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Phylogenomic data support a seventh order of Methylotrophic methanogens and provide insights into the evolution of Methanogenesis.

Borrel G, O'Toole PW, Harris HM, Peyret P, Brugère JF, Gribaldo S - Genome Biol Evol (2013)

Bottom Line: M. alvus" are obligate H₂-dependent methylotrophic methanogens.Genomic data also suggest that these methanogens may use a large panel of methylated compounds.Phylogenetic analysis including homologs retrieved from environmental samples indicates that methylotrophic methanogenesis (regardless of dependency on H₂) is not restricted to gut representatives but may be an ancestral characteristic of the whole order, and possibly also of ancient origin in the Euryarchaeota. 16S rRNA and McrA trees show that this new order of methanogens is very diverse and occupies environments highly relevant for methane production, therefore representing a key lineage to fully understand the diversity and evolution of methanogenesis.

View Article: PubMed Central - PubMed

Affiliation: EA-4678 CIDAM, Clermont Université, Université d'Auvergne, Clermont-Ferrand, France.

ABSTRACT
Increasing evidence from sequence data from various environments, including the human gut, suggests the existence of a previously unknown putative seventh order of methanogens. The first genomic data from members of this lineage, Methanomassiliicoccus luminyensis and "Candidatus Methanomethylophilus alvus," provide insights into its evolutionary history and metabolic features. Phylogenetic analysis of ribosomal proteins robustly indicates a monophyletic group independent of any previously known methanogenic order, which shares ancestry with the Marine Benthic Group D, the Marine Group II, the DHVE2 group, and the Thermoplasmatales. This phylogenetic position, along with the analysis of enzymes involved in core methanogenesis, strengthens a single ancient origin of methanogenesis in the Euryarchaeota and indicates further multiple independent losses of this metabolism in nonmethanogenic lineages than previously suggested. Genomic analysis revealed an unprecedented loss of the genes coding for the first six steps of methanogenesis from H₂/CO₂ and the oxidative part of methylotrophic methanogenesis, consistent with the fact that M. luminyensis and "Ca. M. alvus" are obligate H₂-dependent methylotrophic methanogens. Genomic data also suggest that these methanogens may use a large panel of methylated compounds. Phylogenetic analysis including homologs retrieved from environmental samples indicates that methylotrophic methanogenesis (regardless of dependency on H₂) is not restricted to gut representatives but may be an ancestral characteristic of the whole order, and possibly also of ancient origin in the Euryarchaeota. 16S rRNA and McrA trees show that this new order of methanogens is very diverse and occupies environments highly relevant for methane production, therefore representing a key lineage to fully understand the diversity and evolution of methanogenesis.

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Phylogenetic position of the Mx order and inferred losses of methanogenesis. (a) Bayesian phylogeny of Euryarchaeota based on a concatenation of 57 ribosomal proteins comprising 7,472 amino acid positions. Values at nodes represent Bayesian posterior probabilities and bootstrap values based on maximum likelihood analysis and 100 resamplings of the original data set. For clarity, only the values corresponding to the monophyly of orders and their evolutionary relationships are shown. “../” symbols indicate that the corresponding node was not recovered in the maximum likelihood phylogeny. The scale bar represents the average number of substitutions per site. For details on analyses, see Materials and Methods. Red crosses indicate complete loss of methanogenesis. Colored spots indicate presence of the genes of the respective methanogenic pathways/reactions as indicated by the colored boxes in figure 1. Crosses within spots indicate that the enzymes are present but not used to perform methanogenesis from H2/CO2 and/or from methylated compounds. Genomes with a green spot harbor the genes needed to use at least one type of methyl compound. (b) Maximum likelihood phylogeny of methanogens based on a concatenation of McrA-B-C-D-G protein sequences comprising 1,159 amino acid positions. Values at nodes represent bootstrap proportions calculated based on 100 resamplings of the original alignment and Bayesian posterior probabilities. For clarity, only the values corresponding to the monophyly of orders and their evolutionary relationships are shown. The scale bar represents the average number of substitutions per site. For details on analyses, see Materials and Methods.
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evt128-F2: Phylogenetic position of the Mx order and inferred losses of methanogenesis. (a) Bayesian phylogeny of Euryarchaeota based on a concatenation of 57 ribosomal proteins comprising 7,472 amino acid positions. Values at nodes represent Bayesian posterior probabilities and bootstrap values based on maximum likelihood analysis and 100 resamplings of the original data set. For clarity, only the values corresponding to the monophyly of orders and their evolutionary relationships are shown. “../” symbols indicate that the corresponding node was not recovered in the maximum likelihood phylogeny. The scale bar represents the average number of substitutions per site. For details on analyses, see Materials and Methods. Red crosses indicate complete loss of methanogenesis. Colored spots indicate presence of the genes of the respective methanogenic pathways/reactions as indicated by the colored boxes in figure 1. Crosses within spots indicate that the enzymes are present but not used to perform methanogenesis from H2/CO2 and/or from methylated compounds. Genomes with a green spot harbor the genes needed to use at least one type of methyl compound. (b) Maximum likelihood phylogeny of methanogens based on a concatenation of McrA-B-C-D-G protein sequences comprising 1,159 amino acid positions. Values at nodes represent bootstrap proportions calculated based on 100 resamplings of the original alignment and Bayesian posterior probabilities. For clarity, only the values corresponding to the monophyly of orders and their evolutionary relationships are shown. The scale bar represents the average number of substitutions per site. For details on analyses, see Materials and Methods.

