coimbatore, Tamil Nadu, India e-mail: [email protected] © The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2021 G. Seneviratne, J. S. Zavahir (eds.), Role of Microbial Communities for Sustainability, Microorganisms for Sustainability 29, https://doi.org/10.1007/978-981-15-9912-5_6

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T. Muthukumar

Introduction

The first and foremost challenge that is faced by world agriculture today is the everincreasing world population. It is estimated that the world population will be around ten million by 2050. This increasing population will increase the food demand by 50% over the present estimates. This will thus cause an enormous pressure on the agriculture and the already dwindling natural resources. Adding to these, the change in climate with erratic rainfall and increase in the frequency of drought and floods will be the major hurdle in meeting the world food demand. Though climate change may benefit a few countries by increasing their possible arable land area, it would drastically affect arable lands in many of the continents especially in the hunger hot spots of Africa and Asia (Zhang and Cai 2011). Most of the increased food production in the past has resulted from the expansion of the arable lands (FAOSTAT 2018). Even the existing land area under cultivation is facing production constraints due to land mismanagement resulting in salinization and low fertility. Around 20% of the arable lands worldwide and 33% of the irrigated agricultural lands are affected by salinization (Shrivastava and Kumar 2014). The current crop production mostly depends on huge synthetic inputs in the form of fertilizers and biocides which in long run deteriorates soil health. For example, the world consumption of phosphatic fertilizers (P2O5) for crop production has increased by 33.54% from 22.54 kg/ha in 2002 to 30.10 kg/ha in 2015. Similarly, the use of nitrogen (N) fertilizers has increased by 27.33% from 53.88 to 68.61 kg/ha for the same period (FAOSTAT 2018). Extensive use of synthetic chemicals in agriculture leads to soil degradation and certain estimates indicate a 60% reduction in soil ecosystem services due to soil degradation (Lal 2015). The use of integrated nutrient management involving soil microorganisms is one way to alleviate soil degradation and to conserve the soil quality and agriculture for the future. Soil is a living entity streaming with a wide range of organisms both microscopic and macroscopic belonging to different groups. Most of these soil organisms play an important role in various ecosystem processes with a few causing diseases in plants. Some of the soil microorganisms also associate with plant roots forming symbiosis of different kinds. Two of the most popular symbiosis in the plant kingdom is the association of plants with the nodulating bacteria and the more common mycorrhizal fungi. The arbuscular mycorrhiza is highly prevalent and most widespread among the different types of mycorrhizal symbiosis. It is estimated that greater than 70% of the terrestrial plant species including many of the food and commercial crops are arbuscular mycorrhizal (AM). Some speculate that AM symbiosis might have evolved much earlier than the nodulating bacterial symbiosis around 1,000,000,000 years ago (Bücking et al. 2012). Further, these fungi constituting more than 50% of the soil microbial biomass have coexisted with plants for more than 400,000,000 years without any changes in their morphology (Ryan and Graham 2002; Parniske 2008). Moreover, the evolution of this symbiosis has enabled plants to colonize the water and nutrient stressed terrestrial habitats.

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149

Arbuscular Mycorrhizal Fungi

The coarse endophytic soil fungi of the phylum Glomeromycota and the fine endophytic fungi of Mucoromycotina form symbiosis with most of the crop species. These fungi known as the Arbuscular mycorrhiza (AM) fungi are obligate biotrophs and depend on the host plant’s sugar supply and lipids to complete their life cycle. Arbuscular mycorrhizal fungi are coenocytic with the fungal hyphae and spore containing several hundred nuclei. The relatively large size and polymorphic nature of the genome have made the genome sequencing and annotation of these fungi highly challenging. In spite of being asexual, these fungi can exchange their genetic material through anastomosis (Bücking et al. 2012). The AM fungi form unique structures called arbuscules in the cortical cells of plant root that act as transit points for the exchange of resources between the symbionts. The arbuscule is a highly branched structure with limited lifespan (Fig. 6.1). The development of arbuscule depends on the nutrient demand of the host plant and this structure is either absent or very low when the roots of non-mycorrhizal plants are colonized by AM fungi. Most of the AM fungi also form lipid-rich storage structures in the roots called vesicles. The development of vesicles happens later than the arbuscules and is abundant in the older and senescing

Fig. 6.1 (a–d) Structures of arbuscular mycorrhizal (AM) fungi in root and soil. (a) Hyphae of AM fungi penetrating the root and forming hyphal coils in the epidermal cells; (b) arbuscules in the cortical cells; (c) intracellular vesicles; (d) spores produced on the extraradical hyphae

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roots of non-mycorrhizal plants (Fig. 6.1). The terminal or intercalary vesicles that are formed on the intraradical hyphae can also act as propagules in initiating colonization. The extraradical mycelium of AM fungi originating from roots explores the soil well beyond roots. Estimates indicate that there is an increase of 15–200 cm3 of soil explored for each centimeter of root colonized by AM fungi depending upon environmental conditions (Sieverding 1991). Further, the ratio of AM fungal hyphal length to those of roots could be 100:1 or even more (George et al. 1995). The extraradical mycelium of AM fungi whose density ranges from 270 to 2050 cm/g of soil can increase the surface area of absorption by 40 times (Pepe et al. 2016). Moreover, the extraradical mycelium can grow at a rate of 74–110 cm/day (Giovannetti and Avio 2002; Mikkelsen et al. 2008). The viability of the extraradical mycelium of AM fungi can extend well beyond the lifespan of the host plant. In a recent study, Pepe et al. (2018) showed that the extraradical hyphae of Rhizoglomus irregular is (Błaszk., Wubet, Renker & Buscot) Sieverd., G.A. Silva & Oehl and Funneliformis mosseae (T.H. Nicolson & Gerd.) C. Walker & A. Schüßler originating from the shootless chicory (Cichorium intybus L.) roots maintained viability and established mycorrhizal symbiosis with plants even after 5 months of shoot removal. The initiation of the symbiosis starts with the germination of the soil-borne spores, extramatrical hyphae in the soil, or the intraradical mycorrhizal propagules. The highly dynamic mycorrhization process can therefore be divided into: (1) initial presymbiotic communication, (2) fungal contact and perforation of the root epidermis, (3) intraradical colonization of the cortex, (4) formation of the arbuscules, and (5) vesicle and spore development. Although the intricate sequential phenological and molecular mechanisms in the establishment of AM symbiosis are beyond the scope of this chapter, these have been reviewed in detail recently by Choi et al. (2018). In this chapter, I discuss the occurrence of AM symbiosis in agroecosystems with its role in improving crop health and productivity.

6.2.1

AM Fungi in Crops

All the staple food crops including the three major cereals [wheat (Triticum aestivum L.), rice (Oryza sativa L.), and maize (Zea mays L.)] are mycorrhizal. Rice is mostly mycorrhizal under the upland conditions than under flooded conditions (Bernaola et al. 2018). However, studies have shown that rice growing under flooded low land conditions are not only mycorrhizal they can also benefit from the symbiosis (Sánchez et al. 2015). Similarly, vegetable crops like tomato (Solanum lycopersicum L.), potato (Solanum tuberosum L.), cassava (Manihot esculenta Crantz), onion (Allium cepa L.), sweet potato [Ipomoea batatas (L.) Lam.], yams (Dioscorea spp.), and fruit crops are also mycorrhizal. Though majority of the crop plants are mycorrhizal, those belonging to Brassicaceae and Chenopodiaceae are usually non-mycorrhizal (Cosme et al. 2018). These two plant families contain some of the important condiments, vegetable, oil, and industrial crops like beetroot (Beta vulgaris L.), sugar beet (Beta vulgaris subsp. vulgaris), glasswort (Salicornia

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europaea L.), cabbage (Brassica oleracea L.), cauliflower (Brassica oleraceae var. botrytis L.), rapeseed (Brassica napus L.), and radish [Raphanus raphanistrum subsp. sativus (L.) Domin]. The non-mycorrhizal plants appear to lack several putative genes that are known to control the symbiotic processes like the perisymbiotic phase (NFP, DMI2, DMI3, CASTOR, IPD3), the entry of the fungus into roots (RAM1, RAM2), spread of the intraradical hyphae, and arbuscule formation (VAPYRIN, STR, STR2, PT4) (Cosme et al. 2018).

6.2.2

Diversity of AM Fungi in Agricultural Soils

Changes in the occurrence of AM fungi in agricultural soils happen at two levels: abundance and diversity (Verbruggen et al. 2013). It is well known that conversion of natural vegetation into agricultural lands results in the disappearance of certain taxa, thereby decreasing the diversity of AM fungi. For example, taxa in Gigasporales that chiefly perennate as spores and sporocarp forming Sclerocystis are less frequent or totally absent in intensely managed agricultural soils (Castillo et al. 2016; Oehl et al. 2017). The diversity and abundance of AM fungi in cultivated soils are often low compared to natural soils (Verbruggen and Kiers 2010; Oehl et al. 2017). The intense activities in conventional agriculture such as high nutrient inputs—especially phosphorus (P), tillage, and fallow periods as discussed later decrease the abundance of AM fungal propagules like the spores and the extraradical mycelium in the soils (Verbruggen et al. 2013). As a result, cultivated soils are dominated by few selected AM fungal taxa that are resilient to the cultivation practices. For instance, the widespread occurrence of F. mosseae in agricultural soils worldwide relates to the ability of this fungus to spread and adapt successfully to agricultural situations (Rosendahl et al. 2009). In addition, AM fungal species like Funneliformis caledonius (T.H. Nicolson & Gerd.) C. Walker & A. Schüßler and Pacispora franciscana Sieverd. & Oehl occur more frequently in cultivated than in natural soils (Oehl et al. 2017). A review on the diversity of AM fungi in the southern-central zones of Chile has shown that cultivated soils are predominated by taxa in Glomeraceae in contrast to Acaulosporaceae that dominate natural soils (Castillo et al. 2016). Nevertheless, efficient management practices that facilitate crop growth or improve soil conditions like organic amendments and irrigation in semiarid or arid regions can increase AM fungal diversity (Al-Yahya’ei et al. 2011).

6.3

Role of AM Fungi in Plant Growth and Yield

The role of AM fungi in improving crop growth and yield is a well known response. An increase in crop growth in response to AM symbiosis has been reported in wheat (Daei et al. 2009), rice (Suzuki et al. 2015; Hoseinzade et al. 2016), maize (Sabia et al. 2015), sorghum [Sorghum bicolor (L.) Moench, Nakmeea et al. 2016], millets

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(Bielders et al. 2010; Saharan et al. 2018), pulses (Oliveira et al. 2017; Shukla et al. 2018), and vegetables (Hijri 2016; Lu et al. 2015) both under normal or stressed conditions. Inoculation of different species of AM fungi [Claroideoglomus etunicatum (W.N. Becker & Gerd.) C. Walker & A. Schüßler, F. mosseae and Rhizophagus intraradices (N.C. Schenck & G.S. Sm.) C. Walker & A. Schüßler] improved the yield of field-grown wheat varieties by 5–38% (Daei et al. 2009). As C. etunicatum was most effective in improving the yield in two varieties of wheat (Kavie and Tabasi), F. mosseae was found to be effective in the third variety (Roshan) (Daei et al. 2009). A positive influence in grain yield in rice both under upland and wetland conditions have been reported (Solaiman and Hirata 1995). Inoculation of greenhouse-grown tomato with F. mosseae significantly improved the fruit fresh weight and yield by 7% and 42%, respectively (Latef and Chaoxing 2011). Similarly, inoculation of Chilli (Capsicum annuum L.) var. PKM with R. intraradices increased the yield parameters like the fruit length, girth, and yield per plant by 11%, 44%, and 36%, respectively (Selvakumar and Thamizhiniyan 2011). In a field study, four varieties of onion (Early Grano, Pusa Madhvi, Pusa White Round, and Pusa White Flat) were inoculated with a cocktail of indigenous AM fungi belonging to Gigaspora, Glomus, and Scutellospora and grown at two recommended P levels (100 and 50%). The results of the study indicated that AM fungal inoculation increased the bulb yield by 6–31% at 100% P level and 9–30% at 50% P level (Sharma and Adholeya 2000). Studies have shown that AM symbiosis not only improves the quantity of the agricultural produces, but also its quality. For example, field inoculation of maize with AM fungal consortium consisting of R. intraradices, Rhizophagus aggregatus (N.C. Schenck & G.S. Sm.) C. Walker, Viscospora viscosa (T.H. Nicolson) Sieverd., Oehl & F.A. Souza, C. etunicatum, and Claroideoglomus claroideum (N.C. Schenck & G.S. Sm.) C. Walker & A. Schüßler improved total grain number and dry weight per spike by 31% and 53%, respectively (Berta et al. 2014). This study also showed that AM fungal inoculation in spite of reducing the seed starch content by 4%, enriched the seed iron (Fe) content by 29% and zinc (Zn) content by 27%. Similarly, R. intraradices colonized plants possessed significantly higher concentrations of mineral elements [Calcium (Ca)-15%; P-59%; Zn-19%] than the uncolonized plants. The lycopene content of mycorrhizal tomato fruits was 19% higher than the non-mycorrhizal fruits (Giovannetti et al. 2012).

6.4 6.4.1

Plant Benefits by AM Fungi Increased Nutrient Uptake

One of the most important benefits of the AM symbiosis is the improved acquisition of nutrients by the host plants. Many studies have clearly demonstrated the increased nutrient content in AM plants than non-AM plants. The competition for nutrients is very intense between plants and microorganisms in the plant rhizosphere. This

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competition results in the depletion of nutrients around the roots resulting in the development of nutrient depletion zone. Therefore, plants have to continuously form new roots to explore the soil beyond these depletion zones for acquiring nutrients. Many plant species invest around 20–70% of their gross productivity in the development of roots for soil exploration (Poorter et al. 2012). This large investment in root production is confounded by limitations like the limited lifespan of the root structures, especially the fine roots and the root hairs. The major benefit of AM symbiosis lies in the ability of the AM fungi to aid plants in their uptake of nutrients like P and N from stressed soils. In addition to these AM fungi can also help plants in the acquisition of potassium (K), sulfur (S), magnesium (Mg), and trace elements like copper (Cu), manganese (Mn), and Zn (Giovannetti et al. 2017).

6.4.1.1

Phosphorus

AM plants can acquire nutrients from the soil by both plant and mycorrhizal pathways. In the plant pathway, the plants take up soil nutrients directly through their roots via the epidermis of the roots and root hairs. The direct uptake of nutrients from the soil by plant roots is often limited by the reduced mobility of certain nutrients like P in the soil solution. The mobility of P in the soil is so low that a P-depletion zone quickly surrounds the roots due to the differences in the uptake and diffusion rates of P in the soil (Smith and Smith 2011). This limits the uptake of P directly from the soil. The nutrients in mycorrhizal pathway enter the roots through the extraradical mycelium and are transferred within the roots through the intraradical mycelium of the AM fungi. These nutrients are later transferred to the root cortical cells through the interfacial apoplast of the arbuscules, arbusculate, or hyphal coils. The AM fungal mediated nutrient uptake is not complementary as the plant shares around 4–22% of its photoassimilates with the fungi (Fellbaum et al. 2012). In AM plants both direct and mycorrhizal pathways can act additively. This led to the speculation that P taken up through the mycorrhizal pathway fails to happen when the concentration of P in the soil solution is high and as a result mycorrhizal plants do not exhibit a positive response. Nevertheless, this view has been objected to and it has been proposed that the mycorrhizal pathway, though hidden, can contribute significantly to the total P uptake by the plants (Smith and Smith 2011; Smith et al. 2011). For example, Li et al. (2006) showed that 50% of the nonresponsive wheat plants P uptake occurred through the mycorrhizal pathway. This shows that the AM fungi can contribute considerably to the P acquisition of mycorrhizal plants even under optimum or high P availability. Under high concentrations of P in the soil, the P transporters that play an essential role in the uptake of P through direct pathway are downregulated in AM plants. Nevertheless, the proportion of the AM contribution to the plant’s total P uptake depends both on the plant and fungal species. This indicates that mycorrhizal plants change their nutrient acquisition strategy and that even under high P availabilities in the soil; the mycorrhizal fungus can still

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contribute substantially to the uptake of P by the plants. For instance, the downregulation of P transporters by R. intraradices was much higher when compared to F. mosseae (Smith et al. 2003). Similarly, tomato totally depended on the R. intraradices for its P uptake; whereas its dependence on Gigaspora rosea T.H. Nicolson & N.C. Schenck was much lower (Smith et al. 2003). The P uptake and transport may be host-specific or independent of the host species. For example, the uptake and transport of P by Funneliformis caledonium (T.H. Nicolson & Gerd.) C. Walker & A. Schüßler was independent of the host species, whereas Rhizophagus invermaius (I.R. Hall) C. Walker was specific and transferred significant quantities of P only to flax (Linum usitatissimum L., Ravnskov and Jakobsen 1995). The well-known effect of AM fungi on P uptake from the soil is due to: (a) The exploration of the soil by the extraradical hyphae of the AM fungi for nutrients well beyond the nutrition depletion zone surrounding the roots; (b) The small hyphal diameter not only increases the surface area but also allows AM fungi to explore soil pores that are too small for plant roots to penetrate; (c) The ability to produce and secrete phosphatases enables AM fungi to acquire P from bound sources; and (d) The potential of AM fungi to maintain a low internal P concentration by storing P as polyphosphates enables the movement of P from the extraradical to the intraradical mycelium. 6.4.1.2

Nitrogen

The form of N available to plants and microorganisms in the soil varies with soil types. For example, nitrate (NO3 ) is the predominant form of N in most of the agricultural soils and is virtually absent in most undisturbed and extremely acidic soils where ammonium (NH4+) is dominant (Bücking and Kafle 2015). The understanding of the role of AM fungi in the plant’s acquisition of N is very limited compared to P. The mobility of the NO3 and NH4+ in the soil is much higher than P and therefore the chances of N depletion zone developing around the roots do not exist. The improved N status has been ascribed to the better P nutrition of the AM plants. But there is substantial evidence to show the significant involvement of AM fungi in the N nutrition of plants (Bücking and Kafle 2015). Recent investigations do suggest that the affinity of AM fungal hyphae for NH4+ uptake is fivefold higher than the roots thus enabling fungi to acquire NH4+ more efficiently even from soils low in N (Pérez-Tienda et al. 2012). In addition to inorganic N, AM fungi are also known to take up and transport organic forms of N like argenine, cysteine, glycine, glutamate, glutamine, methonine, ornitine, and urea (Bücking and Kafle 2015). A significant proportion of N in organic forms in many soils and AM fungi were previously presumed to be incapable of utilizing organic forms of N. Earlier studies suggest that the hyphae of AM fungi can grow into organic patches in the soil and can uptake and translocate radiolabelled N (15N) to their host plants (Leigh et al. 2009; Hodge and Fitter 2010). Although AM fungi lack saprophytic capabilities, they can accelerate the decomposition of the organic matter through modulating activates of the soil microorganisms

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(Herman et al. 2012). The extraradical mycelium of AM fungi can take up N from a considerable distance from the roots and transfer it to the intraradical mycelium. This transport of N can be very quick through the AM fungal hyphae and the N is transported in the form of arginine along with polyphosphate from the extraradical to the intraradical mycelium. In the intraradical mycelium, both polyphosphate and arginine are broken down for efflux into the mycorrhizal interface. Nevertheless, at present, the actual mechanisms that govern the efflux of nutrients through the fungal plasma membrane or the processes of nutrient release into the mycorrhizal interface are rather obscure (Bücking and Kafle 2015).

6.4.2

Improved Water Relations

There is reliable evidence to show that the extraradical hyphae of AM fungi can acquire water from the soil and transfer it to plant roots (Augé et al. 2007; Lazcano et al. 2014). Generally, AM fungi are known to better the hydraulic conductance in the roots (Bárzana et al. 2014), alter the water retention capabilities of the soil, or mediate osmotic adjustment (Aroca et al. 2007). In a greenhouse study, Zhao et al. (2015) showed that colonization of maize plants by R. intraradices improved the percentage of leaf moisture, rehydration rate, and water-use efficiency under different soil moisture conditions. In addition to these, AM fungi can also alter the stomatal behavior in plants thereby playing an important role in the water status of the plants. The stomatal conductance of AM plants is ~24% higher than non-mycorrhizal plants. This stomatal conductance increases by two to four times depending upon water availability (Augé et al. 2014). The hydraulic benefit rendered to plants tends to differ with AM fungal species. An experiment performed in a plant growth chamber using lettuce (Lactuca sativa L. cv. Romana) plants colonized individually by six AM fungi [Funneliformis geosporum (T.H. Nicolson & Gerd.) C. Walker & A. Schüßler, F. mosseae, C. claroideum, Septoglomus constrictum (Trappe) Sieverd., G.A. Silva & Oehl, Funneliformis coronatum (Giovann.) C. Walker & A. Schüßler, R. intraradices] showed that the mycorrhizal plants depleted more water and increased the plants’ relative water uptake by 22–33% than non-mycorrhizal plants. Further, the AM mediated water uptake was related to the quantity of the extraradical hyphal production of the AM fungal species and to the frequency of root colonization (Marulanda et al. 2003). The benefit from AM symbiosis also varies with the functional groups of plants and the AM fungi involved. For instance, Jayne and Quigley (2013) in their meta-analysis showed that trees and shrubs benefit more from the symbiosis during water-limiting conditions than herbs. Similarly, Chitarra et al. (2016) showed that tomato plants were more hydrated when colonized by R. intraradices under normal soil moisture conditions; whereas plants colonized by F. mosseae were hydrated more under water-limiting conditions. These evidences clearly suggest that AM symbiosis has a prominent role in plant hydration especially for crops grown under rainfed conditions of the tropics.

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Interaction of AM Fungi with Other Soil Microorganisms

Arbuscular mycorrhizal symbiosis alters the composition and function of the microorganisms in the soil. The rhizosphere surrounding the roots is extended in AM plants by the extraradical mycelium that originates from the mycorrhizal roots and spreads into the adjacent soil. The soil surrounding the AM fungal hyphae is also influenced by the hyphal exudates and is known as the hyposphere. The rhizosphere along with the hyposphere is termed as mycorrhizosphere (Priyadharsini et al. 2016). In addition to influencing the microbial diversity and processes in the soil AM fungi can also directly interact with soil microorganisms to improve the plant growth. A large number of studies have reported the influence of co-inoculation of AM fungi along with plant growth promoting bacteria like Azotobacter, Azosprillum, Bacillus, Pseudomonas (Barea et al. 2008) and fungi belonging to Trichoderma and yeasts on plant growth and protection against pathogens (Table 6.1). Further, the role of AM fungi in the process of nodulation and N fixation in leguminous plants is well known. Generally, legumes are inoculated with an efficient bacterium as a large variation exists in the symbiotic N fixing capabilities among the nodulating bacteria (Meena et al. 2018). High requirement for P is one of the key factors in nodulation and the subsequent symbiotic N fixation as these are high energy-demanding processes (Javaid 2010). Subsequently, the AM fungi satisfy the legume’s P demand through increased uptake and transfer of this soil element. A reciprocal relation between soil microorganisms and AM fungi has often been reported. For example, the extraradical mycelium of AM fungi can affect the abundance of members of Oxalobacteraceae, Streptomycetes, and the Firmicutes in the mycorrhizosphere (Nuccio et al. 2013; Scheublin et al. 2010) and many bacteria act as mycorrhiza helper bacteria in promoting root colonization and hyphal growth (Frey-Klett et al. 2007; Battini et al. 2017). Contrarily certain soil bacteria could also negatively influence AM symbiosis. Svenningsen et al. (2018) showed that high abundance of Acidobacteria, Actinobacteria, Bacteriodetes, Firmicutes, and Proteobacteria could suppress the formation and function of the extraradical mycelium of AM fungi in the soil.

6.4.4

Tolerance to Drought and Salinity

One of the important challenges of modern agriculture is the increasing drought and salinity stress in the cultivable soils. This constitutes a major threat to crop productivity especially in the rainfed tropical regions. Soil salinization seriously affects the soil water potential and ionic balance thereby reducing the capacity of the roots to acquire water and nutrients. Further, the reduction in growth and yield of crops in saline soils is often related to the reduction in photosynthesis and its associated changes in plant metabolism (Chandrasekaran et al. 2019). Drought stress decreases

R. intraradices, F. mosseae, Claroideoglomus etunicatum Funneliformis geosporum

Acaulospora morrowae, Gigaspora margarita, Septoglomus constrictum, F. mosseae, R. aggregatus, Scutellospora calospora F. mosseae

AM fungi Funneliformis mosseae, Acaulospora laevis Acaulospora longula, Glomus clarum, Rhizophagus intraradices Rhizophagus fasciculatus, Rhizophagus aggregatus Capsicum annuum

Methylobacterium oryzae strains (CBMB20 and CBMB110) Pseudomonas strains P10, P13

Zea mays

Solanum lycopersicum F1 Hybrid, Delba S. lycopersicum F1 Hybrid, GS-15 Capsicum chinense

Azotobacter chroococcum, Pseudomonas aeruginosa, Azospirillum brasilense, Streptomyces sp.

