Béatrice Clouet-d'Orval is Research Director at the CNRS and works at the Center for Integrative Biology, Toulouse, France. Her main research areas focus on the post-transcriptional regulation of gene expression.Bruno Franzetti is Research Director at the CNRS, France, where he specializes in the structural biology of archaea. His research areas include biophysical and cellular mechanisms that maintain proteome integrity under extreme conditions.Philippe Oger is Research Director at the CNRS, France. His research areas include understanding the adaptations of prokaryotes in response to extreme conditions, using a multidisciplinary approach combining the methods derived from atomic physics and cutting-edge molecular biology and modeling.

• Preface xiBéatrice CLOUET-D’ORVAL, Bruno FRANZETTI and Philippe OGERChapter 1 The Discovery of Archaea 1Patrick FORTERRE1.1 Introduction 11.2 Prokaryotic–eukaryotic dichotomy 21.3 Two domains for prokaryotes: archaebacteria and eubacteria 31.3.1 Ribosomal RNA as a molecular marker: a historical choice 31.3.2 Atypical ribosomal RNA of methanogenic “bacteria” 71.3.3 The concept of archaeobacteria 81.3.4 The grouping of halophilic and thermo-acidophilic “bacteria” with methanogens within archaeobacteria 91.4 The living trilogy 111.4.1 The concept of archaeobacteria confirmed by the uniqueness of their membrane phospholipids 111.4.2 German biochemists: champions of the archaeobacteria concept 121.4.3 The evolutionary link between archaeobacteria and eukaryotes and the introduction of the term archaea 131.5 Archaea and high-temperature living 141.5.1 The discovery of anaerobic hyperthermophilic archaea 141.5.2 The race for the thermophilia record 181.5.3 The discovery of viruses in hyperthermophilic archaea 201.6 Non-extremophilic archaea discovered by molecular ecology: a new vision of the third domain 221.7 Conclusion 231.8 References 24Chapter 2 Evolution of Archaea and Their Taxonomy 29Patrick FORTERRE2.1 Introduction 292.2 One domain, three major branches and a few isolated “phyla” 302.2.1 One domain, two phyla 302.2.2 A first orphaned phylum, the korarchaeota 312.2.3 The first phylogenies based on conserved proteins 322.2.4 The special case of Methanopyrus kandleri 352.2.5 The special case of Nanoarchaeum equitans 362.2.6 Thaumarchaea 372.3 From phyla to superphyla 392.3.1 Metagenomics and the explosion in the number of archaeal phyla 392.3.2 The superphylum TACK 412.3.3 The DPANN 452.3.4 The Asgard archaea 502.3.5 Stygia/Hadarchaeota 552.3.6 Hydrothermarchaeota 552.4 Euryarchaea 562.4.1 Group I Euryarchaea 572.4.2 Group II Euryarchaea 592.5 A new nomenclature for the taxonomy of archaea? 642.6 Reconstructing the last common ancestor of archaea: LACA 672.6.1 Rooting the archaeal tree 672.6.2 Two opposing visions of LACA: simple or complex 712.6.3 The likely hyperthermophilic nature of LACA 722.6.4 The possibility of a methanogenic LACA 742.7 Conclusion 762.8 References 76Chapter 3 Archaea and the Tree of Life 89Patrick FORTERRE3.1 Introduction 893.2 The progenote concept 903.3 Archaea: prokaryotes related to eukaryotes 913.4 Rooting the universal tree 923.5 The nature of LUCA 973.5.1 A simpler LUCA compared to the organisms of the three current domains 973.5.2 An RNA genome for LUCA? 973.5.3 A presumably mesophilic LUCA 1003.5.4 LUCA’s proteome 1053.6 The topology of the universal tree under debate 1103.6.1 Early challenge to the Woese tree: the eocyte hypothesis 1103.6.2 Searching for the archean ancestor of eukaryotes 1113.6.3 Discovery of the Asgard archaea: validation of the 2D hypothesis? 