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Methanogenic archaea: ecologically relevant differences in energy conservation

Key Points

  • This Review focuses on the energy metabolism of methanogenic archaea growing on H2 and CO2, with the emphasis on differences between methanogens with and without cytochromes.

  • The authors point out that the differences in the electron-carrier apparatus are reflected in differences in growth yields, ATP gains and H2 threshold concentrations. These differences can explain why methanogens without cytochromes generally out-compete those with cytochromes at the low H2 concentrations that prevail in their natural environments.

  • After highlighting the ecologically relevant phenotypic differences, the authors outline how methanogens with and without cytochromes probably conserve energy. Whereas in methanogens with cytochromes, the first and last steps in methanogenesis from CO2 are coupled chemiosmotically, the available evidence indicates that in methanogens without cytochromes, these steps are energetically coupled by a cytoplasmic enzyme complex that mediates flavin-based electron bifurcation, a coupling mechanism that was recently discovered in clostridia.

  • Finally, the authors discuss how by involving flavoprotein-linked electron bifurcation one can also explain how Methanosphaera stadtmanae can grow on methanol and H2, for which there has never been a convincing explanation.

Abstract

Most methanogenic archaea can reduce CO2 with H2 to methane, and it is generally assumed that the reactions and mechanisms of energy conservation that are involved are largely the same in all methanogens. However, this does not take into account the fact that methanogens with cytochromes have considerably higher growth yields and threshold concentrations for H2 than methanogens without cytochromes. These and other differences can be explained by the proposal outlined in this Review that in methanogens with cytochromes, the first and last steps in methanogenesis from CO2 are coupled chemiosmotically, whereas in methanogens without cytochromes, these steps are energetically coupled by a cytoplasmic enzyme complex that mediates flavin-based electron bifurcation.

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Figure 1: Methane as an intermediate in the global carbon cycle.
Figure 2: The coupling sites that are proposed to be involved in energy conservation in Methanosarcina barkeri growing on CO2 and H2.
Figure 3: The reaction catalysed by the butyryl-CoA dehydrogenase (Bcd)–electron transfer flavoprotein (EtfAB) complex from Clostridium kluyveri.
Figure 4: Proposed scheme for the reduction of CoM-S-S-CoB with H2 that is catalysed by the hydrogenase (MvhADG)–heterodisulphide reductase (HdrABC) complex in methanogens without cytochromes.
Figure 5: The coupling sites that are proposed to be involved in energy conservation in methanogens without cytochromes growing on CO2 and H2.
Figure 6: Proposed energy conservation by the Ehb complex in Methanosphaera stadtmanae growing on methanol and H2.

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Acknowledgements

This work was supported by the Max Planck Society, the Deutsche Forschungsgemeinschaft and the Fonds der Chemischen Industrie.

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Correspondence to Rudolf K. Thauer.

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DATABASES

Entrez Genome Project: 

Clostridium kluyveri

Desulfovibrio vulgaris

Escherichia coli

Methanocaldococcus jannaschii

Methanococcus maripaludis

Methanopyrus kandleri

Methanosarcina acetivorans

Methanosarcina barkeri

Methanosarcina mazei

Methanosphaera stadtmanae

Methanothermobacter thermoautotrophicus

Pyrococcus furiosus

FURTHER INFORMATION

Rudolf K. Thauer's homepage

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Glossary

Syntrophic

A nutritional situation in which two or more organisms combine their metabolic capabilities to catabolize a substance that cannot be catabolized by either one of them alone.

Electron bifurcation

Separation of the two electrons from ubiquinol at the quinol oxidation site of the bc1 complex (complex III) of the respiratory chain, which leads to a bifurcation of the two electrons to a high and a low potential pathway.

Menaquinone

Abbreviation for methylnaphthoquinone, an electron carrier in the cytoplasmic membrane of many bacteria and archaea. Reduction by one electron yields the menasemiquinone anion, which upon further reduction by a second electron takes two protons and thus forms menahydroquinone (also called menaquinol).

Hyperthermophily

A growth temperature optimum of 80 °C or higher.

Corrinoid

A cobalt-containing tetrapyrrole, such as vitamin B12 or coenzyme B12.

Proton motive Q cycle

A cycle that is catalysed by the bc1 complex (complex III) of the respiratory chain and that mediates the oxidation of ubiquinol with cytochrome c and couples this reaction with the electrogenic translocation of four protons in a cyclic process.

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Thauer, R., Kaster, AK., Seedorf, H. et al. Methanogenic archaea: ecologically relevant differences in energy conservation. Nat Rev Microbiol 6, 579–591 (2008). https://doi.org/10.1038/nrmicro1931

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