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The Pangenome Diversity, Dynamics and Evolution of Genomes the Pangenome Hervé Tettelin • Duccio Medini Editors

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The Pangenome Diversity, Dynamics and Evolution of Genomes the Pangenome Hervé Tettelin • Duccio Medini Editors Hervé Tettelin Duccio Medini Editors The Pangenome Diversity, Dynamics and Evolution of Genomes The Pangenome Hervé Tettelin • Duccio Medini Editors The Pangenome Diversity, Dynamics and Evolution of Genomes Editors Hervé Tettelin Duccio Medini Department of Microbiology and GSK Vaccines R&D Immunology, Institute for Genome Siena, Italy Sciences University of Maryland School of Medicine Baltimore, Maryland, USA ISBN 978-3-030-38280-3 ISBN 978-3-030-38281-0 (eBook) https://doi.org/10.1007/978-3-030-38281-0 This book is an open access publication. © The Editor(s) (if applicable) and The Author(s) 2020. Open Access This book is licensed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence and indicate if changes were made. The images or other third party material in this book are included in the book’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the book’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. The publisher, the authors, and the editors are safe to assume that the advice and information in this book are believed to be true and accurate at the date of publication. Neither the publisher nor the authors or the editors give a warranty, expressed or implied, with respect to the material contained herein or for any errors or omissions that may have been made. The publisher remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. This Springer imprint is published by the registered company Springer Nature Switzerland AG. The registered company address is: Gewerbestrasse 11, 6330 Cham, Switzerland Preface Serendipitous discoveries are fascinating events of science inducing, at times, paradigm shifts that give rise to new disciplines tout-court. This is what happened with pangenomics: a novel discipline at the intersection of biology, computer science and applied mathematics, whose discovery, development to state of the art and future perspectives are tentatively collected in this book for the first time, 15 years after its inception. In simple terms, the pangenome concept is the realization that the genetic repertoire of a biological species, i.e. the pool of genetic material present across the organisms of the species, always exceeds each of the individual genomes and can be, in several cases, “unbounded”:anopen pangenome. This notion was conceived in 2005 as an unexpected, data-driven outcome of the comparative analyses of a few bacterial genomes. This early example of big data in biology—in which a mathematical model, developed to address a practical question in vaccinology, transformed established concepts—opened biology to the unbounded. Since then, the advent of next-generation sequencing and computational technol- ogies has afforded the generation of pangenomes from thousands of isolates and non-cultured samples of many microbial species, first, and then of eukaryotes encompassing all the kingdoms of life, confirming and extending the original hypothesis beyond the most ambitious expectations. The first part of the book, Genomic diversity and the pangenome concept, opens with a historical account of the original discovery, the observed analogy between genomic sequences and text corpora that allowed the application of mathematical linguistics to the analysis of genomic diversity and the emergence of the pangenome concept in bacteria. In the second chapter, the reader will find an extensive introduction of the biological species concept with its challenges, the processes associated with the birth and development of a new species and the implications for its pangenome limits. v vi Preface The following chapter provides a perspective on genome plasticity, pangenome size and functional diversity from the unique point of view of the bacterium itself, followed in the last chapter of the section by a systematic review of the increasingly sophisticated and performant bioinformatic pipelines that have been made available to the scientific community, transforming pangenomics into a commodity tool for the twenty-first century biologist. The second part, Evolutionary biology of pangenomes, aims at making sense of pangenomics through the explanatory perspective of evolution. As Theodosius Dobzhansky attested half a century ago,1 nothing in biology makes sense except in the light of evolution. Pangenomes are no exception, as the genetic diversity observed in a species is the direct result of the evolutionary interplay between its member organisms and their environment. The effort is facilitated by the significant advances made in the last decade by mathematical modelling, systems theory and computational simulations, in an attempt to clarify the functional mechanisms underpinning diversity generation at the population level, especially in prokaryotes. The first chapter of this section2 moves from the dynamic forces that shape pangenome variations, particularly horizontal gene transfer, to discuss the implica- tions for population structures and their ecological significance. The second chapter analyses the microevolution of bacterial populations by introducing a neutral phylogenetic framework open to the assessment of natural selection and discusses how to reconstruct the microevolutionary history of an entire pangenome. The relationship between pangenomes and selection is further explored in the following chapter, which proposes a stimulating view of pangenomics based on the economic theory of public goods, resulting in the hypothesis that pangenomes are constructed and maintained by niche adaptation. The section closes with a zoom into the alarming public health crisis of antimicrobial resistance, where the authors consider how the pangenome affects the response to antibiotics, the development of resistance and the role of the selective pressures induced by antibiotics and discuss how the pangenome paradigm can foster the development of effective therapies. The third part, Pangenomics: an open, evolving discipline, takes the reader on a journey through applications of pangenome approaches beyond just genes and sequences for prokaryotes and into the realm of eukaryotes. Indeed, as the pangenome concept evolves and genomes from multiple isolates/individuals within virtually all living species become available, it is important to study and challenge the concept beyond the primary genomic sequence and beyond the bacterial world. While most of the pangenome studies published to date focus on genes as the unit, 1Theodosius Dobzhansky, The American Biology Teacher, Vol. 35 No. 3, March, 1973; (pp. 125–129) DOI: https://doi.org/10.2307/4444260 2Contributed by the brave scholar who once told the late Prof. Stanley Falkow “this is simply because, Stan, you don’t understand population biology” [Conference on “Microbial population genomics: sequence, function and diversity”, Novartis Vaccines Research Center, Siena (Italy), 17–19 January, 2007]. Preface vii any sequence (e.g. promoter, intron, intergenic region and mobile element) could be used as the unit to account for the many levels of variation and regulation governing a population, including entire communities occupying a particular niche. The first chapter of section three provides a vision of how pangenome analyses can be applied to the study of multiple species within a community or microbiome and how outcomes will lead to the characterization of pan-metagenomes across niches or environments. The second chapter describes procedures to infer the biological impact of pangenomic diversity, translating it into functional pathways and their rendition as phenotypes, or panphenomes. The third chapter brings the additional layer of epigenetic regulation into the picture, describing modification processes, methods to detect them and their relationship with the pangenome. Finally, the application of pangenome studies to other kingdoms of life beyond bacteria is a natural extension of the concept. Chapter four provides a detailed overview of eukaryotic genome projects, their genome dynamics and associated pangenome analyses, while the fifth and last chapter of this book compares and contrasts computational strategies that can be implemented towards the characteri- zation of eukaryotic pangenomes. We hope that this book, thanks to the extraordinary quality of the contributions from each of the authors involved, will provide a broad readership of life scientists with a useful tool for getting acquainted with—or delving deeper into—the pangenome concept and its theoretical foundations, for getting up to speed with the latest technologies and applications of pangenomics, or simply to explore one of the most exciting novelties of twenty-first century biology. Should pangenomics continue to develop at the current pace, this volume would soon be outdated by the forthcoming developments, killed
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