- Email: [email protected]
Editorial: Archaea and the Tree of Life
Research in Microbiology 162 (2011) 1e4 www.elsevier.com/locate/resmic
Editorial
Editorial: Archaea and the Tree of Life The discovery of Archaea as one of the three domains of life by Carl Woese in 1977 (Woese and Fox, 1977) has been one of the major discoveries of the XXth century in Biology. Since then, the phylogenetic position of Archaea in the universal tree of life has been the topic of hot debates among evolutionists. In 2009, we have organised an international interdisciplinary meeting “Archaea and the Tree of Life” at the Fondation Des Treilles (France), in order to discuss this issue, based on the most recent discoveries obtained on the physiology and molecular biology of Archaea. Scientists from two distinct communities were gathered: on one hand, biochemists and molecular biologists working actively on different archaeal model organisms and on the other hand several evolutionists experts in comparative genomics and phylogenetics. The underlying idea of the meeting was to encourage biochemists and molecular biologists to discuss openly their most recent data in an evolutionary context. In parallel, evolutionists were made aware of the most recent data gathered by the biochemists and molecular biologists covering the whole spectrum of archaeal physiology. The special issue “Archaea and the Tree of Life” represents a collection of most contributions presented at the meeting. During the meeting, various aspects of archaeal biology (cell division, transcription, DNA repair, membrane transport, RNA modification and degradation, and metabolism) were presented by some of the world leaders in these fields: Steve Bell (Oxford, UK), Malcom White (Saint Andrew, UK), Henri Grosjean (Orsay, France), John Van der Ost (Wagenigen, NL), Arnold Driessen (Groningen, NL), Finn Werner (London, UK), Gary Olsen (Urbana, USA), Karl-Peter Hopfner (Munich, DE). These talks emphasized the extensive similarities observed at the molecular level between Archaea and Eukarya (see Rouillon and White, 2010; Grohmann and Werner, 2010; Matsumi et al., 2010); for other recent reviews by meeting participants, see (Makarova et al., 2010; Chia et al., 2010; Hartung and Hopfner, 2009, de CrecyLagard et al., 2010; Berthon et al., 2009). Indeed, it has been known for nearly thirty years ago that Archaea display more similarities with Eukarya than with Bacteria in several informational molecular mechanisms (i.e. processes involved in the transmission of genetic information, including DNA replication, transcription, translation, and associated processes). These mechanisms are now being analysed more in detail at the molecular level. For example, Malcolm White
reviewed the latest advances in research on the components of archaeal DNA repair and their similarities with their eukaryotic counterparts (Grohmann and Werner, 2010; Rouillon and White, 2010), Finn Werner presented an overview of the latest findings in the structural analysis of archaeal RNA polymerases (Grohmann and Werner, 2010), Karl-Peter Hopfner discussed the similarities and differences between the archaeal and eukaryotic exosomes (Buttner et al., 2006; Hartung and Hopfner, 2009), and Henri Grosjean showed the evolutionary link between the RNA modification systems of Archaea and Eukarya (de Crecy-Lagard et al., 2010; Grosjean et al., 2010). These kind of analyses allow discussing the evolutionary relationships between Archaea and Eucarya beyond simple sequence homology and may be used to try inferring the polarization of traits commons to Archaea and Eukarya: are these derived characters testifying for the sisterhood of these two domains, or are these ancestral traits that were lost or replaced in Bacteria? Importantly, although it is generally put forward that bacterial features are more primitive compared to archaeal and eukaryotic characters, the meeting made aware all participants that the question is still open (Grohmann and Werner, 2010) and that more research on various molecular mechanisms in the Archaea will eventually allow to obtain a consensus on this crucial question. Importantly, the similarity between Archaea and Eukarya does not hold simply for informational systems (as currently assumed) but also for operational systems such as cell division, protein secretion or membrane vesicle formation. This last point was dramatically demonstrated by the recent finding that homologues of components of the eukaryotic vesiclesorting system ESCRTIII are involved in cell division in some members of the Crenarchaeota (for recent reviews, see (Ettema and Bernander, 2009; Makarova et al., 2010; Samson et al., 2008)). This finding is a major breakthrough because operational systems in Eukarya are traditionally viewed as bacterial-like, and used as a recurrent argument in favour of scenarios in which Eukarya originated by combining informational systems of an archaeon and operational systems from a bacterium (Lopez-Garcia and Moreira, 1999). Arnold Driessen and John Van der Oost reported clear cases where operational systems in Archaea (membrane transport, cell division, energy production) can also be evolutionarily closely related to those of Eukarya or exhibit a mixture of eukaryotic and bacterial traits (Gribaldo et al., 2010). This is the case of
