sign in sign up
<<
Home , Archaea

Theoretical Population 61, 409–422 (2002) doi:10.1006/tpbi.2002.1592

Evolution of the Archaea

Patrick Forterre Institut de Ge!ne!tique et Microbiologie, UMR 8621 CNRS, Bat 409, Universite! Paris-Sud, 91405 Orsay Cedex, France E-mail: forterre@igmors:u À psud:fr and

Celine Brochier and Herve! Philippe Phyloge!nie, Bioinformatique et Ge!nome, UMR 7622 CNRS, Universite! Pierre et Marie Curie, 9 quai St Bernard Ba#t. C 75005 Paris, France

Received February 27, 2002

Archaea, members of the third of , are bacterial-looking that harbour many unique genotypic and phenotypic properties, testifying for their peculiar evolutionary status. The archaeal ancestor was probably a hyperthermophilic anaerobe. Two archaeal phyla are presently recognized, the and the . was the main invention that occurred in the euryarchaeal and is now shared by several archaeal groups. Adaptation to aerobic conditions occurred several independently in both Euryarchaeota and Crenarchaeota. Recently, many new groups of Archaea that have not yet been cultured have been detected by PCR amplification of 16S ribosomal RNA from environmental samples. The phenotypic and genotypic characterization of these new groups is now a top priority for further studies on archaeal . & 2002 Elsevier Science (USA)

1. INTRODUCTION Eubacteria). In the following decades, this discovery prompted a flood of new hypotheses about the of the Last Universal Cellular Ancestor (LUCA) and the The discovery, by Woese and colleagues in the , phylogenetic relationships between the three domains of that three forms are present in living organ- life (Archaea, and Eukarya) (for recent reviews isms initiated a revolution in evolutionary biology and alternative viewpoints, see Gupta, 1998; Forterre (Woese and Fox, 1977; Woese, 1987; Woese et al., and Philippe, 1999; Lopez-Garcia and Moreira, 1999; 1990). This tripartite division of the appara- Penny and Poole, 1999; Glansdorff, 2000; Woese, 2000; tus had been previously obscured by early observation Cavalier-Smith, 2002; Gribaldo and Philippe, 2002, this of ribosome structure that fitted well with the binary issue). classification of into (80S ribo- The evolution of Archaea per se is an important field somes) and prokaryotes (70S ). However, of evolutionary biology. Since Archaea exhibit a wide when comparative sequence analysis of the ribosome variety of phenotypic and genotypic characters, it would components became available, it turned out that ribo- be interesting to have a clear idea of the history of the somal (rRNA) and ribosomal of some archaeal domain, in order to understand the origin and prokaryotes (the Archaea, formerly Archaebacteria) evolution of these characters. In this review, we will try were drastically different from those of both eukaryotes to sum up the state of the art regarding archaeal and those of ‘‘classical’’ bacteria (the Bacteria, formerly evolution. This is timely, as data from comparative

409 0040-5809/02 $35.00 # 2002 Elsevier Science (USA) All rights reserved. 410 Forterre, Brochier and Philippe can now be combined with more traditional phylogenetic and taxonomic approaches. At the of writing this review, 12 of Archaea have been completely sequenced and are available in public databases (http://www.ncbi.nlm.nih.gov/PMGifs/Gen- omes/a g.html). Furthermore, an up-to-date description of all identified archaeal has been recently published in Volume I of the new Bergey’s Manual edition (Boone and Castenholz, 2001). Finally, archaeal rRNA probes have been widely used by molecular ecologists to investigate the worldwide distribution of the organisms of this domain, as well as its phylogenetic depth (for recent papers see Massana et al., 2000; Lopez- Garcia et al., 2001; Takai et al., 2001a, b).

2. BRIEF DESCRIPTION OF THE DOMAIN ARCHAEA

The Archaea are prokaryotes ( without nucleus) that cannot be easily distinguished from Bacteria by size or shape. However, although most Archaea look like typical Bacteria, some have morphologies that are not found in Bacteria, such as polygonal in halophilic Archaea or very irregular cocci in particular hyperther- mophiles (Fig. 1). This could reflect the absence of a rigid in most Archaea (see below) and/or novel (still unknown) mechanisms for morphogenesis. Ar- chaea exhibit a wide diversity of phenotypes, as is the case for Bacteria. The first three phenotypes to be recognized were the (strict anaerobes and producers), the (strict aerobes living in high- environments) and the (aerobes living in hot and acidic environments) (Woese and Fox, 1977). Organisms with such disparate pheno- FIG. 1. (A) Electron micrograph of the euryarchaeon types were first unified based on the similarities of their (formerly ‘‘square bacteria’’), from Dr. Rodriguez-Valera, (B) electron rRNA sequences, and later on also by the unique micrograph of the crenarchaeon abyssi (a hyperthermo- phile that can grow up to 1108C), the cells are inserted into a structure of their membrane (see below). reticulated network whose function is still unknown and (C) Many additional phenotypes were discovered among transmission electron micrograph of P. abyssi. EM pictures of P. Archaea in the following decades, such as hyperthermo- abyssi are from Reinhard Rachel and . philic or psychrophilic methanogens, halophilic and/or alkaliphilic methanogens, anaerobic, alkaliphilic and neutrophilic (Mathrani et al., 1988; Franzmann et al., 1997; Ollivier et al., 1998; Huber et al., Crenarchaeota account for nearly 20% of the total 2000). Finally, the explosion of environmental studies marine oceanic worldwide based on PCR amplification of 16S rRNA has revealed (Karner et al., 2001). Many of these not yet cultivated the widespread occurrence in water and of Archaea probably exhibit novel phenotypes. For mesophilic Archaea with otherwise unknown pheno- instance, previously unsuspected archaeal methano- types (Fig. 2). For example, a recent study has trophs were predicted recently from geomicrobiological estimated that mesophilic Archaea of the phylum data (Orphan et al., 2001). Archaea are often viewed as Evolution of the Archaea 411

FIG. 2. Phylogeny of the archaeal domain based on 16S rRNA of both cultured and uncultured species. A neighbour-joining was constructed from 342 archaeal nearly complete sequences of SSU rRNA (1235 positions). The distances were calculated with the Tamura and Nei method (Tamura and Nei, 1993) and the a-parameter was computed with PAUP 4b8. Scale bars correspond to 10 substitutions per 100 positions for a unit branch length. The tree was arbitrarily rooted. The size of the triangles is proportional to the number of sequences analysed. Grey triangles include SSU rRNA from both cultured and uncultured species, whereas the white triangle includes only environmental sequences (uncultured species).

predominant over Bacteria in all extreme environments. in all other situations (high salt, low or high pH, low This is indeed true for high-temperature environments, temperature, high pressure), Bacteria are found together since only Archaea can thrive at temperatures above with Archaea and Eukarya (Rothschild and Mancinelli, 958C (and up to 1138C) (Huber et al., 2000). However, 2001). 412 Forterre, Brochier and Philippe

