Electron flow in hydrogenotrophic methanogens under nickel limitation

Shunsuke Nomura, Pablo San Segundo-Acosta, Evgenii Protasov, Masanori Kaneko, Jörg Kahnt, Bonnie J. Murphy () and Seigo Shima ()
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Shunsuke Nomura: Max Planck Institute for Terrestrial Microbiology
Pablo San Segundo-Acosta: Max Planck Institute of Biophysics
Evgenii Protasov: Max Planck Institute for Terrestrial Microbiology
Masanori Kaneko: Max Planck Institute for Terrestrial Microbiology
Jörg Kahnt: Max Planck Institute for Terrestrial Microbiology
Bonnie J. Murphy: Max Planck Institute of Biophysics
Seigo Shima: Max Planck Institute for Terrestrial Microbiology

Nature, 2025, vol. 644, issue 8076, 490-496

Abstract: Abstract Methanogenic archaea are the main producers of the potent greenhouse gas methane1,2. In the methanogenic pathway from CO2 and H2 studied under laboratory conditions, low-potential electrons for CO2 reduction are generated by a flavin-based electron-bifurcation reaction catalysed by heterodisulfide reductase (Hdr) complexed with the associated [NiFe]-hydrogenase (Mvh)3–5. F420-reducing [NiFe]-hydrogenase (Frh) provides electrons to the methanogenic pathway through the electron carrier F420 (ref. 6). Here we report that under strictly nickel-limited conditions, in which the nickel concentration is similar to those often observed in natural habitats7–11, the production of both [NiFe]-hydrogenases in Methanothermobacter marburgensis is strongly downregulated. The Frh reaction is substituted by a coupled reaction with [Fe]-hydrogenase (Hmd), and the role of Mvh is taken over by F420-dependent electron-donating proteins (Elp). Thus, Hmd provides all electrons for the reducing metabolism under these nickel-limited conditions. Biochemical and structural characterization of Elp–Hdr complexes confirms the electronic interaction between Elp and Hdr. The conservation of the genes encoding Elp and Hmd in CO2-reducing hydrogenotrophic methanogens suggests that the Hmd system is an alternative pathway for electron flow in CO2-reducing hydrogenotrophic methanogens under nickel-limited conditions.

Date: 2025
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DOI: 10.1038/s41586-025-09229-y

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