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

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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 lineages 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 ecosystem 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 populations 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 different 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 transcription 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 question 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. In this regard, mechanisms of lithotrophy are espe- cially informative. Given the likely chemistry of ancient earth, what would the bio- energetics of early organisms look like? What types of enzyme catalysts might be present? In the second approach, ancient fossils and sediments are examined for evidence about ancient life. While stromatolites provide strong evidence for prokaryotic life 3 billion years ago, the evidence becomes increasingly ambiguous prior to that time. Eukaryotes almost certainly evolved in a world dominated by prokaryotes, but the same is true of the modern prokaryotic lineages. Sime-Ngando et al. explore the consequences of this insight in Chap. 5. Most modern prokaryotes are members of communities comprised of other prokaryotes but also viruses, plants, animals, fungi, and other eukaryotes. The communities form ecosystems whose functions sustain the lives of its members. These interactions with these communities are ancient and highly complex, formed at multiple scales of biological organization, from gene to organism to ecosystem. They shape ecosystem functioning through major evolutionary forcing processes such as Red Queen dynamics, inter-actomics, molecular dialogue, host manipulation, coevolution, effects on food webs, and biogeochemical cycles. Studies on the interactions within these communities continue to provide novel insights into the evolution of these organisms. There is also no reason to assume that prokaryotic evolution has not continued in the modern world. The enormous growth in populations of humans and domestic animals, large-scale conversion of forests and prairies to farms and pastures, and massive introduction of chemicals into the biosphere have all created novel habitats for prokaryotes. One challenge facing prokaryotic biology is to identify and under- stand how the prokaryotes have and will respond to these changes. As described by Wielgoss et al. in Chap. 6, one approach to this problem is experimental evolution or evolution in the laboratory. This allows detailed examination of the mechanisms of mutation, selection, and evolution. Alternative approaches examine the evolution of prokaryotes in response to well-documented modern events. For instance, the release of antibiotics in the last 80 years constitutes a “natural” experiment and makes it possible to chart the prevalence and nature of resistance in natural populations. Likewise, vascular plants colonized the continents about 400 million years ago, leading to the formation of soil and the rhizosphere habitats. The adaptation of viii Foreword: The Importance of Prokaryotic Evolution in the Study of Biology nodulating bacteria, such as Rhizobium, to these new environments elucidates the capacity of prokaryotes to respond to these enormous changes. Laboratory studies can then complement observations of natural populations to examine the mecha- nism of this process in detail. Lastly, life on earth is dominated by prokaryotes. If an alien came to earth from another planet and said, “Take me to your leader,” it would not expect to go to Paris, Moscow, Tokyo, Beijing, or Washington. It would want to go to the soils, oceans, and sediments, all habitats densely populated by prokaryotes. Knowledge of the evolution of the prokaryotes is key to our understanding of all aspects of modern life, from its molecular biology and biochemistry to its biogeochemistry.

Department of Microbiology William B. Whitman University of Georgia Athens, GA, USA Contents

1 Prokaryote/Eukaryote Dichotomy and Bacteria/Archaea/Eukarya Domains: Two Inseparable Concepts �� 1 Jean-Claude Bertrand, Pierre Caumette, Philippe Normand, Bernard Ollivier, and Télesphore Sime-Ngando 2 Phylogeny and Biodiversity of Prokaryotes �� 23 Philippe Normand and Pierre Caumette 3 Importance of Prokaryotes in the Functioning and Evolution of the Present and Past Geosphere and Biosphere �� 57 Bernard Ollivier, Nina Zeyen, Gregoire Gales, Keyron Hickman-Lewis, Frédéric Gaboyer, Karim Benzerara, and Frances Westall 4 Evolutionary Success of Prokaryotes �� 131 Jean-Claude Bertrand, Patricia Bonin, Bernard Ollivier, Karine Alain, Anne Godfroy, Nathalie Pradel, and Philippe Normand 5 The Evolution of Living Beings Started with Prokaryotes and in Interaction with Prokaryotes �� 241 Télesphore Sime-Ngando, Jean-Claude Bertrand, Didier Bogusz, Jean-François Brugère, Claudine Franche, Marie-Laure Fardeau, Emilie Froussart, Anne Geiger, Maria Soledad Goñi-Urriza, Bernard Ollivier, and Paul W. O’Toole 6 Evolution Underway in Prokaryotes �� 339 Sébastien Wielgoss, Pierre Leblond, Catherine Masson-Boivin, and Philippe Normand

Index �� 393