The metabolic diversity of Archaea is also reminiscent with other archaeal proteins when their homologues are of Bacteria. Apart from methanogenesis (presently searched in public databases. This is especially true for unknown in Bacteria) all metabolic pathways discovered informational proteins (those involved in DNA replica- in Archaea also exist among Bacteria. They can be either tion, and translation) that are usually heterotrophs or (chemio- or photo-lithoau- present in most archaeal genomes and are nearly always totroph) and use a large variety of electron donors and more similar between one archaeon and another than acceptors (Huber et al., 2000). based on between one archaeon and any bacterium or . chlorophyll has not been found in Archaea, whereas These archaeal informational proteins are also usually photosynthesis based on , once be- much more similar to those of Eukarya than to those of lieved unique to halophilic Archaea, has been recently Bacteria. detected in planktonic Bacteria as well (Beja et al., In addition, archaeal genomes encode many informa- 2001). formers or organisms with complex cell tional proteins that have homologues in Eukarya but cycle and multicellular stages are unknown among not in Bacteria. This is especially striking in the case of Archaea, but this could be simply due to our incomplete DNA replication, since archaeal genomes encode sampling of this domain. The only way to discriminate homologues of nearly all eukaryal DNA replication between Archaea and Bacteria is thus by looking at the proteins but only one homologue of a bacterial DNA molecular level. replication (Edgell and Doolittle, 1997; Forterre, Beside their specific rRNA, Archaea can be distin- 1999; Leipe et al., 1999). The eukaryotic-like putative guished from Bacteria by the nature of their membrane replication proteins identified in archaeal genomes are glycerolipids that are of and isoprenol, most likely involved in actual archaeal DNA replication, whereas bacterial and eukaryal are of as indicated by recent observation such as direct glycerol and fatty (Kates, 1993). Archaeal interaction in vivo between the chromosomal origin glycerolipids are also ‘‘reverse lipids’’, since the en- (oriC) and the eukaryotic-like initiator protein antiomeric configuration of their glycerophosphate (Matsunaga et al., 2001) and the similar size of Okazaki backbone is the mirror image of the configuration fragments in Archaea and Eukarya (Matsunaga and found in bacteria and eukaryal lipids. Another differ- Myllykallio, pers. comm.). ence between Archaea and Bacteria is the absence of It is often considered that informational proteins murein in Archaea, whereas this compound is present in constitute the ‘‘core’’ of the of any , the cell wall of most Bacteria. Archaea exhibit a great because they are less subject to lateral transfer diversity of cell envelopes (Kandler and Konig, 1998), (LGT), and are therefore more representative of the most Archaea have a simple S-layer of actual history of the organisms (Jain et al., 1999). covering the cytoplasmic membrane, whereas a few of Indeed, except for well-documented LGT between them () only have a cytoplasmic Archaea and Bacteria in the case of amino-acyl tRNA membrane containing glycoproteins. Some Archaea synthetases (Wolf et al., 1999; Woese et al., 2000), few have a rigid cell wall based either on heteropolysacchar- LGTs of informational proteins have been identified ides () or pseudomurein (Methanobacter- between the two prokaryotic domains. For example, an iales), the latter being Gram positive. The difference exhaustive study has shown that no LGT had occurred between Archaea and Bacteria at the molecular level is between Archaea and Bacteria in the case of ribosomal exemplified by the resistance of Archaea to most proteins (Brochier et al., 2002) even if LGTs were active on Bacteria. Early studies on the discovered within Bacteria (Brochier et al., 2000, 2002) of Archaea have shown that this and Archaea (Matte-Tailliez et al., 2002). resistance was due indeed to critical differences in the The close similarity between eukaryal and archaeal targets (e.g., RNA polymerase or ribosomal informational proteins can be explained by two hypoth- proteins) (for an early review on archaeal molecular eses: either Archaea and Eukarya are sister groups, and biology, see Zillig, 1991). the ‘‘eukaryotic’’ characters of Archaea are synapomor- The coherence of Archaea at the molecular level is phies, or these characters are primitive (already present now also well documented by comparative genomics in the LUCA, thus symplesiomorphies) and divergent in (Olsen and Woese, 1997; Forterre, 1997; Forterre Bacteria. We will not discuss this problem here (for a and Philippe, 1999; Fitz-Gibbon and House, 1999; review see Forterre and Philippe, 1999; Poole et al., Makarova et al., 1999; Snel et al., 1999; Tekaia et al., 1999; Woese, 2000; Cavalier-Smith, 2002; Gribaldo and 1999; Wolf et al., 2001). In all archaeal genomes Philippe, this issue) since we will focus on the evolution sequenced so far, most encoded proteins give first hits of the archaeal domain per se. Evolution of the Archaea 413

Interestingly, in contrast to informational proteins, bacterial genomes exhibit no synteny and very little most operational proteins of Archaea are ‘‘bacterial- conservation of gene order, in agreement with rapid like’’. This category includes of the primary genomic evolution by recombination (Huynen and and secondary , membrane receptors, Bork, 1998). Comparison of the two closely related transporters and so on, but also some Archaea abyssi and Pyrococcus horikoshi has proteins (Koonin et al., 1997; Jain et al., 1999). This is shown that the terminus of DNA replication is a hot often interpreted as testifying for extensive LGT of spot of recombination, as in the case of Bacteria operational proteins between the two prokaryotic (Myllykallio et al., 2000). Furthermore, the main domains (Faguy and Doolittle, 1999; Makarova et al., rearrangement between the two Pyrococcus genomes 1999). However, although LGTs between hyperthermo- has occurred symmetrically to the axis formed by the philic Bacteria and Archaea have been well documented origin and the terminus of replication (Makino and by phylogenetic and/or genome context analyses (Gri- Suzuki, 2001; Zivanovic et al., 2002). This characteristic baldo et al., 1999; Forterre et al., 2000; Nesbo et al., feature has been also observed in Bacteria, suggesting 2001), a supertree inferred only on operational proteins that major recombination events occurred between bi- is very similar to the one inferred from informational directional replication forks (Tillier and Collins, 2000). proteins (Daubin and Gouy, 2001), suggesting that These similarities in the mechanisms of genome evolu- LGTs are not so frequent for operational . More tion of the two prokaryotic domains could reflect a analyses are thus required to test the hypothesis that the common structural organization of the replication similarity between Archaea and Bacteria for operational apparatus (for example, association of the two replica- genes is only due to LGTs. Alternative hypotheses that tion forks into a single replication factory) and of the have been proposed to explain this similarity are the segregation machinery (in relation with the fusion of ancient bacterial and eukaryotic lineages to presence in Archaea of homologues of the bacterial produce extant Archaea (Koonin et al., 1997) or the proteins Xer C/D), which are involved in the resolution monophyly of Archaea and Bacteria, if the universal of recombinant at the end of replication, is rooted in the eukaryotic branch (Forterre and of the bacterial proteins MinD and FtsZ, which are and Philippe, 1999). involved in the formation of septum for cell division. However, it should be stressed that study of the mechanisms of chromosome structure and evolution in Archaea is still in its infancy, and that the diversity 3. IN ARCHAEA of Archaea in this respect remains to be explored. For instance, two possible (instead of one) replica- tion origins have been predicted in silico in Comparative genomics suggests that the mechanisms (Kennedy et al., 2001) and the bacterial of genome evolution in Archaea are quite similar to cell division proteins FtsZ and MinD are lacking in those identified in Bacteria. This can be explained by the all Crenarchaeota. resemblance between the genome organizations in the In addition to chromosomal rearrangements linked to two domains. For instance, despite eukaryotic-like DNA replication, recombination events have been replication proteins, hyperthermophilic Archaea of the associated to IS elements in several archaeal genomes Pyrococcus replicate their chromosome at high (Kennedy et al., 2001; Bruugger. et al., 2002). IS elements speed, bi-directionally and using a single replication are especially abundant in S. solfataricus and Halobac- origin, as in Bacteria (Lopez et al., 1999; Myllykallio terium NRC1. Comparison of the three completely et al., 2000; Matsunaga et al., 2001). Most highly sequenced Pyrococcus genomes suggested that a family transcribed genes are transcribed co-directionally with of IS elements, only present in P. furiosus, has been DNA replication, as in Bacteria, probably to avoid involved in most chromosomal rearrangements ob- frequent head-to-head collision between the replication served in the latter species (Maeder et al., 1999; and transcription apparatuses (Zivanovic et al., 2002). Lecompte et al., 2001). In Pyrococcus and , Shine–Dalgarno sequences are found in some Archaea chromosomal rearrangements linked to IS elements as in Bacteria, and archaeal genes are often organized occur preferentially in the limit of one replichore (the in . Finally, mechanisms of gene regulation in half chromosome comprised between the origin and Archaea involve bacterial-like regulator proteins terminus of replication), suggesting a principle of (Aravind and Koonin, 1999; Bell and Jackson, 2001). genome organization that is not yet understood Except for closely related organisms, archaeal and (Zivanovic et al., 2001, 2002; Bruugger. et al., 2002). 414 Forterre, Brochier and Philippe

