*Institut de Génétique et Microbiologie, Université Paris-Sud, Orsay, France;
Phylogénie, Bioinformatique et Génome, Université Pierre et Marie Curie, Paris, France
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Abstract |
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Introduction |
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The study of Archaea is essential to understand the history of molecular mechanisms and metabolism diversity on our planet as well as to unravel the mechanisms by which life can prosper in extreme environments. In order to fully benefit from such studies, a sound phylogeny of the archaeal domain should be available. The phylogeny of Archaea currently used and adopted in textbooks is based on 16S rRNA sequence comparison. From this rRNA-based phylogeny, the archaeal domain has been divided into two phyla, the Euryarchaeota and the Crenarchaeota. The Euryarchaeota include all described halophilic and methanogenic species as well as thermoacidophiles and hyperthermophiles, whereas cultivated species of the Crenarchaeota include only thermoacidophiles and hyperthermophiles. In addition, many phylotypes corresponding to likely yet uncultured mesophilic (or even psychrophilic) species have been detected for both phyla (Pace 1997
). rRNA sequence comparison has also shown a specific relationship between halophiles and Methanomicrobiales, suggesting that halophiles evolved from methanogens by the loss of methanogenesis and the acquisition of an aerobic lifestyle.
The division of Archaea into two phyla, inferred from rRNA sequences, is also supported by genomic analyses (She et al. 2001
). For example, all Crenarchaeota lack eukaryotic-like histones, DNA polymerases of the D family, and cell division proteins of the MinD and FtsZ families, all generally present in Euryarchaeota (Bernander 2000
). Other relationships suggested by rRNA are not firmly established. In particular, Thermoplasmatales (moderate thermophiles and acidophiles) and Archaeoglobales (sulfate reducers) are located within methanogens (with the Thermococcales emerging first), but the relationships between these subgroups are not resolved (Ludwig and Klenk 2001
). On the contrary, it has been observed that the structure of Thermoplasmatales RNA polymerase (B type) is similar to that of Crenarchaeota and Thermococcales, and distinct from that of methanogens (B' + B'' type) (Klenk et al. 1992
).
It has recently been shown that rRNA phylogenies can be sometimes grossly misleading in inferring phylogenies in the presence of unequal rates of evolution or differences in base composition (Philippe and Laurent 1998
). For example, several early-branching lineages in the eukaryotic 18S rRNA tree turned out to be misplaced because of the long-branch attraction (LBA) artifact (Philippe, Germot, and Moreira 2000
). This raises concerns about the reliability of the archaeal tree based on 16S rRNA, all the more so that this domain contains many extremophiles, which can bias the assessment of rRNA sequence evolution. For example, rRNA sequences of hyperthermophilic species are G + C rich, a well-known source of tree reconstruction artifacts (Woese et al. 1991
; Lockhart et al. 1994
), and those of halophiles display very long branches, which can produce LBA artifacts (Felsenstein 1978
).
The recent discovery of the very high occurrence of lateral gene transfers (LGTs) in prokaryotes (Lan and Reeves 1996
; Ochman, Lawrence, and Groisman 2000
) raises a different, but nonetheless major, problem. It has been suggested that a prokaryotic phylogeny itself did not exist because prokaryotic genomes are a complete mosaic of genes from various origins (Doolittle 1999
). In fact, many archaeal phylogenies are based on single protein trees (Klenk, Palm, and Zillig 1994
; Brown and Doolittle 1997
; Philippe and Forterre 1999
; Woese et al. 2000
). Although most of them validate the Euryarchaeota/Crenarchaeota phyla division, they are often in contradiction both with each other and with the rRNA tree concerning the position of the various lineages within each phylum. LGTs could provide a simple explanation of these incongruencies. Yet, it has been proposed that a core of genes (especially the ones involved in numerous protein-protein interactions, the complexity hypothesis) may be refractory to transfer and could thus provide the raw material necessary to infer organismal phylogeny (Jain, Rivera, and Lake 1999
). However, this hypothesis was recently weakened by the in vitro demonstration that in Escherichia coli the rRNA operon can be successfully replaced by that of a distantly related species (Asai et al. 1999
) and by the numerous cases of LGTs involving the ribosomal protein rps14 in Bacteria (Brochier, Philippe, and Moreira 2000
).
