The number of sequenced genomes of sulfate reducing organisms (SRO) has increased significantly in the recent years, providing an opportunity for a broader perspective into their energy metabolism. In this work we carried out a comparative survey of energy metabolism genes found in 25 available genomes of SRO. This analysis revealed a higher diversity of possible energy conserving pathways than classically considered to be present in these organisms, and permitted the identification of new proteins not known to be present in this group. The Deltaproteobacteria (and Thermodesulfovibrio yellowstonii) are characterized by a large number of cytochromes c and cytochrome c-associated membrane redox complexes, indicating that periplasmic electron transfer pathways are important in these bacteria. The Archaea and Clostridia groups contain practically no cytochromes c or associated membrane complexes. However, despite the absence of a periplasmic space, a few extracytoplasmic membrane redox proteins were detected in the Gram-positive bacteria. Several ion-translocating complexes were detected in SRO including H+-pyrophosphatases, complex I homologs, Rnf, and Ech/Coo hydrogenases. Furthermore, we found evidence that cytoplasmic electron bifurcating mechanisms, recently described for other anaerobes, are also likely to play an important role in energy metabolism of SRO. A number of cytoplasmic [NiFe] and [FeFe] hydrogenases, formate dehydrogenases, and heterodisulfide reductase-related proteins are likely candidates to be involved in energy coupling through electron bifurcation, from diverse electron donors such as H2, formate, pyruvate, NAD(P)H, β-oxidation, and others. In conclusion, this analysis indicates that energy metabolism of SRO is far more versatile than previously considered, and that both chemiosmotic and flavin-based electron bifurcating mechanisms provide alternative strategies for energy conservation.

Highlights d C-terminal helix alteration unfolds APOL1, increasing APOL1 interaction with APOL3 d APOL3 binds to NCS-1, promoting NCS-1-PI4KB interaction and PI4KB activation d C-terminal APOL1 variants interfere with APOL3-NCS-1 interaction, inactivating PI4KB d PI4KB inactivation occurs in podocytes from kidney disease patients with APOL1 variants

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.

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