Freshwater Microbiology: Perspectives of Bacterial Dynamics in Lake Ecosystems 0128174951, 9780128174951

Table of contents :
Cover
FRESHWATER MICROBIOLOGY
Copyright
List of contributors
Preface
Acknowledgments
1 - Bacterial community composition in lakes
Introduction
Historical perspective of lake bacterial communities
Study of bacteria in lake environments; why is it so important?
Bacterial biogeography in lakes
Biodiversity and abundance of bacteria from freshwater lakes
Bacterial alpha diversity
Bacterial beta diversity
Bacterial abundances and spatial patterns
Bacterial population dynamics
Diversity-productivity relationship in freshwater bacterial communities
Microbial dormancy
Influence of habitat heterogeneity and submerged macrophytes on bacterial community composition in freshwater lakes
Habitat heterogeneity
Submerged macrophytes
Top-down and bottom-up induced shifts in bacterial abundance production and community composition
Zooplankton and aquatic bacterial linkages in freshwater lakes
Bacterial community resistance and resilience in lakes
Novel bacteria from freshwater lake ecosystems
Case studies of bacterial community of lake ecosystems
Lake Baikal, Russia
Dianchi Lake, China
Lake Tanganyika, Africa
Yunnan Plateau, China
Chandra Tal and Dashair Lake, India
Manasbal Lake, India
Dal Lake, India
Gurudongmar Lake, India
Comparative study of some freshwater lakes in India
Conclusions
Acknowledgments
References
2 - Bacterial diversity of the rock-water interface in freshwater ecosystem
Introduction
Sessile bacteria
Attachment of freshwater bacteria to solid surfaces
Microbial epilithic and endolithic biofilms
Microbial dynamics of epilithic mat communities
Role of epilithic and endolithic microbes
Colonization pattern of bacterial communities in endolithic habitats
Epilithic bacteria and mineral formation
Chemolithotrophic microbial mats on subsurface rocks
Microbial life in deep granitic rocks
Identification of lithic bacteria
Effect of different factors on bacterial attachment to submerged rock surfaces
Case study
Bacterial diversity of rock-water interface in Lake Tawani
Hydrobionts at the water-rock interface in Lake Baikal
Microorganisms in deep igneous rock aquifers of Finland
Conclusions
References
3 - Impact of environmental changes and human activities on bacterial diversity of lakes
Introduction
Sources of bacteria in lake water
Association of lake bacterial diversity with changing environmental features
Temperature
Hydrogen ion concentration (pH)
Salinity
Total dissolved solids
Dissolved oxygen
Alkalinity
Nitrogen and phosphorus
Biological oxygen demand
Chemical oxygen demand
Human activities and lake bacterial diversity
Climatic variables and lake bacterial diversity
Socioeconomic factors and lake bacterial diversity
Fecal contamination of surface waters
Advances in aquatic microbial detection and quantification
Conclusions
References
4 - Spatio-temporal patterns of bacterial diversity along environmental gradients and bacterial attachment to organic aggregates
Introduction
Spatio-temporal distribution of microbial communities
Drivers of microbial communities in lakes
Lake bacterial assemblages along the altitudinal gradient
Lake bacterial assemblages along the latitudinal gradient
Lake bacterial assemblages along the urban water quality gradient
Lake bacterial assemblages and microcystis decomposition
Effect of grazers on bacterial community structure and production in trophic lakes
Diversity-functioning relationships in lake bacterial communities
Environmental heterogeneity and diversity-functioning relationship
Organic aggregates in surface water bodies
Structural composition of aggregate-associated bacterial communities
Diversity of organic aggregate–attached bacteria in lakes
Organic aggregate–associated bacterial communities in deep lakes
Organic aggregate–associated bacterial communities in shallow eutrophic lakes
Abundance of organic aggregate–attached bacteria in lakes
Growth efficiency of organic aggregate–associated bacteria
Aggregate-associated organic matter and bacterial turnover
Ecological significance of organic aggregate–attached bacteria
Conclusions
References
5 - Metagenomic insights into the diversity and functions of microbial assemblages in lakes
Introduction
Metagenomics: historical perspectives
Sequencing technologies
Metagenomics of freshwater lakes—basic steps (Fig. 5.1)
Sample collection and preparation
DNA extraction
Amplification and sequencing
Bioinformatics
Assembly
Phylogenetic binning
Metagenome gene prediction and functional annotation
Metagenomic data sharing, storage, and management
Freshwater lakes metagenomic studies
Freshwater lakes and toxic cyanobacterial blooms
Freshwater lakes and viral metagenomics
Freshwater lakes and prokaryotic metagenomics
Freshwater lakes and antibiotic resistance genes
Conclusions
References
6 - Depth distribution of microbial diversity in lakes
Introduction
The neuston layer
Planktonic freshwater prokaryotes
Phototrophic bacteria
Sediment layer
Vertical distribution of sulfate-reducing bacteria
Vertical distribution of iron-oxidizing bacteria
Vertical distribution of manganese-oxidizing bacteria
Vertical distribution of ammonia-oxidizing archaea in lakes
Case studies
Lake Pavin and Lake Aydat
Lake Piburger
Lake Grosse
Lake Pavin
Lonar Lake
Lake Kivu
Lake Fryxell
English Lake district
Dianchi Lake and Erhai Lake
Conclusions
References
Further reading
7 - Exploring bacterial diversity: from cell to sequence
Introduction
Microbial diversity and its importance
Microbial cell structure
Bacillus
Coccus
Vibrio
Spirilla
Structural components of a bacterial cell
Capsule
Cell wall
Plasma membrane
Cytoplasm
Surface appendages
Flagella
Pili
Fimbriae
Bacterial genome
Plasmids
Exploring microbial diversity
Phenotypic approach
Plate counting
Community level physiological profiling
Phospholipid fatty acid analysis
Fatty acid methyl ester analysis
Identification of microorganisms using fatty acid methyl ester analysis
Molecular approach
Barcodes/molecular markers of microbial world
16S rRNA gene
gyrB
23S rRNA gene
rpoB
dnaK
dsrAB
16S-23S rDNA ISR
Molecular tools for exploring microbial diversity
Polymerase chain reaction
Basic concept of PCR
Steps in PCR
Types of PCR
Multiplex PCR
RT-PCR
qPCR and RT-qPCR
Touchdown polymerase chain reaction
Assembly polymerase chain reaction
Colony polymerase chain reaction
Nested polymerase chain reaction
Denature gradient gel electrophoresis (DGGE)
Terminal restriction fragment length polymorphisms (T-RFLP)
Single-strand conformation polymorphism
Amplified ribosomal DNA restriction analysis (ARDRA)
Fluorescent in situ hybridization
Clone libraries
Gel electrophoresis
Polyacrylamide gel electrophoresis
Sequencing of DNA
Sanger sequencing
Next-generation sequencing
Conclusions
References
Further reading
8 - Bacterial biofilms: the remarkable heterogeneous biological communities and nitrogen fixing microorganisms in lakes
Introduction
Availability of biofilms in fresh water systems
Biofilm diversity
Biofilm structure
Biofilm formation
Biofilm maturation
Factors influencing bacterial biofilm formation
Quorum sensing and biofilm development
General stress response
Persisters
Culturing biofilms
Static microtiter plate assays
Tube biofilms
Colony biofilms
Rotating disk and concentrical cylinder reactors
Biofilm growth on peg lids
Methods for characterization of biofilms
Confocal laser scanning microscopy
Scanning electron microscopy
Nuclear magnetic resonance spectroscopy
Techniques for studying biofilms
Staining assays
Crystal violet assay
DMMB assay
Fluorescein-di-acetate assay
Live/dead BacLight assay
Metabolic assays
Resazurin assay
XTT assay
BioTimer assay
Genetic assays
qRT-PCR
Fluorescence in situ hybridization
Role of biofilms in bioremediation
Types of pollutants remediated by biofilms
Nitrogen fixing microorganisms in lakes
Conclusions
References
9 - Microbial diversity in freshwater ecosystems and its industrial potential
Freshwater lake characteristics
Microbial diversity of cyanobacteria
Classification of microalgae and its significance
Origin of microalgal diversity
Chlorophyta
Rhodophyta
Haptophyta
Dinophyta
Eustigmatophyceae
Bacillariophyceae
Labyrinthulomycetes
Biotechnological importance of Cyanobacteria and microalgae
Cyanobacteria
Bioremediation by Cyanobacteria
Fine chemicals from Cyanobacteria
Pharmaceutical production by Cyanobacteria
Cyanobacterial bioplastics (polyhydroxyalkanoates, PHAs)
Microalgae
Future industrial potentials of Cyanobacteria (blue-green algae) and microalgae
Hydrogen from Cyanobacteria
Biodiesel from microalgae
Bioactive products from microalgae
Other products from microalgae
Environmental applications of microalgae
Industrial processes for microalgae and cyanobacteria
Conclusions
References
10 - Bacteria: the natural indicator of environmental pollution
Introduction
Air pollution
Water pollution
Fresh water pollution
Marine pollution
Fecal contamination of fresh and marine waters
Eutrophication
Soil and land pollution
Antibiotic-resistant bacteria as pollution indicators
Pollutant-specific bacterial indicators
Conclusions
Acknowledgments
References
Further reading
Index
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B
C
D
E
F
G
H
I
K
L
M
N
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P
Q
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T
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Z
Back Cover

Citation preview

FRESHWATER MICROBIOLOGY Perspectives of Bacterial Dynamics in Lake Ecosystems

Edited by

SUHAIB A. BANDH SANA SHAFI NOWSHEEN SHAMEEM P. G. Department of Environmental Science Sri Pratap College Campus Cluster University, Srinagar, India

Academic Press is an imprint of Elsevier 125 London Wall, London EC2Y 5AS, United Kingdom 525 B Street, Suite 1650, San Diego, CA 92101, United States 50 Hampshire Street, 5th Floor, Cambridge, MA 02139, United States The Boulevard, Langford Lane, Kidlington, Oxford OX5 1GB, United Kingdom Copyright © 2019 Elsevier Inc. All rights reserved. No part of this publication may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopying, recording, or any information storage and retrieval system, without permission in writing from the publisher. Details on how to seek permission, further information about the Publisher’s permissions policies and our arrangements with organizations such as the Copyright Clearance Center and the Copyright Licensing Agency, can be found at our website: www.elsevier.com/permissions. This book and the individual contributions contained in it are protected under copyright by the Publisher (other than as may be noted herein). Notices Knowledge and best practice in this field are constantly changing. As new research and experience broaden our understanding, changes in research methods, professional practices, or medical treatment may become necessary. Practitioners and researchers must always rely on their own experience and knowledge in evaluating and using any information, methods, compounds, or experiments described herein. In using such information or methods they should be mindful of their own safety and the safety of others, including parties for whom they have a professional responsibility. To the fullest extent of the law, neither the Publisher nor the authors, contributors, or editors, assume any liability for any injury and/or damage to persons or property as a matter of products liability, negligence or otherwise, or from any use or operation of any methods, products, instructions, or ideas contained in the material herein. Library of Congress Cataloging-in-Publication Data A catalog record for this book is available from the Library of Congress British Library Cataloguing-in-Publication Data A catalogue record for this book is available from the British Library ISBN: 978-0-12-817495-1 For information on all Academic Press publications visit our website at https://www.elsevier.com/books-and-journals Publisher: Andre Gerhard Wolff Acquisition Editor: Linda Versteeg-buschman Editorial Project Manager: Sandra Harron Production Project Manager: Sreejith Viswanathan Cover Designer: Miles Hitchen Typeset by TNQ Technologies