1123.6.4 Controversies over the position of Asgard archaea 1133.7 The origin of new eukaryotic-like proteins discovered in Asgard archaea 1253.8 Asgard archaea and the origin of eukaryotes 1303.8.1 Asgard archaea at the origin of eukaryotes: a new paradigm 1303.8.2 The inside-out model based on nanotubes discovered in Asgard archaea 1313.8.3 The two-bacteria 2D model 1323.8.4 The origin of eukaryotic cell complexity 1323.9 The biological issues posed by the 2D model 1333.10 Viruses and the universal tree of life 1363.11 Conclusion 1413.12 References 141Chapter 4 Archaea: Habitats and Associated Physiologies 153Karine ALAIN, Marc COZANNET, Maxime ALLIOUX,Sarah THIROUX and Jordan HARTUNIANS4.1 Introduction 1534.2 Archaea of extreme habitats: extremophiles 1564.2.1 Psychrophiles 1584.2.2 Thermophiles/hyperthermophiles 1614.2.3 Acidophiles 1644.2.4 Alkalophiles 1664.2.5 Halophiles 1674.2.6 Piezophiles 1684.2.7 Radiotolerant archaea 1694.2.8 Poly-extremophilic archaea 1704.2.9 Record-holding archaea 1714.3 Archaea populating ordinary, non-extreme environments 1724.3.1 Phytobiomes, rice paddies and peatlands 1744.3.2 Aquatic habitats: lakes, oceans and estuaries 1784.3.3 Environments linked to human activities: example of waste treatment and anaerobic digesters (methanizers) 1834.3.4 Animal microbiomes 1854.4 Archaea resistant to cultivation efforts 1884.5 Challenges and success stories 1914.6 Conclusion 1934.7 References 193Chapter 5 Methanogenic Archaea 205Tristan WAGNER, Laurent TOFFIN and Guillaume BORREL5.1 Diversity of methanogens and their environments 2055.1.1 Methane sources and sinks 2055.1.2 Taxonomic and metabolic diversity 2075.1.3 Ecological diversity of methanogens 2105.2 Interactions of methanogens with their environment 2165.2.1 Competition for substrates 2165.2.2 Ecological and syntrophic interactions 2175.2.3 Human–methanogen association 2185.3 Bioenergetics and biochemistry of methanogenesis 2195.3.1 Energy extremophiles 2195.3.2 Cofactors used in methanogenesis 2195.3.3 Different types of methanogenesis 2225.3.4 MCR, the unique enzyme capable of generating biogenic methane 2305.4 Anaerobic methanotrophs and anaerobic oxidation of multi-carbon alkanes 2325.5 Evolution of methanogenesis 2335.5.1 An ancestral metabolism 2335.5.2 Metabolic adaptations 2345.6 The impact of methanogens in our modern society 2345.7 References 236Chapter 6 Hyperthermophilic Archaeal Viruses 247Diana BAQUERO, Mart KRUPOVIC, Claire GESLIN and David PRANGISHVILI6.1 Introduction 2476.2 Morphological and structural diversity 2486.2.1 Viruses with unique morphologies: families Ampullaviridae, Spiraviridae and Guttaviridae 2486.2.2 Filamentous viruses: families Rudiviridae, Lipothrixviridae, Tristromaviridae and Clavaviridae 2496.2.3 Spherical and icosahedral viruses: families Globuloviridae, Ovaliviridae, Portogloboviridae and Turriviridae 2516.2.4. Fusiform viruses: families Fuselloviridae andBicaudoviridae 2536.3 Genomic features of hyperthermophilic archaeal viruses 2546.3.1 Genome content 2546.3.2 Structural genomics 2576.4 Virus–host interactions 2586.4.1 Virus entry 2596.4.2 Virion egress 2596.5 Conclusions 2606.6 References 261List of Authors 269Index 271

Béatrice Clouet-d'Orval is Research Director at the CNRS and works at the Center for Integrative Biology, Toulouse, France. Her main research areas focus on the post-transcriptional regulation of gene expression.Bruno Franzetti is Research Director at the CNRS, France, where he specializes in the structural biology of archaea. His research areas include biophysical and cellular mechanisms that maintain proteome integrity under extreme conditions.Philippe Oger is Research Director at the CNRS, France. His research areas include understanding the adaptations of prokaryotes in response to extreme conditions, using a multidisciplinary approach combining the methods derived from atomic physics and cutting-edge molecular biology and modeling.

