Cited by 203Anaerobic Digestion and Biogas ProductionMetalloenzymes and iron-sulfur proteinsMicrobial metabolism and enzyme function

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Protein complexing in a methanogen suggests electron bifurcation and electron delivery from formate to heterodisulfide reductase

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Costa, Kyle C., Wong, Phoebe M., Wang, Tiansong, Lie, Thomas J., Dodsworth, Jeremy A., Swanson, Ingrid, Burn, June A., Hackett, Murray, Leigh, John A.·2010·Proceedings of the National Academy of Sciences

DOI 10.1073/pnas.1003653107PMC PMC2890747

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Abstract

In methanogenic Archaea, the final step of methanogenesis generates methane and a heterodisulfide of coenzyme M and coenzyme B (CoM-S-S-CoB). Reduction of this heterodisulfide by heterodisulfide reductase to regenerate HS-CoM and HS-CoB is an exergonic process. Thauer et al. [Thauer, et al. 2008 Nat Rev Microbiol 6:579–591] recently suggested that in hydrogenotrophic methanogens the energy of heterodisulfide reduction powers the most endergonic reaction in the pathway, catalyzed by the formylmethanofuran dehydrogenase, via flavin-based electron bifurcation. Here we present evidence that these two steps in methanogenesis are physically linked. We identify a protein complex from the hydrogenotrophic methanogen, Methanococcus maripaludis , that contains heterodisulfide reductase, formylmethanofuran dehydrogenase, F 420 -nonreducing hydrogenase, and formate dehydrogenase. In addition to establishing a physical basis for the electron-bifurcation model of energy conservation, the composition of the complex also suggests that either H 2 or formate (two alternative electron donors for methanogenesis) can donate electrons to the heterodisulfide-H 2 via F 420 -nonreducing hydrogenase or formate via formate dehydrogenase. Electron flow from formate to the heterodisulfide rather than the use of H 2 as an intermediate represents a previously unknown path of electron flow in methanogenesis. We further tested whether this path occurs by constructing a mutant lacking F 420 -nonreducing hydrogenase. The mutant displayed growth equal to wild-type with formate but markedly slower growth with hydrogen. The results support the model of electron bifurcation and suggest that formate, like H 2 , is closely integrated into the methanogenic pathway.

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Authors: Costa, K. C., Wong, P. M., Wang, T., Lie, T. J., Dodsworth, J. A., Swanson, I., Burn, J. A., Hackett, M., & Leigh, J. A.
Affiliations: U.S. National Science Foundation (US)
University of Washington (US)
ORCID: Costa, Kyle C.
Wang, Tiansong
Dodsworth, Jeremy A.
Venue: Proceedings of the National Academy of Sciences
Publisher: National Academy of Sciences
Published: 2010-06
Volume: 107
Issue: 24
Pages: 11050-11055
ISSN: 0027-8424 (ISSN-L)
1091-6490
DOI: 10.1073/pnas.1003653107
PMC: PMC2890747
OpenAlex: W2084094775
Cited by: 203
References: 36
Citations by year: 2026: 12 · 2025: 16 · 2024: 9 · 2023: 14 · 2022: 14 · 2021: 15 · 2020: 15 · 2019: 10 · 2018: 15 · 2017: 7 · 2016: 10 · 2015: 9 · 2014: 13 · 2013: 17 · 2012: 8
FWCI: 33.13
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Locations: Proceedings of the National Academy of Sciences (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: National Science Foundation (0504219)
U.S. Department of Energy (DE‐FG02‐, DEFG0205ER15709, FG02-05ER15709)
University of Washington
Division of Graduate Education
Basic Energy Sciences (DE-FG02)
Topics: Physical Sciences › Energy › Renewable Energy, Sustainability and the Environment › Anaerobic Digestion and Biogas Production
Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Metalloenzymes and iron-sulfur proteins
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Microbial metabolism and enzyme function
Keywords: methanogenesis, electron bifurcation, heterodisulfide reductase, formate dehydrogenase, protein complexes, Methanococcus maripaludis, hydrogenotrophic methanogens, electron flow, coenzyme M, coenzyme B, energy conservation, hydrogen as electron donor
MeSH terms: Alcohol Oxidoreductases, Aldehyde Oxidoreductases, Base Sequence, Electron Transport, Formate Dehydrogenases, Formates, Models, Biological, Multienzyme Complexes, Oxidoreductases, Methanococcus, DNA Primers, Archaeal Proteins, Multiprotein Complexes

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Protein complexing in a methanogen suggests electron bifurcation and electron delivery from formate to heterodisulfide reductase

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