Download Evolution of the Archaea

Theoretical Population Biology 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 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 domain of life, are bacterial-looking prokaryotes 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
Euryarchaeota and the Crenarchaeota. Methanogenesis was the main invention that occurred in the
euryarchaeal phylum and is now shared by several archaeal groups. Adaptation to aerobic conditions
occurred several times 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 evolution. & 2002 Elsevier Science (USA)
Eubacteria). In the following decades, this discovery
prompted a flood of new hypotheses about the nature of
the Last Universal Cellular Ancestor (LUCA) and the
phylogenetic relationships between the three domains of
life (Archaea, Bacteria and Eukarya) (for recent reviews
and alternative viewpoints, see Gupta, 1998; Forterre
and Philippe, 1999; Lopez-Garcia and Moreira, 1999;
Penny and Poole, 1999; Glansdorff, 2000; Woese, 2000;
Cavalier-Smith, 2002; Gribaldo and Philippe, 2002, this
issue).
The evolution of Archaea per se is an important field
of evolutionary biology. Since Archaea exhibit a wide
variety of phenotypic and genotypic characters, it would
be interesting to have a clear idea of the history of the
archaeal domain, in order to understand the origin and
evolution of these characters. In this review, we will try
to sum up the state of the art regarding archaeal
evolution. This is timely, as data from comparative
1. INTRODUCTION
The discovery, by Woese and colleagues in the 1970s,
that three ribosome forms are present in living organisms initiated a revolution in evolutionary biology
(Woese and Fox, 1977; Woese, 1987; Woese et al.,
1990). This tripartite division of the translation apparatus had been previously obscured by early observation
of ribosome structure that fitted well with the binary
classification of organisms into eukaryotes (80S ribosomes) and prokaryotes (70S ribosomes). However,
when comparative sequence analysis of the ribosome
components became available, it turned out that ribosomal RNAs (rRNA) and ribosomal proteins of some
prokaryotes (the Archaea, formerly Archaebacteria)
were drastically different from those of both eukaryotes
and those of ‘‘classical’’ bacteria (the Bacteria, formerly
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Forterre, Brochier and Philippe
genomics can now be combined with more traditional
phylogenetic and taxonomic approaches. At the time of
writing this review, 12 genomes of Archaea have been
completely sequenced and are available in public
databases (http://www.ncbi.nlm.nih.gov/PMGifs/Genomes/a g.html). Furthermore, an up-to-date description
of all identified archaeal species 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; LopezGarcia et al., 2001; Takai et al., 2001a, b).
2. BRIEF DESCRIPTION OF THE
DOMAIN ARCHAEA
The Archaea are prokaryotes (cell 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 hyperthermophiles (Fig. 1). This could reflect the absence of a
rigid cell wall in most Archaea (see below) and/or novel
(still unknown) mechanisms for morphogenesis. Archaea exhibit a wide diversity of phenotypes, as is the
case for Bacteria. The first three phenotypes to be
recognized were the methanogens (strict anaerobes and
methane producers), the halophiles (strict aerobes living
in high-salt environments) and the thermoacidophiles
(aerobes living in hot and acidic environments) (Woese
and Fox, 1977). Organisms with such disparate phenotypes were first unified based on the similarities of their
rRNA sequences, and later on also by the unique
structure of their membrane phospholipids (see below).
Many additional phenotypes were discovered among
Archaea in the following decades, such as hyperthermophilic or psychrophilic methanogens, halophilic and/or
alkaliphilic methanogens, anaerobic, alkaliphilic and
neutrophilic hyperthermophiles (Mathrani et al., 1988;
Franzmann et al., 1997; Ollivier et al., 1998; Huber et al.,
2000). Finally, the explosion of environmental studies
based on PCR amplification of 16S rRNA has revealed
the widespread occurrence in water and soils of
mesophilic Archaea with otherwise unknown phenotypes (Fig. 2). For example, a recent study has
estimated that mesophilic Archaea of the phylum
FIG. 1. (A) Electron micrograph of the euryarchaeon Haloarcula
(formerly ‘‘square bacteria’’), from Dr. Rodriguez-Valera, (B) electron
micrograph of the crenarchaeon Pyrodictium abyssi (a hyperthermophile that can grow up to 1108C), the cells are inserted into a
reticulated network whose function is still unknown and (C)
transmission electron micrograph of P. abyssi. EM pictures of P.
abyssi are from Reinhard Rachel and Karl Stetter.
Crenarchaeota account for nearly 20% of the total
marine picoplankton oceanic biomass worldwide
(Karner et al., 2001). Many of these not yet cultivated
Archaea probably exhibit novel phenotypes. For
instance, previously unsuspected archaeal methanotrophs were predicted recently from geomicrobiological
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 phylogenetic tree
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.
