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

Brochier C, Forterre P, Gribaldo S - Genome Biol. (2004)

Bottom Line: 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.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.

View Article: PubMed Central - HTML - PubMed

Affiliation: Equipe Phylogénomique, Université Aix-Marseille I, Centre Saint-Charles, 13331 Marseille Cedex 3, France. celine.brochier@up.univ-mrs.fr

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.

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Related in: MedlinePlus

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.
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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.

Mentions: The trees resulting from the transcription and translation datasets (hereafter referred to as the 'transcription tree' and the 'translation tree') are shown in Figure 2a and 2b, respectively. The same topologies were recovered with the three methods used for phylogenetic reconstruction, but with little variation in bootstrap values (data not shown). The transcription and the translation trees presented interesting similarities, such as the Crenarchaeota/Euryarchaeota dichotomy (100% BP), the sister grouping of Sulfolobales and Aeropyrum pernix (84% and 100% BP) and the monophyly of a large group comprising Thermoplasmatales, Archaeoglobus fulgidus, Methanosarcinales and Halobacteriales (96% and 100% BP), with the latter two orders forming a well-sustained cluster (100% BP). However, the transcription tree strongly supported A. fulgidus as the sister group of the Methanosarcinales/Halobacteriales clade (100% BP), whereas in the translation tree A. fulgidus grouped, albeit with weak confidence (41% BP), with Thermoplasmatales. Moreover, the transcription tree recovered a robust monophyly (80% BP) of three methanogens (Methanothermobacter thermoautotrophicum, Methanocaldococcus jannaschii, and Methanococcus maripaludis), while in the translation tree these taxa were paraphyletic with a moderate support (BP 62%). The apparent incongruence between the two trees concerning the positions of A. fulgidus and of the three methanogens most probably reflects a lack of phylogenetic signal rather than LGT or long-branch attraction. Future analyses including more positions and a wider taxonomic sampling will help in resolving these nodes better. The two phylogenies differed remarkably concerning the base of the Euryarchaeota. The transcription tree showed M. kandleri as the first offshoot (100% BP) just before Thermococcales, whereas in the translation tree Thermococcales represented the most basal branch, with M. kandleri grouping paraphyletically with Methanococcales and Methanobacteriales (88% BP).


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

Brochier C, Forterre P, Gribaldo S - Genome Biol. (2004)

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.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC395767&req=5

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.
Mentions: The trees resulting from the transcription and translation datasets (hereafter referred to as the 'transcription tree' and the 'translation tree') are shown in Figure 2a and 2b, respectively. The same topologies were recovered with the three methods used for phylogenetic reconstruction, but with little variation in bootstrap values (data not shown). The transcription and the translation trees presented interesting similarities, such as the Crenarchaeota/Euryarchaeota dichotomy (100% BP), the sister grouping of Sulfolobales and Aeropyrum pernix (84% and 100% BP) and the monophyly of a large group comprising Thermoplasmatales, Archaeoglobus fulgidus, Methanosarcinales and Halobacteriales (96% and 100% BP), with the latter two orders forming a well-sustained cluster (100% BP). However, the transcription tree strongly supported A. fulgidus as the sister group of the Methanosarcinales/Halobacteriales clade (100% BP), whereas in the translation tree A. fulgidus grouped, albeit with weak confidence (41% BP), with Thermoplasmatales. Moreover, the transcription tree recovered a robust monophyly (80% BP) of three methanogens (Methanothermobacter thermoautotrophicum, Methanocaldococcus jannaschii, and Methanococcus maripaludis), while in the translation tree these taxa were paraphyletic with a moderate support (BP 62%). The apparent incongruence between the two trees concerning the positions of A. fulgidus and of the three methanogens most probably reflects a lack of phylogenetic signal rather than LGT or long-branch attraction. Future analyses including more positions and a wider taxonomic sampling will help in resolving these nodes better. The two phylogenies differed remarkably concerning the base of the Euryarchaeota. The transcription tree showed M. kandleri as the first offshoot (100% BP) just before Thermococcales, whereas in the translation tree Thermococcales represented the most basal branch, with M. kandleri grouping paraphyletically with Methanococcales and Methanobacteriales (88% BP).

Bottom Line: 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.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.

View Article: PubMed Central - HTML - PubMed

Affiliation: Equipe Phylogénomique, Université Aix-Marseille I, Centre Saint-Charles, 13331 Marseille Cedex 3, France. celine.brochier@up.univ-mrs.fr

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.

Show MeSH
Related in: MedlinePlus