An important difference of the genome organization Prangishvili et al., 2001). It has been shown that IS between the two prokaryotic domains is that all Bacteria elements present in Sulfolobus species have indeed contain a gyrase and a negatively supercoiled genome, triggered active recombination between chromosomes, whereas most Archaea have no gyrase and relaxed or and (for review, see Bruugger. et al., positively supercoiled genome (Charbonnier and For- 2002), in agreement with the above hypothesis on the terre, 1994). Some Euryarchaeota, including the hyper- role of viruses in LGT. The recent analysis of the fulgidus, have acquired complete genome of the halobacteriophage HF2 is bacterial gyrases by LGT and have negatively super- especially relevant to the idea that viruses have been a coiled genomes (Lopez-Garcia and Forterre, 1999). It is major vector for LGT between domains, since it not known presently if differences in genome topology contains a mixture of archaeal, bacterial and bacter- have an effect on the mechanisms of genome evolution. iophage-like genes (Tang et al., 2002). In particular, its LGTs between different archaeal species, and also DNA polymerase seems more closely related to bacter- between Bacteria and Archaea, have been involved as a iophage T4 DNA polymerase than to archaeal DNA major mechanism of genome evolution in Archaea. polymerases (Fileee! et al., in press). Accordingly, LGTs LGTs appear to be predominant between organisms are probably not limited by environmental barriers since living in similar environment. This has been shown both mechanisms for genetic exchanges (e.g., or by genome wide comparison (Aravind et al., 1998; transposable elements) should have evolved and adapted Nelson et al., 1999; Ruepp et al., 2000) and in the case themselves to various environments together with their of some ribosomal proteins inside the archaeal hosts. domain (Matte-Tailliez et al., 2002). For example, many LGTs have been detected between the thermoacido- philic Archaea and Sulfolobus that are otherwise phylogenetically very distant (Ruepp 4. ARCHAEAL PHYLOGENY, THE TWO et al., 2000). MAJOR PHYLA IS elements are likely often involved in these LGTs. For instance, a 16 kb DNA fragment flanked by two IS has been transferred between littoralis Phylogenetic trees of the archaeal domain based on and (Diruggiero et al., 2000). IS 16S rRNA have led to split this domain into two phyla elements could have also played a critical role in LGT (according to Bergey’s Manual definition), the Eur- between Bacteria and Archaea since many of the IS yarchaeota and the Crenarchaeota (Woese et al., 1990). detected in Archaea belong to families previously The Euryarchaeota have been named from the Greek detected in Bacteria (Bruugger. et al., 2002). The precise word euruB; meaning wide, because they encompass the mechanism of LGT between the two prokaryotic greatest phenotypic diversity among known cultivable domains remains mysterious. In particular, trans- species, with the halophiles, the methanogens, some formation by naked DNA appears highly unlikely thermoacidophiles and some hyperthermophiles. in the case of hyperthermophiles considering the In contrast, the phenotypic diversity of cultivable high instability of DNA fragments at high tempera- Crenarchaeota is much more limited, with only ture (Marguet and Forterre, 1994). LGT could hyperthermophilic species. This phylum has thus been possibly involve transfection by viruses, especially named from the Greek word krZnZ meaning spring, if one considers that operational proteins similar from the popular hypothesis that hyperthermophiles are between Bacteria and Archaea include some outer at the origin of all present-day organisms. This name has membrane proteins (e.g., sugar transporters) known been conserved, despite the detection by PCR in various to be potential viral receptors. One can thus imagine environments of many groups of mesophilic and that sometimes interact with archaeal probably psychrophilic Crenoarchaeota that have not homologues of their usual bacterial receptors, and yet been cultivated (Fig. 2). then inject by mistake their DNA into archaeal cells Some data of comparative genomics support the (and vice versa). Such rare events could readily division of Archaea into two distinct phyla, since many lead to LGT if the injected DNA fragment contains proteins present in all euryarchaeal genomes are missing mobile IS elements that can function in both prokar- in Crenarchaeota and vice versa. In particular, several yotic domains. striking differences have been noticed between the two Viruses and plasmids seem to be as common in phyla for some key proteins involved in DNA replica- Archaea as in Bacteria (Benbouzid-Rollet et al., 1997; tion, chromosome structure and cell division, such as the Evolution of the Archaea 415 absence of eukaryal-like , eukaryal RPA-like undergone LGT events during archaeal evolution, with proteins and bacterial cell division proteins in all a bias for LGTs between Thermoplasmatales and Crenarchaea (Bernander, 2000; Myllykallio and For- Crenarchaeota, and were thus not suitable for inferring terre, 2000). However, it remains to be known if these species phylogeny. The phylogeny based on the remain- differences are specific to cultivable hyperthermophilic ing 45 genes was very similar to the rRNA phylogeny Crenarchaeota, or if they are a general characteristic of and strongly supported the partitions between Cre- this phylum. Furthermore, some global genomic ana- narchaeota and Euryarchaeota. We have now carried lyses have failed to recover the division of Archaea into out the same analysis, but including the genomes of two phyla. For example, using five different approaches Sulfolobus tokodai and of that (e.g., gene content, gene order, concatenated ribosomal were published after our initial work was completed, proteins) on ten archaeal genomes, Wolf et al. (2001) and we obtained similar results (Fig. 3). It should be failed to recover the monophyly of the two phyla. noted that the and the Thermoplasma- Nevertheless, their phylogeny based on gene content tales display very long branches. Therefore, when a very is very likely biased by frequent LGTs between distant outgroup is used to root the archaeal phylogeny Thermoplasmatales (Euryarchaeota) and (i.e., the Bacteria), the long-branch attraction artefact (Crenarchaeota) (Ruepp et al., 2000). If Thermo- (Felsenstein, 1978) is a major problem (Philippe and plasmatales are not taken into account, the two phyla Laurent, 1998). Accordingly, the long branches of are monophyletic, in agreement with a previous study Halobacteriales and Thermoplasmatales likely emerge based on gene content (Huynen et al., 1999). Similarly, early in ribosomal proteins’ phylogeny because they are the use of a much more refined phylogenetic method attracted by the bacterial branch, as previously sug- (through maximum likelihood inference of individual gested (Wolf et al., 2001). genes and supertree reconstruction), performed on 459 In conclusion, the division of Archaea into Crenarch- genes from seven Archaea, also recovered the mono- aeota and Euryarchaeota can be viewed as supported by phyly of the two phyla (Daubin and Gouy, 2001; see phylogenetic analyses, at least for cultivable species also Brown et al., 2001). (Fig. 2). Indeed, the analysis of archaeal sequences from The lack of monophyly in the phylogeny based on the environment has somehow complicated the picture ribosomal proteins obtained by Wolf and coworkers is of the archaeal domain from the 16S rRNA viewpoint. more surprising (Wolf et al., 2001). We recently Although many of the new archaeal lineages that have performed a detailed analysis of 53 ribosomal proteins been detected by PCR analysis of environmental present in most of 14 archaeal species (Matte-Tailliez samples branch among Crenarchaeota and Euryarch- et al., 2002). We found that eight genes have likely aeota, some of them branch in between. A tentative