This is indeed true for high-temperature environments,
since only Archaea can thrive at temperatures above
958C (and up to 1138C) (Huber et al., 2000). However,
in all other situations (high salt, low or high pH, low
temperature, high pressure), Bacteria are found together
with Archaea and Eukarya (Rothschild and Mancinelli,
2001).
412
The metabolic diversity of Archaea is also reminiscent
of Bacteria. Apart from methanogenesis (presently
unknown in Bacteria) all metabolic pathways discovered
in Archaea also exist among Bacteria. They can be either
heterotrophs or autotrophs (chemio- or photo-lithoautotroph) and use a large variety of electron donors and
acceptors (Huber et al., 2000). Photosynthesis based on
chlorophyll has not been found in Archaea, whereas
photosynthesis based on bacteriorhodopsin, once believed unique to halophilic Archaea, has been recently
detected in planktonic Bacteria as well (Beja et al.,
2001). Spore formers or organisms with complex cell
cycle and multicellular stages are unknown among
Archaea, but this could be simply due to our incomplete
sampling of this domain. The only way to discriminate
between Archaea and Bacteria is thus by looking at the
molecular level.
Beside their specific rRNA, Archaea can be distinguished from Bacteria by the nature of their membrane
glycerolipids that are ethers of glycerol and isoprenol,
whereas bacterial and eukaryal lipids are esters of
glycerol and fatty acids (Kates, 1993). Archaeal
glycerolipids are also ‘‘reverse lipids’’, since the enantiomeric configuration of their glycerophosphate
backbone is the mirror image of the configuration
found in bacteria and eukaryal lipids. Another difference between Archaea and Bacteria is the absence of
murein in Archaea, whereas this compound is present in
the cell wall of most Bacteria. Archaea exhibit a great
diversity of cell envelopes (Kandler and Konig, 1998),
most Archaea have a simple S-layer of glycoproteins
covering the cytoplasmic membrane, whereas a few of
them (Thermoplasmatales) only have a cytoplasmic
membrane containing glycoproteins. Some Archaea
have a rigid cell wall based either on heteropolysaccharides (Halococcus) or pseudomurein (Methanobacteriales), the latter being Gram positive. The difference
between Archaea and Bacteria at the molecular level is
exemplified by the resistance of Archaea to most
antibiotics active on Bacteria. Early studies on the
molecular biology of Archaea have shown that this
resistance was due indeed to critical differences in the
antibiotic targets (e.g., RNA polymerase or ribosomal
proteins) (for an early review on archaeal molecular
biology, see Zillig, 1991).
The coherence of Archaea at the molecular level is
now also well documented by comparative genomics
(Olsen and Woese, 1997; Forterre, 1997; Forterre
and Philippe, 1999; Fitz-Gibbon and House, 1999;
Makarova et al., 1999; Snel et al., 1999; Tekaia et al.,
1999; Wolf et al., 2001). In all archaeal genomes
sequenced so far, most encoded proteins give first hits
Forterre, Brochier and Philippe
with other archaeal proteins when their homologues are
searched in public databases. This is especially true for
informational proteins (those involved in DNA replication, transcription and translation) that are usually
present in most archaeal genomes and are nearly always
more similar between one archaeon and another than
between one archaeon and any bacterium or eukaryote.
These archaeal informational proteins are also usually
much more similar to those of Eukarya than to those of
Bacteria.
In addition, archaeal genomes encode many informational proteins that have homologues in Eukarya but
not in Bacteria. This is especially striking in the case of
DNA replication, since archaeal genomes encode
homologues of nearly all eukaryal DNA replication
proteins but only one homologue of a bacterial DNA
replication protein (Edgell and Doolittle, 1997; Forterre,
1999; Leipe et al., 1999). The eukaryotic-like putative
replication proteins identified in archaeal genomes are
most likely involved in actual archaeal DNA replication,
as indicated by recent observation such as direct
interaction in vivo between the chromosomal origin
(oriC) and the eukaryotic-like initiator protein Cdc6
(Matsunaga et al., 2001) and the similar size of Okazaki
fragments in Archaea and Eukarya (Matsunaga and
Myllykallio, pers. comm.).
It is often considered that informational proteins
constitute the ‘‘core’’ of the genome of any organism,
because they are less subject to lateral gene transfer
(LGT), and are therefore more representative of the
actual history of the organisms (Jain et al., 1999).
Indeed, except for well-documented LGT between
Archaea and Bacteria in the case of amino-acyl tRNA
synthetases (Wolf et al., 1999; Woese et al., 2000), few
LGTs of informational proteins have been identified
between the two prokaryotic domains. For example, an
exhaustive study has shown that no LGT had occurred
between Archaea and Bacteria in the case of ribosomal
proteins (Brochier et al., 2002) even if LGTs were
discovered within Bacteria (Brochier et al., 2000, 2002)
and Archaea (Matte-Tailliez et al., 2002).
