Structural Basis for the Oxidation of Protein-bound Sulfur by the Sulfur Cycle Molybdohemo-Enzyme Sulfane Dehydrogenase SoxCD

Abstract

Reduced inorganic sulfur compounds like hydrogen sulfide, sulfur, or thiosulfate are attractive prokaryotic energy sources, and their oxidation to sulfuric acid is one of the major reactions of the global sulfur cycle as shown for thiosulfate (Equation 1).Oxidation of inorganic sulfur compounds to sulfate is mainly mediated by various specialized aerobic chemotrophic and anaerobic phototrophic prokaryotes, bacteria and archaea (1-3). Two different modes for bacteria have been proposed recently; one as present in e.g. the anaerobic phototrophic sulfur oxidizing bacterium Allochromatium vinosum involves the reverse acting dissimilatory sulfite dehydrogenase (DsrAB) (Equation 2) which is with 13 other proteins encoded by the dsr operon (4). The product sulfite is subsequently oxidized to sulfate by adenosine 5Ј-phosphosulfate reductase or sulfite:acceptor oxidoreductase (5).The other mode as present in e.g. the aerobic facultative chemotrophic bacterium Paracoccus pantotrophus (6) involves sulfane dehydrogenase SoxCD, which is together with 14 other proteins encoded by the sox operon in this strain. SoxCD is an ␣ 2 ␤ 2 heterotetrameric complex of the molybdoprotein SoxC and the hybrid di-heme cytochrome c like protein SoxD. This sulfane dehydrogenase (formerly designated sulfur dehydrogenase (7)) is a key enzyme of the sulfuroxidizing (Sox) 3 enzyme system and catalyzes the oxidation of protein-bound sulfane-sulfur (oxidation state Ϫ1) to sulfone (oxidation state ϩ5) in a six-electron transfer reaction (8, 9) (Equation 3). SoxZY-SThe current model of the Sox reaction cycle involves sequential activity of four different periplasmic proteins SoxXA, SoxB, SoxYZ, and SoxCD ( Fig. 1) (2, 9). The four proteins oxi-* This work was supported by Deutsche Forschungsgemeinschaft Grants Fr318/10-1 and Sche545/9-1. □ S The on-line version of this article (available at http://www.jbc.org) contains supplemental Table 1 and Fig. 1

Biostimulation induces syntrophic interactions that impact C, S and N cycling in a sediment microbial community

“…The missing soxXAB genes (not detected by homology searches) are normally required for thiosulfate (and presumably sulfide and sulfur) attachment to SoxYZ, activation to sulfane, and release after oxidation by SoxCD (Friedrich et al, 2005;Sauvé et al, 2007;Zander et al, 2011). Hence, the exact function of Sox in sulfur oxidation by r9c2 and r9c3 cannot be deduced from our data.…”

Comparison of sulfide‐oxidizing Sulfurimonas strains reveals a new mode of thiosulfate formation in subsurface environments

“…The current model for the Sox(CD) 2 ‐mediated oxidation of the SoxY‐Cys persulfide anion involves iterative hydroxylation steps to yield SoxY‐Cys‐S‐sulfinate as an intermediate and SoxY‐Cys‐S‐sulfonate as final oxidation product (Zander et al ., ). We therefore posit that the sulfite detected in CVO cultures is a by‐product of incomplete oxidation of S 0 as a result of the truncated SOX enzyme system, possibly due to premature release of the SoxY‐bound sulfur substrate at the level of a SoxY‐Cys‐S‐sulfinate and involving SoxH (Fig.…”

Thiosulfate oxidation by Thiomicrospira thermophila: metabolic flexibility in response to ambient geochemistry

“…However, it has been shown that the optimal pH for sulfite dehydrogenase activity of the Sox(CD) 2 complex is 8.0, with a 10% decline at pH 7.3 and 8.5 (Lu and Kelly, ). In addition, the crystal structure of Sox(CD) 2 in Paracoccus pantotrophus indicates that after the addition of the third oxygen atom onto the SoxY‐bound sulfane, the newly created SoxY‐S‐ complex is displaced by OH − , regenerating the oxidized molybdenum cofactor (Zander et al ., ). At low pH, this displacement reaction could be inhibited.…”