Unifying concepts in anaerobic respiration: Insights from dissimilatory sulfur metabolism

Abstract

Behind the versatile nature of prokaryotic energy metabolism is a set of redox proteins having a highly modular character. It has become increasingly recognized that a limited number of redox modules or building blocks appear grouped in different arrangements, giving rise to different proteins and functionalities. This modularity most likely reveals a common and ancient origin for these redox modules, and is obviously reflected in similar energy conservation mechanisms. The dissimilation of sulfur compounds was probably one of the earliest biological strategies used by primitive organisms to obtain energy. Here, we review some of the redox proteins involved in dissimilatory sulfur metabolism, focusing on sulfate reducing organisms, and highlight links between these proteins and others involved in different processes of anaerobic respiration. Noteworthy are links to the complex iron-sulfur molybdoenzyme family, and heterodisulfide reductases of methanogenic archaea. We discuss how chemiosmotic and electron bifurcation/confurcation may be involved in energy conservation during sulfate reduction, and how introduction of an additional module, multiheme cytochromes c, opens an alternative bioenergetic strategy that seems to increase metabolic versatility. Finally, we highlight new families of heterodisulfide reductase-related proteins from non-methanogenic organisms, which indicate a widespread distribution for these protein modules and may indicate a more general involvement of thiol/disulfide conversions in energy metabolism. This article is part of a Special Issue entitled: The evolutionary aspects of bioenergetic systems.

New Model for Electron Flow for Sulfate Reduction in Desulfovibrio alaskensis G20

“…4). The recent proposal that the transmembrane complex QmoABC participates in a confurcation of electrons to APS reductase for bisulfite production (45,47,48) provides a feasible explanation of the phenotype of the I2 mutant. In that scheme, reduced menaquinone (E 0= menaquinol ϭ Ϫ75 mV) in partnership with an electron donor of lower potential would be needed to overcome the membrane potential and provide electrons to APS (E 0= APS/ HSO 3 Ϫ ϭ Ϫ60 mV).…”

Evidence for a Hexaheteromeric Methylenetetrahydrofolate Reductase in Moorella thermoacetica

“…In dissimilatory sulfate reduction, a function in coupling of cytoplasmic redox reactions to membrane-associated redox reactions has been proposed (16,69). The HdrABC complex appears to be an electron-bifurcating module used over and over again in different contexts, as is the EtfAB complex (70), which is used in many anaerobes as an electronbifurcating module in crotonyl-CoA reduction (71), caffeyl-CoA reduction (72), and lactate oxidation (73).…”

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

“…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). The truncation of the contig containing these genes precluded linking the predicted proteins directly to other related mechanisms by genomic associations, and the exact mechanisms of such complexes are not understood in many other microorganisms.…”