The close similarity between eukaryal and archaeal
informational proteins can be explained by two hypotheses: either Archaea and Eukarya are sister groups, and
the ‘‘eukaryotic’’ characters of Archaea are synapomorphies, or these characters are primitive (already present
in the LUCA, thus symplesiomorphies) and divergent in
Bacteria. We will not discuss this problem here (for a
review see Forterre and Philippe, 1999; Poole et al.,
1999; Woese, 2000; Cavalier-Smith, 2002; Gribaldo and
Philippe, this issue) since we will focus on the evolution
of the archaeal domain per se.
Evolution of the Archaea
Interestingly, in contrast to informational proteins,
most operational proteins of Archaea are ‘‘bacteriallike’’. This category includes enzymes of the primary
and secondary metabolisms, membrane receptors,
transporters and so on, but also some cell division
proteins (Koonin et al., 1997; Jain et al., 1999). This is
often interpreted as testifying for extensive LGT of
operational proteins between the two prokaryotic
domains (Faguy and Doolittle, 1999; Makarova et al.,
1999). However, although LGTs between hyperthermophilic Bacteria and Archaea have been well documented
by phylogenetic and/or genome context analyses (Gribaldo et al., 1999; Forterre et al., 2000; Nesbo et al.,
2001), a supertree inferred only on operational proteins
is very similar to the one inferred from informational
proteins (Daubin and Gouy, 2001), suggesting that
LGTs are not so frequent for operational genes. More
analyses are thus required to test the hypothesis that the
similarity between Archaea and Bacteria for operational
genes is only due to LGTs. Alternative hypotheses that
have been proposed to explain this similarity are the
fusion of ancient bacterial and eukaryotic lineages to
produce extant Archaea (Koonin et al., 1997) or the
monophyly of Archaea and Bacteria, if the universal
tree of life is rooted in the eukaryotic branch (Forterre
and Philippe, 1999).
3. GENOME EVOLUTION IN ARCHAEA
Comparative genomics suggests that the mechanisms
of genome evolution in Archaea are quite similar to
those identified in Bacteria. This can be explained by the
resemblance between the genome organizations in the
two domains. For instance, despite eukaryotic-like
replication proteins, hyperthermophilic Archaea of the
genus Pyrococcus replicate their chromosome at high
speed, bi-directionally and using a single replication
origin, as in Bacteria (Lopez et al., 1999; Myllykallio
et al., 2000; Matsunaga et al., 2001). Most highly
transcribed genes are transcribed co-directionally with
DNA replication, as in Bacteria, probably to avoid
frequent head-to-head collision between the replication
and transcription apparatuses (Zivanovic et al., 2002).
Shine–Dalgarno sequences are found in some Archaea
as in Bacteria, and archaeal genes are often organized
in operon. Finally, mechanisms of gene regulation in
Archaea involve bacterial-like regulator proteins
(Aravind and Koonin, 1999; Bell and Jackson, 2001).
Except for closely related organisms, archaeal and
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bacterial genomes exhibit no synteny and very little
conservation of gene order, in agreement with rapid
genomic evolution by recombination (Huynen and
Bork, 1998). Comparison of the two closely related
Archaea Pyrococcus abyssi and Pyrococcus horikoshi has
shown that the terminus of DNA replication is a hot
spot of recombination, as in the case of Bacteria
(Myllykallio et al., 2000). Furthermore, the main
rearrangement between the two Pyrococcus genomes
has occurred symmetrically to the axis formed by the
origin and the terminus of replication (Makino and
Suzuki, 2001; Zivanovic et al., 2002). This characteristic
feature has been also observed in Bacteria, suggesting
that major recombination events occurred between bidirectional replication forks (Tillier and Collins, 2000).
These similarities in the mechanisms of genome evolution of the two prokaryotic domains could reflect a
common structural organization of the replication
apparatus (for example, association of the two replication forks into a single replication factory) and of the
chromosome segregation machinery (in relation with the
presence in Archaea of homologues of the bacterial
proteins Xer C/D), which are involved in the resolution
of recombinant chromosomes at the end of replication,
and of the bacterial proteins MinD and FtsZ, which are
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
of Archaea in this respect remains to be explored.
For instance, two possible (instead of one) replication origins have been predicted in silico in
Halobacterium (Kennedy et al., 2001) and the bacterial
cell division proteins FtsZ and MinD are lacking in
all Crenarchaeota.