0923-2508/$ - see front matter Ó 2010 Institut Pasteur. Published by Elsevier Masson SAS. All rights reserved. doi:10.1016/j.resmic.2010.11.007
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Editorial / Research in Microbiology 162 (2011) 1e4
cell division, since most archaea harbour a homologue of the major bacterial cell division protein FtsZ whereas other harbour components of the eukaryotic ESCRTIII complex or both (Makarova et al., 2010). The unique character of some major archaeal features is of course exemplified by their lipids. With respect to stereochemistry and composition, archaeal lipids are very different from the ester-linked, fatty acid-based phospholipids in bacterial and eukaryotic membranes (Pereto et al., 2004). However, John Van der Oost and colleagues remind that their building blocks (isoprenoids) are made by a universal and possibly ancestral pathway (Pereto et al., 2004; Lombard and Moreira, 2010). They review the main metabolic pathways leading to archaeal lipids and the evolutionary scenarios that have been proposed to explain how two different types of lipids arose in modern cells (Matsumi et al., 2010). They suggest exciting experiments to test some of these scenarios by expressing archaeal lipids in bacterial cells, or vice versa (Matsumi et al., 2010). The nature of viruses and other extra-chromosomal entities in the three domains has rarely been taken into account in scenarios that try to capture the evolutionary relationships between the three domains. Roger Garrett emphasized the similarity between the antiviral defence mechanisms (CRISPR) found in Archaea and Bacteria that appears evolutionarily unrelated to the eukaryotic siRNAs antiviral defence system (Shah and Garrett, 2010). This is in striking contrast with the clear difference between Archaea and Bacteria at the molecular level. Indeed, whereas eukaryotic molecular biology can be dubbed “archaeal-like”, Eukarya have unique viruses (e.g. retrovirus) and viral defence elements (siRNA) that have no counterparts in Archaea. During the meeting, Patrick Forterre emphasized the important role that viruses might have played in the formation of modern cells, especially in the emergence of various DNA replication machineries (Forterre, 2006). In this issue, he discusses more specifically the idea that viruses have played a critical role in the evolution of Eukarya towards complexity by introducing new genes in the eukaryotic lineage and by triggering an arms race with proto-eukaryotic lineages (Forterre, 2010). A better understanding of the evolutionary relationships between Archaea and Eukarya can be gathered by trying to reconstruct the nature of the last common ancestor of Eukarya and of the last common ancestor of Archaea through comparative genomics and phylogenetic analyses. Analyses of the evolution of components of the DNA replication apparatus (Jonathan Berthon, Paris), the mitochondrial ribosome (Elie Desmond, Paris) and of the eukaryotic midbody (Laura Eme, Marseille) indicate that the ancestors of Eukarya and Archaea were at least as complex as their present-day descendants (Berthon et al., 2009; Desmond et al., 2010; Eme et al., 2009). Puzzlingly, Elie Desmond presented evidence for a dynamic evolutionary history of the archaeal ribosome, a unique feature with respect to its counterparts in Bacteria and Eukarya and paralleled only by mitochondrial ribosomes (Desmond et al., 2010). It appears indeed that some streamlining has occurred during the evolution of Archaea (Desmond et al., 2010, de Crecy-Lagard et al., 2010; Csuros and Miklos, 2009; Chia et al., 2010).
The monophyly of Archaea has been disputed for a long time, some authors having suggested that Crenarchaeota share an exclusive ancestor with Eukarya, whereas others suggested that Eukarya originated as a chimera from the merging of a bacterium and an archaeon (reviewed in Gribaldo et al., 2010; Koonin, 2010). Simonetta Gribaldo reviewed a number of recent large-scale phylogenomic analyses published on this subject, showing that various authors obtained different results albeit using similar gene datasets (Gribaldo et al., 2010). She argued for the need of new approaches to tackle this fundamental question, which remains unresolved (Gribaldo et al., 2010). Anthony Poole reminded that all innovations that can be inferred to have been already present in the ancestor of Eukarya (sex, splicesomes, nuclear pores, complex cytoskeleton, etc.) must have evolved along the stem of a protoeukaryotic lineage (Gribaldo et al., 2010; Poole and Neumann, 2010). In the hypothesis of an origin of Eukarya from an archaeon, all these features should have evolved in the protoeukaryotic lineage from modern archaeal traits. On the contrary, if Eukarya and Archaea evolved independently from a common ancestor, the question remains more open (Gribaldo et al., 2010). A number of logical considerations appear to go against the hypothesis of Eukarya deriving from an bona fide archaeon (Poole and Neumann, 2010). Celine Brochier-Armanet presented recent results representing a breakthrough in understanding archaeal evolution and their place in the Tree of Life by the proposal of a third