• Preface xiBéatrice CLOUET-D’ORVAL, Bruno FRANZETTI and Philippe OGERChapter 1 The Discovery of Archaea 1Patrick FORTERRE1.1 Introduction 11.2 Prokaryotic–eukaryotic dichotomy 21.3 Two domains for prokaryotes: archaebacteria and eubacteria 31.3.1 Ribosomal RNA as a molecular marker: a historical choice 31.3.2 Atypical ribosomal RNA of methanogenic “bacteria” 71.3.3 The concept of archaeobacteria 81.3.4 The grouping of halophilic and thermo-acidophilic “bacteria” with methanogens within archaeobacteria 91.4 The living trilogy 111.4.1 The concept of archaeobacteria confirmed by the uniqueness of their membrane phospholipids 111.4.2 German biochemists: champions of the archaeobacteria concept 121.4.3 The evolutionary link between archaeobacteria and eukaryotes and the introduction of the term archaea 131.5 Archaea and high-temperature living 141.5.1 The discovery of anaerobic hyperthermophilic archaea 141.5.2 The race for the thermophilia record 181.5.3 The discovery of viruses in hyperthermophilic archaea 201.6 Non-extremophilic archaea discovered by molecular ecology: a new vision of the third domain 221.7 Conclusion 231.8 References 24Chapter 2 Evolution of Archaea and Their Taxonomy 29Patrick FORTERRE2.1 Introduction 292.2 One domain, three major branches and a few isolated “phyla” 302.2.1 One domain, two phyla 302.2.2 A first orphaned phylum, the korarchaeota 312.2.3 The first phylogenies based on conserved proteins 322.2.4 The special case of Methanopyrus kandleri 352.2.5 The special case of Nanoarchaeum equitans 362.2.6 Thaumarchaea 372.3 From phyla to superphyla 392.3.1 Metagenomics and the explosion in the number of archaeal phyla 392.3.2 The superphylum TACK 412.3.3 The DPANN 452.3.4 The Asgard archaea 502.3.5 Stygia/Hadarchaeota 552.3.6 Hydrothermarchaeota 552.4 Euryarchaea 562.4.1 Group I Euryarchaea 572.4.2 Group II Euryarchaea 592.5 A new nomenclature for the taxonomy of archaea? 642.6 Reconstructing the last common ancestor of archaea: LACA 672.6.1 Rooting the archaeal tree 672.6.2 Two opposing visions of LACA: simple or complex 712.6.3 The likely hyperthermophilic nature of LACA 722.6.4 The possibility of a methanogenic LACA 742.7 Conclusion 762.8 References 76Chapter 3 Archaea and the Tree of Life 89Patrick FORTERRE3.1 Introduction 893.2 The progenote concept 903.3 Archaea: prokaryotes related to eukaryotes 913.4 Rooting the universal tree 923.5 The nature of LUCA 973.5.1 A simpler LUCA compared to the organisms of the three current domains 973.5.2 An RNA genome for LUCA? 973.5.3 A presumably mesophilic LUCA 1003.5.4 LUCA’s proteome 1053.6 The topology of the universal tree under debate 1103.6.1 Early challenge to the Woese tree: the eocyte hypothesis 1103.6.2 Searching for the archean ancestor of eukaryotes 1113.6.3 Discovery of the Asgard archaea: validation of the 2D hypothesis? 1123.6.4 Controversies over the position of Asgard archaea 1133.7 The origin of new eukaryotic-like proteins discovered in Asgard archaea 1253.8 Asgard archaea and the origin of eukaryotes 1303.8.1 Asgard archaea at the origin of eukaryotes: a new paradigm 1303.8.2 The inside-out model based on nanotubes discovered in Asgard archaea 1313.8.3 The two-bacteria 2D model 1323.8.4 The origin of eukaryotic cell complexity 1323.9 The biological issues posed by the 2D model 1333.10 Viruses and the universal tree of life 1363.11 Conclusion 1413.12 References 