Archaeal phylogeny based on proteins of the transcription and translation machineries: tackling the Methanopyrus kandleri paradox

Abstract

Background: Phylogenetic analysis of the Archaea has been mainly established by 16S rRNA sequence comparison. With the accumulation of completely sequenced genomes, it is now possible to test alternative approaches by using large sequence datasets. We analyzed archaeal phylogeny using two concatenated datasets consisting of 14 proteins involved in transcription and 53 ribosomal proteins (3,275 and 6,377 positions, respectively).

Results: Important relationships were confirmed, notably the dichotomy of the archaeal domain as represented by the Crenarchaeota and Euryarchaeota, the sister grouping of Sulfolobales and Aeropyrum pernix, and the monophyly of a large group comprising Thermoplasmatales, Archaeoglobus fulgidus, Methanosarcinales and Halobacteriales, with the latter two orders forming a robust cluster. The main difference concerned the position of Methanopyrus kandleri, which grouped with Methanococcales and Methanobacteriales in the translation tree, whereas it emerged at the base of the euryarchaeotes in the transcription tree. The incongruent placement of M. kandleri is likely to be the result of a reconstruction artifact due to the high evolutionary rates displayed by the components of its transcription apparatus.

Conclusions: We show that two informational systems, transcription and translation, provide a largely congruent signal for archaeal phylogeny. In particular, our analyses support the appearance of methanogenesis after the divergence of the Thermococcales and a late emergence of aerobic respiration from within methanogenic ancestors. We discuss the possible link between the evolutionary acceleration of the transcription machinery in M. kandleri and several unique features of this archaeon, in particular the absence of the elongation transcription factor TFS.

Figure 1

Unrooted neighbor-joining phylogenetic tree of the RNA polymerase subunit H computed from a Γ-corrected matrix of distances. Numbers close to nodes are bootstrap proportions. The scale bar represents the number of changes per position per unit branch length. For each taxon, the portion of the alignment from positions 57 to 83 is displayed. For clarity, identical amino acids shared by the current taxa and the first taxon (Aeropyrum pernix) are indicated by dashes, whereas stars correspond to missing amino acids.

Figure 2

Unrooted maximum likelihood (ML) phylogenetic trees obtained from the transcription and translation datasets. (a) Transcription; (b) translation. The best tree and the branch lengths were calculated using the program PUZZLE with a Γ-law correction. Numbers at the nodes are ML bootstrap supports computed with the RELL method using the MOLPHY program without correction for among-site variation. The scale bars represent the number of changes per position per unit branch length.

Figure 3

Unrooted neighbor-joining phylogenetic tree of the RNA polymerase subunits A' and A" computed from a Γ-corrected matrix of distances. (a) Polymerase A'; (b) polymerase A". Numbers close to nodes are bootstrap proportions. The scale bars represent the number of changes per position per unit branch length.

Figure 4

Comparison between the percentage of differences observed in the transcription and ribosomal datasets for each couple of taxa. The x-axis represents the percentage of amino-acid differences observed between two taxa for the concatenated transcription dataset. The y-axis represents the percentage of amino-acid differences observed between two taxa for the concatenated ribosomal dataset. Circles show for each pair of taxa the comparison between the observed percentage of differences for the concatenated transcription and ribosomal datasets. The majority of circles are localized close to the diagonal indicating a strong correlation (R = 0.88) between the differences observed into the two concatenated datasets. White circles represent the comparisons of Methanopyrus kandleri with other taxa.

Figure 5

Unrooted neighbor-joining phylogenetic tree of the RNA polymerase subunit B computed from a Γ-corrected distance matrix. Numbers close to nodes are bootstrap proportions. The scale bar represents the number of changes per position for a unit branch length. In Methanococcus maripaludis, Methanocaldococcus jannaschii, Methanopyrus kandleri, Methanothermobacter thermoautotrophicus, Archaeoglobus fulgidus, Thermoplasmatales, Methanosarcinales and Halobacteriales genomes, the gene for the RNA polymerase subunit B is split in two parts: B' and B". The black and white boxes correspond to the B' and B" parts of the gene, respectively. S and F represent the split and fusion event hypotheses of the B' and B" parts of the gene.

Figure 6

An example of an indel being flanked by divergent regions in Methanopyrus kandleri. The portion of the alignment corresponds to positions 1,281 to 1,340 in our RNA polymerase subunit A' dataset. For clarity, identical amino acids shared by each taxon and the first taxon (Sulfolobus tokodaii) are indicated by dashes, whereas stars correspond to missing amino acids.