Pseudomonas putida, A. chroococcum

P. putida, A. chroococcum, Azosprillum lipoferum

Pseudomonas fluorescens, A. chroococcum

Sorghum bicolor cv. CSV-15

Crop species Capsicum frutescens

PGPR Pseudomonas fluorescens

Normal condition

Normal condition

Normal condition

Normal condition

Normal condition

Experimental condition Normal condition Normal condition

Increased growth and yield, early flowering, nutrient content

Maximized lycopene content, antioxidant activity, and total soluble solids Increased lycopene, antioxidant activity, and K contents

Increased IAA, GA3, EPS, siderophore, and ‘P’ solubilization; increased plant biomass, leaf area, total chlorophyll, and mycorrhizal colonization Taller plants; more shoot and root biomass

Plant/soil parameters Improved growth, yield, P uptake, phosphatase activity Increased plant growth, chlorophyll and nutrient contents

(continued)

Surendirakumar et al. (2019)

Ordookhani et al. (2010)

Ordookhani and Zar (2011)

Kumar et al. (2015b)

Kumar et al. (2012)

Reference Jangra et al. (2017) Kim et al. (2010)

Table 6.1 Influence of arbuscular mycorrhizal (AM) fungi and plant growth promoting rhizobacteria (PGPR) co-inoculation on different plant and soil parameters in different crop species

6 Arbuscular Mycorrhizal Fungi for Sustainable Crop Protection and Production 157

S. lycopersicum cv. Boludo Z. mays

Trifolium repens

Oryza sativa

P. mendocina

Variovorax paradoxus 5C-2

P. fluorescens

P. mendocina

P. putida, Pseudomonas sp., Bacillus megaterium

A. brasilense

F. mosseae

Rhizophagus irregularis

F. mosseae

F. mosseae

Glomus coronatum, Glomus constrictum, or Glomus claroideum R. intraradices

L. sativa

L. sativa L. cv. Tafalla

S. lycopersicum F1 Hybrid, Delba and S. lycopersicum F1 Hybrid, Tivi Lactuca sativa cv. Tafalla

Pseudomonas mendocina

F. mosseae

F. mosseae

Crop species Vigna unguiculata

PGPR Bradyrhizobium sp., Paenibacillus brasilensis P. putida, A. chroococcum

AM fungi C. etunicatum

Table 6.1 (continued)

Well-watered/ Drought condition

Drought

Water deficit stress Drought

Drought

Salinity

Salinity

Experimental condition Normal condition Normal condition

Increased plant height, biomass, shoot proline, and ascorbate content; reduced oxidative damage to lipids

Increased concentrations of leaf K and lower concentrations of leaf Na Decreased soil aggregate stability Reduced AM colonization; improved plant biomass; decreased proline content Higher plant vegetative and reproductive traits Increased glomalin-related soil protein, and soil dehydrogenase and phosphatase activities Higher plant biomass

Plant/soil parameters Increased AM colonization, shoot biomass, N content Increased plant growth; improved P, Mg, and Ca contents

Ruíz-Sánchez et al. (2011)

Marulanda et al. (2009)

Ghorchiani et al. (2018) Kohler et al. (2009a)

Kohler et al. (2010) Calvo-Polanco et al. (2016)

Kohler et al. (2009b)

Reference Tavares de Lima et al. (2011) Zare et al. (2011)

158 T. Muthukumar

Z. mays var. Ostiglia

Z. mays

Z. mays

S. lycopersicum cv. Jinguan P. vulgaris

Pseudomonas fluorescens Pf4

Pseudomonas protegens Pf-5, Pseudomonas chlororaphis O6

P. fluorescens

Bacillus polymyxa, Bacillus sp.

P. fluorescens

Pseudomonas putida KT2440

Pseudomonas jessenii strain R62, Pseudomonas synxantha strain R81

R. intraradices, R. aggregatus, Glomus viscosum, C. etunicatum, G. claroideum Rhizophagus, Funneliformis, Septoglomus, Claroideoglomus, Rhizoglomus R. irregularis

Glomus versiforme, F. mosseae

Glomus sinuosum, Gigaspora albida

R. irregularis isolate 09

R. irregularis

Triticum aestivum cv. Mercato and Avalon S. lycopersicum cv. PT-3

Phaseolus vulgaris

Bacillus subtilis, P. fluorescence

Glomus spp.

O. sativa

Herbaspirillum seropedicae

F. mosseae

Pest control

Pathogen defense

Disease control

Different fertilization regimes Pest control

Field experiment

Field condition

Integrated nutrient management (field study) Greenhouse and field experiment

Increased plant growth; decreased nematode (M. incognita) infestation;

Greater plant growth and control of root-knot nematode, Meloidogyne incognita Increased plant growth and yield; control of root rot caused by Rhizoctonia solani Higher plant growth, callose deposition

Increased growth and Mg, Mn and Zn concentrations

Increased yield and protected roots from rootworm damage

Increased plant biomass, survival, decreased damping-off; increased protective enzyme activity Increased plant growth and yield, improved grain quality

Increased growth and yield, nutrient content

(continued)

Pèrez-deLuque et al. (2017) Sharma and Sharma (2017)

Neeraj and Singh (2011)

Liu et al. (2012)

Rocha et al. (2019)

Jaffuel et al. (2019)

Berta et al. (2014)

Mohamed et al. (2019)

Hoseinzade et al. (2016)

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PGPR

Streptomyces, Azotobacter, Pseudomonas, Paenibacillus Acinetobacter sp.

AM fungi

Glomus, Acaulospora, Scutellospora R. intraradices

Table 6.1 (continued)

Pennisetum glaucum, Sorghum bicolor Avena sativa cv. Baiyan No.7

Crop species

Iron contaminated soil Petroleum contaminated soil

Experimental condition higher activities of phenolics and defense enzymes Increased plant growth and Fe absorption Increased plant height, biomass, superoxide dismutase, catalase, and peroxidase activities; decreased malondialdehyde (MDA) and free proline

Plant/soil parameters

Mishra et al. (2016) Xun et al. (2015)

Reference

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leaf area, induces stomatal closure, reduces shoot growth and root development, alters plant water relations, increases tissue oxidative load, minimizes the water-use efficiency, and incite mortality (Farooq et al. 2009; Sun et al. 2017). The use of AM fungi is considered to be an efficient approach for the amelioration of drought and salinity stresses. In addition to affecting plant growth, drought and salinity can directly affect the abundance, diversity, and functioning of AM fungi. Studies have shown that long-term drought can seriously affect the abundance of AM fungi in the soil (Augé 2001). Soil moisture is an important factor that affects AM spore viability, germination, and infectivity in soils (Giovannetti et al. 2010). In addition, drought stress could also affect the extramatrical hyphal development of AM fungi in the soil (Neumann et al. 2009). Like drought, salinity also delays AM fungal spore germination and hyphal growth (Juniper and Abbott 2006; Evelin et al. 2009) leading to reduced colonization of plant roots (Kumar et al. 2015a). In spite of these shortfalls, a large number of studies have clearly proven beyond doubt the role of AM fungi in the bio-amelioration of these abiotic stresses (Muthukumar et al. 2017). The mechanisms of tolerance of AM plants to salinity and/or drought tolerance include the dilution of the Na+ and Cl ions through increased plant biomass accumulation, changes in soil hydraulic properties, modifications of root architecture, altered stomatal conductance, acquisition of nutrients and ion homeostasis, osmoregulation, counteraction of oxidative stress, increased photosynthetic efficiency, improved water relations, and regulation of phytohormones (Chandrasekaran et al. 2019; Evelin et al. 2019). Nevertheless, the AM fungal benefit to plants against abiotic stresses can vary with the fungal species. For example, inoculation of Rhizoglomus arabicum (Błaszk., Symanczik & Al-Yahya’ei) Sieverd., G.A. Silva & Oehl (endemic to hyperarid ecosystems) improved the transpiration efficiency and N and P uptake of sorghum more than when inoculated with R. irregularis (typical for temperate climates) under drought stress (Symanczik et al. 2018). The increased drought amelioration by R. arabicum compared to R. irregularis was attributed to the increased production of the extramatrical hyphae by the former in water-stressed soils (Symanczik et al. 2018). Moreover, this study also shows that the origin of the AM fungal isolates has a significant role in the amelioration of abiotic stresses. This view is exemplified in another study where R. intraradices and C. etunicatum strains isolated from the saline environment of the Cabo de Gata Natural Park, Almería, Spain was able to promote maize growth better under different levels of soil salinity than the strains of these species originating from the nonsaline environment (Estrada et al. 2013). Plant mortality is a common phenomenon under prolonged or intense abiotic stress. A few studies have shown that AM symbiosis could reduce or eliminate plant mortality resulting from abiotic stress. Inoculation of forage sorghum (cultivar Hunnigreen) with F. mosseae not only alleviated growth retardation but also significantly extended the plant’s lifespan under prolonged drought stress (Sun and Tang 2013). Further, the formation of the common mycelial network also appears to play a significant role in the AM benefit under water limitation. For instance, sorghum plants that were connected by the common mycelial network earlier during their

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development benefited more with prolonged lifespan and abundant intact arbuscules under water-limiting conditions (Sun and Tang 2013). This suggests that resource sharing may be an important strategy adopted by mycorrhizal plants to cope with the abiotic stress under field conditions.

6.4.5

Resistance to Biotic Agents

As pathogens often infect roots that are mycorrhized, it often raises the doubt on the ability of AM fungi to restrict or control plant diseases. The occurrence of root diseases in mycorrhizal plants indicates that pathogens have successfully adjusted to infect mycorrhizal roots. This prompted Rhodes (1980) to suggest that pathogens actually attack mycorrhiza and not roots. Nevertheless, AM fungal symbiosis enhances plant’s resistance against a wide range of bacterial and fungal pathogens. The extent of AM-mediated plant protection against pathogens could vary with the fungal taxa. For example, taxa in Glomus reduce the abundance of pathogens in the host roots to a greater extent than taxa in Gigaspora (Maherali and Klironomos 2007). As the AM fungi and the pathogens share the common niche within roots there could be competition for space and resources. But the evidence is meager to suggest the direct competition of AM fungi with other pathogens for plant resources and cortical space. Other possible mechanisms proposed include the biochemical and structural changes induced in the root cortex or the changes in the microflora in the mycorrhizosphere (Graham 2001). Changes in the accumulation of defense compounds and modifications in the metabolic profile can occur in response to mycorrhization. For instance, R. intraradices colonization of barrel clover (Medicago truncatula Gaertn.) roots triggers the formation of the cyclohexenone and mycorradicin derivatives, the apocarotenoids (Schliemann et al. 2008). These compounds are responsible for the yellow coloration of the mycorrhized roots in many plant species. Further, the apocarotenoids are also important in controlling the extent of colonization and functionality of the symbiosis (Schliemann et al. 2008; Jung et al. 2012). In addition to these, qualitative and quantitative variations in the flavonoid content (Akiyama et al. 2002), phytohormones involved in plant defense, phenolic compounds, and reactive oxygen species have also been noted (Jung et al. 2012). In addition to pathogenic fungi, plant roots are also infected by nematodes that may be either ecto- or endoparasitic. These pests cause extensive damage to crop roots resulting in tremendous yield losses (Wesemael et al. 2011). In addition to direct damage, nematode infestation also increases the chances of secondary infections by other soil-borne pathogens and at times may also act as vectors for plant viruses (Hao et al. 2012). Both greenhouse and field experiments involving several crop species have adequately demonstrated the AM fungal ability to protect plants against parasitic nematodes (Schouteden et al. 2015). The protective effect ranges from reduced infection and reproduction of nematodes to improved plant tolerance against nematode infestation. The mechanism of nematode control by AM fungi may

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be either direct or indirect. The direct mechanism involved in AM mediated control involves competition for nutrients and space or altered root morphology. The indirect mechanism covers plant-mediated responses like induced systemic resistance, changes in root exudation leading to altered rhizosphere interactions (Schouteden et al. 2015). Improved plant growth, nutrient uptake, or yield of AM in the presence of parasitic nematodes has been reported in apple (Malus domestica Borkh., Ceustermans et al. 2018), banana (Musa sp.), chickpea (Cicer arietinum L., Vos et al. 2012b; Reen et al. 2014), peach-almond hybrid (Calvet et al. 2001), tomato (Vos et al. 2012a, 2013), and coffee (Coffea arabica L., Alban et al. 2013; Koffi et al. 2013). There is mounting evidence to show that AM symbiosis can also have a significant impact on the above-ground parts of mycorrhizal plants (Pozo et al. 2009; Aloui et al. 2011). Most of these effects are related to stress tolerance and plant defense (Pozo and Azcón-Aguilar 2007). Though less studied than the control of soil-borne pathogens, AM fungi can also confer systemic protection against pests and pathogens attacking the aerial parts of plants (Jung et al. 2012). Previous studies though reported higher susceptibility of mycorrhizal plants to viruses and other biotrophic pathogens increased tolerance as evidenced by increased growth and yield have been reported in these plants. In short, AM association sets the plant in an alert state thereby efficiently controlling the plant diseases. This priming stimulus does not activate the plant defenses, instead of the defense response of the plant to a pathogenic invasion in a quick and fast manner than plants that are not exposed to this stimulus (Jung et al. 2012). Wehner et al. (2010) suggested that increased AM fungal diversity could improve pathogen protection through functional complementation as individual species in the AM fungal community could provide varied benefits like the uptake of nutrients, lignification of the roots, competition with pathogens, and other beneficial activities.

6.4.6

Weed Suppression

Competition from weeds for resources is a serious threat in crop production and yield loss arising from weeds menace can account for up to 34% each year (Oerke 2006). AM fungi are known to alter competition among plants in plant communities. This raises the possibility of AM fungi altering the crop-weed competition in the agroecosystems. In a controlled greenhouse study, inoculation of an AM fungal consortia (R. intraradices, F. mosseae, and C. claroideum) significantly reduced the growth of three weeds like Echinochloa crus-galli (L.) Beauv, Solanum nigrum L., and foxtail [Setaria viridis (L.) P. Beauv.]. Further, the presence of the crop plant (maize) amplified the suppressive effect of AM fungi on these weeds (Veiga et al. 2011). In a microcosm experiment growth of the weed species, foxtail was suppressed by the mycorrhizal faba bean (Vicia faba L.) or maize connected through a common mycelial network of F. mosseae (Qiao et al. 2016). Jordan et al. (2000) suggested two possible influences of AM fungi on weed communities. First, the AM

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fungi can alter the composition of the weed communities and second, they can change the outlook of the weeds making them more beneficial in the agroecosystems. A large gradient in the level of mycorrhizal dependence exists among weeds ranging from strongly mycorrhizal to non-mycorrhizal. The AM fungi may benefit the highly mycorrhizal dependent weeds in their growth, seed production, and seed quality (e.g., Koide and Lu 1995). Contrarily AM fungi can reduce or deter the growth of weakly mycorrhizal or non-mycorrhizal weeds by increasing the competitive advantage of the mycorrhizal crop hosts (Muthukumar et al. 1997). In a controlled glasshouse experiment, Daisog et al. (2012) examined the competitive ability, growth performance, and nutrient use of the mycorrhizal crop maize against two weeds S. nigrum (mycorrhizal) and Chenopodium album L. (non-mycorrhizal) either in pure stand or in different planting combinations. The results of the study suggest that both the weeds negatively affected maize growth performance. The decline in maize performance was more severe when grown in the presence of C. album than S. nigrum. Similarly, C. album also affected the biomass and N uptake by S. nigrum. This clearly suggests that weed species varying in their mycorrhizal status can influence the mycorrhizal crop host differently. In addition to altering crop–weed interactions, AM fungi can also reduce the extent of damage caused by parasitic weeds like witch-weed (Striga). Lendzemo et al. (2006) showed both in pot and field experiments that AM fungi can alter the nature of interaction between witch-weed and cereals by negatively affecting seed germination, seedling attachment, and delayed the emergence of the root parasite.

6.5

Influence of Cultural Practices on AM Fungi

A wide range of cultural methods are practiced in agriculture to improve crop health and productivity. These include developing crop varieties for desirable traits, use of synthetic fertilizers and organic manures to improve crop nutrition and chemicals in addition to different cropping patterns to protect the crops from weeds, pests, and pathogens. Though practices in organic farming are reported to be beneficial to AM symbiosis, many practices adopted in conventional agriculture are known to adversely affect AM formation and function. These aspects are discussed in detail in the following sections.

6.5.1

Plant Breeding

Breeding crops for improved yield or tolerance to different types of abiotic or biotic stresses is important to sustain high agricultural productivity. Studies have shown that the AM dependence not only vary between crop species but also varies among the cultivars of the same species (Eo and Eom 2009). Such types of variation among

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the cultivars of species have been shown for banana, maize, peanut (Arachis hypogea L.), millet, onion, soybean, tomato, and wheat (Tawaraya 2003; Taylor et al. 2015; Salloum et al. 2016; Ferrer et al. 2017). Plenchette et al. (2005) hypothesized that crop varieties selected through breeding programs would have high P demand or less mycorrhizal dependency. This is based on the fact that increased availability of soil nutrients reduces AM development and plant breeding programs are conducted in soils or conditions where nutrients are adequate for plant growth. In an extensive study, Martín-Robles et al. (2018) examined the influence of domestication on AM dependency of 27 crop species. The results of the study clearly indicated that the wild progenitors of the crop species were benefitted more by AM symbiosis under all levels of P in the soil. In contrast, mycorrhizal benefit was evident only under low soil P in domesticated crop species. It has been suggested that crop species may lose some of their symbiotic related genes during breeding programs. This is evidenced in studies where modern wheat cultivars were shown to be less mycorrhizal-dependent than their ancestors and maize varieties that are resistant to diseases are less mycotrophic than the susceptible varieties (Hetrick et al. 1992; Toth et al. 1990). It is therefore essential to develop strategies in future plant breeding programs to develop crop varieties that are responsive to AM symbiosis in addition to the desired traits.

6.5.2

Biocides

Biocides in the form of fumigant, pesticides, nematicides, and herbicides are routinely used to improve crop growth and yield. These synthetic chemicals have a widespread effect on nontarget organisms including AM fungi. Results of biocides on AM fungi are rather contradictory with many negatively affecting AM symbiosis while others have no effect or at times are stimulatory. In addition, the type of biocide application also has a varied effect on AM fungi. The influence of both contact and systemic fungicides are well studied among the different biocides.

6.5.2.1

Fungicides

Commercial crop seeds are treated with fungicides to control deterioration by fungal pathogens during storage and prophylactic coating of seeds with fungicides are widespread to protect the emerging seedlings (Munkvold 2009). The influence of this prophylactic fungicidal application on AM associations is rather inconsistent. Coating of chickpea and pea (Pisum sativum L.) seeds with metalaxyl-based systemic fungicides negatively affects root colonization by R. irregularis and indigenous AM fungi to varied levels (Jin et al. 2013). This study also showed that the sensitivity to metalaxyl fungicides can vary with AM fungal taxa and the associated crop species. For example, Acaulospora in chickpea and Simiglomus hoi (S.M. Berch & Trappe) G.A. Silva, Oehl & Sieverd., Rhizoglomus proliferum

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(Dalpé & Declerck) Sieverd., G.A. Silva & Oehl, and V. viscosa in pea were sensitive to metalaxyl fungicides (Jin et al. 2013). In contrast, a field study by Murillo-Williams and Pedersen (2008) using mefenoxam, fludioxonil, and mefenoxam plus fludioxonil coated soybean seeds had no significant effect on root colonization by native AM fungi. Similarly, in a greenhouse study, Cameron (2016) evaluated the interactive effect of seed-applied fungicides and crop varieties on AM fungi in three maize hybrids, three varieties of soybean [Glycine max (L.) Merr.], and two varieties of oats (Avena sativa L.). The results of the study indicated that the coating of seeds with fungicides did not significantly affect AM colonization in any of the crop varieties. The AM colonization in these three crop varieties was more affected by the host genotypes than the fungicides. These results clearly indicate that fungicides had no or minimal effect when used as a prophylactic seed coating. A pot study examining the effects of soil application of fungicides like Benomyl, Bavistin, Captan, and Mancozeb on Rhizophagus fasciculatus (Thaxt.) C. Walker & A. Schüßler associated with Proso millet (Panicum miliaceum L.) showed that the application of Captan significantly increased the mycorrhization and spore numbers in addition to improved plant growth and grain yield. In contrast, Benomyl had a deleterious effect on AM symbiosis (Channabasava et al. 2015). Soil drenching of mancozeb, mefenoxam, and azoxystrobin fungicides significantly reduced AM fungal colonization but not spore numbers (Vuyyuru et al. 2018). Available evidence does indicate that systemic fungicides that are absorbed by the roots and translocated through the xylem to the various parts of the plants when applied to the soil are more toxic to AM fungi than contact fungicides. Benomyl, the common systemic fungicide that is used to control pathogenic fungi has been shown to reduce the germination of F. mosseae spores even at recommended rates under in vitro conditions. However, benomyl at half the recommended rate or lower concentrations did not affect the germination of F. mosseae spores. Contrarily, all doses of benomyl inhibited the development of F. mosseae hyphae (Chiocchio et al. 2000). The systemic fungicide topsin used as the substitute for benomyl also has a negative influence on native AM fungi (Wilson and Williamson 2008). The systemic fungicide fenpropimorph inhibits the extraradical hyphal development of R. intraradices associated with RiT-transformed chicory roots through slowing down of the sterol pathway (Campagnac et al. 2009). In a further study, Campagnac et al. (2009) showed that the AM fungus R. intraradices protected the RiT-transformed chicory roots from the oxidative damage caused by the sterol biosynthesis inhibitor systemic fungicides fenhexamid and fenpropimorph in spite of the fungicides negatively affecting the extraradical hyphal development and sporulation of the fungus. These sterol biosynthesis inhibiting fungicides decreases the P transport and alkaline phosphatases and succinate dehydrogenase activities and MtPT4 expression levels associated with the extraradical mycelium affecting the metabolic and physiological activities of the AM fungus (Zocco et al. 2011). Fumigants like methyl bromide or formaldehyde eliminate all soil organisms including AM fungi. Nevertheless, the effect of fumigants are only temporary as AM fungal propagules within roots and organic matter that are unaffected by fumigants soon reestablishes in the soil (Udaiyan et al. 1995, 1999).

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Herbicides

Unlike fungicides, herbicides are less toxic to AM fungi at recommended levels. Nevertheless, herbicides can affect AM symbiosis when applied higher than the recommended levels. For instance, application of the herbicide nicosulfuron at 100 or 1000 times the recommended levels inhibited the diversity and colonization of maize roots by native AM fungi (Karpouzas et al. 2014). However, application of nicosulfuron even five times more than the recommended levels had no influence on the indigenous AM fungi under field conditions. However, the systemic, broadspectrum glyphosate herbicide can significantly decrease root mycorrhization, spore biomass in the soil, vesicles, and propagule numbers (Zaller et al. 2014). Glyphosate at higher doses is also known to reduce colonization, arbuscule, and vesicle formation by F. mosseae in roots of C. annuum (Ronco et al. 2008). In addition to affecting mycorrhization and root length with AM fungal structures, glyphosate or its degradation products can also reduce AM fungal spore viability thereby affecting the infecting potential of the fungi (Druille et al. 2013). The extraradical mycelium of C. etunicatum colonizing the roots of maize was shown to accelerate the degradation of the herbicide atrazine through modifications in the soil microbial activities and soil enzymes (Huang et al. 2009).

6.5.2.3

Nematicides

Generally, it is presumed that nematicides at recommended doses do not influence AM fungi and may be useful in improving mycorrhization as they control or eliminate fungivorous nematodes that feed on AM fungal hyphae. Though the application of nematicides like prophos, aldicarb, and carbofuran had no significant influence on root colonization, spore numbers, or infective propagules of R. fasciculatus at half their recommended dosages, all these nematicides significantly affected all the mycorrhizal variables when applied at recommended levels (Sreenivasa and Bagyaraj 1989). In contrast, Pattinson et al. (1997) found no significant negative effect of Fenamiphos nematicide on root colonization of cotton (Gossypium sp.) seedlings by F. mosseae. Though many studies have shown organophosphorus pesticides at recommended rates have either negligible or no significant effect on AM colonization, Wang et al. (2011) showed that increasing concentrations of phoxim a widely used organophosphorus pesticide in vegetable cultivation, could negatively affect AM root colonization in carrot (Daucus carota L. cv. Changfeng) and green onion (Allium fistulosum L. cv. Fengwang) by R. intraradices BEG 141 and F. mosseae BEG 167. From these studies, it is clear that application rates appear to be an important factor in determining the toxicity of pesticides on AM fungi.

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Biopesticides

In addition to xenobiotics, biopesticides are frequently used in organic farming to control plant pathogens and pests. However, the influence of these biopesticides on AM fungal symbiosis is very limited. Ipsilantis et al. (2012) examined the influence of four biopesticides azadirachtin, spinosad, pyrethrum, and terpenes on AM fungi both under pot and field conditions using pepper (C. annuum cv. Ozho). The results of the study indicated that spinosad, pyrethrum, and terpenes failed to influence the pepper root colonization by R. intraradices, C. etunicatum, and F. mosseae strains in pot culture and the native AM fungal community under field conditions. In contrast, application of azadirachtin resulted in the inhibition of the C. etunicatum in pot culture and persistent shifts in the AM fungal community in the field (Ipsilantis et al. 2012).

6.5.3

Tillage

In agriculture, tillage is used to prepare the field for crop establishment. Tillage has a certain advantage like weed control, burying crop residues, incorporating fertilizers, and increasing water percolation (Roger-Estrade et al. 2010). As tillage may accelerate soil erosion, reduced or no-tillage management is currently practiced in sustainable agriculture. The abundance and diversity of AM fungi reduce with soil depth and certain AM fungal species may be more prominent in some soil layers (Yang et al. 2010). A recent high-throughput molecular analysis revealed that the subsoil may harbor unique AM fungal taxa (Sosa-Hernández et al. 2018). Based on these observations, Sosa-Hernández et al. (2018) hypothesized that AM fungal taxa possessing intraradical lifestyle could colonize soils in different horizons and are little affected by soil factors. Nevertheless, soil tillage may redistribute the AM fungal propagules by turning over the propagule rich soil to the root free surface profile. Sosa-Hernández and coworkers further speculated that AM fungi with a ruderal strategy like rapid growth rates and abundant sporulation may dominate the topsoil and stress tolerators with slow growth and long-lived mycelium may characterize subsoils. Tillage also reduces the glomalin concentration in the soils (Wright et al. 2007). In a recent study, conventional tillage was shown to reduce the AM fungal species richness and the average spore densities associated with soybean compared to no-tillage (de Pontes et al. 2017). Tillage stress also results in the evolution of certain AM fungal indicator species. For example, based on the Monte Carlo test, de Pontes et al. (2017) identified Acaulospora denticulata Sieverd. & S. Toro, Acaulospora scrobiculata Trappe, Dentiscutata cerradensis (Spain & J. Miranda) Sieverd., F.A. Souza & Oehl, Paraglomus occultum (C. Walker) J.B. Morton & D. Redecker, and Sclerocystis coremioides Berk. & Broome as indicators for the no-tillage systems and Gigasporales species like Gigaspora margarita W.N. Becker & I.R. Hall, Racocetra coralloidea (Trappe, Gerd. & I. Ho)

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Oehl, F.A. Souza & Sieverd., and Racocetra fulgida (Koske & C. Walker) Oehl, F.A. Souza & Sieverd., indicators of conventional tillage systems. Tillage also reduces the AM species composition in vineyards. Vineyard soils with no-tillage had higher diversity and harbored 42% more AM fungal species than tilled soils (Oehl and Koch 2018). Brito et al. (2012) showed that conventional tillage may reduce AM fungal diversity by 40% in Mediterranean soils and negatively influenced AM fungal spore abundance and the root length colonization in wheat cv. Coa and sunflower (Helianthus annuus L.) (Brito et al. 2012). The extraradical hyphae that explore the soil are also the major fungal propagules for initiating symbiosis in many AM fungal taxa. Soil tillage fragments these hyphal networks reducing the fungal inoculum potential in the soil. Therefore, the AM system is more stable in no-till conditions than in reduced or conventional tillage.