List of contributors Insha Amin Department of Environmental Science, University of Kashmir, Srinagar, India Uqab ali Baba Department of Environmental Science, University of Kashmir, Srinagar, India Suhaib A. Bandh P.G. Department of Environmental Science, Sri Pratap College Campus, Cluster University, Srinagar, India Deepali Bhagat School of Biotechnology, Shri Mata Vaishno Devi University, Katra, India Vinay Singh Chauhan Department of Biotechnology, Bundelkhand University, Jhansi, India Rubiya Dar Center of Research for Development (CORD)/P.G. Department of Environmental Science, University of Kashmir, Srinagar, India Bashir A. Ganai Center of Research for Development (CORD)/P.G. Department of Environmental Science, University of Kashmir, Srinagar, India Qazi A. Hussain P. G. Department of Environmental Science, Sri Pratap College, Srinagar, Kashmir, India M.M.M. Islam Ministry of Planning, Sher-­e-­Bangla Nagar, Dhaka, Bangladesh Azra N. Kamili Center of Research for Development (CORD)/P.G. Department of Environmental Science, University of Kashmir, Srinagar, India Divjot Kour Department of Biotechnology, Akal College of Agriculture, Eternal University, Baru Sahib, India Akhilesh Kumar Department of Botany, Dayalbagh Educational Institute, Agra, India Amit Kumar Department of Botany, Dayalbagh Educational Institute, Agra, India Halil Kurt Department of Earth and Environmental Engineering, Columbia University, United States, New York City Ruqeya Nazir Centre of Research for Development, University of Kashmir, Srinagar, India xi

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Marofull Nisa Centre of Research for Development, University of Kashmir, Srinagar, India Neelu Raina School of Biotechnology, Shri Mata Vaishno Devi University, Katra, India Ali A. Rastegari Department of Molecular and Cell Biochemistry, Falavarjan Branch, Islamic Azad University, Isfahan, Iran Sabeehah Rehman Centre of Research for Development, University of Kashmir, Srinagar, India Shashwati Ghosh Sachan Department of Bio-­Engineering, Birla Institute of Technology, Mesra, Ranchi, India Lateef B. Salam Department of Biological Sciences, Microbiology Unit, Summit University, Offa, Kwara State, Nigeria Anil Kumar Saxena ICAR-­National Bureau of Agriculturally Important Microorganisms, Mau, India Sana Shafi P.G. Department of Environmental Science, Sri Pratap College Campus, Cluster University, Srinagar, India Nowsheen Shameem P.G. Department of Environmental Science, Sri Pratap College Campus, Cluster University, Srinagar, India Preeti Sharma School of Biotechnology, Shri Mata Vaishno Devi University, Katra, India Bhanumati Singh Department of Biotechnology, Bundelkhand University, Jhansi, India Parvez Singh Slathia School of Biotechnology, Shri Mata Vaishno Devi University, Katra, India Ajar Nath Yadav Department of Biotechnology, Akal College of Agriculture, Eternal University, Baru Sahib, India Kritika Yadav Department of Botany, Dayalbagh Educational Institute, Agra, India Neelam Yadav Gopi Nath P.G. College,Veer Bahadur Singh Purvanchal University, Ghazipur, India Mir Riasa Zaffar Department of Environmental Science, University of Kashmir, Srinagar, India

Preface Microbiology—the study of miniscule organisms is an exceptionally diverse discipline including many branches like food microbiology, industrial microbiology, soil microbiology, freshwater microbiology, environmental microbiology, and microbial ecology. Microbial ecology—the study of microorganisms in relation to their biotic and abiotic environments is a link between all the branches of microbiology. Although the study of freshwater microbiology involves all the major disciplines within biology including taxonomy, molecular biology, biochemistry, and structural biology, this book has been compiled as a systematic and comprehensive guide of microbial ecology in lakes with particular reference to the dynamics of bacteria in freshwater lakes. It is designed to cater to the needs of the students and researchers in the related fields, who otherwise find themselves in a chaotic situation due to lack of concentrated literature in this growing and all important field of science. It has been designed as an effective research tool, as it is easy for the researchers to use because of its enhanced readability due to the use of simple, organized, and direct outline formatting. The content of the book is arranged in a logical progression from the fundamental to the more advanced concepts. It provides a detailed overview of the bacterial diversity, its ecological interactions, spatiotemporal dynamics in relation to the various water quality parameters, and metagenomic insights into the diversity and functions of microbial assemblages in lakes. It provides the basic information on how well the bacterial community composition varies vis-à-vis the changing seasons and the anthropogenic activities taking place in the catchment of the lakes along with the evaluation of the bioindicator species of bacteria. It identifies the factors of potential importance in structuring the bacterial communities in the lakes. Although lots of books are available on the different microbiological themes, none of them gives a detailed compilation of the bacterial diversity of aquatic ecosystems, especially freshwater lakes. The book contains many illustrations in the form of tables, diagrams, and case studies to better understand the basic facts about microbes and factors affecting them without drowning the student in unexplained jargons and impenetrable details. The book provides a detailed description of the methods involved for exploring the bacterial diversity from freshwater ecosystems and the students and researchers will find it useful in further evaluating the diversity of bacteria in the lake ecosystems.We hope this book proves useful for researchers and students. Suhaib A. Bandh xiii

Acknowledgments “If every project has its secret inspiration or at least its one motivation, here that is the PEACE of my life” In the name of Allah, the most Gracious, the most Merciful. May the praise of Allah, in the highest of assemblies, and His peace, safety and security, both in this world and the next, be on Prophet Mohammad (peace be upon Him), the best of mankind, the most respectable personality for whom Allah created the whole universe and the seal of the Prophets and Messengers. We are highly thankful to Allah, Who in his great mercy and benevolence provided us the courage, the guidance, and the love to undertake and complete this project. First and foremost, we would like to thank all our teachers who held our finger to tread the path of learning and enabled us to compile a book. We deeply thank them for the advice and encouragement which became the guiding light towards our personal and professional development.To be very honest, publication of a research article, review article, or for that matter a book requires the efforts of many people besides the authors. We wish to express our special appreciation to the editorial and production staff of Elsevier for their excellent and efficient work. In particular, we would like to thank Linda Versteeg-Buschman, our Acquisitions Editor, for her unwavering confidence in us and Sandra Harron, our editorial project manager, for her time, guidance, patience, and support. She was there whenever needed. Inevitably, a book of this type relies heavily on previously published work, and I would like to thank holders of copyright for granting permission to publish original diagrams and data. Special thanks are due to our copyright coordinator Indhumathi Mani who supervised all the copyright permissions for the material used in the form of images, etc., in the production of this book. Our production manager Sreejith Viswanathan supervised the production of this project with commendable attention to all the minute and vivid details. Our special thanks go to all the authors who have contributed chapters for this book, but we would fail in our duty if we fail to give the most special thanks to Dr. Lateef Salam one of the authors who wrote on the metagenomic insights into the microbial diversity for the timely and accurate completion of his assignment to help us to meet all the deadlines from the publisher.We would also like to thank those who first agreed to contribute chapter for the book but finally pulled out xv

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of the same that too at some crucial junctures.We wish to extend our appreciation to all the people who assisted us individually in the completion of this project. Suhaib Bandh is grateful to his friends particularly Dr. J. A. Parray and Dr. B. A. Lone for commenting on some sections of some chapters, and for the helpful and detailed comments of other reviewers on the rest of the work. Finally, our thanks are due to all those who have directly or indirectly worked for the successful completion of the project. Finally, but most importantly we wish to extend our appreciation to our families for their patience and encouragement during the compilation of the project. We owe a debt of gratitude to them for their patient forbearance and u ­ nwavering support. We would also like to take the opportunity to thank our friends, colleagues, and students in the Department of Environmental Science, Sri Pratap College Campus at the Cluster University Srinagar and outside. Suhaib A. Bandh Sana Shafi Nowsheen Shameem

CHAPTER 1

Bacterial community composition in lakes Ajar Nath Yadav1, Neelam Yadav2, Divjot Kour1, Akhilesh Kumar3, Kritika Yadav3, Amit Kumar3, Ali A. Rastegari4, Shashwati Ghosh Sachan5, Bhanumati Singh6, Vinay Singh Chauhan6, Anil Kumar Saxena7 1Department

of Biotechnology, Akal College of Agriculture, Eternal University, Baru Sahib, India; 2Gopi Nath P.G. College,Veer Bahadur Singh Purvanchal University, Ghazipur, India; 3Department of Botany, Dayalbagh Educational Institute, Agra, India; 4Department of Molecular and Cell Biochemistry, Falavarjan Branch, Islamic Azad University, Isfahan, Iran; 5Department of Bio-Engineering, Birla Institute of Technology, Mesra, Ranchi, India; 6Department of Biotechnology, Bundelkhand University, Jhansi, India; 7ICAR-National Bureau of Agriculturally Important Microorganisms, Mau, India

Introduction During the course of evolution of life on earth, microbes evolved long before the origin of plants and animals, thus making them the oldest life forms on earth. They are more than 3.5–3.8 billion years old, single-celled organisms, so small in size that millions of microbes fit in the eye of a needle. Microbes are omnipresent on earth, inhabiting almost every part of the earth including soil, water, air, and even other organisms (Canganella & Wiegel, 2011; Yadav, Kumar et al., 2017; Yadav, Verma, Kumar, Sachan, & Saxena, 2017). They also inhabit the extreme habitats including hot springs (Brock, 2012; Brook, 1980; Kumar,Yadav, Tiwari, Prasanna, & Saxena, 2014; Sahay et al., 2017; Suman, Verma, Yadav, & Saxena, 2015; Verma, Yadav, Suman, & Saxena, 2012; Yadav, Verma et al., 2015), deep sea hydrothermal vents (McCollom & Shock, 1997); saline environments (Antón, RossellóMora, Rodríguez-Valera, & Amann, 2000; Saxena et al., 2016;Yadav, Sharma et al., 2015); cold environments—Permafrost soils, glaciers, ice sheets, and snow cover (Boyd et al., 2011; Singh et al., 2016;Yadav, 2015, p. 234;Yadav, Sachan,Verma, & Saxena, 2015;Yadav, Sachan,Verma,Tyagi et al., 2015); acid mine drainages (Baker & Banfield, 2003); and kilometers beneath earth’s surface (White, Phelps, & Onstot, 1998). The extremophilic microbes have also been reported as associated with plants growing in extreme environmental conditions (Kour et al., 2017; Rana, Kour,Yadav, Kumar, & Dhaliwal, 2016; Srivastava et al., 2013;Yadav,Verma, Sachan, Kaushik, & Saxena, 2013). Freshwater Microbiology ISBN 978-0-12-817495-1 https://doi.org/10.1016/B978-0-12-817495-1.00001-3

© 2019 Elsevier Inc. All rights reserved.

