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Altered electron flow in hydrogenotrophic methanogens under nickel limitation

ABSTRACT: In the methanogenic pathway from CO2 and H2, low potential electrons for CO2 reduction are generated by a flavin-based electron branching reaction catalysed by heterodisulphide reductase (Hdr) in complex with [NiFe]-hydrogenase (Mvh). The F420-reducing [NiFe]-hydrogenase (Frh) provides electrons for the methane formation pathway via the electron carrier F420. The production of both [NiFe]-hydrogenases in Methanothermobacter marburgensis is strongly down-regulated under strictly nickel-limited conditions. The Frh reaction is replaced 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.

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ORGANISM(S): Methanothermococcus Thermolithotrophicus Methanothermobacter Marburgensis

SUBMITTER: Timo Glatter

LAB HEAD: Timo Glatter

PROVIDER: PXD063936 | Pride | 2025-08-18

REPOSITORIES: Pride

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Project description:Hydrogen can be an important source of energy for chemolithotrophic acidophiles, especially in the deep terrestrial subsurface. Nevertheless, the current knowledge of microbial hydrogen utilization in acidic environments is minimal. A multi-omics analysis was applied on Acidithiobacillus ferrooxidans growing aerobically and anaerobically (with ferric iron) on hydrogen as an electron donor, and a respiratory model proposed from the results obtained. In this model, both [NiFe] hydrogenases, cytoplasmic uptake and membrane-bound respiratory, oxidize molecular hydrogen to two protons and two electrons. The electrons are used to reduce membrane-soluble ubiquinone to ubiquinol. Genetically associated [FeS]-binding proteins mediate electron relay from the hydrogenases to the ubiquinone pool. Under aerobic conditions, reduced ubiquinol transfers electrons to either cytochrome aa3 oxidase via cytochrome bc1 complex and cytochrome c4 or the alternate directly to cytochrome bd oxidase, resulting in proton efflux together with the reduction of molecular oxygen to water. Under anaerobic conditions, reduced ubiquinol transfers electrons to outer membrane cytochrome c (ferric iron reductase) via cytochrome bc1 complex and a cascade of electron transporters (cytochrome c4, cytochrome c552, rusticyanin, and high potential iron-sulfur protein), resulting in proton efflux together with the reduction of ferric iron to ferrous iron. The proton gradient generated by molecular hydrogen oxidation maintains the membrane potential and allows the generation of ATP via ATP synthase and NADH via NADH-ubiquinone oxidoreductase. To a lesser extent, NADH can also be generated by another bidirectional cytoplasmic hydrogenase. ATP and NADH are further utilized in the Calvin–Benson–Bassham cycle for inorganic carbon uptake and assimilation. These results further clarify the role of extremophiles in biogeochemical processes and their impact on the composition and features of the deep terrestrial subsurface from the distant past to the present.

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Altered electron flow in hydrogenotrophic methanogens under nickel limitation

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