Mentions: Analysis of a concatenation of ribosomal proteins from 84 euryarchaeal genomes and comprising 7,472 amino acid positions robustly shows that M. luminyensis and “Ca. M. alvus” represent a monophyletic lineage that is not phylogenetically associated with any of the previously known orders of methanogens or the anaerobic methanotrophic ANME1 lineage (fig. 2a). Interestingly, the Mx order, albeit evolutionarily close to Thermoplasmatales as previously noted, robustly clusters with two lineages without cultured representatives: the planktonic Marine Group II (MG-II) and the sediment dwelling Marine Benthic Group D (MBG-D) for which the first genomic sequences were recently obtained (Iverson et al. 2012; Lloyd et al. 2013).Fig. 2.—


Phylogenomic data support a seventh order of Methylotrophic methanogens and provide insights into the evolution of Methanogenesis.

Borrel G, O'Toole PW, Harris HM, Peyret P, Brugère JF, Gribaldo S - Genome Biol Evol (2013)

Phylogenetic position of the Mx order and inferred losses of methanogenesis. (a) Bayesian phylogeny of Euryarchaeota based on a concatenation of 57 ribosomal proteins comprising 7,472 amino acid positions. Values at nodes represent Bayesian posterior probabilities and bootstrap values based on maximum likelihood analysis and 100 resamplings of the original data set. For clarity, only the values corresponding to the monophyly of orders and their evolutionary relationships are shown. “../” symbols indicate that the corresponding node was not recovered in the maximum likelihood phylogeny. The scale bar represents the average number of substitutions per site. For details on analyses, see Materials and Methods. Red crosses indicate complete loss of methanogenesis. Colored spots indicate presence of the genes of the respective methanogenic pathways/reactions as indicated by the colored boxes in figure 1. Crosses within spots indicate that the enzymes are present but not used to perform methanogenesis from H2/CO2 and/or from methylated compounds. Genomes with a green spot harbor the genes needed to use at least one type of methyl compound. (b) Maximum likelihood phylogeny of methanogens based on a concatenation of McrA-B-C-D-G protein sequences comprising 1,159 amino acid positions. Values at nodes represent bootstrap proportions calculated based on 100 resamplings of the original alignment and Bayesian posterior probabilities. For clarity, only the values corresponding to the monophyly of orders and their evolutionary relationships are shown. The scale bar represents the average number of substitutions per site. For details on analyses, see Materials and Methods.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3814188&req=5