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Bacteria appear more abundantly than other creatures, like plants and animals, in these diverse habitats on the face of earth, with their numbers ranging from 4 × 1030 to 6 × 1030 on earth (Horner-Devine, Carney, & Bohannan, 2004). They are also abundantly found in oceanic and terrestrial environments, for example, in marine waters bacterial numbers range from 0.2 to 2.0 × 109 cells/L (Turley & Mackie, 1994). These extreme environments usually present hostile conditions to humans and the majority of life forms on earth, but the extremophilic bacteria found therein have evolved to tolerate or even thrive well within these environments (Canganella & Wiegel, 2011; Yadav, Verma, Sachan, Kaushik, & Saxena, 2018). Such environments contain relatively simplified microbial communities that have evolved specific life history strategies to survive in these environments (Oren, 2002). Thermophiles, for example, have amino acid substitutions in many of their most important proteins that decrease their flexibility and increase their resilience (Aguilar, Ingemansson, & Magnien, 1998). Psychrophiles, in contrast, have experienced mutations that increase protein flexibility to maintain stable active sites in very cold environments (Lonhienne, Baise, Feller, Bouriotis, & Gerday, 2001;Yadav,Verma, Sachan et al., 2018). In hot deserts the bacteria like Deinococcus radiodurans has evolved sets of polymerases capable of reassembling the entire genome after being fragmented by years of UV radiation and cellular desiccation, and reviving when water becomes available again (Zahradka et al., 2006). In order to combat the osmotic pressure of high-saline environments, halophile genomes encode multiple Na+/ H+ antiporters, Na+ gradient-powered ATPases, cytoplasmic accumulation of K+, or even the synthesis of organic osmolytes to control osmotic pressure (Ciulla, Diaz, Taylor, & Roberts, 1997; Mesbah & Wiegel, 2011). Freshwater bacteria are a very dense assemblage of prokaryotic organisms with varied morphology, physiology, and ecological preferences. Bacteria are widespread in freshwater environments, forming extensive pelagic and benthic populations in a wide range of habitats including mudflats, bogs, sulfur springs, lakes, and rivers. In lake environments, different species of pelagic bacteria position themselves in the water column in relation to local conditions like light intensity, oxygen level, and nutrient concentration. So, bacterial community composition (BCC) among lakes varies with different environmental variables (Van der Gucht et al., 2005; Yang, Jiang, Wu, Liu, & Zhang, 2016). Lake water and sediments of the different habitats with unique intrinsic environmental conditions result in their unique bacterial community composition (Yang et al., 2013) and such difference account for different microbial biogeographies in lake environments (Lindström & Langenheder, 2012;Yang et al., 2016).

Bacterial community composition in lakes

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Historical perspective of lake bacterial communities Till recently the traditional culture-based cultivation techniques lead to the notion that the microorganisms inhabiting the terrestrial and aquatic habitats were quite similar (Rheinheimer, 1980). But the advent of modern tools and techniques like the molecular techniques provided unprecedented access to the diversity and composition of bacterial communities helping the scientists to note down a clear distinction between the bacteria found in these distinct habitats (Lozupone & Knight, 2007), thus revealing their unique physical and chemical characteristics (Rappé,Vergin, & Giovannoni, 2000; Zwart et al., 2003).The BCC not only varies along the larger gradient of oceans and continents but also within and between the aquatic habitats, as contrastingly distinct BCC was observed from oceans and freshwater lakes (Lozupone & Knight, 2007; Rappé et al., 2000). Zwart, Crump, Kamstvan Agterveld, Hagen, and Han (2002) gathered the reported 16S rRNA gene sequences from some 11 freshwater lakes and 2, as part of an independent study and resulted in the collection of 689 bacterial 16S rRNA gene sequences and enabled the identification of 10 freshwater phyla and 34 supposed bacterial freshwater clusters, defined as a monophyletic branch of a phylogenetic tree that contained at least two sequences with ≥95% gene identity from more than one freshwater environment. Many of the identified clusters were seen to be common in the freshwater, representing the unique bacterial taxa found only in the freshwater ecosystems. However over the past many years, the frequent use of molecular techniques have helped to fill the gap in the literature about the freshwater bacterial communities to a larger extent by retrieving innumerable bacterial groups from these freshwater ecosystems. Hence a large number of newly observed freshwater lake clusters have come to fore in the recent times. However, the lack of a cohesive collection of the known sequences and defined clusters from these habitats still leaves a huge scope to work in the direction of compiling a comprehensive data base of the sequences and gene clusters of the freshwater environments.

Study of bacteria in lake environments; why is it so important? Prokaryotes are among the most important contributors to the transformation of complex organic compounds and minerals in freshwater sediments (Jurgens et al., 2000). Bacteria the main heterotrophic (using organic substances as a carbon and energy source) microorganisms in various aquatic ecosystems, play

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key roles in biogeochemical cycles and are the key components of the microbial food webs, especially of the microbial loop. They play a very critical role not only for the normal functioning of life on the planet earth but also for its maintenance and continuity. Being the pioneering colonizers, their ability to survive, propagate, and inhabit a wide variety of environs manifests their evolutionary success. Microbial biodiversity is gaining more importance not only to understand the evolution of the bacterial communities in lake ecosystems but also to determine the ecological impact of certain niches and changing climate on the distribution and diversity of the BCC (Joshi, Pande, & Joshi, 2016). In lake ecosystems these bacteria participate in the decomposition of organic material into nutrients taken as food by other organisms and controlling the water quality in lakes (Newton, Jones, Eiler, McMahon, & Bertilsson, 2011). These microorganisms also play a critical role in remineralizing and restoring the nutrients which influence the material circulation in aquatic ecosystems (Tong et al., 2005). Since the bacteria are present in the sediments of the lake ecosystems, they are responsible for biodegradation of contaminant compounds, such as polycyclic aromatic hydrocarbons (PAHs) (McNally, Mihelcic, & Lueking, 1998). Beside these, the microorganisms also act an important food and nutrient sources for other organisms such as protozoans present in the aquatic ecosystems. In absence of aquatic microorganisms, the food chain system may be disturbed greatly and ecosystem imbalance may occur, thereby affecting the existence of the biotic and abiotic system associated with it.The microbes play an important role on nutritional chains as well as maintaining the biological balance (Madsen, 2008). The anthropogenic activities like religious activities, tourism, bathing, washing, open defecation, surface drainage, irrigation runoff, industrial discharge, and domestic wastewaters adversely affect the water quality of the lakes, and lakes being sensitive ecosystems respond quickly to any natural or human-induced change in their watershed. By the nature of their biological activities, autotrophic and heterotrophic microorganisms are sensitive indicators of the ecological and waterquality status of aquatic environments. However, only by thoroughly understanding how microorganisms function in healthy aquatic ecosystems helps us to recognize or accurately predict their responses to water-quality changes or other environmental disturbances. Here comes the role of our tiny natural scavengers (microorganisms in general and bacteria in particular) which are widely distributed in nature for their ability to treat these wastes and maintain the ecological balance. As these microorganisms are well adapted and diversified in almost all lakes, they have been used as an indicator for the suitability of water quality (Okpokwasili & Akujobi, 1996).

Bacterial community composition in lakes

5

Besides working as scavengers, nowadays microbes in these aquatic ecosystems are also gaining attention for their byproducts and are being extracted for production of useful chemicals.These aquatic bacteria as a rich source of hydrolytic enzymes such as amylases, lipases, proteases, phospholipase, catalases, and other important industrial enzymes (Mudryk & Podgorska, 2006). The extracted enzymes have industrial potential due to their wide biochemical applications in food industries, medicinal formulations, detergents, and waste treatment (Saurabh, 2007). Presently, the largest part of the enzyme market is occupied by the alkaline proteases (derived from Bacillus species) having varied applications. Similarly the enzyme phospholipase obtained from lake lipolytic bacteria plays a key role in bakery and is used in bread making, egg yolk industry, and refinement of vegetable oils. Another important enzyme α-amylase obtained from the bacteria, used in hydrolyzing of the starch molecules is important in many industrial processes and constitutes 25% of the worldwide enzyme market (Syed, Agasar, & Pandey, 2009). The microbes by virtue of their pivotal roles in organic matter production and decomposition, by dissolved to particulate organic matter conversions, nutrient uptake and regeneration, and biogeochemical transformations, are essential to the ecological functioning of aquatic systems. Prokaryotes are responsible for biological, geological, and chemical processes in aquatic environments (Matcher, Dorrington, Henninger, & Froneman, 2011). All organisms in an ecosystem rely on the activities of microorganisms. In many aquatic environments, increased phytoplankton numbers like algae are followed by increase in heterotrophic bacterial activities and production.The function and metabolism of an ecosystem is highly influenced by bacterial activities because an important proportion of planktonic biomass is dominated by bacteria. The active bacterial community is involved in uptake of substrates, metabolic process, growth, and reproduction (Freese & Schink, 2011). In aquatic ecosystems 36% of the total bacterial populations were involved in respiration in freshwater samples, while in marine systems they represent only 12% (Zimmermann, Iturriaga, & Becker-Birck, 1978). More than 50 phyla of bacteria and archaea are responsible for decomposition of dissolved organic matter (DOM) in natural aquatic environments (Kirchman, Cottrell, & Lovejoy, 2010). Determination of dominant bacterial groups of heterotrophic nature in freshwater ecosystems is very important because the bacterial groups take up and control dissolved organic matter and contribute to other processes like cycling of matter and energy

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in the environment (Kirchman, Dittel, Findlay, & Fischer, 2004). Study of bacterial community composition is also important to understand the active bacterial cells in the environment, for example, decomposition of organic matter, bacterial entity, and viability (Kenzaka, Yamaguchi, Prapagdee, Mikami, & Nasu, 2001;Verma,Yadav, Kumar, Singh, & Saxena, 2017;Yadav, Kumar, Prasad, Saxena, & Dhaliwal, 2018;Yadav,Verma, Kumar et al., 2018). The study of bacterial community in aquatic environment is important due to following reasons: 1. To acquire knowledge about the diversity of microbial genetic resources in aquatic environment. 2. To understand the distribution pattern of microorganisms in aquatic environment. 3. To understand the functional role of microbial diversity in aquatic environment, and. 4. To understand the regulation of microbial biodiversity in freshwater lake environments.

Bacterial biogeography in lakes Biogeography is the observation, recording, and explanation of the geographic ranges of organisms (Pielou, 1979). Although microbes do have biogeographies, this subject has received very little attention. Microbial biogeography is generally absent from recent books (Bull, 2004; Ogunsseitan, 2005) as are microbes from the discussions on biogeography (Lomolino & Heaney, 2004; Pielou, 1979) or ecological geography (Longhurst, 1998). To some extent this is probably because of the perception that there is no interesting microbial biogeography as all microbes exist potentially everywhere. The earlier application of new molecular tools and techniques to bacterial biogeography in freshwaters showed that the bacterial community composition (like phytoplanktons and zooplanktons) changes with the changing seasons and the nearby lakes differ in BCC (Konopka, Bercot, & Nakatsu, 1999; Lindström, 2000) indicating no clear relationship between lake location and BCC as, for example, Lindström (2000) compared communities of five small lakes in southern Sweden, all within a distance of 75 km from each other, using denaturing gradient gel electrophoresis (DGGE) and observed that the community composition differed with seasons as much as it varied between lakes. Statistical analysis suggested strongest relationships between the variability of BCC and variability in the biomass of microzooplankton, cryptophytes, and chrysophytes rather than

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between lake location or size. A spatial scale comparison of bacterioplankton communities in a set of lakes in different climatic zones of Sweden (northern and southern) and Norwegian Arctic showed little evidence that the neighboring lakes share bacterioplankton communities (Lindström & Leskinen, 2002) which can be an artifact of the spatiotemporal sampling scales. However, it clearly displayed the importance of biological interactions, and/or physiochemical conditions of the lakes to determine the bacterioplankton communities. Considering the spatial variability in the bacterioplankton communities, Yannarell and Triplett (2004) investigated some 13 northern temperate lakes (Wisconsin, USA) using automated ribosomal intergenic spacer analysis (ARISA) (a 16S rDNA community fingerprinting technique) to study the variability within and between the lakes and observed that the bacterial communities differed less within a lake than between the lakes. Within the lake, the average dissimilarity was 17%, while between lakes it was 75%. Further, the lake bacterial diversity positively related to lake productivity is determined through chlorophyll concentration range. In the next year Yannarell and Triplett, found that the bacterial community composition related to both location and lake type from a study carried out on a larger spatial scale in two sets of Wisconsin lakes separated by about 300 km, sampled during the spring, summer, and fall (Yannarell & Triplett, 2005). Studies carried out on northern temperate lakes (both Scandinavian and North American) showed that the overall composition and characteristics of bacterial communities and the lake geography are interrelated, suggesting that the lake location is a poor predictor of BCC, and taxonomic richness is not closely related to lake size. These findings are in conflict with basic predictions of Island Biogeography theory (MacArthur & Wilson, 1967): (1) neighboring lakes should resemble one another in taxonomic composition more than distant lakes; and (2) system size should be related to taxonomic richness. However, Dolan (2005) mentioned in his paper on “Biogeography of aquatic microbes” that a few recent studies (Bell, Ager, Song, Newman,Thompson, Lilley, & vander Gast, 2005; Reche, Pulido-Villena, Morales-Baquero, & Casamayor, 2005) carried out specifically to test predictions of Island Biogeography, concluded that freshwater bacterioplankton communities do conform to the theory of Island Biogeography. In contrast to the contradictory studies, Reche et al. (2005) reported that nearby lakes contained similar taxa. Overall there exist some support that the existence of biogeographic patterns in lake bacteria, in terms of “species” as ribotypes, seems to depend on the spatiotemporal scales.