141Chapter 4 Archaea: Habitats and Associated Physiologies 153Karine ALAIN, Marc COZANNET, Maxime ALLIOUX,Sarah THIROUX and Jordan HARTUNIANS4.1 Introduction 1534.2 Archaea of extreme habitats: extremophiles 1564.2.1 Psychrophiles 1584.2.2 Thermophiles/hyperthermophiles 1614.2.3 Acidophiles 1644.2.4 Alkalophiles 1664.2.5 Halophiles 1674.2.6 Piezophiles 1684.2.7 Radiotolerant archaea 1694.2.8 Poly-extremophilic archaea 1704.2.9 Record-holding archaea 1714.3 Archaea populating ordinary, non-extreme environments 1724.3.1 Phytobiomes, rice paddies and peatlands 1744.3.2 Aquatic habitats: lakes, oceans and estuaries 1784.3.3 Environments linked to human activities: example of waste treatment and anaerobic digesters (methanizers) 1834.3.4 Animal microbiomes 1854.4 Archaea resistant to cultivation efforts 1884.5 Challenges and success stories 1914.6 Conclusion 1934.7 References 193Chapter 5 Methanogenic Archaea 205Tristan WAGNER, Laurent TOFFIN and Guillaume BORREL5.1 Diversity of methanogens and their environments 2055.1.1 Methane sources and sinks 2055.1.2 Taxonomic and metabolic diversity 2075.1.3 Ecological diversity of methanogens 2105.2 Interactions of methanogens with their environment 2165.2.1 Competition for substrates 2165.2.2 Ecological and syntrophic interactions 2175.2.3 Human–methanogen association 2185.3 Bioenergetics and biochemistry of methanogenesis 2195.3.1 Energy extremophiles 2195.3.2 Cofactors used in methanogenesis 2195.3.3 Different types of methanogenesis 2225.3.4 MCR, the unique enzyme capable of generating biogenic methane 2305.4 Anaerobic methanotrophs and anaerobic oxidation of multi-carbon alkanes 2325.5 Evolution of methanogenesis 2335.5.1 An ancestral metabolism 2335.5.2 Metabolic adaptations 2345.6 The impact of methanogens in our modern society 2345.7 References 236Chapter 6 Hyperthermophilic Archaeal Viruses 247Diana BAQUERO, Mart KRUPOVIC, Claire GESLIN and David PRANGISHVILI6.1 Introduction 2476.2 Morphological and structural diversity 2486.2.1 Viruses with unique morphologies: families Ampullaviridae, Spiraviridae and Guttaviridae 2486.2.2 Filamentous viruses: families Rudiviridae, Lipothrixviridae, Tristromaviridae and Clavaviridae 2496.2.3 Spherical and icosahedral viruses: families Globuloviridae, Ovaliviridae, Portogloboviridae and Turriviridae 2516.2.4. Fusiform viruses: families Fuselloviridae andBicaudoviridae 2536.3 Genomic features of hyperthermophilic archaeal viruses 2546.3.1 Genome content 2546.3.2 Structural genomics 2576.4 Virus–host interactions 2586.4.1 Virus entry 2596.4.2 Virion egress 2596.5 Conclusions 2606.6 References 261List of Authors 269Index 271

Béatrice Clouet-d'Orval is Research Director at the CNRS and works at the Center for Integrative Biology, Toulouse, France. Her main research areas focus on the post-transcriptional regulation of gene expression.Bruno Franzetti is Research Director at the CNRS, France, where he specializes in the structural biology of archaea. His research areas include biophysical and cellular mechanisms that maintain proteome integrity under extreme conditions.Philippe Oger is Research Director at the CNRS, France. His research areas include understanding the adaptations of prokaryotes in response to extreme conditions, using a multidisciplinary approach combining the methods derived from atomic physics and cutting-edge molecular biology and modeling.

