Prokaryotes and Evolution Jean-Claude Bertrand • Philippe Normand Bernard Ollivier • Télesphore Sime-Ngando Editors Prokaryotes and Evolution Editors Jean-Claude Bertrand Philippe Normand Unité Mixte de Service, UMS 3470, Laboratoire d’Ecologie Microbienne, OSU Pythéas UMR 5557 Aix Marseille Université Université Claude Bernard Lyon 1 Marseille Cedex, France Villeurbanne, France Bernard Ollivier Télesphore Sime-Ngando Aix Marseille Universite, Universite de Laboratoire “Microorganismes: Génome Toulon, CNRS, IRD, MIO UM 110 et Environnement” (LMGE), CNRS Marseille, France UMR 6023 Université Clermont Auvergne Clermont-Ferrand, France ISBN 978-3-319-99782-7 ISBN 978-3-319-99784-1 (eBook) https://doi.org/10.1007/978-3-319-99784-1 Library of Congress Control Number: 2018962555 © Springer Nature Switzerland AG 2018 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, express 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 Foreword: The Importance of Prokaryotic Evolution in the Study of Biology Even though evolution is one of the major organizing theories in biology, it has had relatively little impact on the study of prokaryotes. Presumably, the absence of eas- ily studied morphological features, a detailed fossil record, and readily identifiable populations created a methodological barrier that was difficult to penetrate prior to the development of modern molecular and chemical techniques. Prokaryotes also appear to be remote from the everyday. Invisible to casual observation, only special- ists fully appreciate their rich evolutionary history. The result is a general lack of interest among many biologists. In fact, some biology texts and natural history museums present life’s evolution on a logarithmic time scale where the last million years appear longer than the first three billion years. In this way, evolution on the early earth, a time dominated by prokaryotes, has been selectively minimized. Nevertheless, the prokaryotes have a lot to tell biology. The early earth before the evolution of eukaryotes is the time when the most salient features of life evolved. As the first ancestors of the earliest life forms, the prokaryotes provide one of the few windows into these events. This is the time when the basic cellular design of life evolved. The capacity to energize cellular membranes with ion gradients and to use this energy to form high-energy chemical bonds, motility, and transport all evolved. The major catabolic and anabolic pathways of central metabolism, such as glycoly- sis and gluconeogenesis and the tricarboxylic acid cycle, evolved. The major bio- synthetic pathways for the building blocks of the cell, including amino acids, nucleotides, lipids, and coenzymes, all evolved. Likewise, the basic mechanisms of information processing, including replication, transcription, and translation sys- tems, evolved. Lastly, early prokaryotic life transformed the planet, forming the first biogeochemical cycles that maintained the early biosphere. Most of the major prokaryotic phyla also evolved in the early earth, likely predat- ing the origin of the eukaryotes. The modern prokaryotes likely descended from about 100 lineages that were present on earth 2 billion years ago. While some lin- eages appear to be represented by only a few small clades, many have undergone remarkable diversification. A major implication of this sequence of events is that eukaryotes evolved in a world fully colonized by prokaryotes and within an ecosys- tem comprised largely of prokaryotes. Thus, modern eukaryotes were shaped not v vi Foreword: The Importance of Prokaryotic Evolution in the Study of Biology only by the chemistry of the environment in which they evolved but also by the biology of prokaryotes. Not only does the evolution of prokaryotes span a much longer time than the eukaryotes, the population sizes are many orders of magnitude larger. For instance, the population of humans now approaches 1010 individuals and that of an abundant group of insects, termites, is about 1017 individuals. In contrast, estimates of the number of a relatively minor gut bacterium Escherichia coli are about 1020 cells and of some of the abundant marine phototrophs are 1027 cells. This difference in scale regarding the population size implies that prokaryotic evolution is fundamentally different from that of eukaryotes. For instance, mutations which are rare in popula- tions of eukaryotes are common in populations of prokaryotes. As a consequence, the opportunities for diversification are correspondingly larger. Due to differences in scale, methodology, and familiarity, the central questions of prokaryotic evolution are fundamentally different from those of eukaryotes. This volume addresses many of them. In contrast to the major groups of eukaryotes, which are well known even outside of biology, most biologists are ignorant about many of the basic features of prokaryotic life. This question of familiarity is addressed by Normand and Caumette, who review the phylogeny, classification, and properties of prokaryotes in Chap. 2. The naming and classification of prokaryotes are fundamentally different from that used in eukaryotes. In addition, Normand and Caumette provide an overview of the properties of the 36 prokaryotic phyla with cultured representatives. The metabolic diversity is illustrated. For instance, photot- rophy and lithotrophy are shown to be widely distributed. Likewise, the physical conditions able to support life span temperatures from below the freezing point to above the boiling point of water, salinities from freshwater to saturated salt solu- tions, and pHs from strongly acidic to strongly basic. Multicellular lifestyles and the variety of resting forms are described. There is no “typical” prokaryote, and these microorganisms possess varied and complex lifestyles. The relationship of the prokaryotes to eukaryotes is another central question. In Chap. 1, Bertrand et al. discuss the alternative interpretations of recent phyloge- nomic analyses. The prokaryotes are known to comprise two phylogenetic domains, the Bacteria and Archaea. Are the Eukarya a third domain or a fundamentally differ- ent type of organism? Bertrand et al. show that the prokaryotes are a fundamentally different type of organism that are united by a large number of shared characteris- tics, including small size, genome structure, absence of meiosis, coupling of tran- scription and translation in the cytoplasm, formation of a characteristic cytoskeleton, functionally specialized cytoplasmic membranes, absence of phagocytosis to assim- ilate nutrients, and simple patterns of cellular differentiation. They further point out that recognition of the differences in the structure of the prokaryotic and eukaryotic cells enriches rather than contradicts the phylogenetic analysis. Given the profound differences between prokaryotes and eukaryotes, is their evolution also fundamentally different? In Chap. 4, Bertrand et al. discuss this ques- tion in detail. First, they examine the relevance to prokaryotes of the major theories of evolution, from natural selection to neutral evolution. Of particular interest are features that might explain the success of prokaryotes and their ability to dominate Foreword: The Importance of Prokaryotic Evolution in the Study of Biology vii the biosphere for 3.5 billion years. Particularly important seem to be their small size, efficient reproduction, short generation times, large populations, capacity for horizontal gene transfer between even distantly related lineages, formation of dor- mant or resting cells, and ability to colonize an enormous variety of biomes. Moreover, the study of prokaryotes has greatly enriched the theories of evolution from Darwin to the modern day. The first cellular organisms of earth were probably prokaryotes, and the study of the origin of life is fundamental to the evolution of prokaryotes. Given the antiquity of the events and the enormous changes that have occurred on earth in the last 3.8 billion years, it is remarkable that anything can be deduced about the origin of life. In Chap. 3, Ollivier et al. discuss the state of our knowledge. Two lines of inquiry dominate. In the first approach, the properties of modern organisms inform the possibilities for ancient life.