Abstract
ABSTRACTHeterodisulfide reductases (Hdr) of the HdrABC class are ancient enzymes and a component of the anaerobic core belonging to the prokaryotic common ancestor. The ancient origin is consistent with the widespread occurrence of genes encoding putative HdrABC homologs in metabolically diverse prokaryotes predicting diverse physiological functions; however, only one HdrABC has been characterized and that was from a narrow metabolic group of obligate CO2-reducing methanogenic anaerobes (methanogens) from the domain Archaea. Here we report the biochemical characterization of an HdrABC homolog (HdrA2B2C2) from the acetate-utilizing methanogen Methanosarcina acetivorans with unusual properties structurally and functionally distinct from the only other HdrABC characterized. Homologs of the HdrA2B2C2 archetype are present in phylogenetically and metabolically diverse species from the domains Bacteria and Archaea. The expression of the individual HdrA2, HdrB2, and HdrB2C2 enzymes in Escherichia coli, and reconstitution of an active HdrA2B2C2 complex, revealed an intersubunit electron transport pathway dependent on ferredoxin or coenzyme F420 (F420H2) as an electron donor. Remarkably, HdrA2B2C2 couples the previously unknown endergonic oxidation of F420H2 and reduction of ferredoxin with the exergonic oxidation of F420H2 and reduction of the heterodisulfide of coenzyme M and coenzyme B (CoMS-SCoB). The unique electron bifurcation predicts a role for HdrA2B2C2 in Fe(III)-dependent anaerobic methane oxidation (ANME) by M. acetivorans and uncultured species from ANME environments. HdrA2B2C2, ubiquitous in acetotrophic methanogens, was shown to participate in electron transfer during acetotrophic growth of M. acetivorans and proposed to be essential for growth in the environment when acetate is limiting.
Highlights
Heterodisulfide reductases (Hdr) of the HdrABC class are ancient enzymes and a component of the anaerobic core belonging to the prokaryotic common ancestor
® mbio.asm.org 1 genomes of diverse species in the domains Bacteria and Archaea are annotated with genes encoding HdrABC homologs, suggesting that these genes play roles in a greater diversity of energy-conserving metabolisms, which include the oxidation of methanol and inorganic sulfur compounds [2,3,4], the reduction of sulfate and ferric iron [4,5,6], syntrophic utilization of fatty acids [7], and the anaerobic oxidation of CH4 [8,9,10]
Of the 150 sequences retrieved, 73 were homologs of the canonical HdrA from both methanogenic and nonmethanogenic species. These results indicate that HdrA2 homologs play roles in metabolically diverse species, warranting investigation of an HdrA2 representative chosen from M. acetivorans that grows by converting acetate to CH4 [17]
Summary
Heterodisulfide reductases (Hdr) of the HdrABC class are ancient enzymes and a component of the anaerobic core belonging to the prokaryotic common ancestor. IMPORTANCE Discovery of the archetype HdrA2B2C2 heterodisulfide reductase with categorically unique properties extends the understanding of this ancient family beyond CO2-reducing methanogens to include diverse prokaryotes from the domains Bacteria and Archaea. ® mbio.asm.org 1 genomes of diverse species in the domains Bacteria and Archaea are annotated with genes encoding HdrABC homologs, suggesting that these genes play roles in a greater diversity of energy-conserving metabolisms, which include the oxidation of methanol and inorganic sulfur compounds [2,3,4], the reduction of sulfate and ferric iron [4,5,6], syntrophic utilization of fatty acids [7], and the anaerobic oxidation of CH4 [8,9,10]. The heterodisulfide product is reduced by Hdr (equation 2), releasing HSCoB and HSCoM for methylation
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