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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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Physical maps of mtaA/mtbA, mtaB, and mtaC. Physical maps of mtaA/mtbA, mtaB, and mtaC genes in “Candidatus Methanomethylophilus alvus” Mx1201, Methanomassiliicoccus luminyensis B10, in comparison with Methanosarcina acetivorans CA2 as a representative of Methanosarcinales, and with Methanosphaera stadtmanae DSM 3091 as a representative of Methanobacteriales. The contigs of M. luminyensis (the assembled genome is not yet available) are separated by slashes. MAP, Methyltransferase Activation Protein.
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evt128-F4: Physical maps of mtaA/mtbA, mtaB, and mtaC. Physical maps of mtaA/mtbA, mtaB, and mtaC genes in “Candidatus Methanomethylophilus alvus” Mx1201, Methanomassiliicoccus luminyensis B10, in comparison with Methanosarcina acetivorans CA2 as a representative of Methanosarcinales, and with Methanosphaera stadtmanae DSM 3091 as a representative of Methanobacteriales. The contigs of M. luminyensis (the assembled genome is not yet available) are separated by slashes. MAP, Methyltransferase Activation Protein.

Mentions: The wide distribution of Mx members in various environments and the fact they are not evolutionarily affiliated to any other previously known methanogenic order may suggest that they harbor specific characteristics. In particular, information on the metabolic capacities of “Ca. M. alvus” and M. luminyensis is important for further investigations of the role of these organisms in the human gut. Surprisingly, “Ca. M. alvus” and M. luminyensis are the first methanogens that appear to have totally lost all the genes involved in both the first six steps of methanogenesis from H2/CO2 and the oxidative part of methylotrophic methanogenesis (fig. 1, blue box, in gray font). These genes are otherwise present in all genomes from methanogens sequenced to date, including those that do not use the CO2 reduction/methyl group oxidation pathway for methanogenesis, such as Methanosphaera stadtmanae (Fricke et al. 2006) and Methanosaeta spp. (Zhu et al. 2012) (fig. 2a). Moreover, genes encoding the synthesis of the F420 coenzyme, an important electron carrier in methanogens, are also absent. This is in agreement with Paul et al. (2012), who observed a lack of F420 autofluorescence in their enrichments of MpT1 and MpM2. The absence of all these enzymes explains the fact that M. luminyensis is unable to grow on H2/CO2, acetate, or on methanol without an H2 external source (Dridi et al. 2012). Such metabolic profile was also observed for the strains belonging to the Mx lineage enriched from a microbial consortium (Paul et al. 2012; Iino et al. 2013), including “Ca. M. alvus” (Borrel et al. 2012), even if this has to be confirmed in pure cultures. Consistently, “Ca. M. alvus” and M. luminyensis harbor homologs of the enzymes that are involved in H2-dependent methylotrophic methanogenesis from methanol in Methanosarcinales and Methanobacteriales (MtaABC, fig. 1). Homologs of enzymes that may be potentially used to reduce other methylated compounds such as monomethylamine (MtmBC), dimethylamine (MtbBC), and trimethylamine (MttBC) (fig. 1) are also present in the two genomes (Borrel et al. 2012; Poulsen et al. 2013). Additionally, we identified genes for enzymes involved in methanogenesis from dimethyl sulfide (MtsAB) in both the “Ca. M. alvus” and M. luminyensis genomes (fig. 1). Such a potentially large range of substrates is unusual in methanogens and was so far restricted to the Methanosarcinales (Thauer et al. 2008). “Ca. M. alvus” has one copy each of mtaB and mtaC that are located close to each other in the genome as observed in other methanol-using methanogens, whereas M. luminyensis has three mtaBC clusters (fig. 4). The close association of mtaB and mtaC in these genomes suggests that they form a transcription unit as in other methanogens (Sauer et al. 1997; Fricke et al. 2006). Similar to mtaB and mtaC, the genes coding for the enzymes involved in the use of methylamines (mtmBC, mtbBC, and mttBC) are in close association with both genomes (data not shown). “Ca. M. alvus” and M. luminyensis have two and four copies of the mtmBC cluster, respectively, and both genomes have one copy each of the mtbBC and mttBC clusters (data not shown). “Ca. M. alvus” has three homologs of mtaA/mtbA and M. luminyensis has two, and all five genes are located apart in the respective genomes (fig. 4).Fig. 4.—


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)