To infer the archaeal phylogeny (if it exists), one needs to be able to demonstrate that a set of genes (the core) has not been laterally transferred during the evolutionary history of this group. Unfortunately, the standard methods used to detect LGTs (e.g., bias in G + C content, in codon usage, or in oligonucleotide frequencies) are designed for recent events only, and they have also recently been shown to provide quite different results (Ragan 2001
). We developed a method based on a phylogenetic criterion to detect LGTs (Brochier et al. in press). When applied to a sample of 57 genes from 45 bacterial species, this method revealed that only 13 genes are affected by LGTs. The phylogeny based on the remaining 44 genes was congruent with the phylogeny based on rRNA (16S and 23S). This strongly suggested that a core of nontransferred genes exists in Bacteria and that, subsequently, a bacterial phylogeny can be inferred.
Here, we constructed a phylogeny of the archaeal domain based on a concatenated data set of all the ribosomal proteins present in most archaeal species. This multiprotein approach was possible thanks to the many archaeal genome projects recently completed (notably those of Thermoplasmatales and Methanomicrobiales, both of uncertain phylogenetic position). The phylogeny of the concatenated ribosomal proteins was in agreement with the rRNA tree. We actually identified a few cases of probable LGT involving archaeal ribosomal proteins. Interestingly, LGTs appear to be biased in favor of transfer between species living in the same environment.
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Materials and Methods |
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As previously reported, we noticed that most archaeal ribosomal proteins were more similar to their eukaryotic homologs than to their bacterial counterparts; several proteins in our data set were not present in Bacteria, some being even absent in Eukarya. Alignment between ribosomal proteins of different domains (even between Archaea and Eukarya) turned out to be difficult, preventing a meaningful use of bacterial/eukaryal ribosomal proteins to root the archaeal tree or to test the monophyly of Archaea. Therefore we did not include any outgroup in order to reduce the noise and increase the number of alignable positions. The trees were rooted between Crenarchaeota and Euryarchaeota, their monophilies being undisputed (Ludwig and Klenk 2001
).
The remaining 53 proteins were concatenated into a large fusion, P1 (7,175 positions). Protein fusions were also constructed and analyzed for the eight proteins for which our principal components analysis (PCA) (see later) indicated likely cases of LGT (fusion P3, 926 positions) and for the 45 proteins remaining when these 8 were excluded (fusion P2, 6,249 positions). A fusion of the 16S and 23S rRNA sequences (fusion R, 3,933 positions) for the 14 archaeal species was analyzed in a similar way.
Phylogenetic Analyses
For all individual and fusion alignments, neighbor-joining, maximum parsimony, and maximum likelihood (ML) analyses were carried out with all individual and concatenated data sets using MUST (Philippe 1993
), PAUP 3.1 (Swofford 1993
), and MOLPHY 2.3 (Adachi and Hasegawa 1996
), respectively. Calculation of
-parameter values and other ML analyses, taking into account among-site rate variation (ASRV), were conducted using the program PUZZLE (Strimmer and von Haeseler 1996
). ML bootstrap proportions were computed using the RELL method (Kishino, Miyata, and Hasegawa 1990
) upon 2,000 top-ranking trees. For distance and parsimony analyses, 1,000 bootstrap replicates were computed. All individual and concatenated alignments and the corresponding phylogenetic trees are available at our web site (http://sorex.snv.jussieu.fr/archaea/rp.html).