In addition to chromosomal rearrangements linked to
DNA replication, recombination events have been
associated to IS elements in several archaeal genomes
(Kennedy et al., 2001; Bru. gger et al., 2002). IS elements
are especially abundant in S. solfataricus and Halobacterium NRC1. Comparison of the three completely
sequenced Pyrococcus genomes suggested that a family
of IS elements, only present in P. furiosus, has been
involved in most chromosomal rearrangements observed in the latter species (Maeder et al., 1999;
Lecompte et al., 2001). In Pyrococcus and Sulfolobus,
chromosomal rearrangements linked to IS elements
occur preferentially in the limit of one replichore (the
half chromosome comprised between the origin and
terminus of replication), suggesting a principle of
genome organization that is not yet understood
(Zivanovic et al., 2001, 2002; Bru. gger et al., 2002).
414
An important difference of the genome organization
between the two prokaryotic domains is that all Bacteria
contain a gyrase and a negatively supercoiled genome,
whereas most Archaea have no gyrase and relaxed or
positively supercoiled genome (Charbonnier and Forterre, 1994). Some Euryarchaeota, including the hyperthermophile Archaeoglobus fulgidus, have acquired
bacterial gyrases by LGT and have negatively supercoiled genomes (Lopez-Garcia and Forterre, 1999). It is
not known presently if differences in genome topology
have an effect on the mechanisms of genome evolution.
LGTs between different archaeal species, and also
between Bacteria and Archaea, have been involved as a
major mechanism of genome evolution in Archaea.
LGTs appear to be predominant between organisms
living in similar environment. This has been shown both
by genome wide comparison (Aravind et al., 1998;
Nelson et al., 1999; Ruepp et al., 2000) and in the case
of some ribosomal proteins inside the archaeal
domain (Matte-Tailliez et al., 2002). For example, many
LGTs have been detected between the thermoacidophilic Archaea Thermoplasma and Sulfolobus that
are otherwise phylogenetically very distant (Ruepp
et al., 2000).
IS elements are likely often involved in these LGTs.
For instance, a 16 kb DNA fragment flanked by two IS
has been transferred between Thermococcus littoralis
and Pyrococcus furiosus (Diruggiero et al., 2000). IS
elements could have also played a critical role in LGT
between Bacteria and Archaea since many of the IS
detected in Archaea belong to families previously
detected in Bacteria (Bru. gger et al., 2002). The precise
mechanism of LGT between the two prokaryotic
domains remains mysterious. In particular, transformation by naked DNA appears highly unlikely
in the case of hyperthermophiles considering the
high instability of DNA fragments at high temperature (Marguet and Forterre, 1994). LGT could
possibly involve transfection by viruses, especially
if one considers that operational proteins similar
between Bacteria and Archaea include some outer
membrane proteins (e.g., sugar transporters) known
to be potential viral receptors. One can thus imagine
that bacteriophages sometimes interact with archaeal
homologues of their usual bacterial receptors, and
then inject by mistake their DNA into archaeal cells
(and vice versa). Such rare events could readily
lead to LGT if the injected DNA fragment contains
mobile IS elements that can function in both prokaryotic domains.
Viruses and plasmids seem to be as common in
Archaea as in Bacteria (Benbouzid-Rollet et al., 1997;
Forterre, Brochier and Philippe
Prangishvili et al., 2001). It has been shown that IS
elements present in Sulfolobus species have indeed
triggered active recombination between chromosomes,
plasmids and viruses (for review, see Bru. gger et al.,
2002), in agreement with the above hypothesis on the
role of viruses in LGT. The recent analysis of the
complete genome of the halobacteriophage HF2 is
especially relevant to the idea that viruses have been a
major vector for LGT between domains, since it
contains a mixture of archaeal, bacterial and bacteriophage-like genes (Tang et al., 2002). In particular, its
DNA polymerase seems more closely related to bacteriophage T4 DNA polymerase than to archaeal DNA
polymerases (Fil!ee et al., in press). Accordingly, LGTs
are probably not limited by environmental barriers since
mechanisms for genetic exchanges (e.g., virus or
transposable elements) should have evolved and adapted
themselves to various environments together with their
hosts.
4. ARCHAEAL PHYLOGENY, THE TWO
MAJOR PHYLA
Phylogenetic trees of the archaeal domain based on
16S rRNA have led to split this domain into two phyla
(according to Bergey’s Manual definition), the Euryarchaeota and the Crenarchaeota (Woese et al., 1990).
The Euryarchaeota have been named from the Greek
word euruB; meaning wide, because they encompass the
greatest phenotypic diversity among known cultivable
species, with the halophiles, the methanogens, some
thermoacidophiles and some hyperthermophiles.
In contrast, the phenotypic diversity of cultivable
Crenarchaeota is much more limited, with only
hyperthermophilic species. This phylum has thus been
named from the Greek word krZnZ meaning spring,
from the popular hypothesis that hyperthermophiles are
at the origin of all present-day organisms. This name has
been conserved, despite the detection by PCR in various
environments of many groups of mesophilic and
probably psychrophilic Crenoarchaeota that have not
yet been cultivated (Fig. 2).