6.5.4

Soil Compaction

Compaction is soil stress arising from the use of heavy machinery in conventional agriculture for crop production. Soil compaction greatly affects plant growth by reducing the root development and subsequently decreasing the plant’s acquisition of water and nutrients (Barzegar et al. 2006). For instance, plants’ efficiency to take up N in compacted soil reduces as the result of N emission (Ruser et al. 2006). In addition, soil compaction drastically decreases the proportion of macropore to micropore ratio, increases soil bulk density, and resistance to root penetration (Arvidsson 1999; Pereira et al. 2007). A limited number of studies have examined the influence of soil compaction on AM fungal symbiosis. Some of the earlier studies indicate that soil compaction decreases the root length colonized by AM fungi and the amount of extraradical mycelium produced in the soil (Wallace 1987; Nadian et al. 1997, 1998). Increase in soil densities has also been shown to reduce the number of AM fungal spores in the soil (Sales et al. 2018). These reductions in AM fungal parameters were attributed to the reduction in soil pore size, ethylene production, and a decrease in the oxygen concentration. Inoculation of wheat or maize with C. etunicatum and different strains of F. mosseae increased plant growth, nutrient uptake, and yield characteristics in compacted soils although the AM fungal benefit tended to reduce with increasing compaction (Miransari et al. 2008, 2009; Miransari 2013). Based on these studies, it is clear that soil compaction has a negative effect on AM fungi, but still AM fungi can improve plant growth in compacted soils.

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6.5.5

Cropping Patterns

6.5.5.1

Crop Rotation

The influence of cropping patterns on AM fungal communities and functioning is well known. For example, continuous cultivation of mycotrophic plant species increases the AM inoculum in the soil whereas those of non-AM or less mycotrophic crops tend to reduce it (Plenchette et al. 2005). Crop rotation involving non-mycorrhizal canola (Brassica napus L.) decreased AM colonization in the succeeding crop maize. However, no such negative effect was evident when the preceding crop was soybean. The negative effect of canola on AM fungal colonization in maize was not ameliorated by cover cropping with mycorrhizal winter wheat. Nevertheless, the negative influence of canola on AM colonization in maize was restricted to a single year (Koide and Peoples 2012). In a field study, Bakhshandeh et al. (2017) examined planting of wheat genotypes after crop rotation with canola or chickpea at various rates of N and P fertilization. Average AM fungal colonization in wheat cultivars was 60% higher after chickpea than canola rotation and positively influenced the wheat yield. Further, increased mycorrhizal colonization also reduced water stress in wheat plants as evidenced by leaf δ13C of mycorrhizal plants (Bakhshandeh et al. 2017). A field study involving the succession of wheat and oats along with different types of tillage over a 2-year period indicated no differences in metabolically active hyphae of the native AM fungi in the soil. However, cultivation of wheat increased the abundance of Acaulospora spp. spores than oats (Castillo et al. 2006). Molecular characterization of maize roots growing in western Kenyan soils that were under continuous maize cultivation revealed the abundance of Dentiscutata heterogama (T.H. Nicolson & Gerd.) Sieverd., F.A. Souza & Oehl, than maize rotated with Crotalaria grahamiana Wight & Arn. (Mathimaran 2005). Increased colonization of crop species by native AM fungi and subsequent increase in crop growth and yield facilitated by the preceding mycorrhizal crops is well documented (Harinikumar and Bagyaraj 2005; Grant et al. 2009). A 2-year crop rotation involving the relay cropping of maize followed by horse gram (Dolichos biflorus L.) during the first year and upland rice during the second year increased the activity of native AM fungi and uptake of P by rice (Maiti et al. 2011). In a subsequent study, this 2-year corn– horse gram–rice crop rotation was compared with three other crop rotations widely practiced by farmers like green gram [Vigna radiata (L.) R. Wilczek]—upland rice, black gram [Vigna mungo (L.) Hepper]—upland rice and radish—upland rice. The results of the study indicated that corn–horse gram–rice rotation resulted in maximum root length colonization by native AM fungi, P uptake, and grain yield in upland rice (Maiti et al. 2011). Cropping of sunflower, grain legumes [green gram, peanut, soybean], and green manure legumes [sunn hemp (Crotalaria juncea L.), velvet bean (Mucuna pruriens var. utilis (Wall. ex Wight) L.H. Bailey] prior to planting sugarcane (Saccharum sp.) was studied in São Paulo, Brazil (Ambrosano et al. 2010). Peanut, velvet bean, and sunflower were the rotational crops that had a

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higher percentage of root length colonized by native AM fungi. In contrast, sunn hemp developed least AM fungal colonization among the rotational crops. Moreover, the positive correlation between sugarcane plant height and AM fungal colonization levels of the rotational crops suggests the contribution of the AM colonization levels of the preceding crops on the growth of succeeding crop (Ambrosano et al. 2010).

6.5.5.2

Intercropping

The intercropping practice involves cropping of two or more crops simultaneously with an objective to increase the yield per given unit area (Francis 1986; Vandermeer 1992). Major advantages of intercropping include greater utilization of resources, soil fertility conservation, management of pests, increased income, and insurance against the failure of a particular crop (Vandermeer 1992). Intercropping increases AM colonization, hyphal and spore densities, and infective propagules in addition to plant growth, nutrient uptake, and yield (Table 6.2). Intercropping also facilitates resource sharing between the crop species through the common mycelial network of AM fungi. For example, the transfer of N from legume to cereal crop has been demonstrated in soybean–maize intercropping in a greenhouse study (Meng et al. 2015). In addition, intercropping can also benefit coexisting crop species through the sharing of water resources when crops exploring different rooting depths are used. In a microcosm experiment, Saharan et al. (2018) showed that intercropping of the deep-rooted pigeon pea [Cajanus cajan (L.) Millsp.] along with the shallow-rooted finger millet (Eleusine coracana Gaertn.) increased the drought tolerance of the latter. The drought endurance of finger millet was attributed to the uptake and distribution of deeply available water by the pigeon pea through the hydraulic lift and transfer through the common AM fungal mycelial network termed as bioirrigation. In addition to the direct transfer of water to the coexisting plants, the fungal hyphae can also distribute water supporting the activities of microorganisms in the mycorrhizosphere (Worrich et al. 2017). These phenomena of hydraulic lift and bioirrigation can be of great relevance in dryland agriculture of the tropics where legume–cereal intercropping is widely practiced.

6.5.6

Cover Crops

Cover crops are considered important in sustainable agriculture for their benefits in maintaining or enhancing soil quality, mycorrhizal potential, and crop performance. When soils lie fallow after crop harvest a rapid decline in AM fungal population results as the obligate fungi is deprived of the much-needed carbon for sustenance (Kabir and Koide 2002). As a consequence, AM fungal populations are considerably low at the beginning of the next cropping season. In their meta-analysis Bowles et al. (2016) showed that cover cropping can increase AM colonization of the succeeding

Field study

Z. mays—Vigna unguiculata— Gossipium hirsutum Raphanus sativus var. Midoribijin— Paspalum notatum

Field study

Field study

Field study

Field study

Greenhouse

Field study

Z. mays—Phaseolus vulgaris var. Derakhshan

Cajanus cajan—V. unguiculata— Z. mays Z. mays—C. cajan

Z. mays—Glycine max

Musa accuminata. cv. Grande Naine—Ipomea batatas/Arachis hypogaea L.cv A26

Z. mays—Vigna umbellata/ V. unguiculata/Lablab purpureus/ Vigna radiata

Compartmentalized root boxes

Study type Compartmentalized acrylic root boxes

Intercropping system Sclerocarya birrea—Pennisetum glaucum—Zea mays

Native AM fungi

Rhizophagus irregularis

Native AM fungi Rhizophagus clarus Native AM fungi

Funneliformis + Rhizobium leguminosarum

Native AM fungi G. margarita

AM fungi Gigaspora margarita

Increased mycorrhizal colonization. No effect (A. hypogaea), negative effect on plant growth and nutrient uptake (I. batatas) Increased growth and yield, N content, AM spore abundance and density

Improved growth, biomass, grain yield, and nutrient uptake Increased plant shoot P content, AM fungal colonization, spore numbers, and infective propagules

Increased root colonization

Parameters Increased biomass and height of S. birrea. More AM hyphal density and spore numbers Increased spore density, root colonization, Glomalin-related protein Increased protein content. Decreased superoxide dismutase and catalase activities Increased root growth and nutrient uptake

Rice straw, maize straw, and Pongamia pinnata

15 kg of N (KNO3) per hectare at sowing time

Goat manure and gliricidia

Fertilizer/manure application

Punyalue et al. (2018)

Mandou et al. (2016)

Njira et al. (2017) Stephen et al. (2013) Harinikumar et al. (1990)

Marzban et al. (2017)

Sousa et al. (2012) Matsumura et al. (2007)

Reference Muok et al. (2009)

Table 6.2 Influence of different intercropping system and arbuscular mycorrhizal (AM) fungi on plant and fungal variables with or without fertilizer/manure application

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Anethum graveolens—P. vulgaris

Z. mays—Z. mays—Triticum aestivum—Setaria viridis—Vicia faba—V. faba—Z. mays—S. viridis Brassica oleracea var. Italica— Sesamum indicum R. irregularis

Greenhouse: Compartment split-root system Field study F. mosseae

Funneliformis mosseae

Greenhouse

Increased plant biomass, N and P uptake; supression of S. viridis (weed) Increased dry matter, defense response: indole glucosinolates in broccoli roots and leaves Improved dry weight, and P, K, Fe, Zn, and Mn contents (A. graveolens); Increase in cultivable bacterial community and yield of essential oil Weisany et al. (2015)

Tong et al. (2015)

Qiao et al. (2016)

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crops by around 30%. Nevertheless, the extent of the positive influence of cover crops on AM fungal symbiosis was dependent on the type of cover crops used. Though not very consistent, many studies have shown that cover crops could influence the abundance and diversity of AM fungal communities (Bowles et al. 2016). Growing vetch (Vicia villosa L.) or barley (Hordeum vulgare L.) as winter cover crops in a semiarid Mediterranean climate greatly improved the various variables that were directly or indirectly related to AM symbiosis in maize and sunflower grown in spring. Barley as a cover crop performed better compared to vetch or a bare fallow. Cover cropping of barley increased the AM fungal spore abundance by 60–70%, soil enzyme activities by twofold, and the extraradical hyphal length in the succeeding maize. Similarly, in sunflower, the extraradical hyphal length increased by 80%, higher β-glucosaminidase activity and 30% enhancement in other variables in response to cover cropping with barley. In addition, cover crops also increased the soil aggregation stability mediated through AM fungi (GarcíaGonzález et al. 2016). Cover cropping with wheat and Italian ryegrass (Lolium multiflorum L.) on a volcanic ash soil in Japan increased the spore abundance of native AM fungi by twofold than cover cropping with brown mustard (Brassica juncea L.). Subsequently, maize grown on Italian ryegrass and wheat precropped soils had more AM colonization in their roots than those raised on soils precropped with brown mustard. Cover crops also influenced the abundance of C. claroideum and F. mosseae in maize roots (Higo et al. 2018).

6.5.7

Organic Farming

Traditionally amendments of organic matter in the form of crop residues, animal manures, green manures, and composts that possess significant concentrations of nutrients to the soil were used to maintain soil fertility and to enhance crop growth and yield (Quilty and Cattle 2011; Cavagnaro 2014). In direct contrast to inorganic fertilizer application, organic manuring has been shown to improve the populations and diversity of AM fungi. The positive influence of organic manures on AM symbiosis is well demonstrated both under controlled and field conditions (Qin et al. 2015; Arshad et al. 2017). Qin et al. (2015) examined the influence of longterm organic manure (composted pig manure) application on the abundance and community composition of AM fungi in the soil and roots in a subtropical wheat-rice rotation. The results of the study indicated that the application of the pig manure increased the AM fungal hyphal and spore biomass contents. In addition, the study also showed that the AM fungal community was not significantly altered by organic manuring (Qin et al. 2015). In a field study conducted in a Chernozem soil, the effect of different types of fertilization on the AM fungal community associated with maize was studied (Zhu et al. 2016). The results of the study indicated that fertilizer regimes significantly influenced the AM fungal community in the maize rhizosphere. Organic manure was the important factor influencing AM fungal community composition as revealed by

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the redundancy analysis. Moreover, the study also showed that specific chemical components in the dissolved organic matter can significantly influence specific AM fungal taxa in the rhizosphere. For example, as concentrations of 2,6,10trimethyltetradecane and 2-ethylnaphthalene had a negative influence on the relative abundance of Glomus, 3-methylbiphenyl positively influenced the abundance of Rhizophagus in the maize rhizosphere (Zhu et al. 2016). A similar variation in response of different AM fungal taxa to compost addition was reported by Yang et al. (2018). As the abundance of R. fasciculatus associated with soybean increased with increasing concentrations of compost amendment, the abundance of Paraglomus sp., exhibited an inverse trend. However, these trends were evident only during the late stages of plant development and not at the earlier stages. Organic manuring may not always stimulate AM symbiosis as certain studies have shown a lack of influence or even a negative influence of organic manuring on the association. Aguilar et al. (2017) evaluated the effect of organic fertilizers (compost, cow manure, and green manure) and maize genotypes (two hybrids and two landraces) on plant growth and rhizosphere microorganisms. The overall response of AM fungal colonization to organic fertilization in maize cultivars was similar to organic manures exerting no significant influence with the exception being the green manuring with rape where a decline in colonization was evident (Aguilar et al. 2017). In another study, compost addition at different rates had no significant influence on the AM fungal community composition associated with soybean (Yang et al. 2018). The response of AM fungi to an organic amendment can also vary with soil types. Amendment of different rates of poultry compost to loam and peat soil increased the AM colonization and spore numbers in maize inoculated with the fungal consortia [F. mosseae, F. geosporum and C. etunicatum] in both the soil types. Nevertheless, the positive influence of poultry compost on the mycorrhizal parameters was more pronounced in the loamy soil than in peat soil (Abdullahi et al. 2015). Like organic amendments to the soil, liquid organic fertilizers applied as sprays also stimulates AM fungal colonization (Azevedo et al. 2017). Spraying common bean (Phaseolus vulgaris L.) with 5% of an anaerobically fermented mixture of bovine milk, cattle manure, fresh water, mineral salts, and sugarcane molasses increased the percentage root length colonization and spore numbers of indigenous AM fungi. Similarly, spraying of vermiwash increased AM fungal root colonization in Capsicum assamicum Purkayastha & L. Singh, but failed to affect spore numbers (Khan et al. 2014). All these studies clearly show that the influence of organic amendments can vary with host species, soil types, and the associating AM fungi. Of recent, the use of biochar to improve soil fertility is gaining popularity and there are several studies where application of biochar has been shown to enhance plant growth. Application of biochar has been shown to variedly influence AM colonization and function and the effect can be positive, neutral, or negative (see Koide 2017 and references therein). The differences in the influence of biochar on AM fungi can be due to the varied amount of biochar used, physical and chemical characteristics of the biochar used, and the duration of the experiment. Application of biochar and inoculation with AM fungi has been shown to improve plant growth

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(Han et al. 2016), drought tolerance (Hashem et al. 2018), and decrease heavy metal accumulation (Zhang et al. 2019) in different plant species. Moreover, the hyphae of AM fungi can colonize the biochar surfaces, absorb nutrients, and translocate it to plant roots. In a monoxenic culture, the extraradical hyphae of R. irregularis originating from carrot roots strongly attached to the inner and outer surfaces of the biochar and translocated 33P from the biochar to the roots. This clearly demonstrates that AM fungal hyphae can acquire and transfer nutrients from the microsites within biochar that are too small for roots enter (Hammer et al. 2014). As biochar can adsorb phosphate from soil leachates, it could reduce the loss of phosphatic fertilizers applied to the crops and with the aid of AM fungi would help in efficient use of the nutrient applied.

6.6

Conclusion

From the presented evidence it is clear that AM fungi play a significant role in crop growth, health, and productivity. Further, AM fungi also control the fitness and competitiveness of the plants under resource limiting conditions. The role of AM fungi therefore appears to be important in attaining the goals of sustainable agriculture where the emphasis is on the natural cycling of nutrients, limiting the use of non-farm inputs, maximum productive use of crop species, changes in cropping patterns for long-term sustainability, and conservation of soil and biological resources. Most of our present understanding of the resource exchange in the AM symbiosis is based on experiments performed under controlled conditions with individual plants that are associated with a selected single fungus. However, field experiments have also proved that AM symbiosis can be functional under field conditions. Nevertheless, as AM fungi depend on plants for the carbon supply, factors that affect plants invariably also affect the AM fungi. In addition, many of the conventional agricultural management practices like the application of synthetic fertilizers and biocides, tillage and cultivation of non-mycorrhizal crops are known to affect the development and functioning of the AM symbiosis. In spite of the progress that has been made in understanding the AM symbiosis many critical questions still remain unanswered like the varied effect of biocides on AM fungi, changes in the efficiency of the AM fungal communities in cultivated soils, could AM fungi relieve the dependence on agrochemicals or at least to what extent AM fungi could reduce the dependence on synthetic chemicals and differential response of modern crop varieties on AM symbiosis? These aspects should be addressed in future studies. Further research is essential to better understand and work out the costs and benefits of the AM symbiosis in the agroecosystems, and how the indigenous fungal communities could be exploited through changes in management practices in sustainable agriculture.

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Weisany W, Raey Y, Zehtab-Salmasi S, Sohrabi Y (2015) Arbuscular mycorrhizal colonization can improve plant yield in cropping systems. J New Biol Rep 4:197–202 Wesemael W, Viaene N, Moens M (2011) Root-knot nematodes (Meloidogyne spp.) in Europe. Nematology 13:3–16 Wilson GWT, Williamson MM (2008) Topsin-M: the new benomyl for mycorrhizal-suppression experiments. Mycologia 100:548–554 Worrich A, Stryhanyuk H, Musat N, König S, Banitz T, Centler F, Frank K, Thullner M, Harms H, Richnow HH, Miltner A (2017) Mycelium-mediated transfer of water and nutrients stimulates bacterial activity in dry and oligotrophic environments. Nat Commun 8:15472. https://doi.org/ 10.1038/ncomms15472 Wright SF, Green VS, Cavigelli MA (2007) Glomalin in aggregate size classes from three different farming systems. Soil Tillage Res 94:546–549 Xun F, Xie B, Liu S, Guo C (2015) Effect of plant growth-promoting bacteria (PGPR) and arbuscular mycorrhizal fungi (AMF) inoculation on oats in saline-alkali soil contaminated by petroleum to enhance phytoremediation. Environ Sci Pollut Res 22:598–608 Yang FY, Li GZ, Zhang DE, Christie P, Li XL, Gai JP (2010) Geographical and plant genotype effects on the formation of arbuscular mycorrhiza in Avena sativa and Avena nuda at different soil depths. Biol Fertil Soils 46:435–443 Yang W, Gu S, Xin Y, Bello A, Sun W, Xu X (2018) Compost addition enhanced hyphal growth and sporulation of arbuscular mycorrhizal fungi without affecting their community composition in the soil. Front Microbiol 9:169. https://doi.org/10.3389/fmicb.2018.00169 Zaller JG, Heigl F, Ruess L, Grabmaier A (2014) Glyphosate herbicide affects belowground interactions between earthworms and symbiotic mycorrhizal fungi in a model ecosystem. Sci Rep 4:5634. https://doi.org/10.1038/srep05634 Zare M, Ordookhani K, Alizadeh O (2011) Effects of PGPR and AMF on growth of two bred cultivars of tomato. Adv Environ Biol 5:2177–2181 Zhang X, Cai X (2011) Climate change impacts on global agricultural land availability. Environ Res Lett 6:014014. https://doi.org/10.1088/1748-9326/6/1/014014 Zhang F, Liu M, Li Y, Che Y, Xiao Y (2019) Effects of arbuscular mycorrhizal fungi, biochar and cadmium on the yield and element uptake of Medicago sativa. Sci Total Environ 655:1150–1158 Zhao R, Guo W, Bi N, Guo J, Wang L, Zhao J, Zhang J (2015) Arbuscular mycorrhizal fungi affect the growth, nutrient uptake and water status of maize (Zea mays L.) grown in two types of coal mine spoils under drought stress. Appl Soil Ecol 88:41–49 Zhu C, Ling N, Guo J, Wang M, Guo S, Shen Q (2016) Impacts of fertilization regimes on arbuscular mycorrhizal fungal (AMF) community composition were correlated with organic matter composition in maize rhizosphere soil. Front Microbiol 7:1840. https://doi.org/10.3389/ fmicb.2016.01840 Zocco D, Van Aarle IM, Oger E, Lanfranco L, Declerck S (2011) Fenpropimorph and fenhexamid impact phosphorus translocation by arbuscular mycorrhizal fungi. Mycorrhiza 21:363–374

Chapter 7

Role of Microbial Communities in Sustainable Rice Cultivation Thilini A. Perera and Shamala Tirimanne

Abstract Rice is a staple food for more than half of the world population and cultivation to feed the need demands an enormous amount of fertilizers, especially nitrogen. Harmful consequences of fertilizers to the soil and the biogeochemical cycles are being addressed globally and prompt action towards sustainable cultivation is imperative. The positive interactions within the soil microbial communities are a key factor in improved soil health. The soil microbiota and their interactions are therefore considered as a major potential approach towards sustainable cultivation of paddy. Naturally present or induced microbial communities contribute greatly to increase of soil fertility. Starting from undifferentiated chains, these associations could gradually lead up to complex, permanent, more intimate modes of life in biofilms, where remarkable benefits such as irreversible differentiation of cells, division of labor among different cell types, and intercellular cooperation are achieved. A recent development of a nitrogen fixing bacteria-fungal biofilm that led to the reduction of the urea fertilizer usage for rice cultivation by 50% through induced nitrogen fixation is a solid evidence for the massive potential towards sustainability accompanied by microbial communities and interactions. Keywords Rice cultivation · Biofilms · Fertilizer · Rhizosphere

7.1

Introduction

Rice (Oryza sativa), a semi-aquatic annual grass, belonging to the family Poaceae, is a staple food for more than half of the world population, providing 80% of their food requirement. It is an annual monocotyledon plant which is self-fertilized. The genome sequence of the rice plant is known and is about 400–430 million bp (Mb) and it is smaller than most of the major cereals (Sasaki and Burr 2000). T. A. Perera · S. Tirimanne (*) Department of Plant Sciences, Faculty of Science, University of Colombo, Colombo, Sri Lanka e-mail: [email protected]; [email protected] © The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2021 G. Seneviratne, J. S. Zavahir (eds.), Role of Microbial Communities for Sustainability, Microorganisms for Sustainability 29, https://doi.org/10.1007/978-981-15-9912-5_7

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Fig. 7.1 Trend of global rice production yield (Million MT) over the years (Data Extracted from: www.fao.org/faostat) (Million MT) over the years (Data Extracted from: www.fao.org/faostat)

Rice consumption has a very long history. It has been used for human consumption for more than 10,000 years before the use of any other crop (Conteh et al. 2012). From the total global rice cultivated areas, about 85% is cropped under wetland cultivation (Kennedy 1992). Today, rice is grown in a wide range of locations under different climatic zones due to its high adaptability (Yoshida 1981), and as a result 21% of global per capita energy and 15% per capita protein is provided by rice. Rice is consumed and grown mostly by the poor in the world, especially in Asia. About 60% of the global population resides in Asia where 92% of the world rice is produced with 90% of the global rice being consumed in Asia. According to the Knowledge Bank of the International Rice Research Institute (IRRI) (2016), the world’s largest rice producers include China, India, Indonesia, Bangladesh, Vietnam, and Thailand. These countries together account for more than two-thirds of the world’s total rice production. The total global rice production in 2016 July was 495 Million metric tons (mmt) (Food and Agriculture Organization (FAO) 2016). This on average accounts for 29% of the total output of grain crops (Onyango 2014). The graph of global rice production over the years shows a steep increase over the years (Fig. 7.1). The food and agricultural policy research states that the global rice demand is expected to rise up to 496 million tons in 2020 and will rise up to 555 million tons in 2035. Globally 161.2 million hectares of land are being used for rice cultivation, and the average global yields amount to 4.45 tons/hectare (Childs 2016). Paddy cultivation is by far second to only the production, consumption, and cultivation of wheat. Rice could be grown by either direct seeding or transplanting (IRRI 2016). In direct seeding methods, the seeds are sown directly in the field and in transplanting the seedlings are first raised in seedbeds and are then planted in the field (IRRI 2016;

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Mae 1997). The field is leveled and bunded before the seeds are sown or transplanted (Mae 1997). Rice is a crop that is extremely sensitive to water deficit and therefore a good water management system is an essential requirement for a maximum efficiency of growth and yield (IRRI 2016). Also, rice is a heavily fertilized crop (Mae 1997). Depending on the variety, cultivation method, and the existing environmental conditions, rice plants takes around 3–6 months to grow from the seeds to a mature plant (IRRI 2016). In the growth cycle of rice, four agronomic growth phases can be identified, namely, germination phase, vegetative phase, reproductive phase, and the ripening phase as depicted in Fig. 7.2 (Rice Production Manual, IRRI). Depending on the duration that a particular variety takes to complete the life cycle, rice varieties are categorized into two groups, short duration varieties that mature in 105–120 days and the long duration varieties that mature in 150 days (Rice Pedia, IRRI 2016).