archaeal phylum, the Thaumarchaeota (Brochier-Armanet et al., 2008a,b). Interestingly, Thaumarchaeota, were shown to harbour homologues of both eukaryotic and bacterial cell division systems (ESCRT and FtsZ) (Ettema and Bernander, 2009; Makarova et al., 2010). Molecular phylogenetic analyses indicate in fact that these archaea may be the first branching lineage in the archaeal tree and would have conserved a few traits in common with Eukarya that would have been lost in the two other archaeal phyla, the Euryarchaeota and the Crenarchaeota (Spang et al., 2010; Brochier-Armanet et al., 2008a,b). Christa Schleper (Vienna, Austria) presented data from a newly sequenced genome of Thaumarchaeota that supports the unique phylogenetic status of this archaeal group (Spang et al., 2010). The presence of eukaryotic traits in Thaumarchaeota can be interpreted in different ways. If Eukaryotes originated from an archaeon, it can be logically suggested that this archaeon was a thaumarchaeon, as recently assumed by Kelly and co-workers (Kelly et al., 2010). Indeed, it makes more sense to derive Eukarya from a mesophilic thaumarchaeon than from a hyperthermophilic eocyte (Crenarchaeota), as sometimes proposed (Lake et al., 1984; Gribaldo et al., 2010). Patrick Forterre discusses the possibility of introducing Thaumarchaeota in chimeric scenarios for the origin of eukaryotes by combining a thaumarchaeon (the symbiont) and a Planctomycetes-Verrucomicrobia-Chlamydiae (PVC) bacterium (the host) (Forterre, 2010). However, Forterre concludes that this fusion scenario remains plagued by several inconsistencies and argue in favour of a scenario in which Eukarya and Archaea, including Thaumarchaeota, share a common ancestor
Editorial / Research in Microbiology 162 (2011) 1e4
which was neither an archaeon nor a proto-eukaryote, but an organism with the potential to give rise to these two domains (Forterre, 2010). In any case, the discovery of Thaumarchaeota has opened up a fascinating new window on the archaeal world, as exemplified by the recent discovery of giant “multicellular” Thaumarchaeota living in symbiosis with epsilon-proteobacteria (Muller et al., 2010). All discussions around the evolutionary relationship linking Archaea and Eukarya should be considered in the light of another controversial issue in ancient phylogeny: the rooting of the tree of life. Peter Gogarten reminded the terms of this debate and summarized recent data from the amino-acid composition of ribosomal proteins and from the evolutionary rates of ancient paralogous proteins which support a rooting in the “bacterial branch” and a sister relationship between Archaea and Eukarya (Fournier et al., 2010). He also discussed the interest to use lateral gene transfer to identify synapomorphies (shared derived characters) useful to identify ancient evolutionary relationships (Fournier et al., 2010). Finally, an exciting overview of the meeting was presented the last day by Michel Morange (Paris). He discussed in particular the validity of the various questions raised around the notion of “origins” from a philosophical and epistemological viewpoint (Morange, 2010). In conclusion, the boost in evolutionary biology studies triggered at the end of the last century by the discovery of Archaea is still working at an accelerated pace. The development of genetic tools for a wide range of archaeal taxa now allows opening promising avenues of research by dissecting in great detail their molecular mechanisms. Biochemists, molecular biologists and microbiologists working on Archaea will possibly have the last word in testing alternative competing evolutionary scenarios to place these microbes in the tree of life and answer to a major question in Biology with essential consequences in understanding our very origins. References Berthon, J., Fujikane, R., Forterre, P., 2009. When DNA replication and protein synthesis come together. Trends Biochem. Sci. 34, 429e434. Brochier-Armanet, C., Boussau, B., Gribaldo, S., Forterre, P., 2008a. Mesophilic Crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota. Nat. Rev. Microbiol. 6, 245e252. Brochier-Armanet, C., Gribaldo, S., Forterre, P., 2008b. A DNA topoisomerase IB in Thaumarchaeota testifies for the presence of this enzyme in the last common ancestor of Archaea and Eucarya. Biol. Direct 3, 54. Buttner, K., Wenig, K., Hopfner, K.P., 2006. The exosome: a macromolecular cage for controlled RNA degradation. Mol. Microbiol. 61, 1372e1379. Chia, N., Cann, I., Olsen, G.J., 2010. Evolution of DNA replication protein complexes in eukaryotes and Archaea. PLoS One 5, e10866. Csuros, M., Miklos, I., 2009. Streamlining and large ancestral genomes in Archaea inferred with a phylogenetic birth-and-death model. Mol. Biol. Evol. 26, 2087e2095. de Crecy-Lagard, V., Brochier-Armanet, C., Urbonavicius, J., Fernandez, B., Phillips, G., Lyons, B., Noma, A., Alvarez, S., et al., 2010. Biosynthesis of wyosine derivatives in tRNA: an ancient and highly diverse pathway in Archaea. Mol. Biol. Evol. 27, 2062e2077. Desmond, E., Brochier-Armanet, C., Forterre, P., Gribaldo, S., 2010. On the last common ancestor and early evolution of eukaryotes: Reconstructing the history of mitochondrial ribosomes. Res. Microbiol. 162, 53e70.