Some data of comparative genomics support the
division of Archaea into two distinct phyla, since many
proteins present in all euryarchaeal genomes are missing
in Crenarchaeota and vice versa. In particular, several
striking differences have been noticed between the two
phyla for some key proteins involved in DNA replication, chromosome structure and cell division, such as the
Evolution of the Archaea
absence of eukaryal-like histones, eukaryal RPA-like
proteins and bacterial cell division proteins in all
Crenarchaea (Bernander, 2000; Myllykallio and Forterre, 2000). However, it remains to be known if these
differences are specific to cultivable hyperthermophilic
Crenarchaeota, or if they are a general characteristic of
this phylum. Furthermore, some global genomic analyses have failed to recover the division of Archaea into
two phyla. For example, using five different approaches
(e.g., gene content, gene order, concatenated ribosomal
proteins) on ten archaeal genomes, Wolf et al. (2001)
failed to recover the monophyly of the two phyla.
Nevertheless, their phylogeny based on gene content
is very likely biased by frequent LGTs between
Thermoplasmatales (Euryarchaeota) and Sulfolobales
(Crenarchaeota) (Ruepp et al., 2000). If Thermoplasmatales are not taken into account, the two phyla
are monophyletic, in agreement with a previous study
based on gene content (Huynen et al., 1999). Similarly,
the use of a much more refined phylogenetic method
(through maximum likelihood inference of individual
genes and supertree reconstruction), performed on 459
genes from seven Archaea, also recovered the monophyly of the two phyla (Daubin and Gouy, 2001; see
also Brown et al., 2001).
The lack of monophyly in the phylogeny based on
ribosomal proteins obtained by Wolf and coworkers is
more surprising (Wolf et al., 2001). We recently
performed a detailed analysis of 53 ribosomal proteins
present in most of 14 archaeal species (Matte-Tailliez
et al., 2002). We found that eight genes have likely
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undergone LGT events during archaeal evolution, with
a bias for LGTs between Thermoplasmatales and
Crenarchaeota, and were thus not suitable for inferring
species phylogeny. The phylogeny based on the remaining 45 genes was very similar to the rRNA phylogeny
and strongly supported the partitions between Crenarchaeota and Euryarchaeota. We have now carried
out the same analysis, but including the genomes of
Sulfolobus tokodai and of Thermoplasma volcanium that
were published after our initial work was completed,
and we obtained similar results (Fig. 3). It should be
noted that the Halobacteriales and the Thermoplasmatales display very long branches. Therefore, when a very
distant outgroup is used to root the archaeal phylogeny
(i.e., the Bacteria), the long-branch attraction artefact
(Felsenstein, 1978) is a major problem (Philippe and
Laurent, 1998). Accordingly, the long branches of
Halobacteriales and Thermoplasmatales likely emerge
early in ribosomal proteins’ phylogeny because they are
attracted by the bacterial branch, as previously suggested (Wolf et al., 2001).
In conclusion, the division of Archaea into Crenarchaeota and Euryarchaeota can be viewed as supported by
phylogenetic analyses, at least for cultivable species
(Fig. 2). Indeed, the analysis of archaeal sequences from
the environment has somehow complicated the picture
of the archaeal domain from the 16S rRNA viewpoint.
Although many of the new archaeal lineages that have
been detected by PCR analysis of environmental
samples branch among Crenarchaeota and Euryarchaeota, some of them branch in between. A tentative
FIG. 3. Phylogeny of the archaeal domain based on concatenated ribosomal protein amino acid 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
third phylum, the Korarchaeota (from the Greek word
koroB; meaning young man), was suggested (Barns et al.,
1996). Sequences that branch even deeper than Korarchaeota 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
identifies a huge group of environmental sequences that
cannot be attributed to either Euryarchaeota or
Crenarchaeota. The Korarchaeota and other uncultured
lineages form a clade with cultured Crenarchaeota, but
with low bootstrap support (below 50%). It is thus not
clear if the dichotomy of the archaeal domain will
survive future studies. More phyla will very likely have
to be defined in Archaea. This could eventually produce
an archaeal classification more similar to the bacterial
one (23 phyla are presently recognized in the Bacterial
domain, Boone and Castenholz, 2001). Nevertheless,
one has also to be careful in interpreting the diversity of
environmental sequences, since divergent copies of
rRNA can exist within a single organism (Mylvaganam
and Dennis, 1992; Amann et al., 2000).