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Biodiversity and abundance of bacteria from freshwater lakes In order to evaluate any community, it is essential to quantify the different aspects of the community by way of alpha diversity (number of taxa present in a single community or location), beta diversity (variation in the community composition), and gamma diversity (total diversity across a landscape) (Magurran, 2013; Solow & Polasky, 1994). However, in bacterial communities, alpha and beta diversity are the two important measures which are generally used to explain, evaluate, and scrutinize any changes in the community structure across the spatiotemporal environmental gradients. Further selection, drift, dispersal, and mutation are the four processes that structure the microbial communities (Hanson, Fuhrman, Horner-Devine, & Martiny, 2012). The BCC in the freshwater lake ecosystems have been investigated worldwide (Fig. 1.1)

Bacterial alpha diversity Maintaining bacterial alpha diversity in natural and managed ecosystems is critical for both purpose and firmness of ecosystem processes (Bell, Newman, Silverman,Turner, & Lilley, 2005; Eisenhauer, Scheu, & Jousset, 2012) because reduction in bacterial alpha diversity possibly results in the loss of crucial ecosystem services. Bacterial alpha diversity has been revealed to modify across environmental gradients, including crossway gradients of primary productivity (Horner-Devine et al., 2004).The diversity-productivity relationship is not constant for all bacterial taxa, suggesting that patterns of alpha diversity may not be universal for all taxonomic groups of bacteria. The high diversity may be due to the complex and fine-scale chemical gradients established in saline sediments, which present exceptionally high numbers of ecological niches for higher bacterial diversity (Torsvik, Øvreås, & Thingstad, 2002). In comparison to the sediment habitats, aquatic habitats are characteristically considered to host less bacterial taxa, probably as a result of a smaller amount of heterogeneity (Chao, Chazdon, Colwell, & Shen, 2006; Curtis, Sloan, & Scannell, 2002; Hughes, Hellmann, Ricketts, & Bohannan, 2001; Torsvik et al., 2002). The processes generating and maintaining bacterial alpha diversity are budding as patterns of variety (Fierer & Lennon, 2011). Due to rapid mutation and lateral gene transfer, evolution of bacterial taxa having novel phenotypic and/or ecological functions are taking place rapidly thus increasing the bacterial biodiversity (Kassen & Rainey, 2004). Due to the significance of bacterial alpha diversity, microbial ecologists have got interested in unfolding the patterns of bacterial prosperity across space and time (Shaw et al., 2008).

Bacterial community composition in lakes

Figure 1.1  Map of world depicting freshwater lakes for biodiversity of bacterial community. 9

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Bacterial beta diversity Beta diversity, variation of species composition along space or time, is a measure of difference in microbial community composition between pairwise sites. The pioneering investigations on beta diversity can be dated back to Whittaker (1972). Beta diversity has been explicitly and thoroughly examined for microbes in both terrestrial and aquatic ecosystems (Green & Bohannan, 2006; Green et al., 2004; Lozupone, Hamady, Kelley, & Knight, 2007; Shade, Jones, & McMahon, 2008), and has further been used in a framework of microbial biogeography to examine the relative importance of habitat (contemporary environmental factors) and province (historical legacies) (Martiny et al., 2006; Takacs-Vesbach, Mitchell, Jackson-Weaver, & Reysenbach, 2008). Microbial beta diversity is not less important than alpha diversity because information on beta diversity helps in understanding the processes shaping microbial distribution pattern (Martiny et al., 2006), in designing systems for preservation of biodiversity (Franklin & Mills, 2007; Green & Bohannan, 2006), in managing microbial communities for bioremediation, and even in developing ecological theories that can be applied to microorganisms (Hubbell, 2001; Prosser et al., 2007; Ramette & Tiedje, 2007). It was long thought that because bacteria are microscopic and easily dispersed, the geographic separation could not influence diversity but rather environmental filtering structured the bacterial community. However, patterns of BCC across space and time have emerged and made it evident that taxa are distributed nonrandomly across ecosystems (Horner-Devine et al., 2004). Characterizing BCC and drivers of change in beta diversity has provided insight into some process that leads to assembly and structure.The divergence of depositional environments affects the variation of beta diversity, because the subsurface sediment is strongly shaped by the vertical arrangement of geologic units and their weathering profiles (Lehman, 2007). Furthermore, consideration of the spatiotemporal scales in measuring and comparing beta diversity is crucial, as this scale is known to affect ecological studies in microorganisms (Levin, 1992; Martiny, Eisen, Penn, Allison, & Horner-Devine, 2011; Zinger et al., 2011).

Bacterial abundances and spatial patterns Structure of bacterial communities is maintained by variable environmental conditions across space and time that represents habitat heterogeneity (Shade et al., 2008; Stocker & Seymour, 2012). Ecological niche separation of coexisting microbial taxa might be triggered by bottom-up (resource

Bacterial community composition in lakes

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availability) and/or top-down control (mortality factors), leading to distinct spatial (longitudinal and vertical) and temporal patterns of distribution of different microbes (Salcher, 2014) within lakes. These spatial patterns range from microscale to larger-scale patchiness (e.g., Green & Bohannan, 2006; Pinel-Alloul & Ghadouani, 2007; Salcher, Pernthaler, Frater, & Posch, 2011; Van der Gucht et al., 2007). Advance in molecular techniques have resulted in significant knowledge of prokaryotic diversity, allowing the evaluation of patterns of spatiotemporal distribution of bacteria (Logue & Lindstrom, 2008). In freshwater ecosystems it has been found that there are different factors responsible for shaping the bacterial community structure (Barberan & Casamayor, 2010; Corno & Jurgens, 2008; Lindström, Kamst-Van Agterveld, & Zwart, 2005; Logue, Burgmann, & Robinson, 2008). The factors include both intrinsic (e.g., dispersal rate, trophic factors) as well as extrinsic (such as latitude, ecosystem size, habitat isolation) factors responsible for the turnover of community composition in space and time. The relevance of each factor varies across large geographical gradients (Schiaffino et al., 2011; Soininen, 2010). Among the factors that regulate prokaryotic assemblages, some of the most important are temperature, ultraviolet radiation, quality and quantity of dissolved organic matter, nutrient concentrations, and grazing pressure (Glaeser, Grossart, & Glaeser, 2010; Lindström et al., 2005; Logue et al., 2015; Newton & McMahon, 2011; Pernthaler, 2005), which can vary in relation to the geographic position, watershed, and surrounding landscape of the lakes. Recent reports based on high-frequency multiyear datasets of site-specific studies have shown that seasonal patterns in bacterial community structure recur in freshwater ecosystems, and these seasonal patterns indicate that some microbial communities change directionally according to environmental conditions (Kara, Hanson, Hen Hu, Winslow, & McMahon, 2013; Rosel, Allgair, & Grossart, 2012; Tammert, Tsertova, Kiprovskaja, Baty, Noges, & Kisand, 2015). The spatial scale on which bacterial community is analyzed has the ability to influence the interpretation of the relative contribution of selection, mutation, drift, or migration to the community composition (Martiny et al., 2011; Saxena, Yadav, Kaushik, Tyagi, & Shukla, 2015). In terrestrial systems, spatial scale is easily quantified using geographic distance. However, in aquatic ecosystems hydrologic regimes quickly move water parcels thus transporting bacteria and other planktonic organisms with the water mass. A pyrosequencing study compared the composition of bacterial community at three different depths throughout the water column at multiple stations in the North Atlantic Ocean and reported that bacterial community

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composition was most similar within the same water mass, defined by depth, regardless of horizontal space (Agogué, Lamy, Neal, Sogin, & Herndl, 2011; Cram et al., 2015;Yadav, Sachan,Verma, Suman, & Saxena, 2014). Long-term observation of marine ecosystems has provided the data mandatory for showing that, along with spatial scale, bacterial communities also vary over time (Gilbert et al., 2012), which also affects the interpretation of the relative contribution of the underlying processes of bacterial community composition. The transformations in beta diversity over time are typically accredited to environmental variation as a result of seasonal or annual changes within the water mass. Additionally, it is possible that on temporal scales different stochastic events further drive changes in beta diversity, for example, on short time scales, ecological drift arising from stochastic events such as births and deaths contribute to heterogeneity in diversity, while on longer time scales stochastic mutation genetic processes lead to evolutionary drift (Martiny et al., 2011).

Bacterial population dynamics Today, lakes are ecologically regarded as a part of a larger unit, that is, the drainage basin. At a standstill, efforts in lake microbial ecology and diversity have basically focused on within-lake selective forces, rather than external influences on community structure and diversity. Although various studies have shown that lake as well as estuarine community compositions are mainly prejudiced by incoming bacteria (Crump, Adams, Hobbie, & Kling, 2007;Van der Gucht et al., 2005). The degree of isolation a lake bacterial community experiences, and the degree of influence by inside flow in bacteria on structure of local community depends on the hydrological retention time of the lakes. Lakes with short hydrological retention time contain bacterial communities that are approximately similar to those of the incoming water in comparison to lakes having longer hydrological retention times. This difference is due to the larger amount of imported bacteria into the former type of lake.Thus external factors play an important role in determination of lake bacterial communities, similar to other microbial communities in general (Curtis, Koss, & Grier, 2002; Curtis & Sloan, 2004; Lindström, Forslund, Algesten, & Bergström, 2006). The possible method behind the external control of BCC in lakes is cell transport rate. It means the local community structure is controlled by regional processes like dispersal rates. This external control in large number of lakes may be due to the flow through systems rather than as microcosms with respect to bacterial community that comes to the lake with running

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water. The cells and growth media continuously reaching the lake from nearby drainage influence the composition of the bacterial community.