• Preface xiBéatrice CLOUET-D’ORVAL, Bruno FRANZETTI and Philippe OGERChapter 1 The Discovery of Archaea 1Patrick FORTERRE1.1 Introduction 11.2 Prokaryotic–eukaryotic dichotomy 21.3 Two domains for prokaryotes: archaebacteria and eubacteria 31.3.1 Ribosomal RNA as a molecular marker: a historical choice 31.3.2 Atypical ribosomal RNA of methanogenic “bacteria” 71.3.3 The concept of archaeobacteria 81.3.4 The grouping of halophilic and thermo-acidophilic “bacteria” with methanogens within archaeobacteria 91.4 The living trilogy 111.4.1 The concept of archaeobacteria confirmed by the uniqueness of their membrane phospholipids 111.4.2 German biochemists: champions of the archaeobacteria concept 121.4.3 The evolutionary link between archaeobacteria and eukaryotes and the introduction of the term archaea 131.5 Archaea and high-temperature living 141.5.1 The discovery of anaerobic hyperthermophilic archaea 141.5.2 The race for the thermophilia record 181.5.3 The discovery of viruses in hyperthermophilic archaea 201.6 Non-extremophilic archaea discovered by molecular ecology: a new vision of the third domain 221.7 Conclusion 231.8 References 24Chapter 2 Evolution of Archaea and Their Taxonomy 29Patrick FORTERRE2.1 Introduction 292.2 One domain, three major branches and a few isolated “phyla” 302.2.1 One domain, two phyla 302.2.2 A first orphaned phylum, the korarchaeota 312.2.3 The first phylogenies based on conserved proteins 322.2.4 The special case of Methanopyrus kandleri 352.2.5 The special case of Nanoarchaeum equitans 362.2.6 Thaumarchaea 372.3 From phyla to superphyla 392.3.1 Metagenomics and the explosion in the number of archaeal phyla 392.3.2 The superphylum TACK 412.3.3 The DPANN 452.3.4 The Asgard archaea 502.3.5 Stygia/Hadarchaeota 552.3.6 Hydrothermarchaeota 552.4 Euryarchaea 562.4.1 Group I Euryarchaea 572.4.2 Group II Euryarchaea 592.5 A new nomenclature for the taxonomy of archaea? 642.6 Reconstructing the last common ancestor of archaea: LACA 672.6.1 Rooting the archaeal tree 672.6.2 Two opposing visions of LACA: simple or complex 712.6.3 The likely hyperthermophilic nature of LACA 722.6.4 The possibility of a methanogenic LACA 742.7 Conclusion 762.8 References 76Chapter 3 Archaea and the Tree of Life 89Patrick FORTERRE3.1 Introduction 893.2 The progenote concept 903.3 Archaea: prokaryotes related to eukaryotes 913.4 Rooting the universal tree 923.5 The nature of LUCA 973.5.1 A simpler LUCA compared to the organisms of the three current domains 973.5.2 An RNA genome for LUCA? 973.5.3 A presumably mesophilic LUCA 1003.5.4 LUCA’s proteome 1053.6 The topology of the universal tree under debate 1103.6.1 Early challenge to the Woese tree: the eocyte hypothesis 1103.6.2 Searching for the archean ancestor of eukaryotes 1113.6.3 Discovery of the Asgard archaea: validation of the 2D hypothesis? 