7.1.1

High-Intensity Agriculture is a Need

The world population had been 3.9 billion, about 50 years ago in 1970. It had almost doubled, to 7.4 billion people in 2016 and is expected to increase upto 9.5 billion people in 2050 (Food and Agriculture Organization (FAO), World Bank 2016). But the amount of per capita arable land has decreased from 0.4 ha in 1970 to 0.2 ha in 2016 and is expected to reduce up to 0.15 ha in 2050 (FAO, World Bank 2016). To feed this exponentially increasing world population, with the concurrently decreasing arable lands, increase in the productivity of crops per unit land area has become a fundamental need. High yielding, modern varieties of rice and wheat were produced mainly through rice breeding efforts by scientists and were released to the farmers in Asia and Latin America during the early 1960s in the era of “green revolution” or the era of “high intensity agriculture.” According to Evenson and Gollin (2003), high-yielding varieties were a major accomplishment of the era of green revolution. Doubling of the population and the upsurge of food demand were taken care of, by these modern varieties produced. In these high-yielding varieties, a substantial amount of energy was channeled towards the increase of yield and little was used to the production of straw and leaf material. These were much more responsive to fertilizers than traditional varieties, and also more grains or high yields were obtained (Dalrymple 1986). Considering the increasing demand that the world was heading to in relation to food, the qualities of these new varieties were undoubtedly remarkable. Tilman (1998) has pointed out that the most defining feature of the high-intensity agriculture is their need for nitrogen fertilizers and intense use of pesticides. Nitrogen is a major input and the nutrient that determines the yield potential of crops (Mae 1997). Ladha et al. (2016) have stated that Nitrogen as the sine qua none (the absolute necessity) of today’s high yielding agriculture. There is no phase of growth of the life cycle of rice that is not affected by nitrogen. During the vegetative growth phase, nitrogen is highly involved in the increase of plant height, tiller number, leaf

Fig. 7.2 Vegetative, Reproduction and ripening phases of the rice growth cycle (Rice Production Manual, IRRI)

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size (Dobermann and Fairhurst 2000), number of stalk (total tillers/hill) (Ghanbarimalidarreh 2011; Chaturvedi 2005), dry matter content of a stem per hill (Youseftabar et al. 2012; Chaturvedi 2005), root volume (Anil et al. 2014), and many other characteristics. Also, during the vegetative growth, sink organs assimilate nitrogen. The assimilated nitrogen is used for amino acid synthesis, leading to protein and enzyme synthesis, building up the plant architecture, and to build up the components required for photosynthetic machinery (Hirel et al. 2007). During the reproductive and ripening phases of the life of a rice plant, remobilization of the accumulated nitrogen to the seeds occur and the roots and the shoots behave as sources of nitrogen in the process. Proteins stored in source tissues are hydrolyzed releasing amino acids and the amino acids are stored in the reproductive and storage organs (Masclaux et al. 2000). Sinclair and Jamieson (2006) state that generally N becomes the limiting factor to obtain the maximum yields as nitrogen contributes to obtaining an increased number of spikelets (Yoshida et al. 2006) and filling of the grains (Mae 1997); the two most important factors of obtaining high yields. Phosphorous (P) and Potassium (K) are two other major nutrients that are applied as fertilizers in rice cultivation. Phosphorus is mainly added as triple superphosphates while Potassium is added in the form of potassium chloride (KCl) frequently and as potassium sulfate (K2SO4) less frequently (Singh and Singh 2017). Phosphorous is a component of the genetic material of the plant cell (adenosine triphosphate/ ATP). Phosphorous is also involved in the synthesis of phospholipids, nucleotides, glycoproteins, etc. (Singh and Singh 2017). Lack of phosphorous can lead to stunting of the rice plant as well as reduction of leaf elongation and expansion (Marschner 1995). Also, since P aids in rice root growth, panicle number increment, and the increment of the grain weight (Fageria and Gheyi 1999), it influences the growth and the yield of the rice plant. Absence of P leads plants to be low responsive to other nutrients, specifically N and K. In the rice systems resulting in high yields, potassium becomes the limiting factor after nitrogen (Singh and Singh 2017). Potassium contributes to plant growth and development in many ways. It helps to improve root growth, plant vigor, prevent lodging, and increased pest and disease resistance. Potassium also increases the number of spikelets/panicle, percentage number of grains, and 100-grain weight (Singh and Singh 2017).

7.1.2

Negative Impacts Associated with Fertilizers

Although the need to feed the world was addressed unquestionably with highintensity agriculture, the problems arising were substantial. The negative impacts to the soil, soil microbial biomass, groundwaters (contaminations), eutrophication of rivers, lakes, and coastal marine ecosystems, depletion of oxygen in the water bodies, toxic accumulation, impact on the aquatic food webs are a few obvious repercussions (Matson et al. 1998; Vitousek et al. 1997). Some of these damages are irreversible or can take a very long time to reverse. Sustainability of the

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high-intensity agriculture is therefore dubious. The need of a sustainable greener revolution is a task to look forward to. Shiva (2016), the author of the book “Consequences of green revolution” has illustrated the damage done to Panjab (India) due to the green revolution, where she quotes, “Instead of abundance, Punjab has been left with diseased soils, pest-infested crops, waterlogged deserts, and indebted and discontented farmers. Instead of peace, Punjab has inherited conflict and violence.” These are common consequences of green revolution that is common to most of the nations which adopted it.

7.1.2.1

Socioeconomic Impacts of Nitrogen Fertilizers

Urea is an excellent nitrogen fertilizer that is being used to meet the demands for rice cultivation in the world. Although it is incredibly dependable, it is coupled with a massive amount of negative implications in a country’s economy, human and animal well-being, and the environment. To produce urea by the Harbour Bosch process, carbon dioxide and anhydrous ammonia are made to react under high temperatures and pressure (Smil 2001). This process demands high energy and is supplied by fossil fuels which are nonrenewable. Using fossil fuels, more than 100 Tg of reactive nitrogen is produced every year (Galloway et al. 2004; Fowler et al. 2013). Petroleum being the main fuel in the Harbour Bosch process, the fluctuations in the global petroleum market, due to various political and economic issues directly influence the price of fertilizer. Figure 7.3 shows the fluctuations of the world urea fertilizer prices for years, 2010–2018. Highly variant fertilizer prices make it difficult to predict the future trends (Dawe 2008). According to the National Fertilizer Secretariat (NFS) of Sri Lanka, total urea required for agriculture is imported to the country (NFS 2002). Amount of urea used for paddy cultivation in the recent years are graphically shown in Fig. 7.4 (NFS Data unpublished). In most developing countries of Africa and Asia, the fertilizers are given to farmers at a subsidized price to sustain the farmers. Subsidies are a high financial burden to a country (United Nations Population Fund forecast 2015). Currently, there are no subsidy programs being implemented in developed countries (http:// www.oecd.org/tad/agricultural-policies/support-policies-fertilisers-biofuels.htm). Fifty percent of the global fertilizer produced is utilized by three major crops, namely rice, wheat, and maize, out of which rice utilizes about 14–16% of the total fertilizer production (Heffer 2013). International fertilizer association statistics show that out of aggregated fertilizers consumed globally, 54% is subsidized. In a study carried out in five Asian countries and four African countries (IFDC/ FAI report, 2017), the burden on the government by the fertilizer subsidy programs in agriculture are tabulated in Table 7.1. In most of the countries, a large portion of the total government expenditure for agriculture is spent on fertilizer subsidies. The status of the impact of subsidies, whether it is negative or positive, is controversial and is always masked because it is an extremely sensitive issue involving farmer lives.

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DTN Average Retail Urea Prices 800.00

Week Ending 09/28/18

750.00 700.00 650.00

$/ton

600.00 550.00 500.00 450.00 400.00

2/19/16 6/19/16 10/19/16 2/19/17 6/19/17 10/19/17 2/19/18 6/19/18

300.00

2/19/10 6/19/10 10/19/10 2/19/11 6/19/11 10/19/11 2/19/12 6/19/12 10/19/12 2/19/13 6/19/13 10/19/13 2/19/14 6/19/14 10/19/14 2/19/15 6/19/15 10/19/15

350.00

Week Ending

Fig. 7.3 Urea fertilizer price fluctuation over the years. (Source: www.dtnpf.com/agriculture/web/ ag/crops/article/2018/10/03/fertilizer-prices-continue-move)

Fig. 7.4 Total import of three major fertilizers for Paddy in Sri Lanka from 2010 to 2015 (Source: National Fertilizer Secretariat of Sri Lanka, Data unpublished)

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Table 7.1 Comparison of Fertilizer subsidy expenditure (IFDC/FAI report, 2017) Country Bangladesh China India Indonesia Pakistan Nigeria Malawi Rwanda Tanzania Total

7.1.2.2

Total Gov. exp. (as % of GDP) 9.80 22.57 14.30 15.00 17.60 6.00 15.00 15.00 16.60 12.59

Total Gov. exp. (U.S. $ M) 12,607 1,691,042 262,521 133,945 37,621 24,705 844 961 5624 2,169,870

Fertilizer subsidy (U.S. $ M) 1498 21,810 14,610 1520 506 409 148 10 64 40,575

Subsidy as % of total Gov. exp. 11.9 1.3 5.6 1.1 1.3 1.7 17.5 1.0 1.1 1.87

Human Health and Environmental Problems of the Usage of Nitrogen Fertilizers

Impacts of urea fertilization of rice systems on the environment and human health are of major concern. This is basically due to the harmful consequences resulting from the low urea fertilizer efficiencies (30–40%) in rice systems. In most nitrogen fertilizers, two different forms of nitrogen are available, Nitrate-N (NO3
) and Ammonium-N (NH4+). The uptake of NO3
is higher because of its high particle mobility, and also because it is directly taken up by the plants. Ammonium-N is preferred over nitrates because unlike NH4+, NO3
is not held up by the soils (PEI Analytical Laboratories, 2014). NH4+ is retained by the soil particles and converted later into NO3
hence the losses are reduced. Urea fertilizers [NH2CONH2/CO (NH2)2] are much preferred because of its high N content (45–60%), relatively low cost, and rapid conversion to available N (Cornell University Fact sheet 44, 2009). The fate of added urea fertilizers in wetland rice cultivation and its consequences on the health and the environment is illustrated in Fig. 7.5. Being a semi aquatic grass, rice is mainly grown in flooded conditions where nitrogen is preferably taken up by the rice plant as NH4+. According to Kennedy (1992), the reason is the requirement of less energy needed in assimilating NH4+ to amino acids rather than NO3
. When urea is added to the flooded rice systems, catalytic hydrolysis with urease enzyme (Freney et al. 1994) takes place and urea is decomposed into ammonium carbonate leading to the formation of NH4+ ions (De Datta 1981), which consequently increases the concentration of NH4+ ions in the flood water of the rice system (Freney et al. 1994). Nitrifying bacteria, through nitrification converts, NH4+ into NO3
(De Datta 1981). NH4+ binds only lightly to water molecules. This leads to NH3 (non-ionized) formation and its escape from the system through volatilization (De Datta 1986; Xing and Zhu 2000). The pH, temperature of the floodwater, algal growth, crop growth, and soil properties affect the rate of ammonia volatilization (De Datta 1987). When urea is added by

Fig. 7.5 Fate of urea on a paddy field and consequences on the environment and health

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broadcasting, NH3 losses are extremely higher than deep placement in the soil (De Datta 1986). In flooded soils, ammonia volatilization is moderately high if the soil is acidic, and if alkalinity is extremely high (De Datta 1978). In the wetland rice systems, the growing algae absorb CO2 for their photosynthesis leading to the increase in the floodwater pH, followed by increased ammonia volatilization (Broadbent 1978; Freney et al. 1994). Therefore, the percentage of NH3 volatilization could go up to a 60% loss of the added fertilizer (De Datta 1986; Xing and Zhu 2000). Soil particles are negatively charged and the positively charged NH4+ ions bind tightly to clay particles unlike water. In comparison with positively charged NH4+, negatively charged nitric ions NO3
leach or percolate much faster contaminating the groundwaters, and making it toxic for consumption (Marko et al. 2002; Shrestha and Ladah 2002). When this water is used for agriculture, the percolated nitrates can enter the food chains again and if consumed can cause a number of health problems (Shrestha and Ladah 2002). Vitamin A reductions in the liver, methemoglobinemia in infants, and respiratory illness are some of the resulting lethal aftereffects (Bohlool et al. 1992; Phupaibul et al. 2002) of such a contamination. Water containing more than 10 mg/L of NO3
is not safe to be used by people. Carcinogenic compounds such as nitrosamines are formed with nitrate and nitrites and these nitrosamines contribute to gastric cancer (Phupaibul et al. 2002). Following nitrification (NH4+ is converted into NO2
and NO3
), a series of reactions are involved in the denitrification process as given below. NO3
! NO2
! HNO ! NO
! N2O and finally N2O converted in to N2 Nitric oxide (NO), nitrous oxide (N2O), and nitrogen (N2) gases are released into the atmosphere (Reddy and Patrick Jr 1986) hence the added fertilizer nitrogen is lost to the atmosphere. Nitric oxide and ammonia contribute heavily to ill effects in ecosystems leading to acidification, eutrophication, effects on species diversity, and triggering problems in predator parasite relationships (Reeves et al. 2002; Vitousek et al. 1997). Eutrophication is followed by harmful consequences such as excessive algal growth, reduction of oxygen at the bottom of water bodies, and water clarity reductions (Keeney 1982). During the oxidation process of soil organic matter in the wetland rice soils, when the soil is devoid of oxygen, facultative anaerobes use NO3
as an electron acceptor, and this is identified as the primary cause of denitrification (Kennedy 1992). In continuously flooded rice cropped system, 5–10% is lost through denitrification in the fallow period, which could go up to 40% (Fillery and Vlek 1982). Buresh and De Datta (1990) have stated that this denitrification loss could even increase up to 46%. With nitric oxide emitted during denitrification, tropospheric ozone, which is a major atmospheric pollutant which harms human health, agriculture, and natural ecosystems is formed (Chameides et al. 1994; Matson et al. 1998). Tropospheric ozone is a precursor in the formation of nitric acid, a major contributor to acid rains (Kennedy 1992). Nitric oxide also contributes

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to global warming by absorbing the infrared (IR) radiation (Bohlool et al. 1992). One of the other hazardous components produced in the denitrification which contributes to global warming is nitrous oxide. Its effect on global warming is 300 times higher than CO2 (Baggs et al. 2002; Xing 1998) and is known to disrupt the ozone layer (Bohlool et al. 1992).

7.1.2.3

Impacts of Using Phosphorous and Potassium Fertilizers

The phosphates are mined from rock phosphates, which is a nonrenewable energy resource. But it is the primary source of phosphates with 80% of mined rock phosphates being used for agriculture (Smit et al. 2009). Overexploitation of phosphate rocks has become a major concern as it is nonrenewable. In 2008, rock phosphate prices boomed by 800% in the market. Although it decreased after a while, phosphate fertilizer processes remain expensive. The countries that depend on importing phosphates face major challenges due to its constant price fluctuations. Some rock phosphates are contaminated with lower levels of radionuclides of uranium and thorium. Once these phosphates are added to agricultural lands, the soils too can become radioactive over the years (Cordell et al. 2009). Some rock phosphates contain small amounts of the heavy metal Cadmium (Cd). When the P fertilizers made from these are added to agricultural soils, Cd can get accumulated in the agricultural soils, with the possibility of it entering humans and animals through food webs. In western countries, 54–58% of Cd in the environment comes from the application of mineral fertilizer. TSP can also be contaminated with the heavy metal arsenic. Arsenic is a toxic heavy metal that is suspected to be responsible for lethal kidney diseases (Jayasumana et al. 2015). A study done by Jayasumana et al. (2015) in Sri Lanka reports that out of 226 samples of P fertilizer tested for arsenic contaminants, all were contaminated with arsenic. TSP fertilizer had a mean of 31 mg/kg. Out of the phosphate fertilizers that are added to the agricultural systems, only a small portion is taken up by the plant immediately. Plants absorb less than 20% of the applied P fertilizer most of the time (Friesen et al. 1997) with the rest being stored in soils. Farmers therefore add excess amounts of phosphate fertilizers to provide the required amounts to plants. These excess phosphates run-off from the systems through leaching and soil erosion and the excess fertilizers end up in lakes and other water bodies and massively contaminating the water bodies exceeding their tolerance levels (Carpenter and Bennett 2011). To reduce the problems related to phosphates that are associated with the agricultural fields and to recover and recycle the broken P cycle, the phosphate that are fixed in the agricultural lands should be recovered and reused (Tirado and Allsopp 2012). But in many rice cultivated soils, P does not become the yield-limiting factor (Singh and Singh 2017). Potassium (K) fertilization has become a requirement with intensive agriculture. Overfertilization with K fertilizer leads to the leaching of the remaining fertilizers to below-ground levels. Potassium is present in higher amounts in the rice leaves.

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When the rice straw is added back into the field, most of the potassium is returned back to the system and the balance is thus kept (Singh and Singh 2017).

7.2

Conventional Microbial Interventions to Reduce the Fertilizer Usage in Rice Cultivation

Despite the negative impact associated with the use of inorganic fertilizers, they are being used on a daily basis by the farmers to obtain the required rice yields. Scientists point out the prompt need of an alternative to reduce the use of inorganic fertilizers before it destroys the soil and the bio-geocycles completely. The utilization of soil microbial communities to reduce the inorganic fertilizer usage through nitrogen fixation, phosphate solubilization, or through acting as a plant growth promoting rhizobacteria (PGPR) is highly discussed and researched. Use of microbial communities will have minimal negative impacts on the soil and the environment. The challenge is to discover biofertilizers or microbial inoculants that are sustainable with the ability to reduce inorganic fertilizer inputs and provide the targeted rice yields. Until recently (25 years), bacteria were considered strictly to be unicellular organisms. They were considered to be living alone, dividing by binary fission and feeding independently (Claessen et al. 2014). But bacteria do not live alone as a pure culture. Instead, they prefer a multicellular life (Flemming and Wingender 2010). James Shapiro’s paper on “Bacteria as a multicellular organism” was a turning point in the study of microorganisms (Shapiro 1988).

7.2.1

Characteristics and Multicellular Life of a Bacterium

A particular bacterium spends at-least a part of its life as a complex community. Some bacteria always prefer to live in a multicellular complex and sometimes the change from a single cell to multi-cells is permanent (Claessen et al. 2014). Bacteria forms polymicrobial aggregations at various interfaces and they could be in the forms of mats, sludges, biofilms, etc. (Flemming and Wingender 2010). Konopka defines microbial communities as, “multi species assemblages, in which organisms live together in a contiguous environment and interact with each other” (Konopka 2009). In the transition from unicellular organism to a multicellular organism, the key step is the increase in size (Bonner 1998). Bonner (1998) has stated that the origin of multicellularity could be due to a mutation that has stopped the daughter cell from complete division and thus increase in cell size.

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201

Stages of Becoming a Multicellular Organism

There are basic stages of multicellularity. The basic forms of multicellularity are formed through aggregation of individual cells, chains of cells resulting through incomplete fission after cell division, (clustered growth) or syncytial filaments formed by arrested cell division leading to syncytial cells (Claessen et al. 2014). These basic forms can then form into biofilms showing short-term multicellularity, permanent multicellularity, and finally to the forms with irreversible differentiations, division of labor among different cell types, and intercellular cooperation, and this is referred to as complex multicellularity (Claessen et al. 2014).

7.2.1.2

Negative Impacts of Being Multicellular

There are several negative impacts that a cell or a cell cluster can be subjected to by being multicellular. The transition from a unicellular organism to a multicellular organism increases the cell density which leads to increased competition between the cells for available resources. Decreased buoyancy in an aquatic environment and impaired cell motility is considered as other negative impacts that are associated with being multicellular (Bonner 1998). However, frequently, the bacterial cells prefer a multicellular lifestyle because the disadvantages are overruled by the gained advantages which are discussed in detail in the section below.

7.2.1.3

Advantages of Multicellularity

In 2007, Grosberg and Straterthen have clearly stated the advantages an organism gains by being multicellular. The advantages are gained through the increase in size, by the division of labor, metabolic cooperation, and motility mitosis trade-off. Size is one of the major factors that promotes multicellularity. Unicellular organisms are prone to be consumed by phagotrophic organisms (Stanley 1973) and one of the easiest ways of survival is by increment of the cell size by adhesion to other organisms (Grosberg and Strathmann 2007). Division of labor among different cells give the unicells the advantages that are usually present in the multicellular organisms. Unicellular organisms are capable of differentiation into different phenotypes in the presence of an environmental change, but they can divide labor only in time, whereas the multicellular organisms can divide complementary tasks among various cells and this will ultimately lead to increased specialization of tasks among different cells in the same multicellular grouping. Being multicellular could enhance the fitness of the entire population (Pfeiffer and Bonhoeffer 2003). Metabolic cooperation is another advantage gained by being multicellular. Certain microbial processes are impossible to be carried out simultaneously in a single cell. For example, photosynthesis and nitrogen fixation cannot take place in unicellular cyanobacteria and is not possible because the oxygen produced by

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photosynthesis is toxic to the major enzyme involved in nitrogen fixation by the bacterium (Kaiser 2001). Hence, the unicellular bacteria either choose only photosynthesis or fix nitrogen in the absence of photosynthesis. Some filamentous multicellular cyanobacteria have overcome this by the production of heterocyst with thick walls which are less permeable for oxygen than photosynthetic cells, and hence can effectively fix nitrogen (Kaiser 2001). Motility mitosis trade-off is another advantage gained by being multicellular. Certain large spherical colonies contain two types of cells; internal germ cells, without flagella (which can give rise to new colonies) and external cells which cover (suspend) the colony with flagella (somatic cells) (Kirk 1997), and which cannot divide or have a limited ability to divide. This type of germ and somatic cell differentiation is seen in the order Volvocales, the flagellated forms of green algae (Kirk 1997). Some green algae can divide and swim at the same time but in contrast in the Volvocaceans, the flagella are fixed to the cell wall bodies and mitosis cannot occur while still attached to the flagella. The non-motile, germ line cells in the middle does the division while the flagella are still moving. This germ cells and somatic cell differentiation increases the nutrient uptake and overall well-being of the cells.

7.2.2

Biofilms

7.2.2.1

Introduction to Biofilms

Majority of bacterial life in nature is present as surface-bound communities and are called biofilms (Costerton et al. 1995; Kolter and Greenberg 2006). As set out by Madsen et al. “A biofilm is a gathering of bacterial cells enclosed in a self-produced polymeric matrix composed of extracellular polymeric substances (EPS), mainly exopolysaccharides, proteins and nucleic acids. Bacterial biofilms may adhere to an inert or living surface or exist as free-floating communities” (Madsen et al. 2012). The characteristic feature of a biofilm is the organization of the cells in the biofilm into a matrix enclosed structure (Madsen et al. 2012). Cells that are engaged in biofilm formation differ phenotypically and physiologically from the planktonic cells of the same kind. For example, the cells in a biofilm are densely packed and various secretions that are secreted from the cells and enzymes and extracellular polymers are shared among each other (Xavier and Foster 2007). Phenotype and the horizontal gene transfer in a planktonic cell are different from that of a biofilm. Being a biofilm increases antibiotic tolerance and immune responses. Biofilm is an excellent platform for microbial interactions because of the increased density of the microbes, the physical contact between them, and the matrix inclusive of many molecules. Most biofilms in the environment are multispecies (Madsen et al. 2012). These biofilm cells are sessile and one major observation in clinical trials is that higher dose of antibiotics (ten to thousand times stronger concentration than the

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minimum inhibitory concentration) are required to kill the microorganisms in a biofilm than the same in the planktonic form (Stewart and Costerton 2001). Molecular studies on biofilm formation are still not fully understood (Monds and O’Toole 2009). Differentiation from the planktonic state to biofilm state change gives an entirely different lifestyle for microbes. The EPS, which provides extensive benefits to the biofilms, is sometimes referred to as the dark matter of the biofilms because of the presence of a large range of matrix biopolymers which are very difficult to analyze (Xavier and Foster 2007).

7.2.2.2

Biofilm Matrix

Ninety percent of the mass of the biofilm is comprised of the extracellular matrix (ECM) while only 10% is microbes. Microbial cells are embedded in the matrix. The matrix contains various biopolymers, termed as extracellular polymeric substances (EPS) which makes the scaffolding for 3D architecture of biofilms and helps biofilms to adhere/attach to surfaces and enhances cohesion between microbes (Flemming and Wingender 2010). Cooperation and selflessness are main requirement of cells participating in biofilm formation (Kreft 2004). Some strains use resources but they do not contribute to the well-being of the biofilm and are termed cheaters (West et al. 2006; Griffin et al. 2004). Flemming and Wingender (2010) have extensively explained how biofilms are triggered by the ECM. Stabilization of the biofilm matrix can be increased if the bacteria present in a biofilm contains external structures such as pili, flagella, and fimbriae (Zogaj et al. 2001). Biofilm matrices can retain high amounts of water around the organisms in the biofilms, leading to the possible desiccation tolerance by the biofilm (Flemming and Wingender 2010). The matrix sometimes acts as a nutrient reserve, containing C, N, and P containing compounds. Facilitation of the horizontal gene transfer among the organisms in the biofilm, providing a niche for redox activities, providing protection against charged metallic ions, antibiotics, protection from ultraviolet radiation, acting as a protective barrier to resist infections, antibiotics, and disinfectants, sorption of organic compounds (from outside), xenobiotics, and inorganic ions are some of the important facilitations of the biofilm matrix (Flemming and Wingender 2010). Also, the ECM is highly involved in the digestion of external macromolecules which results in nutrients and also sometimes the digestion of the structural EPS which leads to the release of cells from the biofilm (Flemming and Wingender 2010). Life inside a biofilm depends on the concentration, cohesion, 3D architecture of the matrix, and the charge sorption capacity. Biofilm morphologies can be of different types, smooth, flat, fluffy, etc. The main target of all these morphologies are to immobilize cells and maintenance of long-term micro consortia which interact with each other and are highly diverse. Although EPS are considered to be mainly produced by bacteria, fungi can also produce EPS. Other than bacteria and fungi

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microalgae and green algae are also known to produce EPS (Flemming and Wingender 2010).