Diversity-productivity relationship in freshwater bacterial communities Huge volume of ecological literature is witness to the fact that the numbers of morphospecies or functional types of macroorganisms in a given habitat are strongly influenced by the rate of conversion of energy and abiotic resources into biomass, that is, productivity (Waide et al., 1999) and as reported by Smith (2007) in his review on “Microbial diversity-productivity relationships in aquatic ecosystems” there are accumulating evidences from the microbial ecological literature about the obedience of key principles of macroecology by microorganisms.The species–area relationship, considered to be the oldest documented diversity pattern in macroecology (Rosenzweig, 1995), has now been confirmed for bacteria (Bell, Ager et al., 2005; Reche et al., 2005) as well. After a thorough investigation and deeper analysis of the published work (as in Waide et al., 1999) on the diversity-functioning relationships, Smith (2007) classified the relationships into six general categories: (1) flat or random; (2) humped; (3) negative; (4) positive; (5) U-shaped; or (6) variable.The reported shapes of diversity–productivity patterns were found to be dependent on various factors such as geographical region, ecosystem size, community assembly history, or food web structure. Critical analysis of 70 studies carried out on 43 natural systems and 27 experimental or engineered systems could find only one U-shaped relationship in the entire analytical research data set which experimentally obtained relationship for alphaproteobacteria richness (Horner-Devine, Carney, & Bohannan, 2003; HornerDevine, Leibold, Smith, & Bohannon, 2003). Furthermore, roughly equal numbers of the remaining diversity–productivity patterns were found in the data sets. The diversity–productivity patterns from natural systems were predominantly either negative (35%), positive (28%), or humped (23%); and only a few (14%) showed flat, random, or variable relationships. As illustrated in the literature (Ogawa & Ichimura, 1984), humped diversity–productivity patterns have been reported in natural phytoplankton assemblages (Dodson, Arnott, & Cottingham, 2000; Leibold, 1999) as well as in experimental microbial communities (Horner-Devine, Carney et al., 2003; Horner-Devine, Leibold et al., 2003; Kassen, Buckling, Bell, & Rainey, 2000). (Fig. 1.2a) represent the phylogenetic tree showed the relationship among freshwater bacterial community worldwide. The major generalizations of the worldwide bacterial community composition and dynamics is depicted in (Fig. 1.2b-e).

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Figure 1.2a Phylogenetic tree showed the relationship among freshwater bacterial community worldwide.

Bacterial community composition in lakes

Figure 1.2a, cont’d

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Figure 1.2a, cont’d

Bacterial community composition in lakes

Figure 1.2a, cont’d

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18 Freshwater Microbiology

Figure 1.2b Distribution of different phylum and groups of freshwater bacterial community worldwide.

Bacterial community composition in lakes

Figure 1.2c Relative distribution of different phylum of fresh­water bacterial community worldwide. 19

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Figure 1.2d Relative distribution of different genera of freshwater bacterial community.

Bacterial community composition in lakes

Figure 1.2d, cont’d

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Figure 1.2d, cont’d

Bacterial community composition in lakes

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Figure 1.2e Relative distribution and richness of pre-dominant genera reported form lake ecosystems.

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Microbial dormancy As the stability and functioning of both managed and natural ecosystems like lakes, etc., are greatly influenced by the diversity of microbial communities inhabiting them (Bell, Newman et al., 2005; Hashsham et al., 2000; Wittebolle et al., 2009), it is grossly important for the ecologists to develop an understanding of the factors that generate and maintain the microbial diversity (Prosser et al., 2007). Research suggests that the biogeographic processes like local adaptation and patch-scale species sorting drive the spatial scale distribution of microbes in an ecosystem (Martiny et al., 2006). Microbial communities are also structured by their response to different environmental variables that vary on a temporal scale (Fuhrman et al., 2006; Jones & McMahon, 2009). Dormancy is one such trait that allows species to contend with temporal variability of environmental conditions as this trait allows dormant individuals to become members of a seed bank, which then contributes to the diversity and dynamics of any community in future generations. Although it is clearly known as to how dormancy works in case of plant and animal communities (Caceres & Tessier, 2003; Turner, Baker, Peterson, & Peet, 1998) less is known about whether and to what degree dormancy influences the biodiversity of microbial communities. Dormancy is a common life history strategy among microbes that enables microorganisms to resist stressors such as temperature, desiccation, and antibiotics by entering resting states or by forming spores (Roszak & Colwell, 1987; Sussman & Douthit, 1973; Whittington, Marshall, Nicholls, Marsh, & Reddacliff, 2004). Although the molecular and cellular underpinning of dormancy is fairly well known for a few clinically important strains of bacteria (Lewis, 2007), microbial dormancy is thought to be important in case of natural systems as well. The dormancy of microbes is controlled and regulated by the interpretation of environmental cues such as crowding, oxygen or temperature stress, and resource limitation (Lewis, 2007). Despite the enormous complexity surrounding the interpretation of environmental cues (Epstein, 2009), it can be argued that a simple theoretical framework is necessary for generating predictions about the effects of dormancy on the microbial community composition. Jonesa and Lennon (2010) combined mathematical modeling from seed bank models in plant ecology (Chesson, 1994; Cohen, 1966) and molecular survey to test predictions about the role of dormancy in maintaining the microbial diversity. They conducted a spatial survey of

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the active and total fractions of bacterial and eukaryotic microbial communities from a set of temperate lake ecosystems to evaluate their model whose development was guided by three major questions: (1) To what extent does dormancy contribute to the taxon richness of microbial communities? (2) How does dormancy shape local and regional patterns of microbial community composition? (3) Is the “rare biosphere” (Sogin et al., 2006) predominantly comprised of dormant bacterial taxa? The study revealed that dormancy plays a more important role in shaping bacterial communities than eukaryotic microbial communities, as the dormant bacterial proportion was relatively low in productive ecosystems in comparison to nutrient-poor systems where it accounted for up to 40% of taxon richness. Their simulations suggested that regional environmental cues and dormancy synchronize the composition of active communities across the landscape while decoupling active microbes from the total community at local scales. Further it was also proposed that the repeated transitions to and from the seed banks help in the maintenance of high levels of microbial biodiversity observed in nearly all types of ecosystems.

Influence of habitat heterogeneity and submerged macrophytes on bacterial community composition in freshwater lakes Habitat heterogeneity Variability in environmental conditions across space and time give rise to habitat heterogeneities, and these heterogeneities have a strong bearing on the overall dynamics and composition of the microbial communities inhabiting different ecosystems. The natural microbial communities are structured by multiple drivers, but the relative role of these drivers is poorly understood. In order to understand the role of habitat heterogeneity, Shade et al. (2008) used aquatic microbial communities as a model to investigate the relationship between habitat heterogeneity and community composition and dynamics. Defining spatial habitat heterogeneity as vertical temperature and dissolved oxygen (DO) gradients in the water column, and temporal habitat heterogeneity as variation throughout the seasons in these environmental parameters, it was observed that seasonal lake mixing events contribute to temporal habitat heterogeneity by destroying and recreating these gradients. Selection of three lakes along a range of annual mixing frequency (polymictic, dimictic, meromictic) for

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the study showed that the BCC was distinct between the epilimnion and hypolimnion within the stratified lakes, and also more variable within the epilimnia through time. Stark differences were observed in the patterns of epilimnion and hypolimnion dynamics over time and across lakes, suggesting that the specific drivers have distinct relative importance for each community.

Submerged macrophytes Submerged macrophytes like many other factors play a key role in structuring the bacterioplankton communities in lake ecosystems, as they result in the dominance of these communities. To evaluate the effect of submerged macrophytic communities on the bacterial community composition (BCC) Wu, Zwart, Wu, Agterveld, Liu, & Hahn (2007) investigated a large shallow subtropical lake (Taihu) by collecting samples from 17 different sites, covering two alternative states characterized by dominance or lack of submerged macrophytes, along a trophic gradient ranging from mesotrophic to hypertrophic areas. The macrophyte-dominated state was characterized by clear water and immobilized sediment, and the macrophytes-lacking state was characterized by the dominance of phytoplankton, frequent sediments, and a high turbidity. The use of DGGE, reverse line blot hybridization (RLB), and 16S rRNA gene cloning and sequencing, used for BCC analysis, showed a strong variation in the bacterioplankton community composition (BCC) between the two alternative ecological states. Comparative statistical analyses of BCC along the investigated ecological gradient revealed that the most dominant and most influential factor shaping the BCC, responsible for its heterogeneity in Taihu Lake, was the submersed macrophytes.

Top-down and bottom-up induced shifts in bacterial abundance production and community composition To understand the top-down and bottom-up induced shifts in bacterial abundance, Grossart et al. (2008) examined in-situ abundance and activities of the major bacterial groups in two substantially distinct compartments (in terms of major chemical and biological parameter) of an experimentally divided Lake Grosse, Fuchskuhle (Germany) and found a potential influence on the dynamics and composition of microbial communities. Three size fractions of water samples: (1) unfiltered, (2) prefiltered (through 5.0 μm

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pore size membranes to remove large particles and grazers), and (3) prefiltered (through 0.8 μm pore size filters to remove all potential bacterivores) were produced using dialysis bags which allowed for a relatively free exchange of nutrients, limiting solutes, and low molecular organic matter but fully prevented exchange of organisms. A pronounced difference was revealed in the growth rates among the major bacterial groups in relation to the treatments. It was observed that the specific growth rates surprisingly increased in all treatments when being transplanted into the acidic SW basin, indicating that pH and humic substances greatly affected growth of the betaproteobacteria group in the lake. The members of the Sphingobacteria/Flavobacteria group of the Bacteroidetes (both basins) as well as Actinobacteria (SW basin) were less abundant, especially in the presence of flagellates (4.5 × 108 copies per gram dry sediment). Twelve major bacterial phyla including Proteobacteria, Acidobacteria, Actinobacteria, Bacteroidetes, Chlorobi, Chloroflexi, Cyanobacteria, Firmicutes, Gemmatimonadetes, Nitrospirae, Planctomycetes, and Verrucomicrobia among the unclassified bacteria exist in these lakes. Among these bacterial phyla, Proteobacteria consisting of classes Betaproteobacteria, Gammaproteobacteria, and Deltaproteobacteria predominate the lake with Betaproteobacteria as the most dominant (relative abundance no less than 10%) in sediments of plateau freshwater lakes (10.5%–30.5%), except for Puzhehei Lake and Cibihu Lake. Gammaproteobacteria also predominates the Cibihu Lake (78.3%) and also shows dominance in many other lakes (except for Bailonghai, Changqiaohu, Sanjiaohai, and Jianhu Lakes).

