The Heterotrophic Bacterium Cupriavidus pinatubonensis JMP134 Oxidizes Sulfide to Sulfate with Thiosulfate as a Key Intermediate

Abstract

Heterotrophic bacteria actively participate in the biogeochemical cycle of sulfur on Earth. The heterotrophic bacterium Cupriavidus pinatubonensis JMP134 contains several enzymes involved in sulfur oxidation, but how these enzymes work together to oxidize sulfide in the bacterium has not been studied. Using gene-deletion and whole cell assays, we determined that the bacterium uses sulfide:quinone oxidoreductase to oxidize sulfide to polysulfide, which is further oxidized to sulfite by persulfide dioxygenase. Sulfite spontaneously reacts with polysulfide to produce thiosulfate. The Sox system oxidizes thiosulfate to sulfate. Flavocytochrome c sulfide dehydrogenase enhances thiosulfate oxidation by the Sox system, but couples with the Sox system for sulfide oxidation to sulfate in the absence of sulfide:quinone oxidoreductase. Thus, C. pinatubonensis JMP134 contains a main pathway and a contingent pathway for sulfide oxidation. Importance We establish a new pathway of sulfide oxidation with thiosulfate as a key intermediate in Cupriavidus pinatubonensis JMP134. The bacterium mainly oxidizes sulfide by using sulfide:quinone oxidoreductase, persulfide dioxygenase, and the Sox system with thiosulfate as a key intermediate. Although the purified and reconstituted Sox system oxidizes sulfide, its rate of sulfide oxidation in C. pinatubonensis JMP134 is too low to be physiologically relevant. The findings reveal how these sulfur oxidizing enzymes participate in sulfide oxidation in a single bacterium.

Sulfane sulfur post-translationally modifies the global regulator AdpA to influence actinorhodin production and morphological differentiation of Streptomyces coelicolor

“…when sulfane sulfur level is high, cysteine residues are sulfhydrated to form RS n H (n≥2) or RS n R (n≥3) bond, which leads configuration change of the regulator and subsequently high expression of PDO and other genes, and then sulfane sulfur level is decreased through oxidizing to sulfite (19). Therefore, Group I regulators mainly 21 function as managers to maintain the homeostasis of intracellular sulfane sulfur.…”

“…In the latest two decades, intensive studies of sulfane sulfur have been performed with mammalian cells because it is found that sulfane sulfur is involved in the regulation of diverse physiological and pathological processes including apoptosis, carcinogenesis, and redox maintenance (15)(16)(17)(18). On the other hand, studies of microorganism sulfane sulfur are traditionally focused on its metabolism and its role in the global sulfur cycle (19,20). In recent years, the physiological functions of sulfane sulfur in microorganisms also attract attentions.…”

The Mechanisms of Thiosulfate Toxicity against Saccharomyces cerevisiae

“…Thiosulfate is spontaneously produced by reacting sulfite with elemental sulfur [ 1 ], and it is a key intermediate in the biogeochemical cycle of sulfur [ 2 ]. Many heterotrophic bacteria oxidize H 2 S to thiosulfate as a detoxification mechanism [ 3 , 4 , 5 ], and other bacteria oxidize thiosulfate to sulfate to gain energy for growth [ 6 , 7 , 8 ]. Further, bacteria and yeast readily use thiosulfate as a sulfur source for growth [ 9 , 10 , 11 , 12 ].…”

Development of whole-cell catalyst system for sulfide biotreatment based on the engineered haloalkaliphilic bacterium

“…As previously reported, the sulfide oxidation rates of eight heterotrophic bacteria ranged from 0.1 to 50 µmol·min −1 ·g −1 dry cell mass, showing that the rates of sulfide removal are comparable to those of chemoautotrophic bacteria (Hou et al 2018 ). Therefore, the heterotrophic bacteria capable of rapidly oxidizing sulfide offer an alternative for sulfide biotreatment (Xia et al 2017 ; Xin et al 2020 ). Sulfide: quinone oxidoreductase (Sqr) and flavocytochrome c sulfide dehydrogenase (FCSD) are two different enzymes with sulfide oxidation activity in the periplasmic and cytosolic sides of the membrane.…”

“…Sqrs are classified into six types based on the structural analysis (Marcia et al 2010 ). Subsequently, persulfide dioxygenase (Pdo) further oxidizes sulfane sulfur to sulfite and is found in Cupriavidus pinatubonensis JMP134 (Xin et al 2020 ). Some heterotrophic bacteria contained only Sqr, while others contained both Sqr and Pdo, and they were able to oxidize sulfide (Gao et al 2017 ; Xia et al 2017 ).…”