FIG. 3. Phylogeny of the archaeal domain based on concatenated amino sequences. Ribosomal protein sequences have been retrieved from completely sequenced genomes (with the exception of Haloarcula marismortui). Ribosomal proteins for which LGTs were suspected were removed from the analysis, with our recently developed method (Brochier et al., 2002). The only modification was that all the likelihood was computed with a G-law model. A maximum likelihood phylogenetic tree was constructed from the concatenated 47 ribosomal proteins sequence (6220 positions). The calculations of the best tree and the branch lengths were conducted using the program PUZZLE with a G-law correction. Numbers close to nodes are ML bootstrap supports computed with the RELL method upon 2000 top-ranking trees using the MOLPHY program without correction for among-site variation. Scale bars correspond to 10 substitutions per 100 positions for a unit branch length. The tree was arbitrarily rooted between Crenarchaeota and Euryarchaeota. 416 Forterre, Brochier and Philippe third phylum, the (from the Greek word rRNA tree (Fig. 2), together with their analysis with the koroB; meaning young man), was suggested (Barns et al., refined method, will be critical to confirm or invalidate 1996). Sequences that branch even deeper than Kor- the monophyly of Archaea. archaeota in the archaeal 16S rRNA tree were recently reported (Takai et al., 2001a, b). We thus constructed an archaeal phylogeny using all the Archaea for which rRNA sequences are almost complete (Fig. 2). This tree 5. STRUCTURE AND EVOLUTION OF identifies a huge group of environmental sequences that THE TWO ARCHAEAL PHYLA cannot be attributed to either Euryarchaeota or Crenarchaeota. The Korarchaeota and other uncultured lineages form a with cultured Crenarchaeota, but The Euryarchaeota have been divided into nine with low bootstrap support (below 50%). It is thus not orders, five orders for the methanogens (Methanobac- clear if the dichotomy of the archaeal domain will teriales, , , Metha- survive future studies. More phyla will very likely have nosarcinales and ), one for the to be defined in Archaea. This could eventually produce halophiles (Halobacteriales), one for the thermoacido- an archaeal classification more similar to the bacterial philes (Thermoplasmatales) and two for the hyperther- one (23 phyla are presently recognized in the Bacterial mophiles ( and Archaeoglobales) domain, Boone and Castenholz, 2001). Nevertheless, (Fig. 2). one has also to be careful in interpreting the diversity of Phylogenetic trees based on 16S rRNA place the environmental sequences, since divergent copies of Methanopyrales at the base of the euryarchaeal tree, rRNA can exist within a single organism (Mylvaganam followed by Thermococcales, but with very weak and Dennis, 1992; Amann et al., 2000). statistical support (the bootstrap supports for the four For a long time, some authors have advocated the basal nodes are between 4% and 8% in Fig. 2). Since of Archaea, suggesting that Crenarchaeota Methanopyrales are hyperthermophiles (the only species (called eocytes by Lake and colleagues) form a clade of this order, kandleri, can grow up to with Eukarya (Lake, 1988), based for example on an 1108C), this has suggested that ancestral Euryarchaeota insertion in elongation factor 1a (Rivera and Lake, were both methanogens and hyperthermophiles. The 1992). A phylogenetic analysis of rRNA taking among- idea that methanogenesis (formation of methane from site rate variability into account supports this claim H2 and CO2) is an ancestral phenotype was first (Tourasse and Gouy, 1999). It is reasonable to assume advocated to support the name ‘‘Archaebacteria’’ itself that the monophyly of Archaea generally observed in (Woese and Fox, 1977). The discovery of a subterranean rRNA trees (Woese et al., 1990) is due to a long-branch of methanogens thriving on H2 has recently attraction artefact, because Bacteria and Eukarya dis- prompted speculation about the possibility that metha- play much longer branches than Archaea for rRNA. nogens are directly connected to a hot origin of life on The use of methods less sensitive to this artefact and possibly elsewhere (Chapelle et al., 2002). The (Tourasse and Gouy, 1999) provided a good evidence exact position of Methanopyrales in the euryarchaeal in favour of the paraphyly of Archaea. However, tree is thus of critical importance. phylogenies based on genome content (Fitz-Gibbon The recent sequencing of the M. kandleri genome is and House, 1999; Huynen et al., 1999) as well as on thus an important step in our understanding of archaeal multiple markers (Brown et al., 2001; Daubin and evolution (Slezarev et al., 2002). Phylogenetic analysis of Gouy, 2001) recovered the monophyly of Archaea. In concatenated ribosomal proteins suggests that Metha- addition, recent analyses of two crenarchaeal genomes nopyrales do not branch first in the euryarchaeal tree ( pernix and ) failed to but branch with other thermophilic and hyperthermo- identify specific eukaryal-crenarchaeal proteins that philic methanogens (Slesarev et al., 2002). Furthermore, could support the hypothesis of paraphyly (Faguy and our phylogenetic analysis of ribosomal proteins limited Doolittle, 2000; Natale et al., 2000). On the contrary, the to the archaeal domain (thus using more positions and Crenarchaea lack several eukaryal proteins of the limiting the impact of long-branch attraction artefact) informational apparatus that are present in Euryarchaea locates Thermococcales firmly at the base of the (such as histones or some DNA replication proteins, euryarchaeal tree (bootstrap support of 86%, Matte- Bernader, 2000; Myllykallio and Forterre, 2000). The Tailliez et al., 2002). This was confirmed by our new completion of several genomes from Crenarchaeota, analysis with two additional species (bootstrap support Korarchaeota and their relatives at the base of the 16S of 89%, Fig. 3). The position of Thermococcales at the Evolution of the Archaea 417 base of the euryarchaeal tree and the grouping of M. since genomes from have not yet been kandleri with other methanogens thus suggest that sequenced. As in the case of Euryarchaeota, methanogenesis (a very complex ) respiration is most likely a secondary adaptation in has originated in the euryarchaeal domain only after the Crenoarchaeota. However, we should be aware that divergence between Thermococcales and other Eur- hyperthermophilic Crenoarchaeota that have been dis- yarchaea. This would be in agreement with the absence covered in the last two decades represent only a small of relics of methanogenesis in the genomes of Thermo- fraction of this phylum. From examination of Fig. 2, it coccales, whereas such relics have been found in is striking that most of the archaeal groups in both Archaeoglobus (Klenk et al., 1997; Slesarev et al., 2002). Euryarchaeota and Crenarchaeota are in fact presently Both rRNA and ribosomal protein based phylogenies uncultured. There is therefore much research to be have suggested that Halobacteriales are a sister group to done both in classical and environ- Methanomicrobiales (Fig. 3). This grouping makes mental genomics before a complete picture of