7.2.2.3

Stages of Biofilm Formation

There are several stages in forming a biofilm. First cells adhere onto a surface in a reversible attachment. Then the attached cells start producing the extracellular matrix containing several substances, such as extracellular polysaccharides, lipids, nucleic acid, etc. These produce lead to a solid attachment of cells onto the surface (Stoodley et al. 2002; Bjarnsholt et al. 2013). Coordination of group activities of the transition to a biofilm from a single cell is essential for proper transition in form and function (Monds and O’Toole 2009), and the genetic pathways have evolved to facilitate the need. O’Toole et al. (2000) and Monds and O’Toole (2009) describe that the biofilm formation is very similar to the bacterium Myxococcus xanthus fruiting body formation. In the presence of high nutrient concentrations, M. xanthus stays in the vegetative state and keeps dividing actively. If a nutrient limiting condition arises, the vegetative growth of M. xanthus is stopped and it starts to form aggregates ending up with multicellular fruiting body structures. The center cells of the fruiting body stay as myxospores and are stable. If nutrient conditions are suitable these can transfer back to the vegetative cells that are actively dividing. The peripheral cells stay undifferentiated. The biofilm formation exhibits many similarities to M. xanthus fruiting body formation, having its own bacterial genetic pathway dedicated to regulation of biofilm formation. This contradicts the initial thought of biofilm formation as a process depending on the external physical and chemical properties and the composition of the bacterial cell surface. Biofilm formation is governed by bacterial genetic pathway dedicated to its regulation and is an active microbial process with genetic pathways working towards formation of the biofilm (O’Toole et al. 2000; Monds and O’Toole 2009).

7.2.2.4

Advantages of Living in a Biofilm

According to Flemming and Wingender (2010), there are a number of advantages given to a biofilm by the EPS. Biofilms can tolerate harsh conditions and they ensure their survival in unfavorable conditions. Van acker et al. (2014) describe three major mechanisms that are being used by the biofilm for stress resistance; (1) biofilmspecific protection against oxidative stress; (2) biofilm-specific expression of efflux pumps; and (3) protection provided by matrix polysaccharides. The authors also show that the mechanisms of the above stress resistances are similar in bacterial and fungal biofilms even though bacteria and fungi are not closely related. Lethal doses of microbial antibiotics most of the time lead to the formation of highly deleterious reactive oxygen species (ROS) (Van Acker et al. 2014) inside the cell and leads to cell death (Dwyer et al. 2009). When a bacterium is involved in a biofilm the antibiotic tolerance increases up to 10–1000 times (Jefferson et al. 2005).

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It was observed that certain antibiotics, for example, Ceftazidime or Piperacillin are required in higher concentrations to induce ROS production on Pseudomonas aeruginosa biofilms in comparison to planktonic cells (Battán et al. 2004). Also, it has been found that, ciprofloxacin is incapable of ROS production in Proteus mirabilis biofilm even though the antibiotic is capable of inducing ROS formation in planktonic cultures. The levels of superoxide dismutase (SOD) and glutathione levels were observed to increase in biofilm (Aiassa et al. 2010). Through Experiments with Candida albicans, (opportunistic human pathogen) it was observed that C. albicans biofilms tolerate antifungal activity through highly tolerant persister cells (LaFleur et al. 2006). The persister cells are not killed by certain antimicrobial agents and are called as specialized survivor cells (Lewis 2007). A small number of persister cells that are extremely tolerant can be present in a biofilm (Stewart and Costerton 2001) and are considered responsible for biofilm resilience (Van Acker et al. 2014). The avoidance of the exposure to antibiotic-induced ROS is the main mechanism of survival in persister cells and is confirmed by the evidence from tobramycintreated Burkholderia cenocepacia biofilms (Van Acker et al. 2014). An experiment on treatment of B. cenocepacia biofilms with the antibiotic tobramycin revealed that in 99.9% of cells ROS levels increased and the cells senesced, while the remaining 0.1% survived. When the gene expression profiles were compared it was revealed that in the 0.1% that survived, persister cells downregulate the TCA cycle to avoid production of ROS (Van Acker et al. 2014). Gillis et al. (2005) have stated a biofilmspecific defense mechanism through a mexCD Opr-J efflux pump by Pseudomonas aeruginosa biofilms against Azithromycin. Another important method of defense is the protection provided by the biofilm matrix. If a biofilm encounters an antimicrobial agent, due to the presence of the ECM, the penetration of the antimicrobial agent becomes slow. When planktonic cells are mixed with an antibiotic all the cells are exposed to the full dose. When the organism is exposed to a lower concentration of the antibiotic first and the concentration increases gradually, they may have time to elucidate defense responses (Jefferson et al. 2005). Another supportive process is the higher rate of horizontal gene transfer occurring in the cells of a biofilm. By this method, the antibiotic or other genes conferring resistance can be transferred between the members of the group leading to increased tolerance (Madsen et al. 2012). A classic example of a strategy of a biofilm survival in the nutrient-limited environment is explained by Wilking et al. (2013). When the nutrients are limited, the bacterium Bacillus subtilis like many other bacteria enter into a resting stage, the endospore. In Bacillus subtilis biofilms, cells that initiate sporulation produce killing factors and signaling molecules, that together block sister cell sporulation and leads them to lyse (programed cell death (PCD)). This allows remaining cells to obtain the nutrients that are released by the lysed sister cells. The sporulating cells keep on growing without completing the morphogenesis and continue the resting stage until the nutrients are sufficiently available (Gonzalez-Pastor et al. 2003; Vlamakis et al. 2013).

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When biofilms grow bigger, differentiation of cells coordinated with division of labor shows very complex multicellular behavior and show similarities to plants, animals, and fungi. Also, the growth depends on acquisition of nutrients and removal of waste, where diffusion is the main source of transport. In the case of B. subtilis, diffusion becomes insufficient when the biofilm grows bigger. To fulfill the needs of the biofilm, a very well-defined remarkable network of channels showing similarities to circulatory system to transport waste and nutrients for distances is present in this enlarged biofilm (Wilking et al. 2013).

7.2.2.5

Bacterial–Fungal Biofilms

Bacteria and fungi are known to coexist and interact and these interactions have given benefits to both the organisms. Bacteria and fungi form unique associations which are physically and metabolically independent and are different from single components (Tarkka et al. 2009). These bacterial and fungal interactions benefit a diverse array of areas in biotechnology, food processing, ecology and environmental protection, plant and animal pathology, plant and animal nutrient, etc. (Frey-Klett et al. 2011). The associations of bacteria and fungi could range from simple polymicrobial association to a highly symbiotic association (Frey-Klett et al. 2011). Of these, symbiotic associations are the most intimate. These symbiotic associations could be ectosymbiotic relationship where bacteria reside external to the fungal cell membrane or endosymbiotic relationship where the bacteria live inside the fungal cell membrane. In this association both the organisms can be present as mixed complexes or mixed fungi providing support for bacteria to reside (Hogan and Kolter 2002; Seneviratne et al. 2008). Perera et al. (2017) report evidence for a successful colonization of the filaments and sporangia of the fungi Aspergillus spp. by the diazotroph Azorhizobium caulinodans ORS 571, resulting in an Azorhizobium caulinodans—Aspergillus spp. biofilm (AAB). The Green Fluorescent Protein labeled (GFP) Azorhizobia (Perera and Tirimanne 2017) colonized the fungi after 2 days (Fig. 7.6a) of coming in contact with each other. After 3 days the fungal filaments were seen to be completely covered with the bacteria (Fig. 7.6b–d), forming the biofilm (Perera et al. 2017). It is reported that the fungal mycelia of fungal–bacterial biofilms link to the root hairs and therefore help to maintain higher cell densities in contrast to biofilms with only bacteria. Adhesion of the organisms to the surface is an important phenomenon and depending on the physiological status and cellular development specificity can be found. For example, in the biofilms made between the fungus Candida albicans and the bacterium Pseudomonas aeruginosa, Pseudomonas aeruginosa is able to colonize the hyphal form.

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Fig. 7.6 Epifluorescent micrographs showing formation of a biofilm. (a) A 2 days old biofilm: a fungal filament (double arrows) surrounded by bacteria A. caulinodans migrating towards the fungal filament (single arrow) (40), (b) and (c) a 3 days old biofilm (fungal filaments completely surrounded by bacteria) (40), (b) under epifluorescent microscope (fungal filaments cannot be seen because they are completely surrounded by bacteria), (c) under light microscope, (fungal filament—double arrows, bacterial cloud—single arrow), and (d) 3 days old fungal filaments and fungi vesicles (double arrows) surrounded by fluorescing bacteria (single arrow) (40). (Extracted from Perera et al. 2017)

7.2.2.5.1

Interactions and Communication Inside a Bacterial–Fungal Biofilm

The molecular dialog between a bacterium and a fungi occurs via several methods. Antibiosis is the best known and extensively studied method (Frey-Klett et al. 2011). In a bacterial–fungal biofilm, harmful and complex chemical compounds can be diffused among one partner to another and is termed antibiosis (Frey-Klett et al. 2011). The concept of antibiosis was used when the antibiotics were developed. Another method of fungal–bacterial communication is via chemotaxis and cellular contacts. Diffusible molecules are extremely important in bacterial–fungal communication as well as chemotaxis. Chemotaxis is defined by Grewal and Rainey (1991) as “the ability of a motile cell to respond to changes in its chemical environment by altering its pattern of motility. This is a common attribute of many bacteria.” It is an important method for bacteria to locate nutrients and avoid harmful environments (Chet and Mitchell 1976). However, this could be beneficial or

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harmful since both beneficial and harmful species of bacteria could taxis towards the fungus, e.g., taxis of both harmful and beneficial Pseudomonas spp. towards fungi (Grewal and Rainey 1991; Deveau et al. 2010). Bacterial and fungal interactions result in important changes in their physiology. An example of one such type of interaction is the phenomenon of trophic interactions, for example, the competition between bacteria and fungi for carbon resources in the process of decomposing (Møller et al. 1999). Also, if one partner is incapable of producing certain substances or specific compounds they can use the produce of the other partner for their benefits. There are a number of ways from which bacteria get benefitted from the colonization with fungal filaments. One being the possibility of bacterial exploitation of the fungal filament for nutrients (Hogan and Kolter 2002). Bacteria may take nutrients from the fungal cell walls, consume fungal secreted products, and through lysis of the fungal cell the internal components could also be consumed (Hogan et al. 2009). If bacteria and fungi are in a competition for food when they are in a biofilm, bacteria can secrete antifungal compounds that are antagonistic to fungal growth. When bacteria colonize on the fungal surface the bacterium can move along the fungal filament into areas where nutrients are in excess. Sometimes, both the organisms can interact synergistically to breakdown complex substrates. Also, this bacterial and fungal interaction can be an endosymbiotic interaction which is crucial for the rhizosphere function (Dörr et al. 1998). Bacteria and fungi can cooperate to achieve novel catabolic reactions. One such example is the biodegradation of high molecular weight polycyclic hydrocarbons (Boonchan et al. 2000). Bacteria can sometimes destroy self-inhibitory molecules produced by the fungi and thereby act as fungi growth promoting organisms, for example, the ectomycorrrhizal fungi Paxillus involutus secretes phenolic compounds that are toxic to itself but are metabolized by soil bacteria (Duponnois and Garbaye 1990). Certain bacteria can stimulate the growth of certain Basidiomes, for example, growth promotion of Agaricus bisporus by the bacterium Pseudomonas putida (Rainey 1991). In bacterial–fungal biofilms, either one could benefit from toxins produced by the other. The phytopathogenic fungi Rhizopus spp. is responsible for causing rice seedling blight. The disease starts with abnormal swelling in the rice seedling roots in which the fungus is not detected. The initiation of the disease is caused by Rhizoxin, a toxin that has been produced not by the fungi but by the bacteria Burkholderia rhizoxinica and Burkholderia endofungorum that live within the fungus (Partida-Martinez and Hertweck 2005).

7.2.2.5.2

Consequences of Bacterial–Fungal Interactions for Participating Organisms

In bacterial–fungal interactions, the extracellular bacterium can either positively or negatively affect the fungal development or spore production. Chandelier et al. (2006) describes the induction of the spore germination of the plant pathogenic fungi, Phytophthora alni where fungal pathogenicity is influenced when the fungi is in association with a bacterium. Also, in some instances, the fungi promote

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differences in bacterial development since the bacteria is in a new ecological niche in a biofilm compared to free-living organisms. In this niche, bacteria gain physiological differences such as antibiotic stress resistance and the expression of virulent genes in comparison to free-living organisms. De Boer et al. (2004) explains in his study with bacterial strains and pathogenic fungi that pathogenic fungal growth is suppressed when the bacteria are inoculated as a mixture. He further suggests that when bacteria cohabitate, it triggers antibiotic production via interspecific interactions. Growth reduction of fungi could be a side effect caused by the sensitivity of the fungi to secondary metabolites (De Boer et al. 2004). In certain instances, the fungal hyphae act as vectors of transporting bacteria. Kohlmeier et al. (2005) state that certain pollutant degrading bacteria which reside on fungal hyphae use fungal hyphae for their movement.

7.3

7.3.1

Microbial Communities (Biofilms) and Their Contribution Towards the Increase of Rice Plant Growth and Yield Rice Plant Rhizosphere

Rice is commonly cultivated in flooded soils. The rice plant rhizosphere is a unique environment which contains oxic and anoxic zones, and hence facilitates the presence of a diverse array of microbes which include aerobes, anaerobes, facultative aerobes, etc. (Brune et al. 2000). A study done on Italian rice fields using quantitative PCR and 16SrRNA pyro tag analysis revealed that the rice rhizosphere contains twice as much 16S rRNA genes compared with the bulk soil, supplying evidence for the microbial abundance in the rice fields (Breidenbach et al. 2016). These microbes, especially the rhizosphere bacteria are highly dependent on their association with the plants (Panizzon et al. 2016). Jones et al. (2009) have reported that about 17% of the photosynthate from the plants is released into the rhizosphere environment making the rhizosphere a nutrient-rich environment. The microorganisms living in this nutrient-rich rhizosphere, help plant growth through the production of phytohormones, phosphate solubilization, production of iron chelators, releasing antipathogenic metabolites, and competition for nutrients (Araújo and Costa 2007).

7.3.2

Sustainable Rice Cultivation and Biofilms

Biofilms are considered as biofertilizers with a substantial amount of benefits on plant growth and yield. The benefits are far greater than the application of conventional microbial monocultures or the application of fertilizers, in various perspectives as discussed above. Vessey (2003) defines a biofertilizer as “A substance which

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Fig. 7.7 AAB colonization of the rice plant roots after the treatment 2 (AAB + Naringenin). A region of root under high power (40). Regions of biofilm colonization are indicated by a single arrow; the double arrows indicate the root. (Extracted from Perera et al. 2017)

contains living microorganisms which, when applied to seed, plant surfaces, or soil, colonizes the rhizosphere or the interior of the plant and promotes growth by increasing the supply or availability of primary nutrients to the host plant.” Density of naturally occurring biofilms in soil is very low and is not enough to improve productivity, and hence biofilms developed in-vitro have to be added as inocula to improve plant growth (Seneviratne and Jayasinghearachchi 2003). When a fungal–rhizobial biofilm or a fungal–bacterial biofilm is added to a growing medium of a plant, several beneficial effects are provided to the increment of the growth and yields of the plant (Seneviratne et al. 2009). Perera et al. (2017) have experimented on effective strategies for induced colonization of rice roots with the diazotroph Azorhizobium caulinodans. A. cauliodans possesses unique characteristics such as the ability to tolerate up to 3% v/v oxygen (Kitts and Ludwig 1994) and non-symbiotic nitrogen fixation. These characteristics are of extreme importance in non-symbiotic nitrogen fixation. The successful biofilm prepared between A. caulinodans and Aspergillus spp. (Azorhizobial-Aspergillus spp. biofilm (AAB)) (Perera et al. 2017) as discussed above has been tested for its ability to colonize rice plant roots (Perera et al. 2017). It was shown that the GFP-labeled AAB successfully colonize the rice plant roots as observed through epifluorescent microscopy (Fig. 7.7). It was also reported that the flavonoid naringenin has enhanced colonization of AAB significantly (Table 7.2) (Perera et al. 2017). Table 7.2 indicates the significantly higher mean fluorescence intensities in the treatment AAB + Naringenin in comparison to the Treatment 1, Naringenin + A. caulinodans, Treatment 2, Biofilm (AAB), and Treatment 4, Control (only A. caulinodans). Significantly higher Acetylene Reduction Assay values and endophytic colonization values have been also obtained for the same AAB + Naringenin treatment (Perera et al. 2017). This clearly indicates that AAB + Naringenin together act as an extremely successful entity in rice root colonization and possibly carries out

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Table 7.2 Combined effect of the biofilm (AAB) and naringenin on colonization of rice roots, number of endophytes, and nitrogenase activity of rice variety BG 366 (Extracted from Perera et al. 2017)

Treatment Naringenin + A. caulinodans Biofilm (AAB) AAB + Naringenin Control (only A. caulinodans)

Mean fluorescence intensities [a.u] 202 b

No of endophytes per gram fresh weight 1.46  105

ARA values (nmol C2H4/h/ g dry wt) 551

205 b 221 a 178 c

Nil 9.48  105 4.25  104

709 1174 393

Means of fluorescence intensities followed by different letters of the alphabet within a column differ significantly by Duncan’s multiple range test ( p < 0.05). Number of endophytes and ARA values indicate average of three replicates

nitrogen fixing in rice. Flavonoid naringenin is a nod gene inducer and a signaling molecule for Azorhizobium caulinodans (Novák et al. 2002; Gough et al. 1997; Dénarié et al. 1992). Perera et al. (Unpublished data) have also researched the possibility of replacing inorganic nitrogen fertilizers for rice with the developed AAB + Naringenin combination through pot and field trials. The observations have revealed that it is possible to replace 50% of recommended urea fertilizers with this AAB + Naringenin combination, without affecting the growth or the yield of the rice plant. 15N isotopic analysis data has revealed that the rice plants treated with AAB + Naringenin combination have received 67.33% of total nitrogen from the atmosphere, showing the effectiveness of the microbial combination (Perera et al. Unpublished). To increase the growth and yield of a plant, biofilms contribute in numerous ways. Competition suppression, increase of available oxygen in the fields, action of the biofilms as plant growth promoting rhizobacteria, pest and disease control are some major methods and are described in detail below.

7.3.2.1

Competition Suppression

When conventional microbial inocula are used as biofertilizers, the survival rate of the microbes is very low due to various environmental stress factors (Seneviratne et al. 2008). Mixed inocula with arbuscular mycorrhiza and rhizobia had been effective in improving plant growth, nutrient uptake, and abundance of the microsymbionts in experiments done with the plant alfalfa (Medicargo sativa) (Biró et al. 2000). In the same experiment, the mycorrhizal inoculum alone had a drastic reduction of its function due to the competition by the soil native population (Biró et al. 2000). The competition that the inoculant microbes has to face with well adopted native microflora in soil is the main threat to the microbial survival (Bohlool et al. 1992). Abiotic stress factors like temperature, drought, and acidity also

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influence the failure of survival of a microbial inoculant (Graham 1992). Hence, when microbial inoculants are added to the soil, their impact on a plant depends on the other microorganisms present in the rhizosphere. A biofilm can reduce the effect of competition by the native flora to a greater extent as it has its own survival mechanisms mainly due to the extracellular matrix (Seneviratne and Jayasinghearachchi 2005).

7.3.2.2

Increased Oxygen Availability and Active Supply of Nitrogen to Rice Roots

Rice fields contain several unique characteristics that are suitable for the growth of the microorganisms (Roger et al. 1993). The rice soil is anaerobic most of the time because it is submerged. But the rice plant rhizosphere could be aerobic to micro aerobic. The reason is the movement of air to the roots from the shoots of the rice plant. The rice plant has the ability to transport oxygen from the stem to the root. Oxygen is then diffused to the adjacent soil layers (Roger et al. 1993). Since the rice roots are present in large volumes, a larger portion of the rhizosphere is aerobic (Roger et al. 1993), and hence favors healthy growth of the plant as well as the surrounding soil fauna and flora. Active supply of nitrogen is critical to the healthy growth of the rice plant. For this to occur the process of nitrification is extremely essential. According to Morris and Monier (2003), most of the time, the obligatory aerobic ammonia oxidizing bacteria becomes the limiting factor for nitrification. According to observations by Briones et al. (2002) in an experiment done on paddy cultivars, it was observed that the roots had biofilms that contained ammonia oxidizing bacteria. Quantities of ammonia oxidizing bacteria were two to three magnitudes higher than in the normal soil. Oxygen availability measurement closer to the rice roots measured through micro electric measurements showed that the amount of oxygen present is largely sufficient to supply oxygen requirement of Nitrosomonas spp. and Nitrospora spp. (Briones et al. 2002). This shows that, ammonia oxidizing bacteria, when live near the plant root, live in a micro niche of sufficient oxygen and nutrients although water-logged environment near rice roots is not anoxic. Morris and Monier (2003) reports that when biofilms are present near the plant roots the rice plants acquire an adequate amount of nitrogen because the biofilm matrix favors the diffusion of oxygen to bacterial cell and the required nitrite and nitrates into the rice plants.

7.3.2.3

Plant Growth Promoting Rhizobacteria (PGPR)

The rhizosphere of a plant is highly nutritious due to the presence of numerous amino acids, fatty acids, sugars, vitamins, etc., which are released by the plant roots. Due to these nutrients, the rhizosphere is abundant in microorganisms; bacteria, fungi, and protozoans. Among these microorganisms, plant growth is majorly affected by the presence of bacteria (Kloepper et al. 1989) which are called plant

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growth promoting rhizobacteria (PGPR). PGPRs enhance the mineral nutrient solubilization and nitrogen fixation, making the nutrients available to the plant (Figueiredo et al. 2010). These rhizobacteria could be either, rhizosphere colonizers, rhizoplane colonizers, or endophytes (Glick 1995). All three types of organisms are capable of plant growth promotion directly or indirectly. Direct plant growth promotion could happen through fixing of atmospheric nitrogen and providing it to the plant, phosphate solubilization, iron chelation, or the production of phytohormones. Indirect plant growth promotion is done in the ways of plant pathogenic bacterial suppression, inducing resistance in the host plants against pathogens and abiotic stress. PGPRs can enhance the growth of plants by improving the nutrient status of the host, but an intimate relationship between the PGPR and the host is essential (Vessey 2003). Legume-rhizobia symbiosis is an excellent example of improving the nutrient status of the host through symbiosis (Vessey 2003). Hence, the most extensively studied group of PGPRs are the Rhizobia. Most common examples include Allorhizobium spp., Azorhizobiums spp. (the organism used in this research), Bradyrhizobium spp., Mesorhizobium spp., Rhizobium spp., and Sinorhizobium spp. All of these organisms fix nitrogen and provide it to their legume host (Vessey 2003). In the plant rhizosphere, the amount of mineral nitrogen available is low due to the plant uptake of nitrogen. Hence, the nitrogen-fixing PGPR can highly colonize the plant rhizosphere (also, most of the PGPRs are diazotrophs). Although considered insignificant, the amount of nitrogen these PGPRs fix may be highly beneficial to plant (Vessey 2003). Another beneficial characteristic of PGPRs is their ability to increase the availability of plant nutrients in the rhizosphere (Glick 1995). This may occur through the increased nutrient release to the soil by PGPRs (Seneviratne et al. 2008) or phosphate solubilization (Richardson 2001). Richardson in 2001 identified P solubilization as the most common mode of action by PGPRs on increasing the nutrient availability of the host. With reference to this statement and other literature, Vessey (2003) has suggested that despite the availability of soil nutrients, PGPRs effect on the root system is substantial. These bacteria could affect root morphology, increase root surface area (Vessey 2003), increase root weight (Vessey and Buss 2002) leading to the increment of nutrient uptake to a greater extent. PGPR containing biofertilizers when applied to soils could produce phytohormones that could stimulate plant growth. These phytohormones are said to change the assimilate partitioning patterns in plants, affecting plant root growth patterns. Plants will be stimulated to produce bigger, branched roots with more surface area hence nutrient uptake could be increased (Vessey 2003). One such example of a phytohormone is indole-3-acetic acid (IAA) which is commonly involved in root initiation, cell division, and cell enlargement (Salisbury 1994). IAA is commonly produced by PGPRs (Barazani and Friedman 1999). This hormone can increase root growth, root length, and thereafter the surface area, increasing plant’s ability to access soil nutritional reserves. Other than IAA, cytokinins and gibberellins are also now identified as phytohormones that are being secreted by the PGPRs. Cytokinins promote cell division, cell enlargement, and tissue expansion in plants (Salisbury

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1994). The phytohormone gibberellin is involved in modifying the plant morphology by the extension of the plant tissues, particularly stem tissues (Salisbury 1994). Rojas et al. (2001) indicate the PGPRs coexistence in the rhizosphere to stimulate the growth of the plant through synergistic actions.

7.3.2.4

Pest and Disease Control

Biofilms attached to the roots of crops enhance the biocontrol of pests and diseases, and hence help in improved productivity. Seneviratne and Jayasinghearachchi (2003) and Artursson et al. (2006), disclose that arbuscular mycorrhizal fungi and bacteria, synergistically interact to enhance the plant growth through the improved nutrient acquisition and the increased pathogen inhibition (Artursson et al. 2006). Formation of microcolonies and production of toxins to resist protozoa grazing of the biofilms is an important and effective strategy of survival (Matz et al. 2004). Burmølle et al. (2006) report that than the application of monocultures, multispecies biofilms enhances resistance to antimicrobial agents through the action of persister cells which are of a highly protected state.

7.3.2.5

Nutrient Cycling

Microbial inoculants have a highly positive influence on N cycling and plant utilization of fertilizer N (Briones et al. 2002; Adesemoye et al. 2009). Biofilms attached to the roots of crop plants are involved in nutrient cycling (Seneviratne and Jayasinghearachchi 2005). Seneviratne and Jayasinghearachchi (2005) also report that, by the application of fungal–rhizobial biofilms to soil, the availability of nitrogen has improved by twofold and P has improved by 15-folds, in comparison to the inoculation of the monocultures.