Physical maps of mtaA/mtbA, mtaB, and mtaC. Physical maps of mtaA/mtbA, mtaB, and mtaC genes in “Candidatus Methanomethylophilus alvus” Mx1201, Methanomassiliicoccus luminyensis B10, in comparison with Methanosarcina acetivorans CA2 as a representative of Methanosarcinales, and with Methanosphaera stadtmanae DSM 3091 as a representative of Methanobacteriales. The contigs of M. luminyensis (the assembled genome is not yet available) are separated by slashes. MAP, Methyltransferase Activation Protein.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3814188&req=5

evt128-F4: Physical maps of mtaA/mtbA, mtaB, and mtaC. Physical maps of mtaA/mtbA, mtaB, and mtaC genes in “Candidatus Methanomethylophilus alvus” Mx1201, Methanomassiliicoccus luminyensis B10, in comparison with Methanosarcina acetivorans CA2 as a representative of Methanosarcinales, and with Methanosphaera stadtmanae DSM 3091 as a representative of Methanobacteriales. The contigs of M. luminyensis (the assembled genome is not yet available) are separated by slashes. MAP, Methyltransferase Activation Protein.
Mentions: The wide distribution of Mx members in various environments and the fact they are not evolutionarily affiliated to any other previously known methanogenic order may suggest that they harbor specific characteristics. In particular, information on the metabolic capacities of “Ca. M. alvus” and M. luminyensis is important for further investigations of the role of these organisms in the human gut. Surprisingly, “Ca. M. alvus” and M. luminyensis are the first methanogens that appear to have totally lost all the genes involved in both the first six steps of methanogenesis from H2/CO2 and the oxidative part of methylotrophic methanogenesis (fig. 1, blue box, in gray font). These genes are otherwise present in all genomes from methanogens sequenced to date, including those that do not use the CO2 reduction/methyl group oxidation pathway for methanogenesis, such as Methanosphaera stadtmanae (Fricke et al. 2006) and Methanosaeta spp. (Zhu et al. 2012) (fig. 2a). Moreover, genes encoding the synthesis of the F420 coenzyme, an important electron carrier in methanogens, are also absent. This is in agreement with Paul et al. (2012), who observed a lack of F420 autofluorescence in their enrichments of MpT1 and MpM2. The absence of all these enzymes explains the fact that M. luminyensis is unable to grow on H2/CO2, acetate, or on methanol without an H2 external source (Dridi et al. 2012). Such metabolic profile was also observed for the strains belonging to the Mx lineage enriched from a microbial consortium (Paul et al. 2012; Iino et al. 2013), including “Ca. M. alvus” (Borrel et al. 2012), even if this has to be confirmed in pure cultures. Consistently, “Ca. M. alvus” and M. luminyensis harbor homologs of the enzymes that are involved in H2-dependent methylotrophic methanogenesis from methanol in Methanosarcinales and Methanobacteriales (MtaABC, fig. 1). Homologs of enzymes that may be potentially used to reduce other methylated compounds such as monomethylamine (MtmBC), dimethylamine (MtbBC), and trimethylamine (MttBC) (fig. 1) are also present in the two genomes (Borrel et al. 2012; Poulsen et al. 2013). Additionally, we identified genes for enzymes involved in methanogenesis from dimethyl sulfide (MtsAB) in both the “Ca. M. alvus” and M. luminyensis genomes (fig. 1). Such a potentially large range of substrates is unusual in methanogens and was so far restricted to the Methanosarcinales (Thauer et al. 2008). “Ca. M. alvus” has one copy each of mtaB and mtaC that are located close to each other in the genome as observed in other methanol-using methanogens, whereas M. luminyensis has three mtaBC clusters (fig. 4). The close association of mtaB and mtaC in these genomes suggests that they form a transcription unit as in other methanogens (Sauer et al. 1997; Fricke et al. 2006). Similar to mtaB and mtaC, the genes coding for the enzymes involved in the use of methylamines (mtmBC, mtbBC, and mttBC) are in close association with both genomes (data not shown). “Ca. M. alvus” and M. luminyensis have two and four copies of the mtmBC cluster, respectively, and both genomes have one copy each of the mtbBC and mttBC clusters (data not shown). “Ca. M. alvus” has three homologs of mtaA/mtbA and M. luminyensis has two, and all five genes are located apart in the respective genomes (fig. 4).Fig. 4.—

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