the sense since Methanomicrobiales are the only order of archaeal domain structure and evolution can be methanogens that does not include thermophilic species, obtained. A recent development has been the discovery and contains halophilic species. This suggests that of parasitic archaea of reduced size (Nanoarchaeum Halobacteriales originated from halophilic and meso- equitans) and genome (less than 0:5 Mb) that live in philic methanomicrobiales that have lost their ability to parasitic association with hyperthermophilic produce methane and have acquired both oxygen Crenoarchaeota of the genus and branch tolerance and respiratory complexes. Analysis very deeply in the crenoarchaeotal 16S rRNA tree of the genes involved in aerobic respiration that can be (Huber et al., 2002). detected in the genome of Halobacterium sp. NRCl has indicated that these genes have been borrowed from aerobic Bacteria by LGT (Kennedy et al., 2001). Indeed, in one of these clusters, the genes for aerobic respiration 6. NATURE OF THE ARCHAEAL present in Halobacterium NRCl have no archaeal ANCESTOR counterpart, whereas in the others, they are more closely related to their bacterial than to their archaeal homo- logues. Phylogenetic and genomic analyses of cultivable Both rRNA and ribosomal protein based phylogenies Archaea suggest that the ancestor of all present-day also suggest the existence of a large clade grouping Archaea was an anaerobe that probably lived when , Thermoplasmatales, Archaeoglo- oxygen was still absent from the terrestrial . bales, Methanomicrobiales and Halobacteriales. How- Complete adaptation to an aerobic lifestyle is a ever, phylogenies based on other genes or on gene secondary adaptation in the archaeal domain that content failed to retrieve it (Brown et al., 2001; Daubin occurred several times independently: at least once in and Gouy, 2001; Wolf et al., 2001). Furthermore, this Crenarchaeota (Sulfolobales) and twice in Euryarchaeo- group is not recovered when sequences from uncultured ta (Halobacteriales and Thermoplasmatales). However, species are included in the 16s RNA tree (Fig. 2). The several Crenarchaeota are also microaerobes (Aeropyr- analysis of additional genomes will thus be required to um pernix and aerophilum), so we cannot sort out the phylogenetic relationships among these exclude that the archaeal ancestor itself had some different lineages. oxygen tolerance. As previously noticed, this ancestor The cultured Crenoarchaeota have been divided into was probably not a , at least if we consider three orders according to 16S rRNA: the Thermopro- indeed that the rooting of the archaeal tree between teales, the Desulfurococcales and the Sulfolobales Thermococcales and Crenarchaeota (Fig. 3) is correct. (Fig. 2). The first two orders include only anaerobic It is also often considered that the archaeal ancestor was hyperthermophiles that live at neutral pH and include a chemiolithoautotroph, since chemiolithoautotrophic the most hyperthermophilic organisms known today are present in both archaeal phyla. For (with maximal growth temperature up to 1138C), several authors, this is consistent with the theory of an whereas Sulfolobales, which live at low pH (2–3), can autotrophic origin of life (Wachtershauser, 1990). be either aerobes or anaerobes and have lower However, since heterotrophic hyperthermophiles are temperature maxima (up to 858C). present in both archaeal phyla (e.g., Thermococcales are a sister group to Sulfolobales in 16S rRNA trees. in Euryarchaeota and Pyrobaculum, Aeropyrum and Genomic data cannot yet be used to test this phylogeny in Crenarchaeota), one cannot exclude 418 Forterre, Brochier and Philippe that the archaeal ancestor was a heterotroph. In fact, evolved more slowly (Kollman and Doolittle, 2000; considering the extent of LGTs in prokaryotes, it is Matte-Tailliez et al., 2002). The phylogeny of reverse difficult to raise firm conclusions about the origin and gyrase, a unique DNA topoisomerase that introduces evolution of such metabolic pathways. Moreover, the positive superturns in DNA, also argues for a presence of many uncultivated lineages at strategic hyperthermophilic archaeal ancestor, since it is coherent points of the phylogeny renders inference of the with the rRNA phylogeny (e.g., the separation of ancestral very hypothetical until their Euryarchaeota and Crenarchaeota) (Forterre et al., metabolism will be characterized. 2000). A fascinating aspect of the archaeal domain is its Reverse gyrase is present in all hyperthermophiles connection with hyperthermophily. We have already (both Archaea and Bacteria) and absent in all genomes mentioned that only Archaea have apparently been able from or moderate thermophiles. From to colonize biotopes with temperatures above 958C: comparative genomics analysis performed using the Possibly, this can be explained by the unique structure ‘‘Phylogenetic Patterns Search Program’’ of the COG of archaeal lipids that maintain the impermeability of database (Tatusov et al., 2001), extended to the genome the cytoplasmic membrane to at such high of Sulfolobus solfataricus (She et al., 2001), it even temperatures. When the membrane layer becomes turned out that reverse gyrase is the only protein that unable to maintain an efficient barrier to passive exhibits this striking phylogenetic distribution (Forterre, diffusion, the cell cannot build up the ion gradients that 2002). Phylogenetic and genome context analyses have are required to produce ATP. The membrane of indicated that reverse gyrase has been transferred from hyperthermophilic Archaea contains tetraether lipids Archaea to hyperthermophilic Bacteria by LGT (at least that can form a monolayer highly resistant to passive twice independently), suggesting that the common ion transfer. This has been experimentally demonstrated ancestor of all Bacteria was not a in vitro by the analysis of ion transport in reconstituted and that the hyperthermophilic phenotype originated in vesicles formed with archaeal lipids. Hyperthermophilic Archaea (Forterre et al., 2000). This is consistent with Bacteria also have unusual lipids that ‘‘try’’ to resemble the idea that LUCA was not a hyperthermophile, a archaeal ones (tetraester or diether), but they have been viewpoint that is also supported by recent analysis apparently unable to produce membrane that can suggesting that the GC content of LUCA rRNA was too prevent ion leakage at temperatures above 958C (for a low to be compatible with a hyperthermophilic lifestyle recent review on the importance of lipids and membrane (Galtier et al., 1999). permeability in thermoadaptation, see Albers et al., 2001). Interestingly, mesophilic and even some psychrophilic Archaea also have tetraether lipids (Schouten et al., 7. CONCLUSION AND PERSPECTIVE 2000). Indeed, these unique lipids have the ability to maintain a correct membrane fluidity in a wide temperature range. The appearance of such lipids might The study of Archaea has confirmed the two initial have thus predated (and anticipated) the appearance of predictions by Woese and Fox (1977), i.e., that Archaea hyperthermophiles in the archaeal domain. Alterna- will exhibit a phenotypic diversity at least comparable to