7.4

Role of Microbial Communities in Improving Chemical Fertilizers Use Efficiency and Rice Yields

The use of inorganic fertilizers has the tendency to suppress soil microbial communities. In rice cultivations around the world, three major nutrients—N, P, K—are often provided through inorganic fertilizers. These inorganic fertilizers, specifically nitrogen have detrimental effects on soil sustainability due to their negative actions on soil microbial biomass, soil physiochemical properties, and soil and agrobiodiversity (Cruz et al. 2009; Hadgu et al. 2009). Microbial action (particularly nitrogen fixers) suppressed by N-fertilizers is a well-known phenomenon (Cruz et al. 2009). A nitrogen fixer provides multiple benefits to the growth and persistence of microbial communities (Seneviratne et al.

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2011; Van der Heijden et al. 2006). When they are adversely affected it can lead to the reduction of the agrobiodiversity (Hadgu et al. 2009). The inhibition of microbial diversity through inorganic nitrogen occurs due to a number of reasons. These include soil acidification, increased osmotic pressure, soil mineral depletion, increased aluminum toxicity, etc. (U.S. EPA 2008). Also, when the availability of nitrogen in the soil increase, plants tend to invest lesser energy to functioning of the roots and mycorrhizal communities, since lesser effort is required in acquiring energy (Johnson and Thornley 1987). On the other hand, the soil without inorganic fertilizer additions had resulted in increased microbial biomass. In a soil experiment conducted by Cruz et al. (2009), without any addition of inorganic nitrogen or phosphorous, the soil was observed to be replenished with nitrogen. They suggest that the reasons could be the effective nitrogen fixation by the free-living biological nitrogen fixers in the soil. A metaanalyses of the responses of microbial biomass to nitrogen fertilizer addition of 82 rice field sites had been conducted by Treseder in 2008. There the author reports that bacteria, fungi, and microbial community as a whole is altered by the addition of nitrogen fertilizers with a drastic reduction (15%) of the microbial biomass upon the addition of nitrogen fertilizer. Gu et al. (2009) report results of a 22-year-long study where the rice fields were treated with inorganic fertilizers (N, P, K) in combination with organic/farmyard manure and the bacterial community structure analyzed by PCR-DGGE targeting eubacterial 16S rRNA gene. This study has revealed that whenever inorganic fertilizers are added with organic manure/farmyard manure, the soil microbial biomass tend to increase in the paddy soils. A study conducted by Nakhro and Dkhar (2010) on paddy field microbes reports that microbial populations in surface and subsurface horizons can drastically increase when the paddy soils are treated with organic manure compared to inorganic fertilizers. Inorganic fertilizer application together with organic matter has increased the soil microbial content than only application of either alone. Even higher grain yields are achieved when the two treatments were combined (Xu et al. 2018). Zhou et al. (2017) report that the paddy soils treated with organic mature together with the chemical fertilizers have drastically increased the soil bacterial monounsaturated fatty acids, fungal polyunsaturated fatty acid, and the phospholipid fatty acid (PLFA) biomarkers for bacteria and fungi. Even though the application of inorganic fertilizers alone adversely affects the soil microbial communities, addition of inorganic fertilizers in moderation with organic fertilizers or biofertilizers has always yielded beneficial outcome in terms of microbial diversity/biomass as well as the rice yields. No matter how replenished the soil gets through the addition of the microbial fertilizers if the required rice yields are not obtained it is not seen as successful. Biofertilizers made out of biofilms seem to provide an excellent alternative in reducing the inorganic fertilizer requirement while providing the yields required (equivalent or more than the inorganic fertilizer alone application, as discussed in Sect. 7.3). Here, the application of chemical fertilizer in moderation supports the microbes in the biofertilizers (specifically biofilms) for their proper establishment. Once the nutrients or nitrogen supply becomes deficient in the soil, the microbes increase their function and fill the

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nutritional gaps, especially nitrogen through metabolic cooperation (Seneviratne et al. 2009). A proper establishment of a biofilm would provide the benefits to the plant, such as nitrogen fixation, suppression of pathogens, PGPRs production, etc. Remedying of the heavily fertilized, damaged soils is also possible with biofilmed biofertilizers (Seneviratne et al. 2009). When an in-vitro developed biofilmed biofertilizer is added to the soil with 50% of the fertilizer recommendation, a drastic improvement of important plant characteristics such as nitrogenase activity, soil organic carbon levels, and root exudate takes place (Seneviratne et al. 2011). In an application of three microbial biofertilizers coupled with 50% of recommended fertilizers for rice plant, a microbial biomass increments of 55% compared to 100% application of the fertilizers has been observed (Seneviratne et al. 2009).

7.5

Conclusion

Rice being the staple food for more than half of the world population, sustainable cultivation of this crop has become one of the major global concerns. This is further imperative with the adaptation of rice as a meal in cultures where rice has not historically and culturally been the staple diet. Excessive fertilizer usage over the decades has led to detrimental effects on the rice soils. This is exemplified further by the trends in urea fertilizer use in the recent past. Use of microbial biofertilizers as way of reducing inorganic fertilizer usage while providing the target rice yields has become an excellent alternative for only inorganic fertilizer usage. Addition of inorganic fertilizer in moderation coupled with organic or biofertilizers is an effective way to reduce the usage of inorganic fertilizers. The ability of bacterial and fungal biofertilizers to reduce up to 50% of nitrogen fertilizer usage for rice without affecting the targeted yields shows the competency of the newly discovered biofertilizers. The ability of microbial communities to heal the damaged soils whilst enhancing soil microbial and chemical interactions is evident, and the sustainability of rice cultivation can thus be ensured through the rightful manipulation of microbial communities.

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Chapter 8

Applications of Soil Bacterial Community in Carbon Sequestration: An Accost Towards Advanced Eco-sustainability Ved Prakash, Rishi Kumar Verma, Kanchan Vishwakarma, Padmaja Rai, Mohd Younus Khan, Vivek Kumar, Durgesh Kumar Tripathi, and Shivesh Sharma

Abstract Soil carbon content is regulated by multiple factors out of which bacterial communities play a significant role in soil system stability supporting eco-sustainability. In recent times, environmentally friendly approaches have been developed, which are more preferred over the usage of chemical methods in restoring soil stability. Out of various cutting-edge technologies available, which demand high input in terms of resources, a gradual inclination towards soil bacterial communities form a crucial component of soil microbial communities enhancing carbon sequestration. The multifaceted role of bacterial communities in carbon storage basically relies on microbial dynamics and interrelationships between formation and breakdown of end products. The regulation of C-cycling in soil is determined by various factors like microbial load, species richness, bacterial diversity, community structure, and enzyme activity. Soil microbes’ interaction with soil aggregates is a key factor in restoration, conversion, reducing erosion, and eco-sustainability. Gradually changing climates, abiotic stress, and elevated CO2 levels are likely to affect plant–microbe interactions disturbing carbon cycling that lead to a shift in bacterial profile, carbon efflux pattern of roots that leads to hamper rhizosphere diversity and overall plant growth. This chapter highlights the biological aspects of

V. Prakash · R. K. Verma · K. Vishwakarma · P. Rai · M. Y. Khan Department of Biotechnology, Motilal Nehru National Institute of Technology Allahabad, Prayagraj, India e-mail: [email protected]; [email protected] V. Kumar Himalayan School of Biosciences, Swami Rama Himalayan University, Jolly Grant, Dehradun, India D. K. Tripathi · S. Sharma (*) Amity Institute of Organic Agriculture (AIOA), Amity University, Noida, Noida, Uttar Pradesh, India e-mail: [email protected] © The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2021 G. Seneviratne, J. S. Zavahir (eds.), Role of Microbial Communities for Sustainability, Microorganisms for Sustainability 29, https://doi.org/10.1007/978-981-15-9912-5_8

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sequestration, factors affecting it, and application of bacterial diversity in restoring soil organic carbon. Keywords Bacterial diversity · Carbon sequestration · Abiotic stress · Plant– microbe interaction · Organic carbon · Sustainable development

8.1

Introduction

In terrestrial ecosystems, soil organic carbon forms the highest storage pool when compared to plants and atmosphere. It sequesters about 20–30% of the total carbon emission released from anthropogenic activities (Saleska et al. 2003). Forming the largest pool of organic carbon source, soil strongly interacts with atmospheric and climatic changes (Jobbágy and Jackson 2000). In managed ecosystems, soil carbon is estimated to be reduced by half due to past cultivation activities. This reduction suggests the requirement of carbon storage (McCarl et al. 2007). Microbes can be key players in maintaining the biochemistry of soil by recycling nutrients and controlling environmental geochemical cycles. After the realization of the consequences of tremendously increasing carbon dioxide levels in the atmosphere, the scientific community has keenly focused on understanding the mineralization of organic forms of carbon that leads to the release of carbon in the atmosphere. As a result, other aspects such as litter decomposition rates under changing climatic conditions were also studied (Prescott 2010). The balance between soil carbon stock and atmospheric CO2 depends on the community structure of microbes and plants. The variation in community composition could result in a disturbed carbon stockpile that regulates the CO2 and methane levels in the atmosphere and forms a prominent part of terrestrial carbon sequestration (Díaz et al. 2009). Carbon sequestration simply is any natural or artificial process by which the carbon dioxide is removed from the atmosphere and held in a liquid or solid form. Elevation in the environmental temperature is the cause of global climatic change and melting of glaciers which is consequently raising the sea level. Additionally, global warming is also causing an increase in the respiration of soil microbes and greenhouse gases such as carbon dioxide (CO2) and methane (CH4) (Bardgett et al. 2008). Out of various available technologies soil-based carbon capture seeks attention pertaining to its better stability and long-term storage as well as economical and sustainable approach to mitigate global climatic changes (Srivastava et al. 2012). While focussing on the importance of terrestrial ecosystems in maintaining carbon balance in the biosphere, this chapter aims to provide insights into carbon sequestration in soil, factors affecting this process, role of microbial communities and plants in sequestration, and various land management practices that help to reduce carbon levels.

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Carbon Sequestration in Soil

Of the various natural and artificial approaches for carbon sequestration natural processes involving the terrestrial biosphere and plant biomass is most promising as it holds a huge amount of carbon in a locked form. Here, plants fix atmospheric carbon and add it to the organic content of the soil. Wrong land practices deplete the crucial organic content from soil and reduce the soil organic carbon (SOC), which has already accentuated carbon to the atmosphere. Storing carbon in soil helps to mitigate soil degradation, helps purify groundwater, and reduces CO2 escape to the atmosphere (Lal 2004a, b). Currently, advances have been ongoing to understand the mechanism of soil carbon stabilization including both abiotic and biotic processes. Abiotic process includes the soil’s physical structure and disturbance in the stocks of organic soil, while biotic activities of plants include litter, root system, microorganisms, bacteria, fungi, termites, ants, and earthworms (Dignac et al. 2017).

8.2.1

Climate Change Effects on Soil Carbon Pool

The delicate equilibrium between the carbon source and sink is necessary for soil the carbon pool. Carbon input in soil are results of either litterfall or rhizodeposition which enriches soil organic carbon while on the other hand carbon release during decomposition processes account for the carbon output. The soil organic content turnover is in fact affected by carbon source, climatic condition, and the soil chemistry (pH, nutrient, particle size, clay content, moisture). Land management practices widely affect these parameters determining carbon sequestration in soil (Knorr et al. 2005; Trumbore et al. 1996; Percival et al. 2000; Davidson and Janssens 2006; Derner and Schuman 2007). The distribution of carbon in roots has a higher residence period than in shoots, where studies showed carbon derived from roots had 2.4 times more mean residence times than shoots although this is affected by factors like physicochemical factors, root hairs, mycorrhiza, and interaction with metal ions (Rasse et al. 2005) (Fig. 8.1). Soil pH helps in proper functioning of microbial reactions and is associated with the soil enzyme activity. Consistent change in climate and concerns related to global warming have forced us to think critically about measures to decrease the CO2 concentration in the atmosphere. Carbon storage and capture can be one way to reduce our carbon footprint (Leung et al. 2014). Out of various methods available oxyfuel combustion, where air is replaced with pure oxygen for combustion, could help us to reduce the carbon in exhaust gas of coal-fired stations (Buhre et al. 2005). But these techniques involve the consumption of high energy and are not cost-effective, which therefore limits its use (Pfaff and Kather 2009). In contrast, forests and their soils help in sequestrating carbon imparting a positive effect in reducing the effects of the gradually changing climate, so proper management of forest and public policy

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Fig. 8.1 Terrestrial carbon sequestration

may be helpful in this regard (Sedjo and Sohngen 2012). Compared to atmospheric CO2, soils hold two to three times more carbon thus acting as a sink. Further, variation in temperature due to global warming affects decomposition processes which determine amount of carbon being released back to the atmosphere (Davidson et al. 2000). Climate change affects the decomposition of carbon and cold temperatures impede decomposition processes (Jenny 1994). Studies have shown changes in the richness of bacterial and fungal communities under varying climate, CO2 concentration, temperature, and precipitation alter the soil ecosystem with precipitation causing higher effects on community structure (Castro et al. 2010).

8.2.2

Role of Living Organisms on Soil C Sequestration

The persistence of high levels of 397.34 ppmv of CO2 is quite elevated in comparison to natural occurrences being in the range of 180–300 ppmv that has persisted since the past ages. To sequester CO2 from the atmosphere terrestrial plants, microalgae, and different bacteria are extensively useful in maintaining the carbon balance (Kumar and Das 2014). The soil ecosystem comprises of a diverse variety of flora that contribute to organic carbon in soil and regulate carbon flux (Chevallier et al. 2001). Microbial communities form an integral part of soil and its diversity and

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physiology regulate carbon dynamics; out of this saprophytes and decomposers form the functionally diverse elements (Curtis and Sloan 2005). Rhizosphere and bulk soil contain huge amounts of microbial load. As per an estimate 1 g of soil may contain up to one billion bacteria comprising of a variety of species (Gans et al. 2005) and it is estimated to contain one million fungus species (Hawksworth 1991). Changes in climate enhance the exudation of roots of organic compounds into soils. Promotion of carbon loss is accompanied by the liberation of organic compounds from root exudates such as oxalic acid which is associated with minerals (Keiluweit et al. 2015). A regulatory component of terrestrial carbon storage is soil fungi comprising of wood decaying fungi, white rot fungi, lignin degrading fungi, e.g., Phanerochaete chrysosporium, Coriolus hirsutus, Lentinus edodes, and Polyporus sp., that stores carbon in its biomass and forms recalcitrant by-products that reside for longer periods of time storing carbon for years (Mehar and Sundaramoorthy 2018). Sedimentation is also one of the processes responsible for natural absorption of CO2. CO2 also gets converted into bicarbonate rocks naturally. Microbial decomposition of buried organic material from plants, animals, biomass, and agriculture contribute to around 2 Gt carbon sequestration (Oelkers and Cole 2008). Microbial dynamics and rate of formation and degradation regulates the carbon content in soil mainly because carbon sequestration led by microbes depends on microbial biomass, community composition, its side products, and soil properties (Six et al. 2006). In a study Serratia sp. was found to utilize carbon dioxide for its growth and as a by-product formed calcite crystals thus helping in locking carbon to soil (Srivastava et al. 2015). For the promotion of microbial abundance biochars derived from feedstocks can be utilized to promote microbial abundance and community structure (Gul et al. 2015). Biochar can provide shelter and lead to alteration in soil microorganism diversity and may cause variations in the occurrence of microbes, composition of community and its activities. However, there is still lack of knowledge about the causes of variation in the physical and chemical assets of biochar. The possible effects of biochar on organisms present in soil are still an unexplored area and how it modulates soil microorganisms is a questionable subject; however, certain experiments conducted on earthworms have provided us with the knowledge related to biochar (Lehmann et al. 2011).

8.3

Contributions of Plants in Carbon Sequestration

Increasing levels of carbon have led to alarming concerns leading to efforts to reduce the carbon footprint by most developed and developing nations. Various summits like Kyoto protocol, United Nations Framework Convention on Climate Change, Climate Change 2001: Kyoto at Bonn and Marrakech are showing their efforts towards this growing issue (Sands 1992; Protocol 1997; Vespa 2002). Plants play a crucial role in balancing carbon assimilation and regulating net carbon storage in subsurface soil biomass, where it gets released from soil in the form of respiration, leaching, or decomposition (De Deyn et al. 2008). Terrestrial plants utilize CO2 for

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photosynthesis and release CO2 through respiration. However, there is a net CO2 sequestration regulating the level of CO2 in the atmosphere (Hall et al. 1992). Annually about 10% of CO2 from the atmosphere is fixed through photosynthetic processes in the form of carbohydrate (Whitmarsh 1999). Soil forms the storehouse of carbon inhibiting its escape to the atmosphere. But gradually changing the environment may pace up the decomposition process turning this sink to be a production house of carbon (Davidson and Janssens 2006). Carbon sequestered in living vegetation and organic matter possess an enormous amount that if this amount is returned back to the atmosphere in the form of CO2 or methane will risk life forms and will be a serious threat to the global climate (Heimann and Reichstein 2008). Soil as a sink of carbon is more beneficial than locking the carbon in plants and vegetation as the latter will eventually form litter and decompose thus releasing the carbon back to the environment (Lehmann 2007). Reducing the level of organic matter from soil creates obstacles to agricultural productivity. Plants procure this vital carbon and release it in the form of root exudates thus imparting benefits of carbon sequestration (Kumar et al. 2006). Plants are good at sequestering carbon even when grown on roofs that accumulate high amount of biomass such as in the example of Sedum species (Getter et al. 2009). Studies have proposed the existing regulations of carbon in terrestrial biomes occur in two steps. Firstly, plant traits that capture carbon and assimilate it, further transferring it to soil where it interacts with various microorganism that determines its residence time. Secondly, soil carbon pools being regulated by concerted effects of soil biota and plant traits (De Deyn et al. 2008). Overall carbon assimilation is measured through carbon fixation in the form of photosynthesis and losses incurred due to respiration and through root exudates to heterotrophic organisms, but when the net productivity of an ecosystem is taken into account non-respiratory losses are also considered (Schulze 2006). The loss of soilbound carbon is accelerated with the increase in soil degradation and wrong land practices which demands a sustainable and restorative approach on agricultural lands that could lower down CO2 release and have positive roles in improving food security and environmental quality (Lal 2004a, b). In a study conducted in Boreal forest soil, it was found that 50–70% of the soil carbon was contributed from roots or roots-linked microorganisms that help in carbon sequestration for longer periods of time (Clemmensen et al. 2013). Even in tropical forests, it has been estimated that the loss of biodiversity and species richness will lead to a decline in carbon storage potential of these forests (Bunker et al. 2005). The biodiversity and interaction between communities of plant and soil organisms regulate the balance of carbon and the resulting alteration in traits of organisms can lead to a shift in this balance. This influence could be direct like affecting carbon stock in soil or turnover rate (Díaz et al. 2009). Although utility of plants for carbon sequestration is of limited use, at elevated CO2 concentrations afforestation could render better carbon storage in plant biomass since it has been reported that about 30–40% of quenched carbon from the atmosphere is locked down in soil through the network of roots of plants (Manning and Renforth 2012). The biomass accumulation in plants grown under elevated carbon dioxide (550 ppmv) was marginal. However, when nutrients were

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Fig. 8.2 Interactive roles of soil biota with soil and biosphere in sequestering carbon

supplemented along with elevated carbon it resulted in a two- to threefold increase in biomass (Oren et al. 2001). Growth of plants have been shown to be influenced by the soil organic content. Soil biota also determine the composition and functioning of plant diversity. The amount and quantity of root inputs to the soil maybe in the form of root exudates, soil nutrients as well as soil microbial population, all of which are considered to stimulate organic carbon content in soil resulting in plant growth regulation (Eisenhauer et al. 2017) (Fig. 8.2).

8.4

Role of Bacterial Communities in Restoring Soil Structure and Organic Carbon

The tremendous increase in the population has put pressure on agricultural systems for more production resulting in soil carbon degradation (Blair et al. 1995). The dynamic shift in carbon levels occurs due to the cultivation of crops leading to changes in soil distribution and aggregation patterns. Continuous cultivation leads to losses in carbon content and eventually results in depletion of soil (Six et al. 2000). The macro aggregate-micro aggregate model explains the deposition of carbon in soil which is often lost during cultivation (Elliott 1986). Various factors like soil texture, precipitation pattern, temperature, agricultural practices soil management,

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etc., contribute to carbon sequestration to enhance carbon pools in soil. Practices like restoration of woodlands, organic farming, sludge application, less tillage farming, efficient irrigation, sustainable nutrient usage, etc., will be helpful (Lal 2004a, b). Excess tillage causes severe loss of organic matter from soil (Baker et al. 2007). Soil forms the interface for microorganism where they interact with the lithosphere, hydrosphere, and atmosphere under varying climatic conditions. Soil supports tremendous lifeforms and thus supports a huge biomass with an estimated total of 2.6  1029 prokaryotic cells (Voroney 2007). Rhizosphere forms an integral part of plant growth and development along with providing habitat to beneficial microbes contributing towards carbon sequestration and nutrient cycling in the soil. Rhizosphere microbial communities derive nutrients from root exudates of plants (Berg and Smalla 2009). In the rhizosphere, plant– microbe interactions contribute to nutrient recycling, carbon sequestration in agricultural, and terrestrial ecosystem (Singh et al. 2004). The abiotic and biotic factors affect functional and structural composition of bacterial communities residing in the rhizosphere (Philippot et al. 2013; Yang et al. 2009; Simons et al. 1996; Buée et al. 2009). The enormous amount of organic carbon released by roots sustains the rhizosphere and provides ample resources for growth of microbial communities (Bais et al. 2006). Root exudates are rich in nutrients that enhance activity and biomass of microbes and fauna present in the rhizosphere (Butler et al. 2003). Although primary production forms the major contributor to carbon storage in soil, particle size and enzyme activity modulate microbial richness and subsequent carbon sequestration through mineralization of soil organic carbon (Zhu and Miller 2003). Plant–microbe interactions leading to carbon sequestration depend on root turnover, rhizodeposition, and microbial activity (Matamala et al. 2003). Microbial communities in association with plants could be used for quenching carbon and reducing deleterious effects of carbon emission (Lal 2003).

8.5

Land Management Practices Impacts Microbial Biomass and Soil Carbon Content

Agricultural practices affect the amount of microbial biomass as well as accumulation of soil organic matter. Improper land management that utilizes more tillage affects carbon sequestration. It is a common observation that in undisturbed land more carbon is stored and as the disturbance level increases due to cultivation of crops, the accumulation of carbon gradually decreases. Thus, proper management of crops could be helpful in achieving goals of sustainable development for a better ecosystem. The practices mentioned below can play a helpful role in preserving carbon content of terrestrial ecosystems.

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Tillage

Tillage based farming intensively affects soil and water when compared to no-tillage farming. No-tillage farming has been seen to support sequestration of soil organic carbon in varying ecosystems (Blanco-Canqui and Lal 2008). Tillage is correlated with microbial carbon dynamics. In a study where conventional methodology and no-tillage practices were used on oxisol, a higher C and N mineralization with no-tillage was seen. Apart from this no-tillage also enhanced overall carbon by 45% and microbial biomass by 83% at a depth of 0–50 mm (Balota et al. 2004). Under no-tillage farming practice in Brazilian oxisol, results showed that the amount of organic carbon stored in soil was comparatively high, at a depth of 0–20 cm where the carbon quenching rate was found to be 80.6 g Cm 2 year 1 (de Moraes Sá et al. 2001).

8.5.2

Crop Rotation

Cultivating different crops in soil helps soil to retain fertility by enriching the soil with nitrogen and carbon. The crop residue forms a surface cover which under no-tillage conditions enriches soil fertility (Havlin et al. 1990). The beneficial aspects of crop rotation include better microbial biomass ratio, enhanced microbial activity, and high soil enzyme activity which lacks in conventional farming following monocropping (Acosta-Martínez et al. 2003). When legume cover crops are grown in between cash crops it helps to produce synergistic effects on microbial biomass (Lupwayi et al. 1999). Crop rotation may enhance carbon sequestration processes as compared to monotonous cropping. Subsequent crop rotation increases microbial biomass, its activity, community composition, and can also enhance the level of soil biota.

8.5.3

Organic Farming or Cover Crop

Compared to conventional farming where fertilizers are abruptly used organic farming is a more eco-sustainable approach as it increases species richness, reduced evenness, and supports soil microbiota and microbial diversity (Hartmann et al. 2015). Organic farming strongly influences nutrient and soil enzyme activity that effects mineralization. Thus, microbe-derived ecosystems can easily be manipulated for more nutrient recycling (Bowles et al. 2014). Organic farming enhances soil quality and agricultural sustainability. In a long-term study, it was observed that it improved the bacterial pathways linked with soil and favored earthworm growth. Overall it was concluded that no-tillage, crop cover favors soil biota (Henneron et al. 2015).

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In an experiment the positive aspects of organic farming were seen on the quality of soil and microbial community where it enhanced the total microbial richness and activity in agricultural fields (Lori et al. 2017). Soil fungi and bacteria contribute to enrichment of soil organic carbon. In a study done on grasslands, microbial residue was found to contribute to 50% of SOC while for saline land and forest soil it resulted in a 30% contribution towards SOC (Khan et al. 2016). Soil provides a huge storage house for carbon (Pacala and Socolow 2004) especially by means of adding large biomass carbon by practices like cover cropping. Cover crop is grown between two crops which has no economic importance but forms an integral part of agricultural practice. Organic farming often employs cover cropping which alters the soil microbial community and also affects microbe-derived organic matter. An alternate means to sequester carbon in agricultural fields is usage of cover crops in cropping practices. This helps to enhance soil organic carbon without affecting the crop yield (Poeplau and Don 2015) and adds soluble organic carbon to soil (Zhou et al. 2010) as well as improves microbial communities present in soil (Wilson 2002). Varying compositions of microbial communities were observed when maize against maizeCrotalaria (a legume cover crop) rotation with and without the addition of phosphorous was grown (Bünemann et al. 2004). Cover crop of vetch (Vicia sativa L.,) and oat (Avena sativa L.) when compared for their winter fallow showed increased microbial biomass, high N mineralization, respiration, and altered microbial community structure (Schutter and Dick 2002). Mulching in maize plantation was also seen to help to improve carbon and nitrogen content in soil (Chen et al. 2018).