For a long time, some authors have advocated the
paraphyly of Archaea, suggesting that Crenarchaeota
(called eocytes by Lake and colleagues) form a clade
with Eukarya (Lake, 1988), based for example on an
insertion in elongation factor 1a (Rivera and Lake,
1992). A phylogenetic analysis of rRNA taking amongsite rate variability into account supports this claim
(Tourasse and Gouy, 1999). It is reasonable to assume
that the monophyly of Archaea generally observed in
rRNA trees (Woese et al., 1990) is due to a long-branch
attraction artefact, because Bacteria and Eukarya display much longer branches than Archaea for rRNA.
The use of methods less sensitive to this artefact
(Tourasse and Gouy, 1999) provided a good evidence
in favour of the paraphyly of Archaea. However,
phylogenies based on genome content (Fitz-Gibbon
and House, 1999; Huynen et al., 1999) as well as on
multiple markers (Brown et al., 2001; Daubin and
Gouy, 2001) recovered the monophyly of Archaea. In
addition, recent analyses of two crenarchaeal genomes
(Aeropyrum pernix and Sulfolobus solfataricus) failed to
identify specific eukaryal-crenarchaeal proteins that
could support the hypothesis of paraphyly (Faguy and
Doolittle, 2000; Natale et al., 2000). On the contrary, the
Crenarchaea lack several eukaryal proteins of the
informational apparatus that are present in Euryarchaea
(such as histones or some DNA replication proteins,
Bernader, 2000; Myllykallio and Forterre, 2000). The
completion of several genomes from Crenarchaeota,
Korarchaeota and their relatives at the base of the 16S
Forterre, Brochier and Philippe
rRNA tree (Fig. 2), together with their analysis with the
refined method, will be critical to confirm or invalidate
the monophyly of Archaea.
5. STRUCTURE AND EVOLUTION OF
THE TWO ARCHAEAL PHYLA
The Euryarchaeota have been divided into nine
orders, five orders for the methanogens (Methanobacteriales, Methanomicrobiales, Methanococcales, Methanosarcinales and Methanopyrales), one for the
halophiles (Halobacteriales), one for the thermoacidophiles (Thermoplasmatales) and two for the hyperthermophiles (Thermococcales and Archaeoglobales)
(Fig. 2).
Phylogenetic trees based on 16S rRNA place the
Methanopyrales at the base of the euryarchaeal tree,
followed by Thermococcales, but with very weak
statistical support (the bootstrap supports for the four
basal nodes are between 4% and 8% in Fig. 2). Since
Methanopyrales are hyperthermophiles (the only species
of this order, Methanopyrus kandleri, can grow up to
1108C), this has suggested that ancestral Euryarchaeota
were both methanogens and hyperthermophiles. The
idea that methanogenesis (formation of methane from
H2 and CO2 ) is an ancestral phenotype was first
advocated to support the name ‘‘Archaebacteria’’ itself
(Woese and Fox, 1977). The discovery of a subterranean
community of methanogens thriving on H2 has recently
prompted speculation about the possibility that methanogens are directly connected to a hot origin of life on
Earth and possibly elsewhere (Chapelle et al., 2002). The
exact position of Methanopyrales in the euryarchaeal
tree is thus of critical importance.
The recent sequencing of the M. kandleri genome is
thus an important step in our understanding of archaeal
evolution (Slezarev et al., 2002). Phylogenetic analysis of
concatenated ribosomal proteins suggests that Methanopyrales do not branch first in the euryarchaeal tree
but branch with other thermophilic and hyperthermophilic methanogens (Slesarev et al., 2002). Furthermore,
our phylogenetic analysis of ribosomal proteins limited
to the archaeal domain (thus using more positions and
limiting the impact of long-branch attraction artefact)
locates Thermococcales firmly at the base of the
euryarchaeal tree (bootstrap support of 86%, MatteTailliez et al., 2002). This was confirmed by our new
analysis with two additional species (bootstrap support
of 89%, Fig. 3). The position of Thermococcales at the
417
Evolution of the Archaea
base of the euryarchaeal tree and the grouping of M.
kandleri with other methanogens thus suggest that
methanogenesis (a very complex metabolic pathway)
has originated in the euryarchaeal domain only after the
divergence between Thermococcales and other Euryarchaea. This would be in agreement with the absence
of relics of methanogenesis in the genomes of Thermococcales, whereas such relics have been found in
Archaeoglobus (Klenk et al., 1997; Slesarev et al., 2002).
Both rRNA and ribosomal protein based phylogenies
have suggested that Halobacteriales are a sister group to
Methanomicrobiales (Fig. 3). This grouping makes
sense since Methanomicrobiales are the only order of
methanogens that does not include thermophilic species,
and contains halophilic species. This suggests that
Halobacteriales originated from halophilic and mesophilic methanomicrobiales that have lost their ability to
produce methane and have acquired both oxygen
tolerance and respiratory enzyme complexes. Analysis
of the genes involved in aerobic respiration that can be
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
present in Halobacterium NRCl have no archaeal
counterpart, whereas in the others, they are more closely
related to their bacterial than to their archaeal homologues.