tively, these lipids might have appeared in a hyperther- that of Bacteria and that Archaea will be characterized mophilic archaeal ancestor and their presence today in by unique features at the molecular level. In addition, mesophilic and psychrophilic Archaea can be viewed as Archaea turned out to exhibit a mosaic of features from a heritage from their hyperthermophilic ancestor. the two other domains that continue to stimulate The later hypothesis is supported by the presence of discussions among evolutionists. In the course of their many hyperthermophic lineages that emerge at the base history, Archaea have in particular retained (or of both the euryarchaeal and the crenarchaeal phyla (at acquired) in their informational apparatus many char- least for the cultivable species, the picture being much acters that they only share now with Eukarya. Despite more complex with uncultured species). Furthermore, in their differences in this respect, Archaea and Bacteria both rRNA trees and ribosomal protein trees (Figs. 1 have been engaged in a continuous ‘‘dialogue’’ via and 2), the hyperthermophilic Archaea have shorter LGTs, due to their similar prokaryotic lifestyles. branches than their mesophilic counterparts, suggesting Whereas some Bacteria learned from Archaea how to that hyperthermophiles might have retained more bypass the hyperthermophilic barrier (borrowing ancestral characters, since their have reverse gyrase), some Archaea learned from Bacteria Evolution of the Archaea 419 how to utilize oxygen to get surplus. We Benbouzid-Rollet, N., Lopez-Garcia, P., Watrin, L., Erauso, G., have now, with some confidence, the idea of a Prieur, D., and Forterre, P. 1997. of new plasmids from hyperthermophilic and anaerobic archaeal ancestor, hyperthermophilic Archaea of the order Thermococcales, Res. Microbiol. 148, 767–775. suggesting that the invention of reverse gyrase, Bernander, R. 2000. Chromosome replication, nucleoid the acquisition of tetraether lipids and other features segregation and cell division in archaea, Trends Microbiol. 8, of thermoadaptation have been critical for the emer- 278–283. gence of Archaea. However, this view, as all others Boone, D. R., and Castenholz, R. W. 2001. ‘‘Bergey’s Manual of concerning the origin and evolution of phenotypic Systematic Bacteriology,’’ 2nd ed., Vol. 1, Springer-Verlag, New York, Berlin, Heildelberg. traits in Archaea, should still be taken with caution, Brochier, C., Bapteste, E., Moreira, D., and Philippe, H. 2002. considering the limited number of archaeal lineages Eubacterial phylogeny based on translational apparatus proteins, for which cultivable species are available for pheno- Trends Genet. 18, 1–5. typic and phylogenomic analyses. In particular, it Brochier, C., Philippe, H., and Moreira, D. 2000. The evolutionary should be extremely important now to get genotypic history of ribosomal protein RpS14: at the heart of the ribosome, Trends Genet. 16, 529–533. and phenotypic information about all the archaeal Brown, J. R., Douady, C. J., Italia, M. J., Marshall, W. E., and lineages that are presently only known from their Stanhope, M. J. 2001. Universal trees based on large combined phylotypes, especially those branching in between protein sequence data sets, Nat. Genet. 28, 281–285. Euryarchaeota and Crenarchaeota. Bruugger,. K., Redder, P., She, Q., Confalonieri, F., Zivanovic, Y., and Garrett, R. A. 2002. Mobile elements in archaeal genomes, FEMS Microbiol. Lett. 206, 131–141. Cavalier-Smith, T. 2002. The neomuran origin of archaebacteria, the ACKNOWLEDGMENTS negibacterial root of the universal tree and bacterial megaclassifi- cation, Int. J. Syst. Evol. Microbiol. 52, 7–76. Chapelle, F. H., O’Neill, K., Bradley, P. M., Methe, B. A., Ciufo, S. We thank Allan Campbell and Samuel Karlin for providing us with A., Knobel, L. L., and Lovley, D. R. 2002. A -based the opportunity to write this review. Preliminary sequence data of subsurface microbial community dominated by methanogens, and were obtained from the DOE Joint Nature 415, 312–315. Genome Institute (JGI) at http://www.jgi.doe.gov/JGI microbial/ Charbonnier, F., and Forterre, P. 1994. Comparison of DNA html/index.html. We are grateful to Karl O Stetter, Francisco topology among mesophilic and thermophilic eubacteria and Rodriguez-Valera and Purification Lopez-Garcia for the EM pictures. archaebacteria, J. Bacteriol. 176, 1251–1259. We acknowledge Simonetta Gribaldo and David Moreira for a careful Daubin, V., and Gouy, M. 2001. Bacterial molecular phylogeny using reading of the manuscript. supertree approach, Genome Inform. Ser. Workshop Genome lnform. 12, 155–164. Diruggiero, J., Dunn, D., Maeder, D. L., Holley-Shanks, R., Chatard, J., Horlacher, R., Robb, F. T., Boos, W., and Weiss, R. B. 2000. Evidence of recent lateral gene transfer among hyperthermophilic REFERENCES archaea, Mol. Microbiol. 38, 684–693. Edgell, D. R., and Doolittle, W. F. 1997. Archaea and the origin(s) of Albers, S. V., Van de Vossenberg, J. L., Driessen, A. J., and Konings, DNA replication proteins, Cell 89, 995–998. W. N. 2001. Bioenergetics and solute uptake under extreme Faguy, D. M., and Doolittle, W. F. 1999. Lessons from the Aeropyrum conditions, 5, 285–294. pernix genome, Curr. Biol. 9, R883–R886. Amann, G., Stetter, K. O., Llobet-Brossa, E., Amann, R., and Anton, Faguy, D. M., and Doolittle, W. F. 2000. Horizontal transfer of J. 2000. Direct proof for the presence and expression of two 5% –peroxidase genes between archaea and pathogenic bacter- different 16S rRNA genes in individual cells of Haloarcula ia, Trends Genet. 16, 196–197. marismortui, Extremophiles 4, 373–376. Felsenstein, J. 1978. Cases in which parsimony or compatibi- Aravind, L., and Koonin, E. V. 1999. DNA-binding proteins and lity methods will be positively misleading, Syst. Zool. 27, evolution of transcription regulation in the archaea, Nucleic Acids 401–410. Res. 27, 4658–4670. Fileee,! J., Forterre, P., and Laurent, J. 2002. Evolution of Aravind, L., Tatusov, R. L., Wolf, Y. I., Walker, D. R., and Koonin, DNA polymerase families: Evidence for multiple gene exchange E. V. 1998. Evidence for massive gene exchange between archaeal between cellular and viral proteins, J. Mol. Evol., and bacterial hyperthermophiles, Trends Genet. 14, 442–444. in press. Barns, S. M., Delwiche, C. F., Palmer, J. D., and Pace, N. R. 1996. Fitz-Gibbon, S. T., and House, C. H. 1999. Whole genome-based Perspectives on archaeal diversity, thermophily and monophyly phylogenetic analysis of free-living , Nucleic Acids from environmental rRNA sequences, Proc. Natl. Acad. Sci. USA Res. 27, 4218–4222. 93, 9188–9193. Forterre, P. 1997. Archaea: What can we learn from their sequences? Beja, O., Spudich, E. N., Spudich, J. L., Leclerc, M., and DeLong, E. Curr. Opin. Genet. Dev. 7, 764–770. F. 2001. phototrophy in the , Nature 411, Forterre, P., 1999. Displacement of cellular proteins by functional 786–789. analogues from plasmids or viruses could explain puzzling Bell, S. D., and Jackson, S. P. 2001. Mechanism and regulation of phylogenies of many DNA informational proteins, Mol. Microbiol. transcription in archaea, Curr. Opin. Microbiol. 4, 208–213. 33, 457–465. 420 Forterre, Brochier and Philippe