8.6

Concluding Remarks

Tremendous elevation in CO2 is a result of the imbalance lying between carbon emission and its storage occurring due to an unprecedented increase in industrialization and various anthropogenic activities. Today global concern has appeared for issues related to global warming, depleting glaciers, increase in sea level, gradual climate change, etc. Soil forms a major sink of carbon thus related flora and fauna cannot be ignored for its positive role in sequestering carbon. With anthropogenic activities alteration in microbial richness and activity of fungi and bacteria may lead to disrupted carbon cycling and storage occurring because of differential interaction between these microorganisms and soil physical properties. Even roles of proper land management that include crop rotation, tillage, cover crop practices cannot be ignored in carbon sequestration processes. All these managements are expected to drive shifts in microbial community composition. Therefore, proper land management practices if implemented along with usage of microbial community in restoring carbon level in soil has a high probability to combat climate change globally, and thus enhance agricultural sustainability.

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Acknowledgments The authors are thankful to the Director, MNNIT Allahabad for providing the necessary facilities and financial support for this work. The support provided by MHRD sponsored project “Design and Innovation Centre” is also acknowledged.

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Chapter 9

Approach Towards Sustainable Crop Production by Utilizing Potential Microbiome Usha Rani, Manoj Kumar

, and Vivek Kumar

Abstract The natural environment contains a diverse range of microorganisms and plants, which interact with each other in a variety of ways. This interaction may range from two-partite symbiosis (formation of single nodule by symbiotic association of legume and rhizobia which assists in nitrogen fixation in environment) to multi-partite epiphytic or endophytic. There are some exudates produced by soil microorganisms which help in recycling of essential nutrients like phosphorus and nitrogen. A fundamental understanding of evolution, molecular biology, genetics, and ecology are required to promote sustainable agricultural practices based on microbes. The recruitment of such fields of compatible researches may help to have a remarkable productive capacity and versatile function as well. Crop production based upon the microbes has the potential to replace the existing harmful chemicals, with biofertilizers, and therefore aid in economic benefit and enrich the quality of agricultural goods obtained. Keywords Crop production · Microbiome · Nitrogen fixation · Phosphate solubilization

9.1

Introduction

Plants and microbes continuously intercommunicate with each other. Some of these intercommunications are valuable while others are harmful. Further, investigations regarding the favorable or valuable role of microbiomes still need to be explored. A U. Rani · V. Kumar (*) Himalayan School of Biosciences, Swami Rama Himalayan University, Jolly Grant, Dehradun, India e-mail: [email protected] M. Kumar Center for Life Sciences, School of Natural Sciences, Central University of Jharkhand, Ranchi, India © The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2021 G. Seneviratne, J. S. Zavahir (eds.), Role of Microbial Communities for Sustainability, Microorganisms for Sustainability 29, https://doi.org/10.1007/978-981-15-9912-5_9

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plant microbiome comprises of those microbial populations that naturally and habitually interact significantly or considerably with a plant or plant part. Plant microbiomes can proliferate either inside (commonly known as endophytes) or outside of plant parts, executing numerous plant-promoting and beneficial functions including plant growth promotion and biological control of possible phytopathogens (Orozco-Mosqueda et al. 2018). An important part of the plant microbiome includes plant growth promoting microbiome (bacteria and fungi) (PGPM) that commonly reside in the rhizosphere and phyllosphere, and as well as endophytic microbiomes which perform similar functions to PGPM (Yadav and Yadav 2017). The current chapter approaches the study of distinct microbes with respect to their beneficial role in crop improvement and thus in agriculture, which may help to contribute valuable possibilities for the future. At present, the human population is increasing day-by-day, thereby increasing the demand to have proper nutritional needs and development. To meet the growing demands of mass population, a sustainable and applicable approach is required which is both environment friendly as well as has the potential to improve the agricultural goods—not only quantitatively but qualitatively as well. An alternative approach is to use microorganisms in place of conventional agronomic practices, some of which cause high damage to the ecosystem and thus create environmental imbalance. For example, regularly used nitrogen-based fertilizers can lead to the contamination of groundwater. One major concern is that various chemicals such as insecticides and pesticides that protect the crops may enter the food chain. The utilization of microorganisms as plant growth promoters has been reported in the literature as well (Burdman et al. 2000; Dobbelaere et al. 2003). Rhizobacteria are a group of microorganisms which assist in plant growth. These microorganisms play a vital role in enhancing and improving agriculture (Whipps 1997; Lehr 2010; Hermosa et al. 2011). Microorganisms can be utilized to enhance the nutrient uptake ability from the soil of the plants in the form of biofertilizers which help to encourage plant growth and development. It has been reported worldwide that microbes like bacteria, fungi, etc., are helpful in plant growth and development by eliminating plant growth inhibiting substances but their comprehensive exploration is still required in the field of agriculture (Berg 2009). Most of the soil-plant-microbial interactions take place in the rhizospheric zone of the plants. Interactions that exist in the soil-plant-microbiome may be parasitic, associative, symbiotic, or neutralistic (Hayat et al. 2010). It relies on the type of plant nutrients offered by different soils, defense mechanisms of plants, and various types of microbes persisting in soil across the rhizospheric-root-zone. When the microbes invade the plant epidermis, the plant immediately in response starts to secrete the signal molecules or compounds in order to protect themselves from microbial attack. This microbial attack usually occurs frequently in the root zone of plants. This is the phase where microbes form associations with plants where this intercommunication can be pathogenic, associative, or neutralistic. Flavonoids and flavones are the most usually secreted signaling molecules that are produced by plants in case of microbial attack. These are released in the microbial rhizospheric zone. Further, few of these substances act as antimicrobial agents and remain associated with the plant cells.

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The rod-shaped soil bacteria, Rhizobium induces the formation of nitrogen fixing root nodules in most leguminous plants and in rare cases in some non-leguminous plants as well, when synergism between legume and Rhizobium occurs. Bacillus and Pseudomonas are different species of rhizobacteria, which have been detected to have an indigenous role in the development of plants and also help in suppression of different plant pathogens. Approximately 80% of the earth atmosphere’s volume is constituted by Dinitrogen (N2), which is a chemically inert compound. Nitrogen fixing bacteria secrete an enzyme called nitrogenase which reduces the dinitrogen into ammonia. The microbial population which proliferates in synergism with the plants possesses a special microaerobic environment provided by the plants for the appropriate working of the enzyme nitrogenase. Nitrogenase is an oxygen susceptible enzyme. The microbes (mostly bacteria) then fix the nitrogen available in the atmosphere and assimilate the various organic nitrogenous compounds in order to fulfill their biological requirement. As this symbiosis is immensely valuable in the field of agriculture, approaches have been made to increase the efficiency of this synergism. Genetic alterations are done regularly in order to make this synergism suitable for non-leguminous plants as well (Stacey et al. 1980; Fisher et al. 1985; Fisher and Long 1992). The capability of potential microbes to enhance the plant growth happens as an outcome of several mechanisms (direct or indirect). The direct encouragement of plant growth takes place when a microbe either helps in acquisition of basic and key nutrients or regulates the phytohormone level within a plant. The various nutrients uptake and transport are usually facilitated by microbes usually includes N, P, K, Fe, Zn, Cu, etc. In addition to it, some effective microbes can also lower the levels of plant ethylene by manufacturing an enzyme, 1-aminocyclopropane-1-carboxylate (ACC) deaminase. This enzyme cleaves the compound ACC, which is the direct precursor of phytohormone ethylene in all higher plants. ACC after being exuded by plant roots is taken up by a microbe. The ACC is then split into α-ketobutyrate and NH3. Thus, the microbe acts as a sink for ACC which in turn lowers the plant ACC level. Therefore, as a result of the occurrence of an ACC deaminase producing microbe, a plant overcomes the various biotic or abiotic stresses (Glick 2012, 2015). Figure 9.1 shows the plant growth regulation by rhizospheric as well as endophytic microbiomes. Here the plant-associated microbiome provides all-round protection as well as encourages plant growth. Various Plant Growth Promoting Rhizobacteria (PGPR) and nodule promoting rhizobacteria (NPR) have also been recognized by different reports as these microbes have the potential to manufacture/provide compounds that help in enhancement of plant growth. Siderophores are produced by various microbes; these siderophores chelate the cations into insoluble forms and serve in association with plants. Further manufacturing of phytoalexins in plants is induced by these microbes. These phytoalexins act as antibiosis causing agents for various pathogen forms that occur in the rhizosphere (Lugtenberg and Kamilova 2009; Babalola 2010; Verbon and Liberman 2016). Bacillus and Pseudomonas are some microbial species which are particularly associated with such interactions (Capper and Higgin 1993; Guaiquil and Luigi 1992; Parmar and Dadarwal 1997). The current chapter will emphasize on the

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Temperature - some soil microbes play a signficant role in plant growth during adverse temperature conditions

Drought - Arbuscular Mycorrhizal Fungi (AMF) play a significant role in absorption of water and also enhances the plant root surface area

Potential soil microbes also fix atmosheric N, solubilizes P and produce phytohormones

Metal toxicity - Several soil microbes reduces metal toxicity, metals are absorbed on microbial surface

Endophytes - these microbes also improve plant growth as done by common PGPM (Plant growth promoting microbes)

Flood - under excess water conditions plant roots produce ACC. Soil microbes produce the enzyme ACC deaminase which cleaves this ACC

Fig. 9.1 Plant growth regulation by rhizospheric and endophytic microbiome

profitable effects of bacteria sustaining in the rhizospheric zone of soil and will also give insights into the plant–microbial interactions. This chapter will cover the distinct perspectives regarding the microbes which benefit the soil and throw light on the diverse direct and indirect pathways associated with the enhancement of plant growth. Moreover, studies which relate to the mechanisms related with such associations will help to serve as a key tool in promoting sustainable agriculture approaches in the coming future.

9.2

Microbiome Contribution

Microbial contribution may be described as an action or any process that progresses towards the participation in biological activities prevailing in soil or in plants by microorganisms. In most cases, this contribution is advantageous as it leads to the enhancement in nutrient availability to the plants, and thus results in promoting the plant growth and ultimately increasing the yield. High crop yield can be achieved by the utilization of microbial contribution, which can result in the enhancement of distinct biological processes such as the following—making essential nutrients

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available to plants, helping in atmospheric nitrogen fixation, biodegradation of organic wastes which is then recycled in the environment, microbial leaching of inorganic compounds (Brierley 1985; Ehrlich 1990), suppression of some soil-borne pathogens, assisting in production of antibiotics, helping in complexation of heavy metals so as to inhibit their uptake by plants, production of polysaccharides which help in soil aggregation, decomposition of various harmful compounds such as plastics, pesticides, production of basic organic compounds for the utilization of plants (Singh 2014; Al shehrei 2017; Babbal et al. 2017), etc. For any agroecosystem, the important limiting factors are biotic and abiotic stresses, where these stresses lead to reduced plant growth and production. For optimum production, the crop plants try to manage or cope up with these opposing exterior stresses (caused by “NOT” good microbiome or by edaphic and environmental situations) with their inherent and core biological mechanisms. If the plants fail to manage these stresses on their own this leads to poor proliferation, growth, development, and ultimately decreased production. Among the chief regulating factors the hostile climatic conditions are the main culprits, resulting in reduced crop productivity (Grayson 2013; Meena et al. 2017). According to a report by the FAO (2007), merely 3.5% of the world terrestrial area has been left untouched by any environmental constriction. The main abiotic stresses include osmotic stress, high and low temperature, acidic and saline conditions, intensity of light, flood, nutrient depletion, and oxygen limitation (Chaves and Oliveira 2004; Nakashima and Yamaguchi-Shinozaki 2006; Bailey-Serres and Voesenek 2008; Iizumi and Ramankutty 2015). Surprisingly, the drought conditions have influenced about 64% of the total land area of the world, followed by freezing temperature (57%), acidity in soils (15%), flood (13%), nutrients insufficiency (9%), and salinity in soils (6%) (Mittler 2006; Kang et al. 2009; Cramer et al. 2011). Though it is very difficult to accurately estimate the agrarian loss owing to abiotic stresses, it is obvious that these stresses influence a huge land area and considerably influence the quality and quantity loss of crop growth and production (Kang et al. 2009; Cramer et al. 2011). Very often the microbiome present inside the host plant helps in mitigating the abiotic as well as biotic stresses (Turner et al. 2013; Ngumbi and Kloepper 2014). It is well known that microbes play a very significant role in this ecosystem where they are part of soils, plants, and animals. Owing to their known role in soil and agroecosystems, they naturally become an essential part of the cropping system, as early as the seed germination and its radicle movement into soil. The microbiome of host plants offers essential and vital support to the plants in nutrient acquisition, resistance against abiotic strains and diseases (Turner et al. 2013). Microbiome inherent, basic, genetic, and physiological abilities make them an appropriate candidate to overcome severe environmental conditions (Sessitsch et al. 2012; Singh et al. 2014a, b). The microbiome interactions with the host plant induce several types of local and systemic responses resulting in improved plant metabolic ability to combat the abiotic and biotic stresses (Nguyen et al. 2016). Research work on host plant and microbial interactions at physiological, biochemical, and genetic levels recognize

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that microbiome synergism greatly influences the response of host plant towards various stresses (Farrar et al. 2014).

9.3

Plant Microbiome Synergism

Microbes present in the soil microbiome continuously interfere with the root zone in plants and the soil ecosystem. These microorganisms sustain in the ecosystem by fulfilling their nutritional needs with the help of root exudates and plant biomass (Sandhya et al. 2009; Bisseling et al. 2009). As compared to the soils which have no plantation, huge numbers of microorganisms are found in the rhizosphere (region of soil in the root vicinity which is directly affected by the plant root system, secretions, and microbes) and rhizoplane (external surface of the root having soil particles and other debris). The most common reason for the lack of microbes in soil with no vegetation is the absence of root exudates, which act as an attraction for microbes. When seeds germinate, carbon and nitrogen compounds like vitamins, amino acids, sugars, organic acids, etc., are released into the ecosystem in large amounts. A large number of microbial populations is attracted towards these compounds, which as a result leads to competition between distinct species of microbes for survival (Okon and Labandera-Gonzalez 1994). Also, different species of plants have different microbiomes in their rhizospheric zone. Plant growth promoters and biocontrol agents are the microbes which benefit in a variety of ways (Bisseling et al. 2009). By adopting different methods these microbes help in improving overall plant health by direct or indirect means. Population density, alleviation of population dynamics or depression, and other metabolic activities that occur in pathogens present in soil ecosystems are some of the indirect beneficial effects of microbes that help in development of plants. This may happen because of hyperparasitism, competition, antibiosis, lysis, competition for space and essential nutrients which takes place at the surface of roots. Few antagonistic microorganisms also produce lytic enzymes and a wide range of secondary metabolites in nature which act as antimicrobial agents. Hyperparasitism, a relationship between two parasites in which one develops within the other, has been well reported in Trichoderma. Here, it secretes enzymes like cellulases and chitinase, and when a pathogen comes in contact with the host, it digests its outer cell wall by enzymes and then enters into the host (Schuster and Schmoll 2010). Phytostimulation and biofertilization are some direct beneficial effects of rhizospheric microorganisms on plants (Burdman et al. 2000). The main procedures connected with this may involve production of phytohormones, increased access to phosphate present in soil, and non-symbiotical fixation of nitrogen. Pyrolnitrin, prolution, hydrogen cyanide, and phenazines are a few toxic compounds secreted by plant growth promoting rhizobacteria (PGPR) against harmful pathogens (Beneduzi et al. 2012; Vejan et al. 2016). Some antibiotics, phytohormones, metabolites, and enzymes are also produced by PGPR against pathogens where these are some protective ways by which PGPR act and promote plant growth.

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Quorum sensing and chemotaxis are also required for the sustenance of rhizospheric microbes, such as Pseudomonas aeruginosa (Castro-Sowinski et al. 2007; Ramette et al. 2011; Jousset et al. 2011; Abisado et al. 2018), Bacillus cereus, and Bacillus thuringiensis (DeAngelis et al. 2008). High molecular weight siderophores are also produced by the PGPR under certain conditions. When iron availability is low, these siderophores seize the iron in a competitive manner, and thus make iron inaccessible to fungi which are pathogenic (Miethke and Marahiel 2007; Ali and Vidhale 2013).

9.4

Microbiome Growth Promoters

Soil inhabits vast number and types of microbes, which include bacteria, fungi, actinomycetes, algae, and protozoa. Out of these bacteria are the most common and found in the highest number of around 95%. Regardless of the type and microbial population, they influence the plant in three ways; good (beneficial), neutral, and pathogenic. Few microbes have the ability to encourage plant growth and they do so in many ways which include free living, associative, nodulating, and endophytic microbes (Glick 2012). Plant growth promoting microbes and their features are as follows:

9.4.1

Pseudomonas Species

These microbial species produce cytokine, auxin, and ACC deaminase helps in phosphate solubilization, fix nitrogen in symbiotic relationships, produce siderophores (García de Salome et al. 2001; Kamilova et al. 2006a, b; Glick et al. 2007; Rodriguez et al. 2006; Dobbelaere et al. 2003; Lemanceau et al. 2009). Malik and Sindhu (2011) reported the IAA production by Pseudomonas sp. and their effect on chickpea. Inoculation of chickpea with IAA producing Pseudomonas sp. and Mesorhizobium sp. enhanced the shoot and root dry weight as compared to the control. The results were comparable with application of only exogenous IAA. Similarly, ACC deaminase production by many bacteria leads to mitigation of ethylene stress. This enzyme breaks down plant ethylene precursor ACC into α-ketobutyrate and ammonia (Glick 2014) thus preventing the plant from negative effects of ethylene.

9.4.2

Arbuscular Mycorrhizal Fungi (AMF)

These are mycorrhiza in which the symbiont fungus associate with vascular plants by penetrating the cortical cells of their roots and thereby forming arbuscules. Here, mycorrhiza helper bacteria encourage the growth of fungus during pre-symbiotic

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survival phase; AMF secretes Myc factors which stimulates growth of roots and provide safety against different biotic and abiotic stresses and also improve the soil structure; they enhance the uptake of zinc, copper, water, phosphorus and other essential nutrients (Frey-Klett et al. 2007; Maillet et al. 2011; Smith and Read 2008; Clark and Zeto 2000).

9.4.3

Bacillus Species

These bacteria are actively involved in nitrogen fixation and also play a key role in potassium and phosphate solubilization (Idriss et al. 2002; Borriss 2011; Wu et al. 2005; Rodriguez et al. 2006). Among the numerous plant growth promoting rhizobacetrial organisms, Bacillus is widely researched and most comprehensively experimented rhizobacteria that augment the host plant development and growth. There are several studies which have been reported with numerous Bacillus strains, such as B. subtilis, B. pumilis, B. amyloliquifaciens, B. megaterium, B. licheniformis, etc. These are all famous and eminent rhizosphere inhabitants of several crops that exhibit many plant growth-promoting attributes (Tiwari et al. 2019).

9.4.4

Trichoderma Species

These microbes stimulate the production of auxins, degrade the compounds of phenolic nature released by plants, may become an endophyte, enhance the uptake of water and nutrients, help in solubilization of soil nutrients, promote efficient utilization of nitrogen by plant and increase their vigor and vitality, encourage the growth of roots and other plant organs, help in the formation of root hairs, improve the plant’s photosynthetic capacity, they accelerate the germination of seeds, produce secondary metabolites like harzianic acid which encourage plant growth, helps to deal with abiotic stresses, and increase resistance capacity of plants, especially during unsuitable growing conditions (Contreras-Cornejo et al. 2009; Ruocco et al. 2009; Hermosa et al. 2012; Harman 2006; Shoresh et al. 2010; Lorito et al. 2010; Mastouri et al. 2010; Vinale et al. 2009). The chitinolytic system of Trichoderma harzianum consists of five to seven different enzymes (vary from strain to strain) and these enzymes help in killing the pathogenic fungi (Haran et al. 1995). In another study conducted by de Paula et al. (2001), T. harzianum safeguarded the seedlings of bean against preemergence damping-off infection caused by Rhizoctonia solani pathogen, resulting in better growth of bean plants.

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Microbiome as Biofertilizers

Biofertilizers are the substance which contains microorganisms (living or latent cells) which encourage the plant growth. Majority of these microbes have the abilities of phosphate solubilization, N2 fixation, and siderophores production. The main function of biofertilization is to encourage the nutrient availability to plants by fixing the atmospheric nitrogen and phosphate solubilization (Richardson and Simpson 2011). Figure 9.2 depicts the role of a commonly applied biofertilizer or bioinoculant.

9.5.1

Nitrogen Fixation

Nitrogen (N) is the element which is abundantly present in the earth’s ecosystem, but plants do not have the ability to utilize this freely available nitrogen directly. Plants only assimilate nitrogen if it is available in the form of nitrate ions or ammonium. Biological nitrogen fixation, carried out by biological nitrogen fixers or diazotrophs, applies to the transformation of freely available atmospheric nitrogen into ammonium ions. Unicellular organisms or prokaryotes have the terrific potential to fix freely available environmental nitrogen (Dekas et al. 2009). These microbes, mostly bacteria, possess capabilities to form symbiotic relationships with the plants. The formation of nodules in legume-rhizobium synergism is the mostly studied example

Fig. 9.2 Role of a bioinoculant as plant growth promoter

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which explains this relationship precisely. Nodule formation mainly by Rhizobia commonly takes place in leguminous plants, but in a very rare case can take place in the genus Parasponia belonging to the family of Rosales (Markmann and Parniske 2009). Majority of nitrogen fixation in the atmosphere takes place due to this synergism between plants and microbes. According to several reports, higher than 45 million metric tons of nitrogen fixation per year is delivered by this synergism between legumes and Rhizobium species in various terrestrial ecosystems (Vance 2001). It was also reported by Hurek et al. in 2002 that an endophytic, diazotrophic bacteria belonging to Azoarcus species, shows their desirable or valuable effects and have a potential to fix atmospheric nitrogen. A similar condition is observed in Acetobactor diazotrophicus with sugarcane (Sevilla et al. 2001).

9.5.2

Phosphate Solubilization

Next to water and nitrogen, phosphorus (P) is the third chief essential compound, as it plays a pivotal role in several metabolic pathways in plant systems. These include but are not limited to nucleic acid synthesis pathways, in respiration, photosynthetic pathways, energy generation, and cell signaling (Vance et al. 2003). Dihydrogen phosphate (H2PO4 ) and Hydrogen phosphate (HPO42 ) ions are the only forms of phosphorus which can be utilized by plants. Further, although soils have adequate phosphorus content in it, which is required for development, it is mostly in an insoluble form, so plants are not able to utilize it. Moreover, when phosphorus is given by the application of chemically synthesized fertilizers, it gets quickly transformed into an insoluble form and as a result becomes unavailable for plant utilization (Rodriguez and Frago 1999; Igual et al. 2001; Smyth 2011). A lesser availability of phosphorus in soil leads to acidification of the rhizospheric zone, which results in the release of organic anions—specifically oxalates, citrates— combined with protons. Hence the phosphorus is then served for mobilization, i.e., microorganisms improve the capabilities of plants to take phosphorus from soil (Richardson et al. 2009). There are certain microbes (particularly bacteria) which facilitate the solubilization of phosphate thus making it available for the plant’s uptake. These microbes or bacteria are popularly known as phosphorus solubilizing bacteria (PSB) (Igual et al. 2001; Kim et al. 1998; Lipton et al. 1987). Mineralized phosphate acts as a main factor for the liberation of phosphates by the formation of organic acids (Rodriguez et al. 2006). Vyas and Gulati in 2009 reported that several species of Pseudomonas, which have a crucial role in soil phosphate solubilization, also have the ability of encouraging parameters required for essential growth together with phosphorus concentration in most of the maize plants. It was reported by Sundara et al. in 2000 at crop yield, together with phosphorus content in sugarcane plants were improved by Bacillus megaterium. Several Bacillus species which have an essential role in phosphorus solubilization were also found to increase the crop yield in canola by their utilization (Minaxi et al. 2012).

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249

Siderophore Production

Another essential element required for the sustenance of plants is iron (Fe), as it plays a crucial role in photosynthesis, which results in the formation of chlorophyll and transport of oxygen in the entire plant body. It is present abundantly in the crust of earth but in a majority of the cases, it is found in an insoluble form, as a result plants are unable to utilize it. As a response to this, secretion of siderophores through plants takes place, where siderophores act as metal chelators. In siderophores it is observed that they bind with Fe3+ ions and then transport it to the root surface, where it then gets reduced to Fe2+ ions, which can be easily utilized by plants. Fe3+ bounded with siderophores can also be used by plants in the form of Fe3+ ion-siderophore complexes (Lemanceau et al. 2009). In reduced Fe3+ ion concentrations, various bacteria have the ability to produce distinct types of siderophores. Majority of these siderophores bind with Fe3+ ions by a very high-affinity bond. By absorption, plants can easily assimilate these bacterial Fe3+ ion-siderophore complexes. But the significance of this uptake is still unknown (Zhang et al. 2008). Pseudomonas aeruginosa strain FP6 produced siderophore and also inhibited the growth of R. solani and Colletotrichum sp. under laboratory conditions (Sasirekha and Srividya 2016). This bacterium resulted in controlling disease on chili plants. Kesaulya et al. (2018) demonstrated the potential of Bacillus sp. in wilt disease suppression of banana plants. The Bacillus sp. was able to produce siderophores which resulted in controlling banana wilt disease.