Both rRNA and ribosomal protein based phylogenies
also suggest the existence of a large clade grouping
Methanobacteriales, Thermoplasmatales, Archaeoglobales, Methanomicrobiales and Halobacteriales. However, phylogenies based on other genes or on gene
content failed to retrieve it (Brown et al., 2001; Daubin
and Gouy, 2001; Wolf et al., 2001). Furthermore, this
group is not recovered when sequences from uncultured
species are included in the 16s RNA tree (Fig. 2). The
analysis of additional genomes will thus be required to
sort out the phylogenetic relationships among these
different lineages.
The cultured Crenoarchaeota have been divided into
three orders according to 16S rRNA: the Thermoproteales, the Desulfurococcales and the Sulfolobales
(Fig. 2). The first two orders include only anaerobic
hyperthermophiles that live at neutral pH and include
the most hyperthermophilic organisms known today
(with maximal growth temperature up to 1138C),
whereas Sulfolobales, which live at low pH (2–3), can
be either aerobes or anaerobes and have lower
temperature maxima (up to 858C). Thermoproteales
are a sister group to Sulfolobales in 16S rRNA trees.
Genomic data cannot yet be used to test this phylogeny
since genomes from Desulfurococcales have not yet been
sequenced. As in the case of Euryarchaeota, oxygen
respiration is most likely a secondary adaptation in
Crenoarchaeota. However, we should be aware that
hyperthermophilic Crenoarchaeota that have been discovered in the last two decades represent only a small
fraction of this phylum. From examination of Fig. 2, it
is striking that most of the archaeal groups in both
Euryarchaeota and Crenarchaeota are in fact presently
uncultured. There is therefore much research to be
done both in classical microbiology and environmental genomics before a complete picture of the
archaeal domain structure and evolution can be
obtained. A recent development has been the discovery
of parasitic archaea of reduced size (Nanoarchaeum
equitans) and genome (less than 0:5 Mb) that live in
parasitic
association
with
hyperthermophilic
Crenoarchaeota of the genus Ignicoccus and branch
very deeply in the crenoarchaeotal 16S rRNA tree
(Huber et al., 2002).
6. NATURE OF THE ARCHAEAL
ANCESTOR
Phylogenetic and genomic analyses of cultivable
Archaea suggest that the ancestor of all present-day
Archaea was an anaerobe that probably lived when
oxygen was still absent from the terrestrial atmosphere.
Complete adaptation to an aerobic lifestyle is a
secondary adaptation in the archaeal domain that
occurred several times independently: at least once in
Crenarchaeota (Sulfolobales) and twice in Euryarchaeota (Halobacteriales and Thermoplasmatales). However,
several Crenarchaeota are also microaerobes (Aeropyrum pernix and Pyrobaculum aerophilum), so we cannot
exclude that the archaeal ancestor itself had some
oxygen tolerance. As previously noticed, this ancestor
was probably not a methanogen, at least if we consider
indeed that the rooting of the archaeal tree between
Thermococcales and Crenarchaeota (Fig. 3) is correct.
It is also often considered that the archaeal ancestor was
a chemiolithoautotroph, since chemiolithoautotrophic
thermophiles are present in both archaeal phyla. For
several authors, this is consistent with the theory of an
autotrophic origin of life (Wachtershauser, 1990).
However, since heterotrophic hyperthermophiles are
present in both archaeal phyla (e.g., Thermococcales
in Euryarchaeota and Pyrobaculum, Aeropyrum and
Desulfurococcus in Crenarchaeota), one cannot exclude
418
that the archaeal ancestor was a heterotroph. In fact,
considering the extent of LGTs in prokaryotes, it is
difficult to raise firm conclusions about the origin and
evolution of such metabolic pathways. Moreover, the
presence of many uncultivated lineages at strategic
points of the phylogeny renders inference of the
ancestral metabolism very hypothetical until their
metabolism will be characterized.
A fascinating aspect of the archaeal domain is its
connection with hyperthermophily. We have already
mentioned that only Archaea have apparently been able
to colonize biotopes with temperatures above 958C:
Possibly, this can be explained by the unique structure
of archaeal lipids that maintain the impermeability of
the cytoplasmic membrane to ions at such high
temperatures. When the membrane lipid layer becomes
unable to maintain an efficient barrier to passive ion
diffusion, the cell cannot build up the ion gradients that
are required to produce ATP. The membrane of
hyperthermophilic Archaea contains tetraether lipids
that can form a monolayer highly resistant to passive
ion transfer. This has been experimentally demonstrated
in vitro by the analysis of ion transport in reconstituted
vesicles formed with archaeal lipids. Hyperthermophilic
Bacteria also have unusual lipids that ‘‘try’’ to resemble
archaeal ones (tetraester or diether), but they have been
apparently unable to produce membrane that can
prevent ion leakage at temperatures above 958C (for a
recent review on the importance of lipids and membrane
permeability in thermoadaptation, see Albers et al.,
2001).
