DsrMKJOP is the terminal reductase complex in anaerobic sulfate respiration

Abstract

Microbial dissimilatory sulfate reduction is a key process in the Earth biogeochemical sulfur cycle. In spite of its importance to the sulfur and carbon cycles, industrial processes and human health, it is still not clear how reduction of sulfate to sulfide is coupled to energy conservation. A central step in the pathway is the reduction of sulfite by the DsrAB dissimilatory sulfite reductase, which leads to the production of a DsrC-trisulfide. A membrane-bound complex, DsrMKJOP, is present in most organisms that have DsrAB and DsrC, and its involvement in energy conservation has been inferred from sequence analysis, but its precise function was so far not determined. Here, we present studies revealing that the DsrMKJOP complex of the sulfate reducer Archaeoglobus fulgidus works as a menadiol:DsrC-trisulfide oxidoreductase. Our results reveal a close interaction between the DsrC-trisulfide and the DsrMKJOP complex and show that electrons from the quinone pool reduce consecutively the DsrM hemes b, the DsrK noncubane [4Fe-4S]3+/2+ catalytic center, and finally the DsrC-trisulfide with concomitant release of sulfide. These results clarify the role of this widespread respiratory membrane complex and indicate that DsrMKJOP will provide the missing link to energy conservation by generating a proton motive force across the membrane in the last step of dissimilatory sulfate reduction. Significance StatementDissimilatory sulfate reduction (DSR) is a vital microbial process in anoxic environments, namely in sulfate-rich marine sediments that harbor a vast microbial ecosystem. DSR drives the global biogeochemical sulfur cycle and is crucial in remineralization of organic matter on the seafloor. It also has huge environmental impact by preventing release of the greenhouse gas methane from these sediments, through its oxidation coupled to sulfate reduction. Despite its high ecological importance, it is still not clear how microorganisms derive energy to grow through DSR. Here, we disclose the physiological function of a widespread membrane complex in DSR, showing it acts as the terminal reductase in the respiratory chain and providing important insights into how sulfate/sulfite reduction is linked to energy conservation.