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Eme, L., Moreira, D., Talla, E., Brochier-Armanet, C., 2009. A complex cell division machinery was present in the last common ancestor of eukaryotes. PLoS One 4, e5021. Ettema, T.J., Bernander, R., 2009. Cell division and the ESCRT complex: a surprise from the archaea. Commun. Integr. Biol. 2, 86e88. Forterre, P., 2006. Three RNA cells for ribosomal lineages and three DNA viruses to replicate their genomes: a hypothesis for the origin of cellular domain. Proc. Natl. Acad. Sci. U S A 103, 3669e3674. Forterre, P., 2010. A new fusion hypothesis for the origin of Eukarya: better than previous ones, but probably also wrong. Res. Microbiol. 162, 77e91. Fournier, G.P., Dick, A.A., Williams, D., Gogarten, J.P., 2010. Evolution of the Archaea: emerging views on origins and phylogeny. Res. Microbiol. 162, 92e98. Gribaldo, S., Poole, A.M., Daubin, V., Forterre, P., Brochier-Armanet, C., 2010. The origin of eukaryotes and their relationship with the Archaea: are we at a phylogenomic impasse? Nat. Rev. Microbiol. 8, 743e752. Grohmann, D., Werner, F., 2010. Cycling through transcription with the RNA polymerase F/E (RPB4/7) complex: structure, function and evolution of archaeal RNA polymerase. Res. Microbiol. 162, 10e18. Grosjean, H., de Crecy-Lagard, V., Marck, C., 2010. Deciphering synonymous codons in the three domains of life: co-evolution with specific tRNA modification enzymes. FEBS Lett. 584, 252e264. Hartung, S., Hopfner, K.P., 2009. Lessons from structural and biochemical studies on the archaeal exosome. Biochem. Soc. Trans. 37, 83e87. Kelly, S., Wickstead, B., Gull, K., 2010. Archaeal phylogenomics provides evidence in support of a methanogenic origin of the Archaea and a thaumarchaeal origin for the eukaryotes. Proc. Biol. Sci.. Koonin, E.V., 2010. The origin and early evolution of eukaryotes in the light of phylogenomics. Genome Biol. 11, 209. Lake, J.A., Henderson, E., Oakes, M., Clark, M.W., 1984. Eocytes: a new ribosome structure indicates a kingdom with a close relationship to eukaryotes. Proc. Natl. Acad. Sci. U S A 81, 3786e3790. Lombard, J., Moreira, D., 2010. Origins and early evolution of the mevalonate pathway of isoprenoid biosynthesis in the three domains of life. Mol. Biol. Evol.. Lopez-Garcia, P., Moreira, D., 1999. Metabolic symbiosis at the origin of eukaryotes. Trends Biochem. Sci. 24, 88e93. Makarova, K.S., Yutin, N., Bell, S.D., Koonin, E.V., 2010. Evolution of diverse cell division and vesicle formation systems in Archaea. Nat. Rev. Microbiol. 8, 731e741. Matsumi, R., Atomi, H., Driessen, A.J., van der Oost, J., 2010. Isoprenoid biosynthesis in archaea - Biochemical and evolutionary implications. Res. Microbiol. 162, 39e52. Morange, M., 2010. Some considerations on the nature of LUCA, and the nature of life. Res. Microbiol. 162, 5e9. Muller, F., Brissac, T., Le Bris, N., Felbeck, H., Gros, O., 2010. First description of giant Archaea (Thaumarchaeota) associated with putative bacterial ectosymbionts in a sulfidic marine habitat. Environ. Microbiol. 12, 2371e2383. Pereto, J., Lopez-Garcia, P., Moreira, D., 2004. Ancestral lipid biosynthesis and early membrane evolution. Trends Biochem. Sci. 29, 469e477. Poole, A.M., Neumann, N., 2010. Reconciling an archaeal origin of eukaryotes with engulfment: a biologically plausible update of the Eocyte hypothesis. Res. Microbiol. 162, 71e6. Rouillon, C., White, M.F., 2010. The evolution and mechanisms of nucleotide excision repair proteins. Res. Microbiol. 162, 19e26. Samson, R.Y., Obita, T., Freund, S.M., Williams, R.L., Bell, S.D., 2008. A role for the ESCRT system in cell division in archaea. Science 322, 1710e1713. Shah, S.A., Garrett, R.A., 2010. CRISPR/Cas and Cmr modules, mobility and evolution of adaptive immune systems. Res. Microbiol. 162, 27e38. Spang, A., Hatzenpichler, R., Brochier-Armanet, C., Rattei, T., Tischler, P., Spieck, E., Streit, W., Stahl, D.A., et al., 2010. Distinct gene set in two different lineages of ammonia-oxidizing archaea supports the phylum Thaumarchaeota. Trends Microbiol. 18, 331e340. Woese, C.R., Fox, G.E., 1977. Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc. Natl. Acad. Sci. U S A 74, 5088e5090.