Interestingly, mesophilic and even some psychrophilic
Archaea also have tetraether lipids (Schouten et al.,
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
have thus predated (and anticipated) the appearance of
hyperthermophiles in the archaeal domain. Alternatively, these lipids might have appeared in a hyperthermophilic archaeal ancestor and their presence today in
mesophilic and psychrophilic Archaea can be viewed as
a heritage from their hyperthermophilic ancestor.
The later hypothesis is supported by the presence of
many hyperthermophic lineages that emerge at the base
of both the euryarchaeal and the crenarchaeal phyla (at
least for the cultivable species, the picture being much
more complex with uncultured species). Furthermore, in
both rRNA trees and ribosomal protein trees (Figs. 1
and 2), the hyperthermophilic Archaea have shorter
branches than their mesophilic counterparts, suggesting
that hyperthermophiles might have retained more
ancestral characters, since their macromolecules have
Forterre, Brochier and Philippe
evolved more slowly (Kollman and Doolittle, 2000;
Matte-Tailliez et al., 2002). The phylogeny of reverse
gyrase, a unique DNA topoisomerase that introduces
positive superturns in DNA, also argues for a
hyperthermophilic archaeal ancestor, since it is coherent
with the rRNA phylogeny (e.g., the separation of
Euryarchaeota and Crenarchaeota) (Forterre et al.,
2000).
Reverse gyrase is present in all hyperthermophiles
(both Archaea and Bacteria) and absent in all genomes
from mesophiles or moderate thermophiles. From
comparative genomics analysis performed using the
‘‘Phylogenetic Patterns Search Program’’ of the COG
database (Tatusov et al., 2001), extended to the genome
of Sulfolobus solfataricus (She et al., 2001), it even
turned out that reverse gyrase is the only protein that
exhibits this striking phylogenetic distribution (Forterre,
2002). Phylogenetic and genome context analyses have
indicated that reverse gyrase has been transferred from
Archaea to hyperthermophilic Bacteria by LGT (at least
twice independently), suggesting that the common
ancestor of all Bacteria was not a hyperthermophile
and that the hyperthermophilic phenotype originated in
Archaea (Forterre et al., 2000). This is consistent with
the idea that LUCA was not a hyperthermophile, a
viewpoint that is also supported by recent analysis
suggesting that the GC content of LUCA rRNA was too
low to be compatible with a hyperthermophilic lifestyle
(Galtier et al., 1999).
7. CONCLUSION AND PERSPECTIVE
The study of Archaea has confirmed the two initial
predictions by Woese and Fox (1977), i.e., that Archaea
will exhibit a phenotypic diversity at least comparable to
that of Bacteria and that Archaea will be characterized
by unique features at the molecular level. In addition,
Archaea turned out to exhibit a mosaic of features from
the two other domains that continue to stimulate
discussions among evolutionists. In the course of their
history, Archaea have in particular retained (or
acquired) in their informational apparatus many characters that they only share now with Eukarya. Despite
their differences in this respect, Archaea and Bacteria
have been engaged in a continuous ‘‘dialogue’’ via
LGTs, due to their similar prokaryotic lifestyles.
Whereas some Bacteria learned from Archaea how to
bypass the hyperthermophilic barrier (borrowing
reverse gyrase), some Archaea learned from Bacteria
Evolution of the Archaea
how to utilize oxygen to get energy surplus. We
have now, with some confidence, the idea of a
hyperthermophilic and anaerobic archaeal ancestor,
suggesting that the invention of reverse gyrase,
the acquisition of tetraether lipids and other features
of thermoadaptation have been critical for the emergence of Archaea. However, this view, as all others
concerning the origin and evolution of phenotypic
traits in Archaea, should still be taken with caution,
considering the limited number of archaeal lineages
for which cultivable species are available for phenotypic and phylogenomic analyses. In particular, it
should be extremely important now to get genotypic
and phenotypic information about all the archaeal
lineages that are presently only known from their
phylotypes, especially those branching in between
Euryarchaeota and Crenarchaeota.
ACKNOWLEDGMENTS
We thank Allan Campbell and Samuel Karlin for providing us with
the opportunity to write this review. Preliminary sequence data of
Ferroplasma and Methanosarcina were obtained from the DOE Joint
Genome Institute (JGI) at http://www.jgi.doe.gov/JGI microbial/
html/index.html. We are grateful to Karl O Stetter, Francisco
Rodriguez-Valera and Purification Lopez-Garcia for the EM pictures.
We acknowledge Simonetta Gribaldo and David Moreira for a careful
reading of the manuscript.
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