evt128-F2: Phylogenetic position of the Mx order and inferred losses of methanogenesis. (a) Bayesian phylogeny of Euryarchaeota based on a concatenation of 57 ribosomal proteins comprising 7,472 amino acid positions. Values at nodes represent Bayesian posterior probabilities and bootstrap values based on maximum likelihood analysis and 100 resamplings of the original data set. For clarity, only the values corresponding to the monophyly of orders and their evolutionary relationships are shown. “../” symbols indicate that the corresponding node was not recovered in the maximum likelihood phylogeny. The scale bar represents the average number of substitutions per site. For details on analyses, see Materials and Methods. Red crosses indicate complete loss of methanogenesis. Colored spots indicate presence of the genes of the respective methanogenic pathways/reactions as indicated by the colored boxes in figure 1. Crosses within spots indicate that the enzymes are present but not used to perform methanogenesis from H2/CO2 and/or from methylated compounds. Genomes with a green spot harbor the genes needed to use at least one type of methyl compound. (b) Maximum likelihood phylogeny of methanogens based on a concatenation of McrA-B-C-D-G protein sequences comprising 1,159 amino acid positions. Values at nodes represent bootstrap proportions calculated based on 100 resamplings of the original alignment and Bayesian posterior probabilities. For clarity, only the values corresponding to the monophyly of orders and their evolutionary relationships are shown. The scale bar represents the average number of substitutions per site. For details on analyses, see Materials and Methods.
Mentions: Analysis of a concatenation of ribosomal proteins from 84 euryarchaeal genomes and comprising 7,472 amino acid positions robustly shows that M. luminyensis and “Ca. M. alvus” represent a monophyletic lineage that is not phylogenetically associated with any of the previously known orders of methanogens or the anaerobic methanotrophic ANME1 lineage (fig. 2a). Interestingly, the Mx order, albeit evolutionarily close to Thermoplasmatales as previously noted, robustly clusters with two lineages without cultured representatives: the planktonic Marine Group II (MG-II) and the sediment dwelling Marine Benthic Group D (MBG-D) for which the first genomic sequences were recently obtained (Iverson et al. 2012; Lloyd et al. 2013).Fig. 2.—

Bottom Line: M. alvus" are obligate H₂-dependent methylotrophic methanogens.Genomic data also suggest that these methanogens may use a large panel of methylated compounds.Phylogenetic analysis including homologs retrieved from environmental samples indicates that methylotrophic methanogenesis (regardless of dependency on H₂) is not restricted to gut representatives but may be an ancestral characteristic of the whole order, and possibly also of ancient origin in the Euryarchaeota. 16S rRNA and McrA trees show that this new order of methanogens is very diverse and occupies environments highly relevant for methane production, therefore representing a key lineage to fully understand the diversity and evolution of methanogenesis.

View Article: PubMed Central - PubMed

Affiliation: EA-4678 CIDAM, Clermont Université, Université d'Auvergne, Clermont-Ferrand, France.

ABSTRACT
Increasing evidence from sequence data from various environments, including the human gut, suggests the existence of a previously unknown putative seventh order of methanogens. The first genomic data from members of this lineage, Methanomassiliicoccus luminyensis and "Candidatus Methanomethylophilus alvus," provide insights into its evolutionary history and metabolic features. Phylogenetic analysis of ribosomal proteins robustly indicates a monophyletic group independent of any previously known methanogenic order, which shares ancestry with the Marine Benthic Group D, the Marine Group II, the DHVE2 group, and the Thermoplasmatales. This phylogenetic position, along with the analysis of enzymes involved in core methanogenesis, strengthens a single ancient origin of methanogenesis in the Euryarchaeota and indicates further multiple independent losses of this metabolism in nonmethanogenic lineages than previously suggested. Genomic analysis revealed an unprecedented loss of the genes coding for the first six steps of methanogenesis from H₂/CO₂ and the oxidative part of methylotrophic methanogenesis, consistent with the fact that M. luminyensis and "Ca. M. alvus" are obligate H₂-dependent methylotrophic methanogens. Genomic data also suggest that these methanogens may use a large panel of methylated compounds. Phylogenetic analysis including homologs retrieved from environmental samples indicates that methylotrophic methanogenesis (regardless of dependency on H₂) is not restricted to gut representatives but may be an ancestral characteristic of the whole order, and possibly also of ancient origin in the Euryarchaeota. 16S rRNA and McrA trees show that this new order of methanogens is very diverse and occupies environments highly relevant for methane production, therefore representing a key lineage to fully understand the diversity and evolution of methanogenesis.

Show MeSH
Related in: MedlinePlus