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Simonetta Gribaldo* Institut Pasteur, 25 rue du Docteur Roux, 75015 Paris, France *Corresponding author. E-mail address: [email protected] Patrick Forterre* Institut Pasteur, 25 rue du Docteur Roux, 75015 Paris, France Institut de Ge´ne´tique et Microbiologie, Universite´ Paris-Sud, CNRS UMR 8621, 91405 Orsay Cedex, France *Corresponding author. E-mail address: [email protected]
Celine Brochier-Armanet* Universite´ de Provence, Aix-Marseille I, place Victor Hugo, 13331 Marseille Cedex 3, France Laboratoire de chimie bacte´rienne, CNRS UPR9043, IFR88, 31 Chemin Joseph Aiguier, 13402 Marseille, France *Corresponding author. E-mail addresses: [email protected], [email protected] Available online 8 December 2010
Editorial
Editorial: Archaea and the Tree of Life The discovery of Archaea as one of the three domains of life by Carl Woese in 1977 (Woese and Fox, 1977) has been one of the major discoveries of the XXth century in Biology. Since then, the phylogenetic position of Archaea in the universal tree of life has been the topic of hot debates among evolutionists. In 2009, we have organised an international interdisciplinary meeting “Archaea and the Tree of Life” at the Fondation Des Treilles (France), in order to discuss this issue, based on the most recent discoveries obtained on the physiology and molecular biology of Archaea. Scientists from two distinct communities were gathered: on one hand, biochemists and molecular biologists working actively on different archaeal model organisms and on the other hand several evolutionists experts in comparative genomics and phylogenetics. The underlying idea of the meeting was to encourage biochemists and molecular biologists to discuss openly their most recent data in an evolutionary context. In parallel, evolutionists were made aware of the most recent data gathered by the biochemists and molecular biologists covering the whole spectrum of archaeal physiology. The special issue “Archaea and the Tree of Life” represents a collection of most contributions presented at the meeting. During the meeting, various aspects of archaeal biology (cell division, transcription, DNA repair, membrane transport, RNA modification and degradation, and metabolism) were presented by some of the world leaders in these fields: Steve Bell (Oxford, UK), Malcom White (Saint Andrew, UK), Henri Grosjean (Orsay, France), John Van der Ost (Wagenigen, NL), Arnold Driessen (Groningen, NL), Finn Werner (London, UK), Gary Olsen (Urbana, USA), Karl-Peter Hopfner (Munich, DE). These talks emphasized the extensive similarities observed at the molecular level between Archaea and Eukarya (see Rouillon and White, 2010; Grohmann and Werner, 2010; Matsumi et al., 2010); for other recent reviews by meeting participants, see (Makarova et al., 2010; Chia et al., 2010; Hartung and Hopfner, 2009, de CrecyLagard et al., 2010; Berthon et al., 2009). Indeed, it has been known for nearly thirty years ago that Archaea display more similarities with Eukarya than with Bacteria in several informational molecular mechanisms (i.e. processes involved in the transmission of genetic information, including DNA replication, transcription, translation, and associated processes). These mechanisms are now being analysed more in detail at the molecular level. For example, Malcolm White
reviewed the latest advances in research on the components of archaeal DNA repair and their similarities with their eukaryotic counterparts (Grohmann and Werner, 2010; Rouillon and White, 2010), Finn Werner presented an overview of the latest findings in the structural analysis of archaeal RNA polymerases (Grohmann and Werner, 2010), Karl-Peter Hopfner discussed the similarities and differences between the archaeal and eukaryotic exosomes (Buttner et al., 2006; Hartung and Hopfner, 2009), and Henri Grosjean showed the evolutionary link between the RNA modification systems of Archaea and Eukarya (de Crecy-Lagard et al., 2010; Grosjean et al., 2010). These kind of analyses allow discussing the evolutionary relationships between Archaea and Eucarya beyond simple sequence homology and may be used to try inferring the polarization of traits commons to Archaea and Eukarya: are these derived characters testifying for the sisterhood of these two domains, or are these ancestral traits that were lost or replaced in Bacteria? Importantly, although it is generally put forward that bacterial features are more primitive compared to archaeal and eukaryotic characters, the meeting made aware all participants that the question is still open (Grohmann and Werner, 2010) and that more research on various molecular mechanisms in the Archaea will eventually allow to obtain a consensus on this crucial question. Importantly, the similarity between Archaea and Eukarya does not hold simply for informational systems (as currently assumed) but also for operational systems such as cell division, protein secretion or membrane vesicle formation. This last point was dramatically demonstrated by the recent finding that homologues of components of the eukaryotic vesiclesorting system ESCRTIII are involved in cell division in some members of the Crenarchaeota (for recent reviews, see (Ettema and Bernander, 2009; Makarova et al., 2010; Samson et al., 2008)). This finding is a major breakthrough because operational systems in Eukarya are traditionally viewed as bacterial-like, and used as a recurrent argument in favour of scenarios in which Eukarya originated by combining informational systems of an archaeon and operational systems from a bacterium (Lopez-Garcia and Moreira, 1999). Arnold Driessen and John Van der Oost reported clear cases where operational systems in Archaea (membrane transport, cell division, energy production) can also be evolutionarily closely related to those of Eukarya or exhibit a mixture of eukaryotic and bacterial traits (Gribaldo et al., 2010). This is the case of