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Chandra Tal and Dashair Lake, India Yadav, Sachan, Verma, and Saxena (2015) investigated the BCC of three western Himalayan Lakes by 16S rRNA gene sequencing and characterized some 232 bacterial isolates by employing 16S rDNA-Amplified Ribosomal DNA Restriction Analysis with three restriction endonucleases (Alu I, Msp I, and Hae III). 16S rRNA gene-based phylogenetic analysis revealed the presence of 82 distinct species of 31 different genera, belonging to phyla Actinobacteria, Bacteroidetes, Firmicutes, and Proteobacteria. The Himalayan Lakes Chandra Tal Lake (Moon Lake), a deep blue–water lake situated at an altitude of about 4250 masl in Spiti part of Lahul and Spiti district of Himachal Pradesh, India, is a source of the violent Chandra river. A number of bacterial genera including Aeromicrobium, Aeromonas, Arthrobacter, Bacillus, Brevundimonas, Exiguobacterium, Flavobacterium, Janibacter, Jeotgalicoccus, Lysinibacillus, Microbacterium, Paenibacillus, Plantibacter, Pseudomonas, Psychrobacter, Rhodococcus, Sphingobacterium, Sporosarcina, Staphylococcus, and Virgibacillus belonging to the phyla Actinobacteria, Proteobacteria, Firmicutes and Bacteroidetes are believed to be present in the lake (Yadav, Sachan, Verma, & Saxena, 2015). Further the lake is dominated by some niche-specific bacteria represented by Aeromonas hydrophila, Bacillus muralis, Bosea sp., Janthinobacterium lividum, Janthinobacterium sp., Jeotgalicoccus halotolerans, and Rhodococcus qingshengii (Fig. 1.4). In lake Dashair the bacteria which dominated belong to the phyla Actinobacteria, Proteobacteria, Firmicutes, and Bacteroidetes of the genera Aeromicrobium, Arthrobacter, Bacillus, Brevundimonas, Citricoccus, Exiguobacterium, Pantoea, Providencia, Rhodococcus, Sphingobacterium, Sporosarcina, Staphylococcus, Variovorax, Virgibacillus, and Yersinia. In Chandra Tal Lake the niche-specific bacteria are represented by Brevundimonas terrae, Citricoccus sp., Pseudomonas deceptionensis, Pseudomonas peli, and Pseudomonas xanthomarina (Fig. 1.4). Investigation of the culturable bacillus diversity in three subglacial lakes (Fig. 1.5) by Yadav, Sachan et al. (2016) showed that the population of bacillus in the water and sediment, enumerated through enrichment technique using the standard serial dilution plating method varied from 2.2 × 105 to 1.58 × 106 CFU per gram sediment or per mL water. Amplified ribosomal DNA restriction analysis (ARDRA) using three restriction enzymes (Alu I, Msp I, and Hae III) led to the clustering of 136 bacilli into 26, 23, and 22 clusters at 75% similarity index from the three Lakes (Chandra Tal, Dashair, and Pangong), respectively. Phylogenetic analysis based on 16S rRNA gene sequencing showed the presence of 35 bacilli, grouped in seven families

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Figure 1.4  Abundance of bacterial community composition of Chandra Tal and Dashair Lakes. (From, Yadav, A. N., Sachan, S. G., Verma, P., & Saxena, A. K. (2015). Prospecting cold deserts of north western himalayas for microbial diversity and plant growth promoting attributes. Journal of Bioscience and Bioengineering, 119, 683–693.)

(Bacillaceae, Staphylococcaceae, Bacillales incertae sedis, Planococcaceae, Paenibacillaceae, Sporolactobacillaceae, and Carnobacteriaceae) and 12 genera (Bacillus, Desemzia, Exiguobacterium, Jeotgalicoccus, Lysinibacillus, Paenibacillus, Planococcus, Pontibacillus, Sinobaca, Sporosarcina, Staphylococcus, and Virgibacillus) in the lakes (Fig. 1.6). Based on the optimal temperature

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Figure 1.5  Map depicting sampling locations of Chandra Tal and Dashair Lakes, India. (From, Yadav, A. N., Sachan, S. G., Verma, P., Kaushik, R., & Saxena, A. K. (2016). Cold active hydrolytic enzymes production by psychrotrophic Bacilli isolated from three sub-glacial lakes of NW Indian Himalayas. Journal of Basic Microbiology, 56, 294–307.)

required for the growth of these bacilli, they were grouped as psychrophilic, psychrotrophic, or psychrotolerant. Along with predominant bacilli, different niche-specific bacteria in Bacillus amyloliquefaciens, B. psychrosaccharolyticus, Exiguobacterium indicum, Jeotgalicoccus halotolerans, and Sporosarcina psychrophila are dominant in Chandra Tal Lake and Exiguobacterium marinum, Paenibacillus lautus, Sporosarcina globispora, and Virgibacillus halodenitrificans in Dashair Lake (Table 1.3).

Manasbal Lake, India Manasbal lake, located 30 km north of Srinagar, Kashmir, at an altitude of 1584 m above sea level with a predominantly rural surrounding in its immediate catchment is the deepest (about 12 m) of all the freshwater lakes fed by springs. It serves as an important natural water reservoir for the local population. The culturable bacterial diversity in the lake was investigated using

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Figure 1.6  Abundance of different Bacilli; (A) percentage of different families of isolated Bacilli; (B) distribution of total Bacilli (C) distribution of different Bacilli in lakes. (From, Yadav, A. N., Sachan, S. G., Verma, P., Kaushik, R., & Saxena, A. K. (2016). Cold active hydrolytic enzymes production by psychrotrophic Bacilli isolated from three sub-glacial lakes of NW Indian Himalayas. Journal of Basic Microbiology, 56, 294–307.)

serial dilution and spread plate methods with the subjective application of gram’s staining, microscopy, biochemical and molecular characterization (Shafi, Kamili, Shah, & Bandh, 2017). Based on the study it remains an established fact that this freshwater lake embodies a great diversity of culturable bacteria belonging to three major phyla, namely, Firmicutes,

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Table 1.3  Diversity indices and niche-specificity of bacilli isolated from the Chandra Tal Lake. Chandra Tal Lake Dashair Lake

Total abundance Species richness Chao-1 Evenness (J′) Simpson’s (D) Shannon (H) Niche-specific bacilli

37 23 30 0.91 0.95 3.04 Bacillus amyloliquefaciens, B. psychrosaccharolyticus, Exiguobacterium indicum, Jeotgalicoccus halotolerans, Sporosarcina psychrophila

47 22 25 0.91 0.95 2.99 Exiguobacterium marinum, Paenibacillus lautus, Sporosarcina globispora, Virgibacillus halodenitrificans

From,Yadav, A. N., Sachan, S. G.,Verma, P., Kaushik, R., & Saxena, A. K. (2016). Cold active hydrolytic enzymes production by psychrotrophic Bacilli isolated from three sub-glacial lakes of NW Indian Himalayas. Journal of Basic Microbiology, 56, 294–307.

Proteobacteria, and Bacteroidetes with varied contributions. However, the maximum relative abundance was shown by the genus Bacillus, followed by Alcaligenes, Lysinibacillus, Chryseobacterium, Pseudochrobactrum and Paenochrobactrum, Pseudomonas, Stenotrophomonas, Amorphus, Caulobacter, Brevibacillus, Brevundimonas, Pusillimonas, and Advenella. Various species belonging to genus Bacillus present in the lake water are Bacillus aerius, B. altitudinis, B. anthracis, B. cereus, B. ginsengisoli, B. pumilus, B. safensis, B. stratosphericus, B. subtilis, B. tequilensis, B. thermocopriae, and B. thuringiensis (Shafi, Kamili, Shah, Bandh, & Dar, 2017). Lysinibacillus boronitolerans, L. pakistanensis, and L. sphaericus of genus Lysinibacillus are also reported to be present in the lake water along with Brevibacillus agri and many other bacterial species, genuses, and phylas.

Dal Lake, India Dal Lake is an urban lake, which is the second largest in the state of Jammu and Kashmir. It is an important source for commercial operations in fishing and water plant harvesting. Using serial dilution and spread plate technique (Saleem et al., 2011) the bacterial community composition of this lake was investigated and the presence of a substantial number of coliform bacteria in the lake water was revealed. Escherichia coli, E. aerogenes, Bacillus spp., Staphylococcus aureus, Micrococcus luteus, Pseudomonas

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aeruginosa, Klebsiella pneumoniae, Vibrio cholerae, Salmonella spp., Serratia marcescens, and Citrobacter freundii are a few bacterial species present in this urban freshwater lake. Further the culture dependent and culture independent techniques used (Venkatachalam et al., 2015) to investigate the bacterial community composition of Dal Lake revealed the predominance of bacteria belonging to Firmicutes and Proteobacteria. It is revealed that the lake water harbors the bacterial species Bacillus asahii, Bacillus muralis, Exiguobacterium aurantiacum, Pseudomonas graminis, and Pseudomonas vancouverensis. A recent study (Khan, 2018) on bacterial 16S rRNA sequences shows the distribution of Acidovorax, Acinetobacter, Arthrobacter, Bacillus, Bosea, Comamonas, Enterobacter, Hydrogenophaga, Micrococcus, Paenisporosarcina, Pseudomonas, Rheinheimera, Rhodococcus, Sporosarcina, and Streptomyces predominantly available in Dal Lake.

Gurudongmar Lake, India Gurudongmar Lake, at the footfall of Kanchenjunga peak in eastern part of the Himalayas is located at an altitude of 5250 m above mean sea level. The bacterial community composition of this lake studied (Sahay et al., 2013) by culturable techniques revealed the range of bacterial cell counts as 118.4 to 193.3 × 104. The amplified ribosomal DNA restriction analysis using three restriction enzymes facilitated the grouping of the bacterial isolates into 96 genotypes at ≥85% polymorphism. Phylogenetic analysis using 16S rRNA gene sequences revealed that the bacterial strains from the lake belonged to Firmicutes, α-Proteobacteria, β-Proteobacteria, γ-Proteobacteria, and Actinobacteria. The predominantly present bacterial communities in the lake include bacterial species belonging to genus Arthrobacter, Bacillus, Brevundimonas, Caulobacter, Duganella, Herbaspirillum, Janthinobacterium, Lysinibacillus, Paenibacillus, Paucibacter, Pseudoalteromonas, Pseudomonas, Sphingomonas, and Undibacterium.

Comparative study of some freshwater lakes in India The freshwater lakes in cold environments are the hotspots of bacterial biodiversity. Cold adapted microbes are ubiquitous in nature and can be isolated from permanently ice-covered lakes.Yadav,Verma, Sachan, and Saxena (2017) worked on the BCC of various freshwater lakes in India including Dashair Lake, Gurudongmar lake, Chandra Tal Lake, and Roopkund Lake, using culture-dependent techniques and observed the presence of bacteria belonging

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to different phyla like Actinobacteria, Bacteroidetes, Basidiomycota, Chlamydiae, Chloroflexi, Cyanobacteria, Firmicutes, and Proteobacteria of diverse genera like Arthrobacter, Bacillus, Brevundimonas, Cellulosimicrobium, Citricoccus, Enterobacter, Exiguobacterium, Flavobacterium, Janthinobacterium, Lysinibacillus, Methylobacterium, Paenibacillus, Pantoea, Planococcus, Pontibacillus, Providencia, Pseudomonas, Psychrobacter, Rhodococcus, Sanguibacter, Sphingobacterium, Sporosarcina, Staphylococcus, Stenotrophomonas, and Virgibacillus (Pradhan et al., 2010; Sahay et al., 2013; Srivastava et al., 2013; Venkatachalam et al., 2015; Yadav, 2015, p. 234;Yadav, Sachan et al., 2016;Yadav, Sachan,Verma, & Saxena, 2015;Yadav,Verma, Kumar et al., 2017;Yadav,Verma, Sachan et al., 2017). Based on the studies of different habitats of cold freshwater environments from Indian Himalayan regions, it is evident that Arthrobacter, Bacillus, Exiguobacterium, Paenibacillus, Planococcus, Pseudomonas, Psychrobacter, Providencia, Sporosarcina, and Staphylococcus are ubiquitous in nature and are thriving well in Dashair Lake, Gurudongmar Lake, Chandra Tal Lake, Dal Lake, and Roopkund Lake, whereas some unique microbes known as niche-specific bacteria are specific to specific habitats as, for example, Variovorax is found in Dashair Lake, Duganella, Herbaspirillum, Iodobacter, Novosphingobium, Oxalobacteraceae, Paucibacter, Pectobacterium, Pseudoalteromonas, Pseudomonadaceae, and Undibacterium found in Gurudongmar Lake, Microbacterium and Aeromonas found in Chandra Tal Lake, and Agromyces, Brevibacterium, Cedecea, Enterobacter, Erwinia, and Micrococcus found in Dal Lake (Fig. 1.7). The psychrophilic and psychrotolerant microbes from Indian Himalayan regions have engrossed the scientific community due to their potentially beneficial role in ultra-low temperature conditions and could be applied to a broad range of industrial, agricultural, and medical processes. Psychrotrophic microbes could be valuable in agriculture as bioinoculants and biocontrol agents for low temperature habitats. The use of psychrophiles as biofertilizers, biocontrol agents, and bioremediators would be of great use in agriculture under cold climatic conditions.The comprehensive analyses of diversity of different genera by prospecting cold environments helps in the development of a huge database including baseline information on the distribution of psychrotrophic microbes in different niches and identifying nichespecific microbes (Yadav,Verma, Sachan et al., 2017).