Forterre, P. 2002. A hot story from comparative genomic: Reverse sulphatereducing archaeon Archaeoglobus fulgidus, Nature 390, gyrase as the only protein specific for hyperthermophiles, Trends 364–370. Genet. 18, 236–238. Koolman, J. M., and Doolittle, R. F. 2000. Determining the relative Forterre, P., Bouthier De La Tour, C., Philippe, H., and Duguet, M. rate of changes for prokaryotic and eukaryotic proteins with 2000. Reverse gyrase from hyperthermophiles: Probable transfer of anciently duplicated paralogs, J. Mol. Evol. 51, 173–181. a thermoadaptation trait from archaea to bacteria, Trends Genet. Koonin, E. V., Mushegian, A. R., Galperin, M. Y., and Walker, D. R. 16, 152–154. 1997. Comparison of archaeal and bacterial genomes: Computer Forterre, P., and Philippe, H. 1999. Where is the root of the universal analysis of protein sequences predicts novel functions and tree of life? BioEssays 21, 871–879. suggests a chimeric origin for the archaea, Mol. Microbiol. 25, Franzmann, P. D., Liu, Y., Balkwill, D. L., Aldrich, H. C., Conway de 619–637. Macario, E., and Boone, D. R. 1997. frigidum sp. Lake, J. A. 1988. Origin of the eukaryotic nucleus determined by rate- nov., a psychrophilic, H2-using methanogen from Ace Lake, invariant analysis of rRNA sequences, Nature 331, 184–186. Antarctica, Int. J. Syst. Bacteriol. 47, 1068–1072. Lecompte, O., Ripp, R., Puzos-Barbe, V., Duprat, S., Heilig, R., Galtier, N., Tourasse, N., and Gouy, M. 1999. A nonhyperthermo- Dietrich, J., Thierry, J. C., and Poch, O. 2001. Genome evolution philic common ancestor to extant life forms, Sciences 283, 220–221. at the genus level: Comparison of three complete genomes of Glansdorff, N. 2000. About the last common ancestor, the universal hyperthermophilic archaea, Genome Res. 11, 981–993. life-tree and lateral gene transfer: A reappraisal, Mol. Microbiol. Leipe, D. D., Aravind, L., and Koonin, E. V. 1999. Did DNA 38, 177–185. replication evolve twice independently? Nucleic Acids Res. 27, Gribaldo, S., Lumia, V., Creti, R., de Macario, E. C., Sanangelantoni, 3389–3401. A., and Cammarano, P. 1999. Discontinuous occurrence of the Lopez, P., Philippe, H., Myllykallio, H., and Forterre, P. 1999. (dnaK) gene among Archaea and sequence features of Identification of putative chromosomal origins of replication in HSP70 suggest a novel outlook on phylogenies inferred from this Archaea, Mol. Microbiol. 32, 883–886. protein, J. Bacteriol. 181, 434–443. Lopez-Garcia, P., and Forterre, P. 1999. Control of DNA topology Gribaldo, S. and Phillipe, H. 2002. [insert title], Theor. Pop. Biol. during thermal stress in hyperthermophilic archaea: DNA Gupta, R. S. 1998. What are archaebacteria: life’s third domain or topoisomerase levels, activities and induced thermotolerance monoderm prokaryotes related to Gram-positive bacteria? A new during heat and cold shock in sulfolobus, Mol. Microbiol. 33, proposal for the classification of prokaryotic organisms, Mol. 766–777. Microbiol. 229, 695–708. Lopez-Garcia, P., and Moreira, D. 1999. Metabolic at the Huber, H., Hohn, M. J., Rachel, R., Fuchs, T., Wimmer, V. C. and origin of eukaryotes, Trends Biochem. Sci. 24, 88–93. Stetter, K. O. 2002. A new phylum of Archaea represented by a Lopez-Garcia, P., Moreira, D., Lopez-Lopez, A., and Rodriguez- nanosized hyperthermophilic symbiont, Nature 417, 63–67. Valera, F. 2001. A novel haloarchaeal-related is Huber, R., Huber, H., and Stetter, K. O. 2000. Towards the of widely distributed in deep oceanic regions, Environ. Microbiol. 3, hyperthermophiles: Biotopes, new isolation strategies and novel 72–78. metabolic properties, FEMS Microbiol. Rev. 24, 615–623. Maeder, D. L., Weiss, R. B., Dunn, D. M., Cherry, J. L., Gonzalez, J. Huynen, M. A., and Bork, P. 1998. Measuring genome evolution, M., DiRuggiero, J., and Robb, F. T. 1999. Divergence of the Proc. Natl. Acad. Sci. USA 95, 5849–5856. hyperthermophilic archaea Pyrococcus furiosus and P. horikoshii Huynen, M., Snel, B., and Bork, P. 1999. Lateral gene transfer, inferred from complete genomic sequences, 152, genome surveys, and the phylogeny of prokaryotes, Science 1299–1305. 286, 1443. Makarova, K. S., Aravind, L., Galperin, M. Y., Grishin, N. V., Jain, R., Rivera, M. C., and Lake, J. A. 1999. Horizontal gene transfer Tatusov, R. L., Wolf, Y. I., and Koonin, E. V. 1999. Comparative among genomes: The complexity hypothesis, Proc. Natl. Acad. Sci. genomics of the Archaea (Euryarchaeota): Evolution of conserved USA 96, 3801–3806. protein families, the stable core, and the variable shell, Genome Res. Kandler, O., and Konig, H. 1998. Cell wall polymers in Archaea 9, 608–628. (Archaebacteria), Cell Mol. Life Sci. 54, 305–308. Makino, S., and Suzuki, M. 2001. Bacterial genomic reorganization Karner, M. B., DeLong, E. F., and Karl, D. M. 2001. Archaeal upon DNA replication, Science 292, 803. in the mesopelagic zone of the Pacific Ocean, Nature Marguet, E., and Forterre, P. 1994. DNA stability at temperatures 409, 507–510. typical for hyperthermophiles, Nucleic Acids Res. 22, 1681–1686. Kates, M. 1993. Membrane lipids of Archaea, in ‘‘The Massana, R., DeLong, E. F., and Pedros-Alio, C. 2000. A few of Archaea (Archaebacteria)’’, (M. Kates, D. J. Kushnen, and cosmopolitan phylotypes dominate planktonic archaeal assem- A. T. Matheson, Eds.), p. 261–295, Elsevier, Amsterdam. blages in widely different oceanic provinces, Appl. Environ. Kennedy, S. P., Ng, W. V., Salzberg, S. L., Hood, L., and DasSarma, Microbiol. 66, 1777–1787. S. 2001. Understanding the adaptation of Halobacterium Mathrani, I. M., Boone, D. R., Mah, R. A., Fox, G. E., and Lau, P. P. species NRC-1to its extreme environment through computa- 1988. zhilinae sp. nov., an alkaliphilic, tional analysis of its genome sequence, Genome. Res. 11, halophilic, methylotrophic methanogen, Int. J. Syst. Bacteriol. 1641–1650. 38, 139–142. Klenk, H. P., Clayton, R. A., Tomb, J. F. White, O., Nelson, K. E., Matsunaga, F., Forterre, P., Ishino, Y., and Myllykallio, H. 2001. In Ketchum, K. A., Dodson, R. J., Gwinn, M., Hickey, E. K., vivo interactions of archaeal Cdc6/Orcl and minichromosome Peterson, J. D., Richardson, D. L., Kerlavage, A. R., Graham, D. maintenance proteins with the replication origin, Proc. Natl. Acad. E., Kyrpides, N. C., Fleischmann, R. D., Quackenbush, J., Lee, N. Sci. USA 98, 11,152–11,157. H., Sutton, G. G., Gill, S., Kirkness, E. F., Dougherty, B. A., Matte-Tailliez, O., Brochier, C., Forterre, P., and Philippe, H. 2002. McKenney, K., Adams, M. D., Loftus, B., Venter, J. C., et al. Archaeal phylogeny based on ribosomal proteins, Mol. Biol. Evol. 1997. The complete genome sequence of the hyperthermophilic, 19, 631–639. Evolution of the Archaea 421