Principal Components Analysis
To avoid the limitations of standard pairwise statistical comparisons of congruence between tree topologies (such as the Kishino-Hasegawa test [Kishino and Hasegawa 1990
], see Goldman, Anderson, and Rodrigo 2000
), we carried out a simultaneous comparison of all the tree topologies obtained from the individual analyses and multigene fusions using a PCA approach (Brochier et al. in press). For this, tree topologies were obtained from the individual analyses of the 49 ribosomal proteins that included all the 14 archaeal species. These 49 topologies were chosen to represent the tree space (for a detailed discussion see Brochier et al. in press). The likelihood of each data set (both individual and concatenated) was computed for each of the 49 topologies using the programs MOLPHY 2.3 (Adachi and Hasegawa 1996
) or PUZZLE 4.0 (Strimmer and von Haeseler 1996
). Finally, each protein or rRNA was described by the 49 increases of likelihood values with respect to the best tree (measured as the number of standard deviations), which were analyzed by PCA using the program SAS (SAS 1999
). The location of each individual or fusion alignment on a bidimensional diagram (the first two axes of the PCA) allowed studying its congruence on the remaining data sets. Two points (i.e., alignments) that were close in the diagram indicated that the two corresponding genes are congruent (i.e., they similarly supported the various topologies).
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Results |
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Discussion |
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In both ribosomal protein and rRNA trees (fig. 1 ), the branches leading to hyperthermophilic species were systematically shorter than those leading to mesophilic species (if the trees were rooted between Euryarchaeota and Crenarchaeota), indicating that the rates of evolution of rRNA and ribosomal proteins in hyperthermophiles have been slower than in their mesophilic counterparts. The difference between the length of the branches leading to hyperthermoplic and mesophilic species was slightly less pronounced in the ribosomal protein tree than in the rRNA tree. A slower evolutionary rate (i.e., the systematically short branches of hyperthermophilic lineages in the rRNA tree) could be explained by the structural constraints related to their high G + C content and the requirement to stabilize rRNA secondary and tertiary structures at high temperatures. The observation of a similar phenomenon in the ribosomal protein tree could also be explained by structural constraints related to protein thermostability.
It has been previously suggested that the common ancestor of all Archaea was a hyperthermophile, based on the basal position of hyperthermophilic archaea in the rRNA tree (Achenbach-Richter et al. 1988
). Another argument in favor of a hyperthermophilic archaeal ancestor is the similarity between the archaeal rRNA phylogeny and the phylogeny of reverse gyrase, a protein specific to hyperthermophiles (Forterre et al. 2000
). If this is the case, both rRNA and ribosomal proteins from hyperthermophilic archaea would have retained more ancestral characters than their mesophilic or moderately thermophilic counterparts. Moreover, if nonhyperthermophilic species evolved from hyperthermophilic ancestors, they would have adapted to a new environment (often an extreme one, i.e., halophilic or acidophilic), and it is therefore expected that their genes underwent an accelerated evolutionary rate. The LBA artifact probably did not highly bias our cleaned tree (fig. 4A
) because the two longest branches (Thermoplasmatales and Halobacteriales) did not group together but clustered with the slowly evolving species (Archaeoglobus and Methanosarcina, respectively). Yet, these variable evolutionary rates provided serious noise in our alignment, which could explain the low BS in our cleaned tree despite the use of
6,000 orthologous positions. On the contrary, in the rRNA tree (fig. 1B
) the longest branches (Thermoplasmatales, Halobacteriales, and to a lesser extent Methanosarcina) strongly clustered together (BS of 99%), suggesting LBA.