0923-2508/$ - see front matter Ó 2010 Institut Pasteur. Published by Elsevier Masson SAS. All rights reserved. doi:10.1016/j.resmic.2010.11.007
2
Editorial / Research in Microbiology 162 (2011) 1e4
cell division, since most archaea harbour a homologue of the major bacterial cell division protein FtsZ whereas other harbour components of the eukaryotic ESCRTIII complex or both (Makarova et al., 2010). The unique character of some major archaeal features is of course exemplified by their lipids. With respect to stereochemistry and composition, archaeal lipids are very different from the ester-linked, fatty acid-based phospholipids in bacterial and eukaryotic membranes (Pereto et al., 2004). However, John Van der Oost and colleagues remind that their building blocks (isoprenoids) are made by a universal and possibly ancestral pathway (Pereto et al., 2004; Lombard and Moreira, 2010). They review the main metabolic pathways leading to archaeal lipids and the evolutionary scenarios that have been proposed to explain how two different types of lipids arose in modern cells (Matsumi et al., 2010). They suggest exciting experiments to test some of these scenarios by expressing archaeal lipids in bacterial cells, or vice versa (Matsumi et al., 2010). The nature of viruses and other extra-chromosomal entities in the three domains has rarely been taken into account in scenarios that try to capture the evolutionary relationships between the three domains. Roger Garrett emphasized the similarity between the antiviral defence mechanisms (CRISPR) found in Archaea and Bacteria that appears evolutionarily unrelated to the eukaryotic siRNAs antiviral defence system (Shah and Garrett, 2010). This is in striking contrast with the clear difference between Archaea and Bacteria at the molecular level. Indeed, whereas eukaryotic molecular biology can be dubbed “archaeal-like”, Eukarya have unique viruses (e.g. retrovirus) and viral defence elements (siRNA) that have no counterparts in Archaea. During the meeting, Patrick Forterre emphasized the important role that viruses might have played in the formation of modern cells, especially in the emergence of various DNA replication machineries (Forterre, 2006). In this issue, he discusses more specifically the idea that viruses have played a critical role in the evolution of Eukarya towards complexity by introducing new genes in the eukaryotic lineage and by triggering an arms race with proto-eukaryotic lineages (Forterre, 2010). A better understanding of the evolutionary relationships between Archaea and Eukarya can be gathered by trying to reconstruct the nature of the last common ancestor of Eukarya and of the last common ancestor of Archaea through comparative genomics and phylogenetic analyses. Analyses of the evolution of components of the DNA replication apparatus (Jonathan Berthon, Paris), the mitochondrial ribosome (Elie Desmond, Paris) and of the eukaryotic midbody (Laura Eme, Marseille) indicate that the ancestors of Eukarya and Archaea were at least as complex as their present-day descendants (Berthon et al., 2009; Desmond et al., 2010; Eme et al., 2009). Puzzlingly, Elie Desmond presented evidence for a dynamic evolutionary history of the archaeal ribosome, a unique feature with respect to its counterparts in Bacteria and Eukarya and paralleled only by mitochondrial ribosomes (Desmond et al., 2010). It appears indeed that some streamlining has occurred during the evolution of Archaea (Desmond et al., 2010, de Crecy-Lagard et al., 2010; Csuros and Miklos, 2009; Chia et al., 2010).
The monophyly of Archaea has been disputed for a long time, some authors having suggested that Crenarchaeota share an exclusive ancestor with Eukarya, whereas others suggested that Eukarya originated as a chimera from the merging of a bacterium and an archaeon (reviewed in Gribaldo et al., 2010; Koonin, 2010). Simonetta Gribaldo reviewed a number of recent large-scale phylogenomic analyses published on this subject, showing that various authors obtained different results albeit using similar gene datasets (Gribaldo et al., 2010). She argued for the need of new approaches to tackle this fundamental question, which remains unresolved (Gribaldo et al., 2010). Anthony Poole reminded that all innovations that can be inferred to have been already present in the ancestor of Eukarya (sex, splicesomes, nuclear pores, complex cytoskeleton, etc.) must have evolved along the stem of a protoeukaryotic lineage (Gribaldo et al., 2010; Poole and Neumann, 2010). In the hypothesis of an origin of Eukarya from an archaeon, all these features should have evolved in the protoeukaryotic lineage from modern archaeal traits. On the contrary, if Eukarya and Archaea evolved independently from a common ancestor, the question remains more open (Gribaldo et al., 2010). A number of logical considerations appear to go against the hypothesis of Eukarya deriving from an bona fide archaeon (Poole