Conclusions Bacterial community composition in freshwater environment varies with different environmental variables. Lake water and sediments of the different habitats, each with unique intrinsic environmental conditions, result in their

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Figure 1.7 Relative diversity of bacterial community composition among different Indian Himalayan lakes.

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unique bacterial community composition. In the past there was a notion that microbes inhabiting terrestrial and aquatic habitats were quite similar, but the frequent use of molecular techniques has helped in better understanding the freshwater bacterial communities to a larger extent by retrieving innumerably sequenced 16S rRNA genes from these ecosystems. Study of these bacterial communities in lake ecosystems is gaining more importance not only to understand their evolution but also to determine the ecological impact of certain niches and changing climate on their distribution and diversity, as they not only participate in biogeochemical cycles but also decompose organic materials into nutrients which influence the material circulation in aquatic ecosystems and hence control the water quality in these freshwater ecosystems. Besides this, nowadays bacteria are also gaining attention for their byproducts such as enzymes like amylases, lipases, proteases, phospholipases, catalases being extracted for their wide biochemical applications. Thus it becomes important to understand diversity of microbial genetic resources, their distribution pattern, functional annotations, and factors regulating their diversity in these aquatic ecosystems. Structure of bacterial communities in lakes is maintained by variable environmental conditions across space and time representing habitat heterogeneity triggered by bottom-up (resource availability) and/or top-down controls (mortality factors) leading to distinct spatial (longitudinal and vertical) and temporal patterns of distribution.Variability in these environmental conditions give rise to habitat heterogeneities and these heterogeneities have a strong bearing on the overall dynamics and composition of the bacterial communities. Thus, it is critically important to understand how function and composition of bacterial communities respond to such disturbances in different systems. These disturbances together with the effect of geographic location and trophic status of the lake have considerable impact on the bacterial community composition in the lake ecosystems as it is an observed fact that Arthrobacter, Bacillus, Exiguobacterium, Paenibacillus, Planococcus, Pseudomonas, Psychrobacter, Providencia, Sporosarcina, and Staphylococcus are ubiquitous in nature, thriving well in cold freshwater environments whereas some unique microbes known as niche-specific bacteria are specific to specific habitats as, for example, Variovorax, suggesting that the specific drivers have distinct relative importance for community composition.

Acknowledgments The authors are grateful to Prof. Harcharan Singh Dhaliwal,Vice Chancellor, Eternal University, and Baru Sahib, Himachal Pradesh, India, for their constant encouragement and facilitation.

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CHAPTER 2

Bacterial diversity of the rock-water interface in freshwater ecosystem Rubiya Dar1, Suhaib A. Bandh2, Sana Shafi2, Nowsheen Shameem2 1Center

of Research for Development (CORD)/P.G. Department of Environmental Science, University of Kashmir, Srinagar, India; 2P.G. Department of Environmental Science, Sri Pratap College Campus, Cluster University, Srinagar, India

Introduction An interface is the limit between two phases in a heterogeneous system. Solid-fluid (rock-water) interfaces are imperative in microbial ecology, as they impact microbial life in different ways (Marshall, 1976). Microorganisms attach within minutes to most lifeless solid substrates submerged in water (Bitton & Marshall, 1980), where they develop to form biofilms (Characklis & Marshall, 1990). In water bodies, complex combinations of microorganisms named biofilms are formed at the rock-water interface, and most microorganisms on the earth live in such aggregations (Costerton, Cheng, & Geesey, 1987). Biofilms which cover almost every rock-water interface on earth are called as epilithic river biofilms. They are complex matrixenclosed communities, also described as microbial landscapes (Battin et al., 2007). Within these microbial landscapes the prokaryotic and eukaryotic microorganisms are closely associated. Bacteria, mainly belonging to Betaproteobacteria (Araya,Tani,Takagi,Yamaguchi, & Nasu, 2003; Manz,WendtPotthoff, Neu, Szewzyk, & Lawrence, 1999) and diatoms embedded in these microbial landscapes (Battin, Kaplan, Newbold, Cheng, & Hansen, 2003; Besemer et al., 2007) play a fundamental role in their substrate colonization by producing extracellular polymeric substances (EPS) (Stolz, 2000). These pioneering microorganisms facilitate the establishment of the next arrivals, including autotrophic and heterotrophic microorganisms (Roeselers, Van Loosdrecht, & Muyzer, 2007) such as bacteria belonging to Alphaproteobacteria and Bacteroidetes, Cyanobacteria, Microalgae (Barranguet et al., 2005; Brasell, Heath, Ryan, & Wood, 2015; Roeselers et al., 2007), and other microorganisms like archaea, fungi, protozoa, small metazoans, and Freshwater Microbiology ISBN 978-0-12-817495-1 https://doi.org/10.1016/B978-0-12-817495-1.00002-5

© 2019 Elsevier Inc. All rights reserved.

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viruses (Battin et al., 2007; Beraldi-Campesi et al., 2012; Besemer, 2015). From a functional view point, cyanobacteria, diatoms, and green algae are recognized as principal primary producers in periphyton (Lamberti, 1996; Roberts, Sabater, & Beardall, 2004); however, other potentially photosynthetic bacterial taxa including purple bacteria are also frequently detected in the epilithic biofilms (Anderson-Glenna, Bakkestuen, & Clipson, 2008; Beraldi-Campesi et al., 2012; Bricheux et al., 2013; Drury, Rosi-Marshall, & Kelly, 2013) and among them, members of genus Rhodobacter are able to grow under aerobic as well as anaerobic conditions (Blankenship, 2014). The autotrophic microorganisms in these biofilms have been described as the principal producers of the organic matter used by heterotrophic or mixotrophic microorganisms in these biofilms (Kamjunke, Herzsprung, & Neu, 2015; Romani et al., 2004; Romani & Sabater, 1999). Further predators, such as protists exploiting biofilms as a food source, are the drivers of carbon transfer to higher trophic levels (Risse-Buhl et al., 2012). In most studies addressing the microbial communities of stream biofilms, the microalgal and bacterial components have also been described separately. On one hand, the microalgal component has attracted the attention of researchers dealing with the use of these microorganisms as bioindicators of water quality (Fetscher et al., 2014; Kelly & Whitton, 1998; Stevenson & Smol, 2003; Visco et al., 2015) and identification of environmental factors and processes impacting biofilm development in lotic environments (Biggs, 1996), and on the other hand, the composition of bacterial communities in periphytic biofilms using 16S rRNA fingerprinting methods and, more recently, highthroughput sequencing approaches (Besemer et al., 2012), with the goal to better understand the spatial and temporal variation occurring in these communities has been worked out (Jackson, Churchill, & Roden, 2001; Lyautey, Jackson, Cayrou, Rols, & Garabétian, 2005; Margulies et al., 2005). There are no data based on the use of high-throughput sequencing that simultaneously describe the spatiotemporal variation in the composition of bacterial and microeukaryotic communities in epilithic stream biofilms despite the possible application of such approaches for identifying the relative impacts of environmental factors on these two communities and the putative interactions between them. To address the paucity of data, a study was performed on the epilithic biofilms collected at different sampling sites in the Loue River (Zancarini et al., 2017), located in the eastern part of France to better understand the variation in microbial community vis-à-vis the variation in the physicochemical parameters. A network analysis performed to obtain an overview of the positive and negative relationships

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between the dominant bacterial and microeukaryote Operational Taxonmic units (OTUs) within biofilms and some environmental variables was observed in the said river indicating that there exists an effective relationship between the two variables.

Sessile bacteria Sessile bacteria are the initial colonizers of submerged surfaces, and they probably condition the substrate for subsequent colonization by other organisms (Corpe, 1970b; Hirsch & Pankratz, 1970). Adhesion, in many instances, occurs through the excretion of polymeric fibers which anchor the cell to a surface (Corpe, 1970a; Marshall, Stout, & Mitchell, 1971a). Further it is mediated by a network of fibers which, in mass, constitute the layer of slime covering the streambed, as some fibers have been shown to anchor bacteria to inert surfaces in some aquatic environments (Fletcher & Floodgate, 1973; Jones Roth, & Sanders, 1969; Paerl, 1975). Henrici (1933) demonstrated the prolific attachment of bacteria to microscope slides submerged in freshwater while Zeikus and Brock (1972) and Bott (1975) determined the colonization rate of natural stream bacteria on submerged artificial surfaces over short intervals and measured their capacity to take up selected nutrients. Nevertheless, there is a little understanding of the relative importance of this microbial community, in terms of either its relationship with other organisms, its seasonal fluctuations, or its overall number and activities. The establishment and maintenance of the population of sessile bacteria in different habitats is maintained by a number of factors as, for example, the coincident variations in sessile bacterial and algal concentrations in Twin and Middle Forks suggest that it is regulated by epilithic primary production because the epilithic algae provides a solid surface for bacterial colonization. Here the microbial population on the exposed upper surfaces of submerged rocks was to a greater extent controlled by epilithic primary production and those microorganisms which were growing on the underside or less exposed surfaces were more influenced by the decomposition of allochthonous organic carbon.

Attachment of freshwater bacteria to solid surfaces The attachment of bacteria to the submerged solid surfaces is of greater importance in aquatic environments, as it provides nutrients to the freeliving bacteria and (nutrient-deficient) allows the bacteria to grow and

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survive (Corpe, 1970a; Marshall, 1976; Meadows, 1971). Bacteria get attached to a variety of surfaces like ships, oil drilling rigs, pipelines, and heat exchangers and are not eliminated by washout, hence ensuring the first stage in the deterioration of such structures through corrosion or clogging (Corpe, 1970a; Miller, Rapean, & Wbedon, 1948). In bacterial attachment the forces involved are not fully understood, but it is evident from numerous studies of different systems that wettability is an important factor in bacterial adhesion on various surfaces (Dexter, Sullivan,Williams, & Watson, 1975; Pringle & Fletcher, 1983; Wiencek & Fletcher, 1997). Understanding the adhesion properties of bacteria in fresh water environments requires detailed information on the conditioning components of the aquatic environment, the substrata, and the bacterial population present (Fletcher & Loeb, 1979). The properties of substratum have a great influence on the attachment of bacteria especially in the initial stages, for instance, freshwater bacterial isolates prefer to attach to hydrophobic surfaces in comparison to hydrophilic surface (Pringle & Fletcher, 1983). Thus the dominant hydrophobic or hydrophilic surface character plays a fundamental role in bacterial attachment. Bacterial adhesion (Chen & Strevett, 2003) to the surface is determined not only by interfacial exchange between bacteria and the surface but also by interactions between deposited and suspended bacterial cells. As observed on metallic surfaces and silicon oxide surfaces, bacterial adhesions are also enhanced by the increasing surface hydrophobicity (Gallardo-Moreno, Gonzalez-Martın, Perez-Giraldo, Bruque, & GomezGarcıa, 2002; Sheng, Ting, & Pehkonen, 2007). Morais, Bernardes-Filho, and Assis (2009) demonstrated that there exists a good relation between physicochemical properties of the substratum and bacterial attachment and thus provided an interesting reference for material selection for better bacterial adhesion. Besides this there are several other parameters that influence the attachment of bacteria to the solid surfaces such as Van der Waals forces, shape of the electrical double layer (Marshall et al., 1971a), chemotaxis (Young & Mitchell, 1972), ability of the organism to produce polymeric fibrils (Corpe, 1970a; Marshall, Stout, & Mitchell, 1971a,b), and surface charge (Corpe, 1970b; Neihof & Loeb, 1972).