Myllykallio, H., and Forterre, P. 2000. Mapping of a chromosome She, Q., Singh, R. K., Confalonieri, F., Zivanovic, Y., Allard, G., replication origin in an archaeon: Response, Trends Microbiol. 8, Awayez, M. J., Chan-Weiher, C. C., Clausen, I. G., Curtis, B. A., 537–539. De Moors, A., Erauso, G., Fletcher, C.,Gordon, P. M., Heikamp- Myllykallio, H., Lopez, P., Lopez-Garcia, P., Heilig, R., Saurin, W., de Jong, I., Jeffries, A. C., Kozera, C. J., Medina, N., Peng, Zivanovic, Y., Philippe, H., and Forterre, P. 2000. Bacterial mode X., Thi-Ngoc, H. P., Redder, P., Schenk, M. E., Theriault, C., of replication with eukaryotic-like machinery in a hyperthermo- Tolstrup, N., Charlebois, R. L., Doolittle, W. F., Duguet, M., philic archaeon, Science 288, 2212–2215. Gaasterland, T., Garrett, R. A., Ragan, M. A., Sensen, C. W., Mylvaganam, S., and Dennis, P. P. 1992. Sequence heterogeneity and Van der Oost, J. 2001. The complete genome of the between the two genes encoding 16S rRNA from the crenarchaeon Sulfolobus solfataricus P2, Proc. Natl. Acad. Sci. halophilic archaebacterium Haloarcula marismortui, Genetics 130, USA 98, 7835–7840. 399–410. Slesarev, A. I., Mezhevaya, K. V., Makarova, K. S., Polushin, N. N., Natale, D. A., Shankavaram, U. T., Galperin, M. Y., Wolf, Y. I., Shcherbinina, O. V., Shakhova, V. V., Belova, G. I., Aravind, L., Aravind, L., and Koonin, E. V. 2000. Towards understanding the Natale, D. A., Rogozin, I. B., Tatusov, R. L., Wolf, Y. I., first genome sequence of a crenarchaeon by genome annotation Stetter, K. O., Malykh, A. G., Koonin, E. V., and Kozyavkin, S. A. using clusters of orthologous groups of proteins (COGs), Genome 2002. The complete genome of the hyperthermophile Methanopyrus Biol. 1, RESEARCH0009. kandleri AVI9 and monophyly of archaeal methanogens, Proc. Nelson, K. E., Clayton, R. A., Gill, S. R., Gwinn, M. L., Dodson, R. Natl. Acad. Sci. USA 99, 4644–4649. J., Haft, D. H., Hickey, E. K., Peterson, J. D., Nelson, W. C., Snel, B., Bork, P., and Huynen, M. A. 1999. Genome phylogeny based Ketchum, K. A., McDonald, L., Utterback, T. R., Malek, J. A., on gene content, Nat. Genet. 21, 108–110. Linher, K. D., Garrett, M. M., Stewart, A. M., Cotton, M. D., Takai, K., Komatsu, T., Inagaki, F., and Horikoshi, K. 2001a. Pratt, M. S., Phillips, C. A., Richardson, D., Heidelberg, J., Sutton, Distribution of archaea in a black smoker chimney structure, Appl. G. G., Fleischmann, R. D., Eisen, J. A., Fraser, C. M., et al. 1999. Environ. Microbiol. 67, 3618–3629. Evidence for lateral gene transfer between Archaea and bacteria Takai, K., Moser, D. P., Onstott, T. C., DeFlaun, M., and from genome sequence of maritima, Nature 399, Fredrickson, J. K. 2001b. Archaeal diversity in waters from deep 323–329. South African mines. Appl. Environ. Microbiol. 67, 5750–5760. Nesbo, C. L., L’Haridon, S., Stetter, K. O., and Doolittle, W. F. 2001. Tamura, K., and Nei, M. 1993. Estimation of the number of Phylogenetic analyses of two ‘‘archaeal’’ genes in thermotoga substitutions in the control region of mito- maritima reveal multiple transfers between archaea and bacteria, chondrial DNA in humans and chimpanzees, Mol. Biol. Evol. 10, Mol. Biol. Evol. 18, 362–375. 512–526. Ollivier, B., Fardeau, M. L., Cayol, J. L., Magot, M., Patel, B. K., Tang, S. L., Nuttall, S., Ngui, K., Fischer, C., Lopez, P., and Dyall- Prensier, G., and Garcia, J. L. 1998. halotolerans Smith, M. 2002. HF2: A dsDNA tailed haloarchaeal virus with a gen. nov., sp. nov., isolated from an oil-producing well, Int. J. Syst. mosaic genome, Mol. Microbiol. 44, 283–296. Bacteriol. 48 (Part 3), 821–828. Tatusov, R. L., Natale, D. A., Garkavtsev, I. V., Tatusova, T. A., Olsen, G. J., and Woese, C. R. 1997. Archaeal genomics: An overview, Shankavaram, U. T., Rao, B. S., Kiryutin, B., Galperin, M. Y,, Cell 89, 991–994. Fedorova, N. D., and Koonin, E. V. 2001. The COG database: Orphan, V. J., House, C. H., Hinrichs, K. U., McKeegan, K. D., and New developments in phylogenetic classification of proteins from DeLong, E. F. 2001. Methane-consuming archaea revealed by complete genomes, Nucleic Acids Res. 9, 22–28. directly coupled isotopic and phylogenetic analysis, Science 293, Tekaia, F., Lazcano, A., and Dujon, B. 1999. The genomic tree 484–487. as revealed from whole comparisons, Genome Res. 9, Penny, D., and Poole, A. 1999. The nature of the last universal 550–557. common ancestor, Curr. Opin. Genet. Dev. 9, 672–677. Tillier, E. R., and Collins, R. A. 2000. Genome rearrangement by Philippe, H., and Laurent, J. 1998. How good are deep phylogenetic replication-directed translocation, Nat. Genet. 26, 195–197. trees? Curr. Opin. Genet. Dev. 8, 616–623. Tourasse, N. J., and Gouy, M. 1999. Accounting for evolutionary rate Poole, A., Jeffares, D., and Penny, D. 1999. Early evolution: variation among sequence sites consistently changes universal Prokaryotes, the new kids on the block, Bioessays 21, 880–889. phylogenies deduced from rRNA and protein-coding genes, Mol. Prangishvili, D., Stedman, K., and Zillig, W. 2001. Viruses of the Phylogenet. Evol. 13, 159–168. extremely thermophilic archaeon Sulfolobus, Trends Microbiol. 9, Wachtershauser, G. 1990. Evolution of the first metabolic cycles, Proc. 39–43. Natl. Acad. Sci. USA 87, 200–204. Rivera, M. C., and Lake, J. A. 1992. Evidence that eukaryotes and Woese, C. R. 1987. Bacterial evolution, Microbiol. Rev. 51, eocyte prokaryotes are immediate relatives, Science 257, 74–76. 221–271. Rothschild, L. J., and Mancinelli, R. L. 2001. Life in extreme Woese, C. R. 2000. Interpreting the universal phylogenetic tree, Proc. environments, Nature 409, 1092–1101. Natl. Acad. Sci. USA 97, 8392–8396. Ruepp, A., Graml, W., Santos-Martinez, M. L., Koretke, K. K., Woese, C. R., and Fox, G. E. 1977. Phylogenetic structure of the Volker, C., Mewes, H. W., Frishman, D., Stocker, S., Lupas, A. prokaryotic domain: The primary kingdoms, Proc. Natl. Acad. Sci. N., and Baumeister, W. 2000. The genome sequence of the USA 74, 5088–5090. thermoacidophilic scavenger , Nature Woese, C. R., Kandler, O., and Wheelis, M. L. 1990. Towards a 407, 508–513. natural system of organisms: Proposal for the domains Schouten, S., Hopmans, E. C., Pancost, R. D., and Damste, J. S. 2000. Archaea, Bacteria, and Eucarya, Proc. Natl. Acad. Sci. USA 87, From the cover: Widespread occurrence of structurally diverse 4576–4579. tetraether membrane lipids: Evidence for the ubiquitous presence Woese, C. R., Olsen, G. J., Ibba, M., and Sooll,. D. 2000. Aminoacyl- of low-temperature relatives of hyperthermophiles, Proc. Natl. tRNA synthetases, the , and the evolutionary process, Acad. Sci. USA 97, 14,421–14,426. Microbiol. Mol. Biol. Rev. 64, 202–236. 422 Forterre, Brochier and Philippe

Wolf, Y. I., Aravind, L., Grishin, N. V., and Koonin, E. V. 1999. Zillig, W. 1991. Comparative biochemistry of Archaea and Bacteria, Evolution of amino-acyl tRNA synthetases}analysis of unique Curr. Opin. Genet. Dev. 1, 544–551. domain architectures and phylogenetic trees reveals a complex Zivanovic, Y., Lopez, P., Phillipe, H., and Forterre, P. 2002. history of horizontal gene transfer events, Genome Res. 9, 689–710. Pyrococcus genome comparison evidences chromosome suffling- Wolf, Y. I., Rogozin, I. B., Grishin, N. V., Tatusov, R. L., and driven evolution, Nucleic Acids Res. 30, 1902–1910. Koonin, E. V. 2001. Genome trees constructed using five Zivanovic, Y., Myllykallio, H., and Forterre, P. 2001. Bacterial different approaches suggest new major bacterial , BMC genomic reorganization upon DNA replication, response, Science Evol. Biol. 1, 8. 292, 803.