9.6

Biofertilizer Status in India

In India, the total requirement of different types of bioinoculants/biofertilizers that are needed for seed treatment or as root inoculant as well as soil treatment is estimated to be approximately up to 0.426 million ton. This figure is based on the net cultivated area. The Indian government is encouraging and promoting biofertilizers through numerous schemes which include National Mission for Sustainable Agriculture (NMSA), Rashtriya Krishi Vikas Yojana (RKVY), and Paramparagat Krishi Vikas Yojana (PKVY). Several agricultural universities and agricultural institutions are also involved in the development and production of different types of bioinoculants (Singh et al. 2014a, b). Table 9.1 shows some of the Indian companies involved in biofertilizer production or supply.

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Table 9.1 Manufacturer or supplier of biofertilizers in India (Source, website of the company) S. no 1.

Company A. B. Enterprises Mumbai, India

2

Aspire Speciality Chemicals Vapi, India

3

Vanashree Agriculture Pvt. Ltd., Pune, India

4

SUBONEYO Chemicals Pharmaceuticals Pvt. Ltd, Jalgaon, India

5

Ecomatrix Nutrients Pvt. Ltd. Dewas, India

6

Sanghvi Quality Products Pvt. Ltd. Nashik, India

7

Manidharma Biotech Pvt. Ltd., Chennai, India

Products • 3-hydroxyacetophenone • Magnesium bisglycinate, • Anthranilamide derivatives • Aromatic amines • Biofertilizers such as seaweed extracts, axbo G, natural humic acid • Seaweed fertilizer • NPK fertilizers • Micronutrient fertilizers • Humic acid fertilizer • Bio organic manure • Organic neem (Azadirachta indica) biofertilizer • Liquid fertilizer • Vermiculture fertilizer • Microbial organic fertilizers • Deal in Jatropha seeds, neem products, crude herbs, stevia herbs, biofuel oils • Biofertilizers—seaweed extracts, vegetable origin, animal origin, • Organic biofertilizers • Amino acid-based biofertilizers—available in powder and liquid form • Biofertilizer from Rhizobium, Azotobacter, Azospirillum • Brassinolide (from Brassica napus) biofertilizers • Bio-bacterial fertilizers— Ecobium • Organic biofertilizers • Biostimulation fertilizers • Cell wall development fertilizers • Humic acid fertilizers • Phosphate fertilizers • Azospirillum biofertilizer • Phosphorus biofertilizer • Rhizobium biofertlizer • Also offering Beauveria bassiana (as biocontrol agent against insects), Pecilomyces lilacinus, Metarhizium anisopliae

Manufacturer/ exported Manufacturer and exporter

Manufacturer and trader

Exporter and supplier

Manufacturer and supplier

Manufacturer and supplier

Supplier and manufacturer

Manufacturer and supplier

(continued)

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Table 9.1 (continued) S. no 8

Company Richfield Fertilisers Pvt. Ltd., Nashik, India

9

Karpan Technochem International Navi Mumbai, India

10

Maharashtra Biofertilizers India Pvt. Ltd. Maharashtra, India

11

National Agricultural Cooperative Marketing Federation of India Ltd. (NAFED), Indore, India Indian Farmers Fertiliser Cooperative Ltd., (IFFCO), IFFCO Sadan, New Delhi, India

12

13

National Fertilizers Ltd., Noida, India

14

Varsha Bioscience and Technology Pvt. Ltd. (VBT), Telangana, India

15

Agri Life SOM Phytopharma (India) Ltd., Hyderabad, India

16

Planet Biotech India, D-104, Krishna Park, Gujarat, India

Products • Pure biofertilizers • Nitrogen supplying biofertilizers • Biofertilizers • Amino acid chelates • Virus eliminator organic fertilizer • Bio repellant • Organic liquid fertilizer • Plant growth promoter liquid • Organic certified fertilizers • Biofertilizers • Organic pesticides • Manure and sulfur fertilizer • Biofertilizer • Bio-agri-inputs • Nitrogen fixing biofertilizers (Rhizobium, Azotobacter, Acetobacter) • Phosphate Solubilizing Bacteria (PSB) for phosphorus • Potassium Mobilizing Biofertilizer (KMB) • Zinc Solubilizing Biofertilizer (ZSB) • NPK liquid consortia • Biofertilizers-Rhizobium • Phosphate Solubilizing Bacteria (PSB) • Azotobactor • Biocontrol agents— biofertilizers, biopesticides, biofungicides, bio-insecticides, biochemicals, bio-nematicides • Plant growth regulators • Bio solutions for crops and soils • Agri Life manufactures • Biopesticides • Biofertilizers • Biostimulants and other Agri inputs • Biofertilizer • Biopesticide • Bio-organic plant growth promoters • Animal Probiotics-Feed supplements and Enzymes

Manufacturer/ exported Supplier and exporter Manufacturer and exporter

Manufacturer, distributor, and exporter Manufacturer

Manufacturer

Manufacturer and marketer

Manufacturer

Manufacturer

Manufacturer

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9.7

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Concluding Remarks and Future Prospects

Plants and rhizopheric microflora interactions in the ecosystem depends upon the very precise companionship between both the partners. The studies on some of these alliances or mutual relationships, such as interactions between Rhizobium and leguminous plants, have confirmed that these partnerships between microbes and plants show high levels of specificity with respect to the host. Further, there are studies which suggest that the association between the microbes and plants exhibit high specification, with nonrelated species of plants, and even in these nonrelated distinct cultivars of the same species of plants. This leads to the establishment of a nonrelated and different population of microbes in their respective rhizospheric zones when they are propagated in the same soil. Establishment of these groups, associations, or alliances rely on, or at least partially rely on the precise and explicit activation programs of gene expression or outcomes of microbes with respect to the chemical signals liberated from plants. The most common example is the induction of genes responsible for nodulation in rhizobia, which are triggered by the production and liberation of particular flavonoids by the plants in any kind of ecosystem. In the rhizobium–legume interaction, bacteria produce certain kinds of chemical signal to which plants respond; this type of exchange of chemical signals is very distinct and characteristic feature of other plant–microbe interactions. The human population on earth will be doubled by the year 2033. Therefore, the demand for food in the Asian continent will exceed the food supply. This creates a burden on the present agricultural practices. Traditional methods employed for farming are not able to meet the growing demand and are thus found to be insufficient. As countries progress, the population’s demands for nutritionally fresh, rich, and good foods also increase. These demands are creating pressure on present agriculture procedures, which are themselves under the pressure of reduced availability of land for farming, exceeding charges for labor, and reduced interest of people towards farming. Use of microbiological tools via microbes can help to create a sustainable approach to improve the yield and high productivity, in terms of quality and quantity of the agricultural products. Microbe–plant-based strategies have enormous advantages such as helping to prevent crops from pests and enhance crop yield by lowering the use of chemical pesticides which is usually utilized by most farmers. Microbial technology used for the processing of food stuffs and food constituents, provide a wide variety of fermented food goods and products which are widely utilized by the consumers. During the “green revolution” in the twentieth era microbial systems were used effectively in agriculture to produce healthy and safe food with reduced investment of money. Thorough and comprehensive approaches are required for the utilization of valuable microbes for crop improvement and production is a very crucial step towards the development of sustainable agricultural practices. Similarly, technology based on microbial system and their use in the development of sustainable agriculture approaches and safe environmental practices are getting positive responses. The main focus of this chapter was to shed light to scientific groups, students, and researchers on the value and impact as well as the immense potential of microbes in agriculture.

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Chapter 10

Diversity, Function, and Application of Fungal Iron Chelators (Siderophores) for Integrated Disease Management Umesh Dhuldhaj and Urja Pandya

Abstract Plants are an important source of energy, minerals, and nutrients for human beings. Several micro- and macronutrients are necessary for growth and development; among these iron is a vital element. Iron is not freely available in the earth’s crust and is present in the insoluble forms such as ores, minerals of oxides, sulfate, etc. Hence, plants face problems in the uptake of iron from the rhizospheres. The microbes harboring rhizospheres produces special compounds known as “siderophores” or “siderochromes”, which chelate the iron and make it available to the plants. Microbes living inside (Endophytes) and outside (Saprophytes) of the plants can produce siderophores such as fungi (Mycorrhiza, etc.). In this chapter, we focus on the production of siderophores from fungi and their significance in crop yield and disease management. Siderophores play a major role in the maintenance of ecological balance by plant growth promotion, production of phytohormones, and by maintaining soil health. Keywords Iron · Fungi · Rhizobacteria · Siderophores

10.1

Introduction

Fungi are important plant pathogens causing pre- and post-harvest diseases to crop plants and can affect the total crop yields (Fisher et al. 2016). Other than causing diseases some fungi such as Trichoderma have antagonistic activity to compensate the growth of pathogens. These types of fungi as well as some groups of bacteria help in plant growth promotions by secreting essential secondary metabolites U. Dhuldhaj School of Life Sciences, Swami Ramanand Teerth Marathwada University, Nanded, Maharashtra, India U. Pandya (*) Department of Microbiology, Gujarat Vidyapith, Sadra, Gandhinagar, Gujarat, India e-mail: [email protected] © The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2021 G. Seneviratne, J. S. Zavahir (eds.), Role of Microbial Communities for Sustainability, Microorganisms for Sustainability 29, https://doi.org/10.1007/978-981-15-9912-5_10

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(siderophores), enhancing nutrient uptake, and assisting in disease management (O’Sullivan and O’Gara 1992). The mechanism adapted by the fungal species for nutrient uptake is by extension of their hyphal filaments. Siderophores or siderochromes are special compounds secreted by fungal species in the rhizosphere and which have the ability to chelate iron (Fe) and make it available to the plant. They are important for the plant in the accumulation and uptake of iron along with other nutrients (Pandya and Saraf 2010a). These small, iron-chelating compounds rank as some of the strongest soluble iron-binding agents studied. Despite its abundance, iron can be limited in its availability to plants due to the low solubility of the Fe3+ ion. This has major consequences to plants as iron is an essential element in most life processes. The mechanism of the uptake and accumulation of iron is that the siderophores chelates and tightly binds to iron present in the rhizosphere and brings it back into the cell. Fungi are the strong producers of a variety of siderophores, which help them to survive in extreme conditions such as high metal toxicity, scarcity of iron content in the rhizosphere and contaminated soils. Microbes secreting siderophores induce plant growth by increasing iron content in the rhizosphere and depriving plant pathogens (Winkelmann 2007; Pandya and Saraf 2013; Saraf et al. 2014). The microbial system secreting siderophores have a high affinity for iron, and hence by the competitive inhibition of plant pathogens (with less efficient iron uptake system) supplies nutrient (especially Fe) to the crop plants as is seen with Fusarium (Rajkumar and Freitas 2009).

10.2

Importance of Iron to the Crop Plants

Iron is a highly abundant element in the earth’s crust yet with less bioavailability to plants (Patrik et al. 2017). It is one of the main growth-limiting nutrients necessary for the adequate growth of plants. Iron has a vital role in plant metabolism and is involved in several processes including the tricarboxylic acid cycle (TCA), electron transport system (ETS), photosynthesis, and respiration, all of which are vital to increase plant growth (Winkelmann 2007; Messenger and Barclay 1983; Fardeau et al. 2011). It acts as the cofactor and helps in the biosynthesis of nucleic acid, organic compounds (Porphyrins and aromatic compounds, toxins), necessary pigments, siderophores, vitamins, hormones, antibiotics, etc. (Messenger and Barclay 1983). Because of the less bioavailability of iron to the farm fields, some plants tend to secrete phytosiderophores (e.g., Grasses) similar to how microbes secrete siderophores (e.g., Trichoderma), to chelate iron and bring it back to cellular systems to thereby conduct vital cellular processes. Phytosiderophores and siderophores have a high affinity for the iron and increase its uptake into the plant system (Takagi 1976; Mino et al. 1983; Marschner and Kissel 1986; Neilands 1995; Kannahi and Senbagam 2014; Pandya and Dhuldhaj 2017).

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Diversity, Function, and Application of Fungal Iron Chelators (Siderophores). . .

10.3

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Siderophores

These are the low molecular weight compounds (5) the production of VFA is increased whereas more ethanol is produced at lower pH (Batstone et al. 2002; Boe et al. 2010). Fermenting bacteria recovered from anaerobic digestion of piggery waste were mostly affiliated with Firmicutes and Bacteroidetes. Taxa affiliated with these phyla are very metabolically versatile. For example, Clostridium and Porphyromonadaceae degrade glucose (Hsiao et al. 2009; Li et al. 2009); Lactobacillus ferments lactose (Cotta et al. 2003; Ward et al. 2008), Caloramator viterbensis ferments glycerol (Seyfried et al. 2002) and Anaerobaculum ferment peptides (Menes and Muxi 2002). Acidogenesis optimally takes place under mesophilic conditions and at pH 5–6 but fermenting bacteria are fairly tolerant to prevailing environmental conditions (Tang et al. 2008; Lu et al. 2009). They are fast growers (Pavlostathis and Giraldogomez 1991; Batstone et al. 2002; Martinez et al. 2009) and their growth is enhanced by acidic feedstocks, high in soluble sugars, lipids and proteins (Cokgor et al. 2008; Wang et al. 2008). Fermenting bacteria need to be managed carefully because accumulation of their end-products could lead to acidification, inhibition of methanogenesis and possibly even system failure if not rectified quickly (Vavilin et al. 1996; Batstone et al. 2002; Cokgor et al. 2008; Weiland et al. 2009). For this reason, care must be taken to avoid overloading of CAPs that would promote their proliferation (Park and Craggs 2007; Heubeck and Craggs 2010).

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11.3.4 Acetogenesis and Syntrophy Acetogenesis is the third stage, where the VFAs and alcohols are converted into acetate, H2 and CO2 by acetogens (Mata-Alvarez et al. 2000). This stage is crucial for the AD performance since these intermediate compounds cannot be directly used by methanogens (Batstone et al. 2002) and their degradation is thermodynamically unfavourable unless the partial pressure of H2 is maintained at low levels (Batstone et al. 2002; Müller et al. 2011). Consequently, H2-producing acetogens require the cooperation of a second H2-consuming microorganism, usually a methanogen or sulphate reducer (Chauhan and Ogram 2006). This interspecies hydrogen transfer between acetogens (H2 source) to methanogens (H2 sink) is described as a syntrophic relationship and allows the digestion process to continue (Dong et al. 1994). Syntrophy means ‘living together’ where two metabolically distinct microbial groups coexist to degrade a particular substrate (Müller et al. 2011) allowing them to overcome the unfavourable energetics of the reaction (Ike et al. 2010; Müller et al. 2011). A wide range of intermediate compounds including alcohols and VFAs can be oxidised by these bacterial specialists and their syntrophic partner (Chauhan and Ogram 2006; Lykidis et al. 2011; Müller et al. 2011). For example, Syntrophomonadaceae bacteria degrade long-chain fatty acid (LCFA), butyrate and propionate by growing syntrophically with different hydrogen-scavenging partners (Dong et al. 1994; Sousa et al. 2007; Sieber et al. 2010; Müller et al. 2011). The capacity for LCFA degradation is quite widespread including bacterial representatives from Firmicutes, Bacteriodetes and Thermotoga (Chauhan and Ogram 2006; Hatamoto et al. 2007a, b, 2008). Pelotomaculum and Desulfotomaculum syntrophically degrade propionate in syntrophic association with methanogen such as Methanothermobacter thermautotrophicus (Lueders et al. 2004; Ishii et al. 2005; Moser et al. 2005; Imachi et al. 2006; Müller et al. 2011). Due to the high protein and fat content in piggery waste, fermentation is likely to produce a variety of intermediates implying that syntrophy could play an important role during digestion (Medri et al. 2007; Talbot et al. 2010). However, these syntrophic partnerships (e.g., acetogen and methanogen) are slow-growing and sensitive to high organic loading rates and environmental changes such as pH, temperature and toxicity (Chauhan and Ogram 2006; Müller et al. 2011).

11.3.5 Methanogenesis Methanogenesis is the final stage of anaerobic digestion where methanogens produce CH4 and CO2 (Evans et al. 2010; Mata-Alvarez et al. 2010). Being the major microbial group responsible for methane production, it is imperative that their activity is maintained for biogas production. Methanogens are slow-growing specialists that are very sensitive to changes in VFAs and NH3 concentration, pH

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(optimum pH of 6.5–7.5) and temperature (Mata-Alvarez et al. 2000; Evans et al. 2010). Consequently, methanogenesis is considered to be another rate-limiting step in the AD process especially in the treatment of N-rich effluents like piggery waste (Mata-Alvarez et al. 2000; Demirel and Scherer 2008). There has been only a relatively limited number of studies which have conducted 16S RNA gene cloning-based analysis of the microbial community involved in AD. Of the 16S rRNA gene clones conducted microbes retrieved from the (mosty methanogenic) sludge mainly included those from Deltaproteobacteria, Chloroflexi, Firmicutes, Spirochaetes, Bacteroidetes, Methanomicrobia, Methanobacteria and Thermoplasmata (Narihiro and Sekiguchi 2007). Despite the increase in the discovery and number of new anaerobes involved in AD, culturing microorganisms which are resistant or recalcitrant to artificial cultivation remains a hurdle. The difficulties associated with such cultivation is overcome by techniques such as microautoradiography fluorescence in situ hybridisation (MAR–FISH), DNA-based stable isotope probing (SIP) and RNA-SIP (Hatamoto et al. 2007a, b). In AD, methane is formed via two methanogenic pathways namely the acetoclastic and hydrogenotrophic methanogenesis. Acetoclastic methanogenesis is the most common pathway and involves the cleavage of acetate to CH4 and CO2 (Demirel and Scherer 2008). Acetoclastic methanogens are restricted to just two genera Methanosaeta and Methanosarcina. Of these, Methanosaeta with its higher affinity for acetate tends to dominate in most AD systems accounting for approximately 70% of methane produced (Karakashev et al. 2006). However, Methanosaeta are very susceptible to inhibition at high concentrations of VFAs and ammonia and extremes of pH and temperature (Karakashev et al. 2006; Lu et al. 2009). Methanosarcina has a higher maximum growth rate but a lower affinity for acetate (McMahon et al. 2001; Leven et al. 2007). Furthermore, they are more metabolically diverse and can use either methanogenic pathway depending upon the availability of the substrates H2, CO2, methanol, methylamine and acetate (Sonakya et al. 2007; Vavilin 2010) but they generally prefer the acetoclastic pathway. Temperature plays an important role in methanogenesis as the optimum temperature varies for methanogenic bacteria. Methanogens in this rate-limiting stage of AD thus exist as mesophilic bacteria (Methanobacterium bryantii, Methanosarcina barkeri and Methanococcus vannielii) and thermophilic bacteria (Methanosarcina thermophila and Methanosaeta thermophila) (Li et al. 2019). Alternatively, methane is produced by hydrogenotrophic methanogens via a two-step reaction in which acetate is first oxidised to H2 (electron donor) and CO2 (electron acceptor) and then converted to methane (Zinder and Koch 1984; Schnürer et al. 1997; Karakashev et al. 2006). This reaction is performed by acetate-oxidising bacteria (e.g. Clostridium ultunense, Thermacetogenium phaeum and Thermotoga lettingae) in syntrophic association with hydrogenotrophs (Schnürer et al. 1997; Hattori et al. 2000; Hattori 2008; Liu and Conrad 2010). The hydrogenotrophs include the families Methanobacteriaceae, Methanothermaceae, Methanocaldococcaceae and Methanococcaceae (Demirel and Scherer 2008). In general, acetoclastic methanogenesis (Eq. 11.3) is more thermodynamically favourable than the hydrogenotrophic methanogenesis (Eq. 11.2) pathway (Schnürer

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et al. 1999; Karakashev et al. 2006; Boe et al. 2010). However, syntrophic acetate oxidation tends to dominate at higher temperatures (>30  C) in thermophilic digesters (Karakashev et al. 2006; Hao et al. 2011). Hydrogenotrophs are also able to tolerate the presence of inhibitors, particularly ammonia and VFAs (Schink 1997; Ishii et al. 2005; Müller et al. 2011) which is typical of animal waste effluents (Estrada and Hernandez 2002; Medri et al. 2007; Park and Craggs 2007) and during the initial acclimatisation phase of AD (Charles et al. 2009). Thus, hydrogenotrophs may have a fundamental role in supporting the acetoclastic methanogens by preventing accumulation of VFA and hydrogen (Schink 1997; Demirel and Scherer 2008). In fact, recent work has suggested that hydrogenotrophs might be the predominant methanogenic pathway during anaerobic digestion of piggery effluent in CAPs (Talbot et al. 2010; Whiteley et al. 2012; Jenkins 2013). In light of these new findings, the AD models and management guidelines for digesters might need to be revised for CAPs treating animal wastes to include the contribution of hydrogenotrophs. Hydrogenotrophic pathway : CO2 þ 4H2 ! CH4 þ 2H2 O ΔG0 ¼
131 kJ=mol

ð11:2Þ

Acetoclastic pathway : CH3 COOH ! CH4 þ CO2 ΔG0 ¼
30 kJ=mol

ð11:3Þ

Equations 11.2 and 11.3. Acetoclastic methanogenesis is more thermodynamically favourable than the hydrogenotrophic methanogenesis (Adapted from Schink 1997).

11.3.6 Microbial Community Dynamics Within a CAP Recently, polymerase chain reaction (PCR) based analysis of genes (e.g. 16S rRNA) and shotgun metagenomic approaches were used to access temporal and spatial changes in microbial diversity and function within the CAP system (Whiteley et al. 2012; Weerasekara 2015). The CAP is part of the waste treatment process at a piggery in Western Australia that involves five consecutive stages; collection pits in the pig shed, solid separation screens, holding tank, the CAP, and finally a secondary evaporation pond (Weerasekara 2015). The results show that after an initial period of acclimatisation (following pond covering), the microbial community become both temporally and spatially stable. The microbial community was also found to be highly resilient being able to tolerate a range of temperatures, loading rates, feed additions and substrate quality. The microbial communities within the CAP, pits and holding tank (Fig. 11.3) were dominated by the bacterial taxa Clostridia, Synergistia and Bacteroidia, which in turn supported a consortium of syntrophic bacteria and methanogens (Whiteley

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Fig. 11.3 Spatial changes in bacterial composition at different stages of the piggery waste treatment system (Weerasekara 2015)

et al. 2012; Weerasekara 2015). These taxa are metabolically versatile (Müller et al. 2011) and resilient to perturbation, periods of starvation and environmental fluctuations (Tang et al. 2011; Kampmann et al. 2012), which probably accounts for their temporal stability in CAPs. They are often isolated from piggery waste treatment systems (Cook et al. 2010; Patil et al. 2010; Talbot et al. 2010) and other anaerobic digesters (Riviere et al. 2009; Supaphol et al. 2011; Tang et al. 2011; Kampmann et al. 2012) where they are reported to participate in one or more stages of the AD process. For example, Clostridia play a significant role in cellulose degradation whilst members of the Bacteriodia degrade a range of organic substrates (Wirth et al. 2012) making them a good candidate for ‘indicator’ taxa. In contrast, Actinobacteria and Betaproteobacteria predominated in the evaporation pond, which is consistent with other findings and probably reflects the underlying aerobic conditions and low organic matter content (Ben-Dov et al. 2008). Hydrogenotrophic methanogenesis was the dominant methanogenic pathway in the CAP and this is consistent with other anaerobic digestion systems treating piggery waste (Kim et al. 2010; Patil et al. 2010; Talbot et al. 2010). Species within the Methanocorpusculaceae, Methanobacteriales and Methanomicrobiales, that produce methane from H2/CO2 and formate, prevailed throughout the sampling period. A large number of syntrophic bacteria were recovered from the CAP, in particular, the butyrate oxidising bacteria Syntrophus sp. and Syntrophomonas (Müller et al. 2011). These fatty acid degraders can only grow syntrophically in partnership with hydrogenotrophic methanogens (Müller et al. 2011) and their presence suggests an accumulation of butyrate in the CAP during the summer. The

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information gained so far can now be used to identify management practices that enhance biogas recovery and conditions that induce system failure.

11.4

Factors Affecting Anaerobic Digestion

The prospect of an on-farm bioenergy resource is a very attractive option for farmers and a number of studies have shown that biogas production from CAPs is economically feasible (Craggs et al. 2008; Birchall 2009; Heubeck and Craggs 2010; Skerman et al. 2011). However, biogas recovery from CAPs is low when compared to other AD technologies, such as an anaerobic sequencing blanket, continuous stirred tank reactor, and upflow anaerobic sludge blanket reactors (Ward et al. 2008; Amani et al. 2010; Evans et al. 2010; Mata-Alvarez et al. 2010). To date, CAP studies have focussed largely on pond design and consequently, key parameters and microbial activities governing waste degradation and biogas production have been largely overlooked. This must be addressed to improve the efficiency of biogas capture from CAPs. The rate of AD and the amount of biogas generated depends largely on the source of effluent used in CAPs. A study on pigs of four different growth stages showed variations in methane production rates and VFA/TIC rates, which was mainly due to the feed strategy and nutrient digestibility of the different growth stages. For example, manure of post-weaned piglets gave a 28.2% and 32.1% higher methane production rate than gestating sow manure and growing fattening pig manure, respectively (Zhang et al. 2014). Previous research has shown that AD efficiency and stability is dependent on critical indicators such as waste feed type, bioreactor design, temperature, pH, free ammonia concentration, organic loading rate (OLR), process stages (one step or two step), carbon and nitrogen ratio (C:N), hydraulic retention time (HRT) or solid retention time (SRT), the presence of inhibitory substrates and the effect of pretreatment and storage (Chae et al. 2008; Chen et al. 2008; Ward et al. 2008; Weiland et al. 2009; Amani et al. 2010; Boe et al. 2010; Comino et al. 2010; Vavilin 2010). These parameters can be divided as dependent (such as pH and free ammonia concentration) and independent (temperature, C:N ratio, HRT, OLR, etc.) indicators. The most important of these parameters and their roles are discussed below.

11.4.1 Temperature CAPs are not heated and operate at ambient temperature, which means seasonal variations in temperature affect both the degradation rate and biogas yield (Heubeck and Craggs 2010). For every 10  C rise in temperature, the reaction rate doubles with a corresponding increase in biogas yield (van Lier et al. 1997; Boe et al. 2010). For example, the anaerobic digestion of pig manure at 35  C produced 17.4% more biogas compared to AD operating at 25  C (Chae et al. 2008). Anaerobic digesters

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can operate under psychrophilic (