1123.6.4 Controversies over the position of Asgard archaea 1133.7 The origin of new eukaryotic-like proteins discovered in Asgard archaea 1253.8 Asgard archaea and the origin of eukaryotes 1303.8.1 Asgard archaea at the origin of eukaryotes: a new paradigm 1303.8.2 The inside-out model based on nanotubes discovered in Asgard archaea 1313.8.3 The two-bacteria 2D model 1323.8.4 The origin of eukaryotic cell complexity 1323.9 The biological issues posed by the 2D model 1333.10 Viruses and the universal tree of life 1363.11 Conclusion 1413.12 References 141Chapter 4 Archaea: Habitats and Associated Physiologies 153Karine ALAIN, Marc COZANNET, Maxime ALLIOUX,Sarah THIROUX and Jordan HARTUNIANS4.1 Introduction 1534.2 Archaea of extreme habitats: extremophiles 1564.2.1 Psychrophiles 1584.2.2 Thermophiles/hyperthermophiles 1614.2.3 Acidophiles 1644.2.4 Alkalophiles 1664.2.5 Halophiles 1674.2.6 Piezophiles 1684.2.7 Radiotolerant archaea 1694.2.8 Poly-extremophilic archaea 1704.2.9 Record-holding archaea 1714.3 Archaea populating ordinary, non-extreme environments 1724.3.1 Phytobiomes, rice paddies and peatlands 1744.3.2 Aquatic habitats: lakes, oceans and estuaries 1784.3.3 Environments linked to human activities: example of waste treatment and anaerobic digesters (methanizers) 1834.3.4 Animal microbiomes 1854.4 Archaea resistant to cultivation efforts 1884.5 Challenges and success stories 1914.6 Conclusion 1934.7 References 193Chapter 5 Methanogenic Archaea 205Tristan WAGNER, Laurent TOFFIN and Guillaume BORREL5.1 Diversity of methanogens and their environments 2055.1.1 Methane sources and sinks 2055.1.2 Taxonomic and metabolic diversity 2075.1.3 Ecological diversity of methanogens 2105.2 Interactions of methanogens with their environment 2165.2.1 Competition for substrates 2165.2.2 Ecological and syntrophic interactions 2175.2.3 Human–methanogen association 2185.3 Bioenergetics and biochemistry of methanogenesis 2195.3.1 Energy extremophiles 2195.3.2 Cofactors used in methanogenesis 2195.3.3 Different types of methanogenesis 2225.3.4 MCR, the unique enzyme capable of generating biogenic methane 2305.4 Anaerobic methanotrophs and anaerobic oxidation of multi-carbon alkanes 2325.5 Evolution of methanogenesis 2335.5.1 An ancestral metabolism 2335.5.2 Metabolic adaptations 2345.6 The impact of methanogens in our modern society 2345.7 References 236Chapter 6 Hyperthermophilic Archaeal Viruses 247Diana BAQUERO, Mart KRUPOVIC, Claire GESLIN and David PRANGISHVILI6.1 Introduction 2476.2 Morphological and structural diversity 2486.2.1 Viruses with unique morphologies: families Ampullaviridae, Spiraviridae and Guttaviridae 2486.2.2 Filamentous viruses: families Rudiviridae, Lipothrixviridae, Tristromaviridae and Clavaviridae 2496.2.3 Spherical and icosahedral viruses: families Globuloviridae, Ovaliviridae, Portogloboviridae and Turriviridae 2516.2.4. Fusiform viruses: families Fuselloviridae andBicaudoviridae 2536.3 Genomic features of hyperthermophilic archaeal viruses 2546.3.1 Genome content 2546.3.2 Structural genomics 2576.4 Virus–host interactions 2586.4.1 Virus entry 2596.4.2 Virion egress 2596.5 Conclusions 2606.6 References 261List of Authors 269Index 271