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An evolving view of methane metabolism in the Archaea

Nature Reviews Microbiology volume 17, pages 219–232 (2019)Cite this article

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Abstract

Methane is a key compound in the global carbon cycle that influences both nutrient cycling and the Earth’s climate. A limited number of microorganisms control the flux of biologically generated methane, including methane-metabolizing archaea that either produce or consume methane. Methanogenic and methanotrophic archaea belonging to the phylum Euryarchaeota share a genetically similar, interrelated pathway for methane metabolism. The key enzyme in this pathway, the methyl-coenzyme M reductase (Mcr) complex, catalyses the last step in methanogenesis and the first step in methanotrophy. The discovery of mcr and divergent mcr-like genes in new euryarchaeotal lineages and novel archaeal phyla challenges long-held views of the evolutionary origin of this metabolism within the Euryarchaeota. Divergent mcr-like genes have recently been shown to oxidize short-chain alkanes, indicating that these complexes have evolved to metabolize substrates other than methane. In this Review, we examine the diversity, metabolism and evolutionary history of mcr-containing archaea in light of these recent discoveries.

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Fig. 1: Methanogenesis in the context of the global carbon cycle.
Fig. 2: Archaeal genome tree highlighting lineages containing mcr and mcr- like genes.
Fig. 3: Methanogenic and methanotrophic pathways.
Fig. 4: Phylogenetic tree based on McrA and McrA-like sequences.
Fig. 5: Genes encoded in genomes of mcr and mcr- like containing lineages and their metabolism type.
Fig. 6: Incongruences between genome and concatenated Mcr proteins.

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Acknowledgements

This work was supported by the Genomic Science Program of the US Department of Energy Office of Biological and Environmental Research, grants DE-FOA-0001458 and DE-SC0016440. P.N.E. is supported by Australian Research Council (ARC) Discovery Early Career Researcher Award 170100428. B.J.W. is supported by ARC Discovery Early Career Researcher Award 160100248. A.O.L. and J.A.B. are supported through ARC Postgraduate awards. P.H. is supported through an ARC Laureate Fellowship Award. G.W.T. is supported through a University of Queensland Vice Chancellor Research Focused Fellowship.

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  1. Australian Centre for Ecogenomics, School of Chemistry and Molecular Biosciences, University of Queensland, St Lucia, Queensland, Australia

    Paul N. Evans, Joel A. Boyd, Andy O. Leu, Ben J. Woodcroft, Donovan H. Parks, Philip Hugenholtz & Gene W. Tyson

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J.A.B, P.N.E., A.O.L., D.H.P., G.W.T. and B.J.W. researched data for the article. All authors contributed to discussion of the content, wrote the article and reviewed and edited the manuscript before submission.

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Glossary

Methanogens

Archaea that gain energy by forming methane from 1-carbon and 2-carbon compounds such as CO2, acetate and methanol produced during microbial fermentation.

Syntrophic partners

Organisms that have a mutually beneficial relationship. In the case of methanogens, these organisms consume hydrogen produced by bacterial partners to form methane, which increases the energetic efficiency of biomass breakdown.

Anaerobic methanotrophy

The means by which archaea gain energy by the oxidation of methane to CO2 in anaerobic environments, with the electrons generated disposed of either by the reduction of inorganic electron acceptors or by transfer to a bacterial partner.

Hydrogenotrophic

Refers to methanogens that use H2, and sometimes formate, as a source of electrons to reduce CO2 to methane in a stepwise reduction using cofactors such as methanofuran, tetrahydromethanopterin and coenzyme M.

Aceticlastic

Refers to methanogenesis that occurs by the dismutation of acetate to CO2 and transfer of a methyl group to the 1-carbon carrier tetrahydrosarcinapterin (H4SPT). The methyl-group–H4SPT complex is then reduced to methane.

Methylotrophic

Refers to methanogens with disproportionate methylated compounds such as methyl amine, methyl sulfide and methanol to form CO2 and methane. The oxidation of one molecule of these methylated compounds to CO2 via the 1-carbon carrier tetrahydrosarcinapterin provides electrons required to reduce further a three-methyl group to methane.

H2-dependent methylotrophic

A type of methanogenesis that occurs by the oxidation of methylated compounds to methane with electrons generated from H2 oxidation instead of by disproportionation of methyl groups to CO2.

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Evans, P.N., Boyd, J.A., Leu, A.O. et al. An evolving view of methane metabolism in the Archaea. Nat Rev Microbiol 17, 219–232 (2019). https://doi.org/10.1038/s41579-018-0136-7

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