In addition, the archaeal species used in this study live in extreme environments, which could strongly constrain their evolutionary pattern. For example, it is well known that hyperthermophilic species share high G + C in their rRNA sequences (Galtier and Lobry 1997
) and can artifactually cluster together in the corresponding phylogenies (Woese et al. 1991
; Embley, Thomas, and Wlliams 1992
). In the rRNA tree (fig. 1B
), all the species with low G + C content (below 56%, Methanosarcina, Haloarcula, Halobacterium, Thermoplasma, and Ferroplasma) were grouped with a very high statistical support (BS of 99%). This grouping was likely not only the result of an LBA artifact but also of a compositional artifact. For the ribosomal proteins, amino acid compositional biases surely exist because it is obvious for the proteome (Kreil and Ouzounis 2001
), but contrary to the nucleotide bias of rRNA, they are probably not convergent in halophilic and acidophilic species. Indeed, halophilic species have a K+-rich intracellular environment, and their proteins (especially the surface) are rich in aspartic and glutamic acids with an average pI of 5.1 (Ng et al. 2000
). In Thermoplasma the intracellular pH is more acidic, and its proteins have a higher pI (Kawashima et al. 2000
). As a result, from a compositional point of view, Thermoplasmales and Halobacteriales will tend to be repulsed, which could counteract the attraction created by their convergent high evolutionary rate. The compositional bias thus explained why Thermoplasmatales grouped strongly with Methanosarcina/Halobacteriales in the rRNA tree (fig. 1B
) and weakly with Archaeoglobus in the cleaned tree (fig. 4A
), whereas the LBA artifact would simply predict the grouping of Thermoplasmatales and Halobacteriales.
Our ribosomal phylogeny, even when cleared of LGT problems, should only be considered as an approximation of the species tree, not only because of a potential bias caused by ribosome coevolution but also because several additional biases (rate, amino acid composition, or covarion structure) are not well handled by the available tree reconstruction methods. Moreover, given the several weak bootstrap values (42%, 51%, and 86%) in our cleaned tree (fig. 4A
), a complete resolution of the archaeal phylogeny would also require many more positions (i.e., genes) than were used here (7,000). Nevertheless, the topologies of the euryarchaeal rRNA and ribosomal protein trees implied that the ability to perform methanogenesis appeared early on in Euryarchaea and was lost several times independently because methanogens were never retrieved as a coherent group.
Rare Genomic Event as Phylogenetic Marker
The position of Thermoplasmatales in the rRNA tree was previously disputed on the ground that (1) the RNA polymerase of T. acidophilum is of the ABC type, as is the case for the RNA polymerases of Crenarchaeota and Thermococcales, whereas the RNA polymerases of all methanogens, Archaeoglobus, and Halobacteriales are of the AB'B''C type; and (2) T. acidophilum branches before methanogens in an RNA polymerase phylogeny based on nucleotide sequenced comparison (Klenk, Palm, and Zillig 1994
). However, in the present analysis (figs. 1 and 4
) we found that Thermoplasmatales branch after Methanococcus and Methanobacterium in the euryarchaeal part of the tree in both rRNA and ribosomal protein phylogenies. Furthermore, we obtained the same result when we constructed a phylogenetic tree of the available amino acid sequences of all archaeal RNA polymerase B subunits (fig. 5
). This tree also turned out to be identical to the global ribosomal protein tree (fig. 1A
). Our topology was only slightly different from the one found by Klenk, Palm, and Zillig (1994)
, with the monophyly of Thermoplasma/Halobacterium instead of their paraphyly. This discrepancy likely resulted from the use of a different species sampling (6 only by Klenk et al. 1992
and 16 in fig. 5
) and perhaps also by a different tree reconstruction method (ML on nucleotides vs. ML on amino acids).