Microbial epilithic and endolithic biofilms Microbial biofilms defined as living organic interfaces between inorganic physical states of matter act as mediators in interactions that occur at the interfaces between the lithosphere on one side and hydrosphere and

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atmosphere on the other side with some of them having the ability to dissolve the substrate and penetrate into its interior. Microbial populations of the lithobiontic ecological niches thus include both the epilithic (exterior) and endolithic (interior) communities of these niches. Endoliths actively penetrate calcareous substrates and thereby create the endolithic microenvironment, whereas cryptoendoliths and chasmoendoliths take advantage of the existing internal microenvironments which they modify (Golubic, Friedmann, & Schneider, 1981; Schneider & Le Campion-Alsumard, 1999). Microbial endoliths cope successfully with ecological conditions ranging from extremes of polar and alpine deserts to the most optimized environments in tropical reefs (Chazottes, Le Campion-Alsumard, & PeyrotClausade, 1995; Jaag, 1945; Vincent, 2000; Wynn-Williams, 2000). Their colonization involves pioneers of newly exposed substrates (Le CampionAlsumard, 1975), and successions of changing populations toward establishment of stratified microbial ecosystems. The distribution of endolithic biofilms is universal, but the ecological settings under which they occur are extremely diverse and so are the congregations of microbial endoliths that occupy them. Their constituents differ significantly from one another in appearance, complexity, taxonomic composition, metabolic and ecological properties, as well as in the timing of their activities. Within the euphotic zone the autochthonous primary producers, mostly cyanobacteria and algae, usually dominate endolithic communities, while the endolithic communities which extend into the aphotic environments are composed of heterotrophs which depend on organic matter in the substrate they penetrate (Golubic, Perkins, & Lukas, 1975). Many prokaryotic and eukaryotic microbial endoliths leave recognizable and fossilizable traces in the substrate which contain information about the paleoenvironments they once occupied and it is for this reason, microborings of modern and ancient endoliths are analyzed, compared, named, and classified separately from the organisms that made them the trace fossils (Radtke, 1991;Vogel et al., 1999). Understanding the ecological processes that lead to the structure and function of microbial communities in the environment is a field that raised some greater interest in recent years, due to the crucial roles they play in human health, natural ecosystems, and industrial biotechnology (Kastman et al., 2016; Widder et al., 2016). Interestingly, biotic interactions among microbes have been widely described as a force driving the structuring of environmental communities (Maida et al., 2016). The assemblage of different strains in a microbial community is the result of many factors such as random drift, selection by abiotic conditions, and biotic interactions

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(Stoodley, Sauer, Davies, & Costerton, 2002). Abiotic conditions that have been largely studied in the recent past (Mathur et al., 2007; Rubin & Leff, 2007) vary depending on many factors and can be manipulated at laboratory scale to understand their influence on bacterial community composition (Stubbendieck & Straight, 2016). However, the complexity of biotic interactions, which plays a major role by altering the structure and the degree of organization of complex communities is difficult to understand and challenging to investigate at laboratory scale (Battin, Besemer, Bengtsson, Romani, & Packmann, 2016; Moenne-Loccoz, Mavingui, Combes, & Steinberg, 2015). Investigation of the structure and composition of epilithic biofilms (Battin et al., 2007; Kobayashi et al., 2009; Ledger & Hildrew, 1998) lead to the suggestion that the structure and composition of aquatic epilithic biofilms vary in response to many factors such as anthropogenic nutrient and organic matter (Kobayashi et al., 2009). Geographical factors, like the altitudinal gradient, also play an important role in the composition and diversity of epilithic communities (Bartrons, Catalan, & Casamayor, 2012; Besemer et al., 2013; Wilhelm et al., 2015). Further there exists a strong interaction between the prokaryotic and eukaryotic microbial communities in the epilithons (Zancarini et al., 2017). The different factors result in the spatial structuring of these epilithic communities as was observed in the epilithic biofilms of the Acquarossa River (Viterbo), which were particularly intriguing in terms of spatial structuring. Interestingly, they formed two physically separate and colored biofilms that were in part red and in part black existing very close to each other. However, they did not blend together, thus maintaining a well-defined borderline, and this peculiarity raised many questions about the biotic and abiotic phenomena that avoid the mixing of the two biofilms. The Acquarossa site is characterized by the presence of an ancient Etruscan village (625–550 BC), historically known for its metallurgic activity (Harrison, Cattani, & Turfa, 2010), which causes a widespread and significant dispersal of huge amounts of some undesirable heavy metals, especially arsenic into the environment (Hook, 2007). The river also characterized by a high iron concentration, confers a red color to the water and gives it the name Acquarossa, which in Italian means “red water.” From a scientific viewpoint, there is almost a complete lack of information on this site, especially concerning its biological and environmental features as most of the available literature focuses on its archeological and historical characteristics (Meyers, 2003, 2013; Staccioli, 1976). Although a few studies have focused on its biological aspects and characteristics, lack of information on the microbiological aspects of the

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river aroused great interest in this unexplored site. To the best of authors’ knowledge this was the first study exploring the structure and complexity of bacterial communities of rock biofilms along the river course, focusing on both chemical and microbiological aspects. Data obtained from this study somewhat explained the role that biotic factors play in driving the structuring of the bacterial communities of rock biofilms. On the basis of high-throughput sequencing (HTS) data, iron-oxidizing bacteria, mainly related to Sideroxydans sp. and Gallionellaceae represent an important fraction of the entire microbiota of the red-colored biofilms as the iron-oxidizing bacteria are a group of bacteria associated to aqueous environments containing considerable concentrations of Fe(II) (Emerson et al., 2013; Emerson, Fleming, & McBeth, 2010). The presence of high amounts of Fe2+ in the river (Hem & Cropper, 1959) sustains the activity of iron-oxidizing bacteria (Emerson et al., 2010) and deposition of iron hydroxides in biofilms dominated by these microorganisms. Therefore, the red color shown by this biofilm was related to the presence of iron hydroxides that accumulate within the biofilm matrix (presumably due to the formation of Fe2O3), and the color of the black epilithon was related to the presence of other compounds in the river water with one possible explanation being the presence of iron sulfides, known to form a black-colored precipitate (Berner, 1963), a result of the combination of Fe2+ with S by sulfate-reducing bacteria in the biofilm matrix. HTS data revealed the presence of sulfate-reducing bacteria affiliated to Nitrospirae and Deltaproteobacteria both in red and black epilithic biofilms. Among them, the analysis of OTUs at genus level revealed the presence of sulfate-reducing Desulfobulbus and Desulfuromonas. Furthermore, it was also inferred that the possibility of black color might be due to the chemical reactions by other bacterial and/ or archaeal groups leading to the production of black precipitates (Bartrons et al., 2012; Ragon et al., 2012). Moreover a limited number of dominant bacterial phyla prevail in the rock biofilm bacterial communities (McNamara & Mitchell, 2005). The bacterial communities in black and red epilithons were dominated by Acinetobacter and unclassified Gallionellaceae, Sideroxydans sp., and Gallionella sp., respectively. The Acinetobacter sp. was more abundant in black epilithons, whereas Pseudomonas sp. was more abundant in red epilithons. Bacterial plate counts gave comparable results in both red and black epilithon samples revealing that there was not a significant difference between the two biofilms. The complete absence of RAPD haplotype sharing between red and black epilithon both for Acinetobacter and Pseudomonas suggested that the two communities are genetically

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differentiated at the strain level, and such observations help us to understand that when two communities coexist in the same environment and are spatially and physically in contact with each other, there could be some selective pressures that create and/or maintain a barrier to the free intermix of bacterial strains (Chiellini, Iannelli, Lena, Gullo, & Petroni, 2014). These selective pressures may be likely due to biotic conditions such as the production of antibacterial compounds, as previously shown for other bacterial communities (Maida et al., 2016; Mengoni et al., 2014).

Microbial dynamics of epilithic mat communities The need to predict microbial community dynamics has stimulated the development of “black box” mathematical models in which microbial population dynamics is represented by global empirical functions that do not attempt to address the inner workings of the microbial community. Ranging from food science to climate modeling and wastewater treatment, this approach has proved useful. However, such models do not aim to provide mechanistic insight and are necessarily limited by the data sets to which they are fitted. But the high-throughput sequencing, proteomics, and metabolomics now allow us to catalog the diversity of microbial communities to an unprecedented level of detail. These data represent a relatively unbiased compositional snapshot of the species, genes, metabolites, and activities that are present in a given microbial community. However the key challenge now, is to convert this empirical knowledge into fundamental insights and testable predictions, which can be used to improve microbial community function for useful purposes. Here, we claim that addressing this challenge will require the development of mathematical models with a basis in mechanistic understanding, integrated with controlled experiments. This integration between theory and experimentation is a crucial “missing link” in current microbial ecology, and this link is a key step in discovering possible design principles of microbial community assembly and function. Studies were conducted to examine interrelationships between the autotrophic and heterotrophic populations within an epilithic community in the outlet stream of a high alpine lake, and it was found that the level of nitrates, phosphates, and total organic compounds in the lake was consistently near the lower limits of detectability. Microscopic examination of the community by scanning electron microscopy and phase-contrast light microscopy revealed filamentous algae, diatoms, and bacteria embedded within a dense gelatinous matrix. Bacterial heterotrophic activity as measured by Vmax,

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turnover rate, and relative activity increased significantly as the phototrophic community declined, and this trend in heterotrophic activity was not accompanied by an increase in total bacterial numbers as determined by epiilluminated fluorescence microscopy. The catabolic activity of the sessile bacteria appeared to be positively influenced by changes in the mat environment resulting from the decline of the phototrophic populations (Haack & McFeters, 1982). During initial biofilm development, there is usually a dominance of Beta-proteobacteria in the bacterial population followed by a rapid increase of Alpha-proteobacteria and bacteria affiliated to the Cytophaga– Flavobacterium group. In mature biofilms, Alpha-proteobacteria and Cytophaga–Flavobacteria continue to be the prevalent bacterial groups. Beta-proteobacteria constitutes the morphologically most diverse group within the biofilm communities. Further the presence of sulfate-reducing bacteria (SRB) affiliated to the Desulfovibrionaceae and Desulfobacteriaceae confirms the range of metabolic potential within the lotic biofilms (Manz et al., 1999). In a bid to understand the bacterial community composition of epilithic biofilms, Golubic and Schneider (2003) studied the littoral epilithic biofilms in five connected oligotrophic high mountain lakes located at different altitudes by genetic fingerprinting and clone libraries of the 16S rRNA gene. Different intralake samples were analyzed and consistent changes in community structure were observed along the altitudinal gradient, particularly related to the location of the lake above or below the tree line. Epilithic biofilm genetic fingerprints were more diverse among lakes than within lakes and significantly different between montane (below the tree line) and alpine lakes (above the tree line). The genetic richness in the epilithic biofilms was much higher than the planktons of the same lacustrine area studied in previous works, with significantly idiosyncratic phylogenetic composition (specifically distinct from lake plankton or mountain soils). Data suggest the coexistence of aerobic, anaerobic, phototrophic, and chemotrophic microorganisms in the biofilm with Bacteroidetes and Cyanobacteria being the most important bacterial taxa, followed by Alpha-Proteobacteria, Beta-Proteobacteria, Gamma-Proteobacteria, and DeltaProteobacteria, Chlorobi, Planctomycetes, and Verrucomicrobia. More than 35% of the total sequences matched at