Higher-level classification of the Archaea: evolution of methanogenesis and methanogens - PubMed (original) (raw)
Higher-level classification of the Archaea: evolution of methanogenesis and methanogens
Eric Bapteste et al. Archaea. 2005 May.
Abstract
We used a phylogenetic approach to analyze the evolution of methanogenesis and methanogens. We show that 23 vertically transmitted ribosomal proteins do not support the monophyly of methanogens, and propose instead that there are two distantly related groups of extant archaea that produce methane, which we have named Class I and Class II. Based on this finding, we subsequently investigated the uniqueness of the origin of methanogenesis by studying both the enzymes of methanogenesis and the proteins that synthesize its specific coenzymes. We conclude that hydrogenotrophic methanogenesis appeared only once during evolution. Genes involved in the seven central steps of the methanogenic reduction of carbon dioxide (CO(2)) are ubiquitous in methanogens and share a common history. This suggests that, although extant methanogens produce methane from various substrates (CO(2), formate, acetate, methylated C-1 compounds), these archaea have a core of conserved enzymes that have undergone little evolutionary change. Furthermore, this core of methanogenesis enzymes seems to originate (as a whole) from the last ancestor of all methanogens and does not appear to have been horizontally transmitted to other organisms or between members of Class I and Class II. The observation of a unique and ancestral form of methanogenesis suggests that it was preserved in two independent lineages, with some instances of specialization or added metabolic flexibility. It was likely lost in the Halobacteriales, Thermoplasmatales and Archaeoglobales. Given that fossil evidence for methanogenesis dates back 2.8 billion years, a unique origin of this process makes the methanogenic archaea a very ancient taxon.
Figures
Figure 1.
Pathways of methanogenesis: hydrogenotrophic (double-lined arrows), aceticlastic (solid arrows) and methylotrophic (broken gray arrows). The hydrogenotrophic pathway can operate from formate or H2/CO2, obtaining reducing potential from formate or H2, respectively. The aceticlastic pathway obtains electrons from the oxidation of CO produced by the splitting of acetate. The methylotrophic pathway can operate in two ways: (1) the methylated C-1 compound is a source for a methyl group as well as electrons (one molecule oxidized to CO2 provides electrons for three molecules to be reduced to methane, dotted green arrows); and (2) the methylated C-1 compound is reduced to methane using electrons from H2. The names of the proteins studied here are indicated on the pathway. For the synthesis of the cofactors,mptH plays a role in the biosynthesis of tetrahydrofolate of M. jannaschii, and_mptN_ is involved in the biosynthesis of methanopterin. Both tetrahydrofolate and methanopterin are intermediate C1 carriers in methanogenesis. The biosynthesis of the coenzyme F420 rests on the cof enzymes (cofC, cofD,cofE, cofG and_cofH_). The aks enzymes (aksA,aksD, aksE and_aksF_) participate in 2-oxoacid elongation steps of coenzyme B9 biosynthesis, which partners with coenzyme M in the final step of methanogenesis. This lastcoenzyme is the smallest known organic cofactor, but an essential terminal methyl carrier during methanogenesis and is produced by the com enzymes (comA, comB,comC, comD and_comE_) (Graham and White 2002).
Figure 2.
(A) Best maximum likelihood (ML) ribosomal tree obtained from fusion analyses of 53 markers and separate analyses of 23 markers. Two classes of methanogens are proposed. (B) Best ML tree based on the fusion analysis of seven orthologous proteins involved in the synthesis of cofactors (1432 positions). A non-methanogen sequence supposed to be a priori outside these two groups was also retained for the coenzyme data set: either_Archaeoglobus fulgidus_ or_Ralstonia_ solanacearum, if the former was not present. (C) Best ML tree, based on the fusion of nine orthologous proteins of the hydrogenotrophic methanogenesis (2382 positions). For A, B and C, only bootstrap values > 50% are indicated.
Figure A1.
Enzymes are listed along the hydrogenotrophic pathway. Enzymes supporting the monophyly of methanogens are in italics (BV >75%). Enzymes supporting the monophyly of both Class I and Class II are in bold. Enzymes present in methanogens only are underlined. Genes present in Class I only are indicated by an asterisk. Phylogeny supporting the monophyly of Class II only are indicated by a +. Genes without lateral gene transfers between Class I/ Class II are in quotes. Genes with duplication in methanogenes, leading to incongruent position of a species in the tree are denoted by a superscript 2. Sixteen genes out of 20 coding for the seven core enzymes of hydrogenotrophic methanogenesis (_cof_D,fwdA, hmdI, mtrA, mtrB, mtrC, mtrD, mtrE, _mtrF, mtr_G, mtrH, mcrA, mcrB, mcrC, mcrD and mcrG) are consistent with the monophyly of methanogens. In other words, proteins of methanogenesis themselves seem in contradiction with the reference tree based on ribosomal proteins. In fact, 13 of the 15 proteins consistent with the monophyly of methanogens are exclusively present in methanogens (an additional protein is exclusively found in Class I, see Table 1). Such a restricted taxonomical sampling obviously increases the number of markers with monophyletic methanogens, but does not really help to test this monophyly. A crude interpretation could be that methanogenesis is a plesiomorphic trait, ancestral to most of the euryarchaea. It would have been lost several times independently in the Thermoplasmatales, Archaeoglobales and Halobacteriales lineages.
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