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Relative Importance of Phylogenetic or Environmental Distance in LGT Frequencies
During our BLAST searches and preliminary phylogenetic analyses, we failed to detect indication for LGT of ribosomal proteins between Archaea and either Bacteria or Eucarya. It has been suggested that rpl23 of Helicobacter pylori was acquired from Archaea (Hansmann and Martin 2000
). However, an analysis with an extensive species sampling (28 Eucarya, 13 Archaea, and 94 Bacteria) supported the clustering of Helicobacter and the other Bacteria by a weak bootstrap value but also by a very conserved insertion of 13 amino acids specific to Bacteria (data not shown). The previous observation was likely the result of a combination of stochastic effect (less than 70 homologous positions and only 18 species) and LBA artifact (Helicobacter evolving very fast). Similarly, although LGTs can be frequent within Bacteria (Brochier, Philippe, and Moreira 2000
), we failed to detect LGTs between Bacteria and Archaea/Eucarya (Brochier et al. in press). This suggested that the ribosomes of the three domains have sufficiently diverged from each other to prevent the successful interdomain replacement of a ribosomal protein. This is in agreement with the hypothesis that informational proteins are resistant to long-range LGT (Jain, Rivera, and Lake 1999
; Graham et al. 2000
).
According to our PCA approach, we found that 15% of the 53 ribosomal proteins have undergone at least one LGT event during the evolution of Archaea. Interestingly, the phylogeny inferred from the concatenation of the eight LGT proteins (fig. 4B
) was not so different from the cleaned phylogeny (fig. 4A
). This suggested that LGTs were rare for these eight proteins and that they just contributed random phylogenetic noise (i.e., there was no major bias in the direction of the transfer, but see later). The scarcity of LGTs was confirmed by the fact that the monophyly of closely related species (Pyrococcus, Halobacteriales, and Thermoplasmatales) was always recovered, except in four cases, because the time elapsed since the common ancestors of the three groups is too short to have a high probability to be observed. An alternative explanation would be that LGTs of ribosomal proteins occurred only between organisms that are phylogenetically close (Woese 2000
), which could explain why a phylogenetic structure persists in the sequences even if LGTs are frequent.
However, the two major differences between the dirty (fig. 4B
) and the cleaned (fig. 4A
) trees suggested a quite different and probably more plausible explanation. The early emergence of Thermoplasmatales (fig. 4B
) could be explained by an attraction of their branches by the crenarchaeal branches, because of specific LGT between Thermoplasmatales and Sulfolobales. This hypothesis was supported by the phylogenies of rpl12e proteins, where a robust relationship between Thermoplasmatales and Crenarchaeota could be observed (fig. 3
). Indeed, Baumeister and coworkers (Ruepp et al. 2000
) observed that the genome of T. acidophilum contains many genes which are more closely related to Sulfolobus than to the euryarchaeal relatives of Thermoplasmatales, a fact easily explained by the evidence that Sulfolobus and Thermoplasma thrive in the same type of acidic and hot environment. This indicated that the ribosomes had not sufficiently diverged in the two archaeal phyla to prevent protein exchange between them. Indeed, the analyses of complete genomes have already suggested the highest frequency of LGTs between organisms thriving in the same environment: Aquifex and thermophilic Archaea (Aravind et al. 1998
), Thermotoga and thermophilic Archaea (Nelson et al. 1999
), chloroplast, mitochondrion, and nucleus (Marienfeld, Unseld, and Brennicke 1999
; Gallois et al. 2001
), Chlamydia and Rickettsia (Wolf, Aravind, and Koonin 1999
), Sinorhizobium and Streptomyces (B. Golding, personal communication), and Thermoplasma and Sulfolobus (Ruepp et al. 2000
). For ribosomal proteins, LGTs were rare and appeared to be very difficult, if even impossible, between phylogenetically very distant organisms (i.e., between the three domains) and to be mainly directed by the physical proximity of the organisms rather than by their phylogenetic proximity.
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Acknowledgements |
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Footnotes |
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1 These authors contributed equally to the work.
Keywords: Archaea
lateral gene transfer
molecular phylogeny
multigene analysis
ribosomal proteins
Address for correspondence and reprints: Hervé Philippe, Phylogénie, Bioinformatique et Génome, UMR 7622 CNRS, Université Pierre et Marie Curie, 9, quai St Bernard, 75005 Paris, France. herve.philippe{at}snv.jussieu.fr
.
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