and Neumann, 2010). Celine Brochier-Armanet presented recent results representing a breakthrough in understanding archaeal evolution and their place in the Tree of Life by the proposal of a third archaeal phylum, the Thaumarchaeota (Brochier-Armanet et al., 2008a,b). Interestingly, Thaumarchaeota, were shown to harbour homologues of both eukaryotic and bacterial cell division systems (ESCRT and FtsZ) (Ettema and Bernander, 2009; Makarova et al., 2010). Molecular phylogenetic analyses indicate in fact that these archaea may be the first branching lineage in the archaeal tree and would have conserved a few traits in common with Eukarya that would have been lost in the two other archaeal phyla, the Euryarchaeota and the Crenarchaeota (Spang et al., 2010; Brochier-Armanet et al., 2008a,b). Christa Schleper (Vienna, Austria) presented data from a newly sequenced genome of Thaumarchaeota that supports the unique phylogenetic status of this archaeal group (Spang et al., 2010). The presence of eukaryotic traits in Thaumarchaeota can be interpreted in different ways. If Eukaryotes originated from an archaeon, it can be logically suggested that this archaeon was a thaumarchaeon, as recently assumed by Kelly and co-workers (Kelly et al., 2010). Indeed, it makes more sense to derive Eukarya from a mesophilic thaumarchaeon than from a hyperthermophilic eocyte (Crenarchaeota), as sometimes proposed (Lake et al., 1984; Gribaldo et al., 2010). Patrick Forterre discusses the possibility of introducing Thaumarchaeota in chimeric scenarios for the origin of eukaryotes by combining a thaumarchaeon (the symbiont) and a Planctomycetes-Verrucomicrobia-Chlamydiae (PVC) bacterium (the host) (Forterre, 2010). However, Forterre concludes that this fusion scenario remains plagued by several inconsistencies and argue in favour of a scenario in which Eukarya and Archaea, including Thaumarchaeota, share a common ancestor
Editorial / Research in Microbiology 162 (2011) 1e4
which was neither an archaeon nor a proto-eukaryote, but an organism with the potential to give rise to these two domains (Forterre, 2010). In any case, the discovery of Thaumarchaeota has opened up a fascinating new window on the archaeal world, as exemplified by the recent discovery of giant “multicellular” Thaumarchaeota living in symbiosis with epsilon-proteobacteria (Muller et al., 2010). All discussions around the evolutionary relationship linking Archaea and Eukarya should be considered in the light of another controversial issue in ancient phylogeny: the rooting of the tree of life. Peter Gogarten reminded the terms of this debate and summarized recent data from the amino-acid composition of ribosomal proteins and from the evolutionary rates of ancient paralogous proteins which support a rooting in the “bacterial branch” and a sister relationship between Archaea and Eukarya (Fournier et al., 2010). He also discussed the interest to use lateral gene transfer to identify synapomorphies (shared derived characters) useful to identify ancient evolutionary relationships (Fournier et al., 2010). Finally, an exciting overview of the meeting was presented the last day by Michel Morange (Paris). He discussed in particular the validity of the various questions raised around the notion of “origins” from a philosophical and epistemological viewpoint (Morange, 2010). In conclusion, the boost in evolutionary biology studies triggered at the end of the last century by the discovery of Archaea is still working at an accelerated pace. The development of genetic tools for a wide range of archaeal taxa now allows opening promising avenues of research by dissecting in great detail their molecular mechanisms. Biochemists, molecular biologists and microbiologists working on Archaea will possibly have the last word in testing alternative competing evolutionary scenarios to place these microbes in the tree of life and answer to a major question in Biology with essential consequences in understanding our very origins. References Berthon, J., Fujikane, R., Forterre, P., 2009. When DNA replication and protein synthesis come together. Trends Biochem. Sci. 34, 429e434. Brochier-Armanet, C., Boussau, B., Gribaldo, S., Forterre, P., 2008a. Mesophilic Crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota. Nat. Rev. Microbiol. 6, 245e252. Brochier-Armanet, C., Gribaldo, S., Forterre, P., 2008b. A DNA topoisomerase IB in Thaumarchaeota testifies for the presence of this enzyme in the last common ancestor of Archaea and Eucarya. Biol. Direct 3, 54. Buttner, K., Wenig, K., Hopfner, K.P., 2006. The exosome: a macromolecular cage for controlled RNA degradation. Mol. Microbiol. 61, 1372e1379. Chia, N., Cann, I., Olsen, G.J., 2010. Evolution of DNA replication protein complexes in eukaryotes and Archaea. PLoS One 5, e10866. Csuros, M., Miklos, I., 2009. Streamlining and large ancestral genomes in Archaea inferred with a phylogenetic birth-and-death model. Mol. Biol. Evol. 26, 2087e2095. de Crecy-Lagard, V., Brochier-Armanet, C., Urbonavicius, J., Fernandez, B., Phillips, G., Lyons, B., Noma, A., Alvarez, S., et al., 2010. Biosynthesis of wyosine derivatives in tRNA: an ancient and highly diverse pathway in Archaea. Mol. Biol. Evol. 27, 2062e2077. Desmond, E., Brochier-Armanet, C., Forterre, P., Gribaldo, S., 2010. On the last common ancestor and early evolution of eukaryotes: Reconstructing the history of mitochondrial ribosomes. Res. Microbiol. 162, 53e70.
