Electron Bifurcation and Confurcation in Methanogenesis and Reverse Methanogenesis

Abstract

Reduction of the disulfide of coenzyme M and coenzyme B (CoMS-SCoB) by heterodisulfide reductases (HdrED and HdrABC) is the final step in all methanogenic pathways. Flavin-based electron bifurcation (FBEB) by soluble HdrABC homologs play additional roles in driving essential endergonic reactions at the expense of the exergonic reduction of CoMS-SCoM. In the first step of the CO₂ reduction pathway, HdrABC complexed with hydrogenase or formate dehydrogenase generates reduced ferredoxin (Fdx^2-) for the endergonic reduction of CO₂ coupled to the exergonic reduction of CoMS-SCoB dependent on FBEB of electrons from H₂ or formate. Roles for HdrABC:hydrogenase complexes are also proposed for pathways wherein the methyl group of methanol is reduced to methane with electrons from H₂. The HdrABC complexes catalyze FBEB-dependent oxidation of H₂ for the endergonic reduction of Fdx driven by the exergonic reduction of CoMS-SCoB. The Fdx^2- supplies electrons for reduction of the methyl group to methane. In H₂^- independent pathways, three-fourths of the methyl groups are oxidized producing Fdx^2- and reduced coenzyme F₄₂₀ (F₄₂₀H₂). The F₄₂₀H₂ donates electrons for reduction of the remaining methyl groups to methane requiring transfer of electrons from Fdx^2- to F₄₂₀. HdrA1B1C1 is proposed to catalyze FBEB-dependent oxidation of Fdx^2- for the endergonic reduction of F₄₂₀ driven by the exergonic reduction of CoMS-SCoB. In H₂^- independent acetotrophic pathways, the methyl group of acetate is reduced to methane with electrons derived from oxidation of the carbonyl group mediated by Fdx. Electron transport involves a membrane-bound complex (Rnf) that oxidizes Fdx^2- and generates a Na⁺ gradient driving ATP synthesis. It is postulated that F₄₂₀ is reduced by Rnf requiring HdrA2B2C2 catalyzing FBEB-dependent oxidation of F₄₂₀H₂ for the endergonic reduction of Fdx driven by the exergonic reduction of CoMS-SCoB. The Fdx^2- is recycled by Rnf and HdrA2B2C2 thereby conserving energy. The HdrA2B2C2 is also proposed to play a role in Fe(III)-dependent reverse methanogenesis. A flavin-based electron confurcating (FBEC) HdrABC complex is proposed for nitrate-dependent reverse methanogenesis in which the oxidation of CoM-SH/CoB-SH and Fdx^2- is coupled to reduction of F₄₂₀. The F₄₂₀H₂ donates electrons to a membrane complex that generates a proton gradient driving ATP synthesis.

Keywords: acetate; archaea; ferredoxin; formate; heterodisulfide reductase; hydrogen; methane.