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Eugene Rosenberg Current Knowledge and Unanswered Questions The Microbiomes of Humans, Animals, Plants, and the Environment 2 Eugene Rosenberg Microbiomes Current Knowledge and Unanswered Questions The Microbiomes of Humans, Animals, Plants, and the Environment Volume 2 This series covers microbiome topics from all natural habitats. Microbiome research is a vibrant field of science that offers a new perspective on Microbiology with a more comprehensive view on different microorganisms (microbiota) living and working together as a community (microbiome). Even though microbial communities in the environment have long been examined, this scientific movement also follows the increasing interest in microbiomes from humans, animals and plants. First and foremost, microbiome research tries to unravel how individual species within the community influence and communicate with each other. Addi- tionally, scientists explore the delicate relationship between a microbiome and its habitat, as small changes in either, can have a profound impact on the other. With individual research volumes, this series reflects the vast diversity of Microbiomes and highlights the impact of this field in Microbiology. More information about this series at http://www.springer.com/series/16462 Eugene Rosenberg Microbiomes Current Knowledge and Unanswered Questions Eugene Rosenberg Department of Molecular Microbiology & Biotechnology Tel Aviv University Givat Shmuel, Tel Aviv, Israel ISSN 2662-611X ISSN 2662-6128 (electronic) The Microbiomes of Humans, Animals, Plants, and the Environment ISBN 978-3-030-65316-3 ISBN 978-3-030-65317-0 (eBook) https://doi.org/10.1007/978-3-030-65317-0 # Springer Nature Switzerland AG 2021 This work is subject to copyright. All rights are reserved by the Publisher, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilms or in any other physical way, and transmission or information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed. The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. The publisher, the authors, and the editors are safe to assume that the advice and information in this book are believed to be true and accurate at the date of publication. Neither the publisher nor the authors or the editors give a warranty, expressed or implied, with respect to the material contained herein or for any errors or omissions that may have been made. The publisher remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. This Springer imprint is published by the registered company Springer Nature Switzerland AG. The registered company address is: Gewerbestrasse 11, 6330 Cham, Switzerland To Ilana, my scientific and life partner Preface The great scientific news that greeted this century was the campaign to decode the human genome. We must now remind ourselves that much of the biological composition of our bodies consists of genomes other than the human. Multitudes of bacteria and viruses occupy our skin, our mucous membranes, and our intestinal tract. They are likely to play a much larger role in developing—and resisting—disease than we realize. Understanding this cohabitation of genomes within the human body—what I call the microbiome—is central to understanding the dynamics of health and disease. Joshua Lederberg (2004) We are in the midst of a paradigm change in biology. Plants and animals, including humans, can no longer be considered individuals, but rather, all are holobionts consisting of complex interactions between the host and abundant and diverse symbiotic microorganisms. During the last two decades, numerous studies have demonstrated that these symbionts play a critical role in many functions of macroorganisms, including metabolism, behavior, development, adaptation, and evolution (Gilbert et al. 2012; McFall-Ngai et al. 2013). Thus, individual phenotypes result from the combined expression of the host and microbiome genomes, leading to the popularization of notions of the holobiont and the hologenome (Zilber- Rosenberg and Rosenberg 2008; Rosenberg and Zilber-Rosenberg 2013, 2018). I would like to mention briefly how Ilana Zilber-Rosenberg and I came upon the hologenome concept. In 1996, we discovered bacterial bleaching of corals (Kushmaro et al. 1996, 1997). After six years of studying the mechanisms of infection (reviewed in Rosenberg and Falkovitz 2004), we observed that the coral had become resistant to infection and bleaching by the specific coral pathogen, Vibrio shiloi. Because corals possess a restricted adaptive immune system and do not produce antibodies, we presented the coral probiotic hypothesis (Reshef et al. 2006) to explain the coral development of resistance to infection by V. shiloi. The hypothesis posits that the corals acquired “beneficial” bacteria from the marine environment that prevented infection by the pathogen. If it is possible to have epidemics of pathogens, why is it not possible (even more likely) to have epidemics of beneficial bacteria? They simply generally go unnoticed. Subsequently, we published data that support the coral probiotic hypothesis (Mills et al. 2013). A dynamic relationship exists between symbiotic microorganisms and corals under different environmental conditions that selects for the most advantageous coral holobiont in the context of the prevailing conditions. vii viii Preface Although the coral probiotic hypothesis inspired the hologenome concept, the concept was developed by consideration of the vast amount of data published by others. I especially acknowledge Forest Rohwer, whose pioneer article on the coral holobiont had a strong influence on us (Rohwer et al. 2001), Jan Sapp, whose book, Evolution by Association: A History of Symbiosis, was a stimulating introduction into the subject (Sapp 1994), and Eva Jablonka and Marion Lamb for their stimulating book, Evolution in Four Dimensions, which argues that there is more to heredity than genes (Jablonka and Lamb 2005). In a previous book (Rosenberg and Zilber-Rosenberg 2013), we began by putting forth the hologenome concept of evolution. This was followed by a systematic review of the experimental evidence that existed at the time supporting the concept. This book takes a different approach. I first describe in some detail current knowl- edge of the properties of microbiomes, including their microbial abundance and diversity (Chap. 2), interaction with their hosts (Chap. 4), modes of transmission (Chap. 5), and role in genetic variation (Chap. 8) and evolution (Chap. 9)of holobionts. Chaps. 6 and 7 discuss eukaryotic microbiota and viruses, respectively. After presenting information on microbiomes, I then propose that the hologenome concept of evolution provides a useful framework for understanding these data, taking into consideration published theoretical arguments, supporting (e.g., Fraune and Bosch 2010; Bordenstein and Theis 2015; Roughgarden et al. 2018) and challenging (e.g., Moran and Sloan 2015; Douglas and Werren 2016) the concept. Chap. 10 discusses microbiomes in medicine and agriculture, including probiotics, prebiotics, synbiotics, fecal transplantation, and phage therapy. I conclude with a chapter on some philosophical and sociological implications of microbiome research. One of the problems I faced in completing this book was each time I completed a draft, important new publications appeared, which caused me to rewrite many of the chapters. This was not surprising because of the fast-moving nature of this subject (see Fig. P.1). In addition to many high impact journals now devoting sections to microbiomes, several relatively new journals are devoted entirely to microbiome research, including Animal Microbiomes, Microbiome, Human Microbiome, Cell Host and Microbiome, mBio, mSystems, and Gut Microbes. The literature search was completed in July 2020. I thank my partner, Ilana Zilber-Rosenberg, for the enormous help she gave me in writing this book, providing me current references, discussing every chapter, and moderating my tendency to overstate conclusions from the existing data. I also thank Ed Kosower, Gil Sharon, Ariel Kushmaro, Ehud Lamm, Omry Koren, and David Gutnick for providing useful references and interesting discussions. It was a pleasure to work with Markus Spaeth, Bibhuti Sharma, Andrea Schlitzberger, and the other editors of Springer- Verlag in bringing the manuscript to publication. Preface ix Fig. P.1 Occurrence of terms “Holobiont” (N ¼ 695) and “Hologenome” (N ¼ 102) in Web of Science Core Collection from 1991 to 2018. Taken from Simon et al. (2019) References Bordenstein, S. R., & Theis, K. R. (2015). Host biology in light of the microbiome: Ten principles of holobionts and hologenomes. PLoS Biol, 13, e1002226. Douglas, A. E., & Werren, J. H. (2016). Holes in the hologenome: Why host- microbe symbioses are not holobionts. mBio, 7(2), e02099-15. Fraune, S., & Bosch, T. C. G. (2010). Why bacteria matter in animal development and evolution. Bioessays, 32, 571–580. Gilbert, S. F., Sapp, J., & Tauber, A. I. (2012). A symbiotic view of life: We have never been individuals. The Quarterly Review of Biology, 87, 325–341. Jablonka, E. & Marion J. Lamb, M. J. (2005). Evolution in four dimensions:
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