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Eme, L., Moreira, D., Talla, E., Brochier-Armanet, C., 2009. A complex cell division machinery was present in the last common ancestor of eukaryotes. PLoS One 4, e5021. Ettema, T.J., Bernander, R., 2009. Cell division and the ESCRT complex: a surprise from the archaea. Commun. Integr. Biol. 2, 86e88. Forterre, P., 2006. Three RNA cells for ribosomal lineages and three DNA viruses to replicate their genomes: a hypothesis for the origin of cellular domain. Proc. Natl. Acad. Sci. U S A 103, 3669e3674. Forterre, P., 2010. A new fusion hypothesis for the origin of Eukarya: better than previous ones, but probably also wrong. Res. Microbiol. 162, 77e91. Fournier, G.P., Dick, A.A., Williams, D., Gogarten, J.P., 2010. Evolution of the Archaea: emerging views on origins and phylogeny. Res. Microbiol. 162, 92e98. Gribaldo, S., Poole, A.M., Daubin, V., Forterre, P., Brochier-Armanet, C., 2010. The origin of eukaryotes and their relationship with the Archaea: are we at a phylogenomic impasse? Nat. Rev. Microbiol. 8, 743e752. Grohmann, D., Werner, F., 2010. Cycling through transcription with the RNA polymerase F/E (RPB4/7) complex: structure, function and evolution of archaeal RNA polymerase. Res. Microbiol. 162, 10e18. Grosjean, H., de Crecy-Lagard, V., Marck, C., 2010. Deciphering synonymous codons in the three domains of life: co-evolution with specific tRNA modification enzymes. FEBS Lett. 584, 252e264. Hartung, S., Hopfner, K.P., 2009. Lessons from structural and biochemical studies on the archaeal exosome. Biochem. Soc. Trans. 37, 83e87. Kelly, S., Wickstead, B., Gull, K., 2010. Archaeal phylogenomics provides evidence in support of a methanogenic origin of the Archaea and a thaumarchaeal origin for the eukaryotes. Proc. Biol. Sci.. Koonin, E.V., 2010. The origin and early evolution of eukaryotes in the light of phylogenomics. Genome Biol. 11, 209. Lake, J.A., Henderson, E., Oakes, M., Clark, M.W., 1984. Eocytes: a new ribosome structure indicates a kingdom with a close relationship to eukaryotes. Proc. Natl. Acad. Sci. U S A 81, 3786e3790. Lombard, J., Moreira, D., 2010. Origins and early evolution of the mevalonate pathway of isoprenoid biosynthesis in the three domains of life. Mol. Biol. Evol.. Lopez-Garcia, P., Moreira, D., 1999. Metabolic symbiosis at the origin of eukaryotes. Trends Biochem. Sci. 24, 88e93. Makarova, K.S., Yutin, N., Bell, S.D., Koonin, E.V., 2010. Evolution of diverse cell division and vesicle formation systems in Archaea. Nat. Rev. Microbiol. 8, 731e741. Matsumi, R., Atomi, H., Driessen, A.J., van der Oost, J., 2010. Isoprenoid biosynthesis in archaea - Biochemical and evolutionary implications. Res. Microbiol. 162, 39e52. Morange, M., 2010. Some considerations on the nature of LUCA, and the nature of life. Res. Microbiol. 162, 5e9. Muller, F., Brissac, T., Le Bris, N., Felbeck, H., Gros, O., 2010. First description of giant Archaea (Thaumarchaeota) associated with putative bacterial ectosymbionts in a sulfidic marine habitat. Environ. Microbiol. 12, 2371e2383. Pereto, J., Lopez-Garcia, P., Moreira, D., 2004. Ancestral lipid biosynthesis and early membrane evolution. Trends Biochem. Sci. 29, 469e477. Poole, A.M., Neumann, N., 2010. Reconciling an archaeal origin of eukaryotes with engulfment: a biologically plausible update of the Eocyte hypothesis. Res. Microbiol. 162, 71e6. Rouillon, C., White, M.F., 2010. The evolution and mechanisms of nucleotide excision repair proteins. Res. Microbiol. 162, 19e26. Samson, R.Y., Obita, T., Freund, S.M., Williams, R.L., Bell, S.D., 2008. A role for the ESCRT system in cell division in archaea. Science 322, 1710e1713. Shah, S.A., Garrett, R.A., 2010. CRISPR/Cas and Cmr modules, mobility and evolution of adaptive immune systems. Res. Microbiol. 162, 27e38. Spang, A., Hatzenpichler, R., Brochier-Armanet, C., Rattei, T., Tischler, P., Spieck, E., Streit, W., Stahl, D.A., et al., 2010. Distinct gene set in two different lineages of ammonia-oxidizing archaea supports the phylum Thaumarchaeota. Trends Microbiol. 18, 331e340. Woese, C.R., Fox, G.E., 1977. Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc. Natl. Acad. Sci. U S A 74, 5088e5090.
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Simonetta Gribaldo* Institut Pasteur, 25 rue du Docteur Roux, 75015 Paris, France *Corresponding author. E-mail address: [email protected] Patrick Forterre* Institut Pasteur, 25 rue du Docteur Roux, 75015 Paris, France Institut de Ge´ne´tique et Microbiologie, Universite´ Paris-Sud, CNRS UMR 8621, 91405 Orsay Cedex, France *Corresponding author. E-mail address: [email protected]
Celine Brochier-Armanet* Universite´ de Provence, Aix-Marseille I, place Victor Hugo, 13331 Marseille Cedex 3, France Laboratoire de chimie bacte´rienne, CNRS UPR9043, IFR88, 31 Chemin Joseph Aiguier, 13402 Marseille, France *Corresponding author. E-mail addresses: [email protected], [email protected] Available online 8 December 2010