Coupling of ferredoxin and heterodisulfide reduction via electron bifurcation in hydrogenotrophic methanogenic archaea

Abstract

In methanogenic archaea growing on H 2 and CO 2 the first step in methanogenesis is the ferredoxin-dependent endergonic reduction of CO 2 with H 2 to formylmethanofuran and the last step is the exergonic reduction of the heterodisulfide CoM-S-S-CoB with H 2 to coenzyme M (CoM-SH) and coenzyme B (CoB-SH). We recently proposed that in hydrogenotrophic methanogens the two reactions are energetically coupled via the cytoplasmic MvhADG/HdrABC complex. It is reported here that the purified complex from Methanothermobacter marburgensis catalyzes the CoM-S-S-CoB-dependent reduction of ferredoxin with H 2 . Per mole CoM-S-S-CoB added, 1 mol of ferredoxin (Fd) was reduced, indicating an electron bifurcation coupling mechanism: This stoichiometry of coupling is consistent with an ATP gain per mole methane from 4 H 2 and CO 2 of near 0.5 deduced from an H 2 -threshold concentration of 8 Pa and a growth yield of up to 3 g/mol methane.

Genomic and metagenomic surveys of hydrogenase distribution indicate H2 is a widely utilised energy source for microbial growth and survival

“…Electron-bifurcating hydrogenases are bidirectional enzymes that energise the endergonic reaction of the reduction of ferredoxin with H 2 by simultaneously reducing a relatively electropositive acceptor (for example, heterodisulphide, NAD, NADP) (Buckel and Thauer, 2013). The group 3c [NiFe]-hydrogenase in functional complex with heterodisulphide reductase, for example, simultaneously reduces ferredoxin and heterodisulphide during H 2 oxidation (Kaster et al, 2011); these enzymes complete the recently elucidated Wolfe cycle of methanogenesis (Thauer, 2012), and are also distributed in some bacteria (for example, δ-Proteobacteria) (Figure 4). The group A3 [FeFe]-hydrogenases reversibly bifurcate electrons from H 2 to ferredoxin and NAD using trimeric or tetrameric complexes; in the reverse reaction, energy conserved during the oxidation of ferredoxin is used to drive the thermodynamically unfavourable production of H 2 from NADH (Schut and Adams, 2009;Schuchmann and Müller, 2012).…”

“…In anaerobic systems, ultra-minimalistic hydrogenase-containing respiratory chains have been described that efficiently generate energy within oligotrophic environments (Kim et al, 2010;Lim et al, 2014). In parallel, the discovery of electron bifurcation has expanded our understanding of how energy is conserved in anaerobic processes such as cellulolytic fermentation, acetogenesis and methanogenesis (Schut and Adams, 2009;Kaster et al, 2011;Buckel and Thauer, 2013;Schuchmann and Muller, 2014). Other themes, including H 2 sensing within anaerobes (Zheng et al, 2014) and H 2 fermentation in aerobes , are emerging.…”

Microbial dark matter ecogenomics reveals complex synergistic networks in a methanogenic bioreactor

“…In agreement, this organism expresses many Na þ -transporting complexes and, thus, may rely on a transmembrane Na þ gradient metabolically and physiologically. We also identify expression of a novel Methanothermobacter electron-bifurcating hydrogenase-like gene cassette encoding MvhADG hydrogenase subunits and Table S9; Kaster et al, 2011); however, its function remains unclear. Although the complete energy conservation scheme requires further investigation, we infer that Hydrogenedentes syntrophically degrades glycerol and lipids derived from detrital biomass.…”

Genome sequencing of a single cell of the widely distributed marine subsurface Dehalococcoidia, phylum Chloroflexi

“…This cluster was one of the longest and most obvious stretches of ORFs identified (encoding at least 20 ORFs) in our data set, whereby no homologues in known DEH could be identified by BLASTP analyses, yet was downstream of known DEH genes. We hypothesise that the heterodisulfide reductase-like enzymes have important roles in cytoplasmic electron transfer and energy conserving mechanisms, like in other anaerobes such as sulphate reducers, acetogens and methanogens (Stojanowic et al, 2003;Strittmatter et al, 2009;Kaster et al, 2011b;Callaghan et al, 2012). These complexes might be especially important for transferring reducing equivalents released during beta-oxidation and/or conversions of succinate to acetyl-CoA (via the methylmalonyl-CoA pathway), to and from ferredoxins or NADH, possibly by electron bifurcating/confurcating mechanisms that may be linked to other metabolic steps (Buckel and Thauer, 2012;Grein et al, 2012).…”