Electron flow in hydrogenotrophic methanogens under nickel limitation

Abstract Methanogenic archaea are the main producers of the potent greenhouse gas methane 1,2 . In the methanogenic pathway from CO 2 and H 2 studied under laboratory conditions, low-potential electrons for CO 2 reduction are generated by a flavin-based electron-bifurcation reaction catalysed by heterodisulfide reductase (Hdr) complexed with the associated [NiFe]-hydrogenase (Mvh) 3–5 . F 420 -reducing [NiFe]-hydrogenase (Frh) provides electrons to the methanogenic pathway through the electron carrier F 420 (ref. 6 ). Here we report that under strictly nickel-limited conditions, in which the nickel concentration is similar to those often observed in natural habitats 7–11 , 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 F 420 -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 CO 2 -reducing hydrogenotrophic methanogens suggests that the Hmd system is an alternative pathway for electron flow in CO 2 -reducing hydrogenotrophic methanogens under nickel-limited conditions.