A novel bacterial sulfur oxidation pathway provides a new link between the cycles of organic and inorganic sulfur compounds

Abstract

Dimethylsulfide (DMS) plays a globally significant role in carbon and sulfur cycling and impacts Earth's climate because its oxidation products serve as nuclei for cloud formation. While the initial steps of aerobic DMS degradation and the fate of its carbon atoms are reasonably well documented, oxidation of the contained sulfur is largely unexplored. Here, we identified a novel pathway of sulfur compound oxidation in the ubiquitously occurring DMS-degrader Hyphomicrobium denitrificans X that links the oxidation of the volatile organosulfur compound with that of the inorganic sulfur compound thiosulfate. DMS is first transformed to methanethiol from which sulfide is released and fully oxidized to sulfate. Comparative proteomics indicated thiosulfate as an intermediate of this pathway and pointed at a heterodisulfide reductase (Hdr)-like system acting as a sulfur-oxidizing entity. Indeed, marker exchange mutagenesis of hdr-like genes disrupted the ability of H. denitrificans to metabolize DMS and also prevented formation of sulfate from thiosulfate provided as an additional electron source during chemoorganoheterotrophic growth. Complementation with the hdr-like genes under a constitutive promoter rescued the phenotype on thiosulfate as well as on DMS. The production of sulfate from an organosulfur precursor via the Hdr-like system is previously undocumented and provides a new shunt in the biogeochemical sulfur cycle. Furthermore, our findings fill a long-standing knowledge gap in microbial dissimilatory sulfur metabolism because the Hdr-like pathway is abundant not only in chemoheterotrophs, but also in a wide range of chemo- and photolithoautotrophic sulfur oxidizers acting as key players in global sulfur cycling.

Two Chloroflexi classes independently evolved the ability to persist on atmospheric hydrogen and carbon monoxide

“…In turn, we hypothesise that the Hdr complex may oxidise the resultant thiol groups to disulfides and transfer the liberated electrons to the aerobic respiratory chain-linked ETF complex. In support of this premise, the upregulated gene cluster encodes components homologous to a system recently shown to mediate the oxidation of diverse sulfur compounds in Hyphomicrobium denitrificans [54, 55] and the Hdr complex is most closely related to those of sulfuroxidising Sulfobacillus, Hyphomicrobium, and Acidithiobacillus strains. It seems plausible that T. roseum would benefit from a survival advantage if able to harness reduced sulfur compounds available in geothermal springs.…”

Determinants of sulphur chemolithoautotrophy in the extremely thermoacidophilic Sulfolobales

“…In Metallosphaera cuprina , enzymes encoded by tusA and dsrE3A were shown to transfer tetrathionate groups (Liu et al ., ). Across the Sulfolobales , TusA and DsrE homologues are found adjacent to a large, highly conserved cluster with homology to the methanogenic heterodisulphide reductase ( hdr ) system, which oxidizes sulphur compounds to sulphate in bacteria (Koch and Dahl, ), and may provide cellular reducing equivalents by transferring electrons via lipoate to NADH (Cao et al ., ). A model metabolic pathway based on the enzymes found in A. ambivalens has served as the basis for understanding sulphur oxidation in the Sulfolobales (Kletzin, ); an updated version of this model, including the more recently characterized enzymes, is shown in Fig.…”

New Insights Into Acidithiobacillus thiooxidans Sulfur Metabolism Through Coupled Gene Expression, Solution Chemistry, Microscopy, and Spectroscopy Analyses

“…Relatively high hdr expression levels were observed under all conditions in comparison to the low levels of sdo (Figure 3A). The inclusion of solution chemical data and electron microscopy suggest that Hdr is likely the primary S 0 oxidizing enzyme rather than Sdo, which was previously identified as important for internal generation of SO 2− 3 and S 2 O 2− 3 during growth on S 0 (Rohwerder and Sand, 2003;Bobadilla Fazzini et al, 2013;Yin et al, 2014;Koch and Dahl, 2018). Catalysis by Hdr rather than Sdo is energetically more favorable since conversion of S 0 to SO 2− 3 is a non-quinone/cytochrome metabolic step for Sdo.…”

“…In contrast, catalysis of the hdr gene also found in A. caldus (Mangold et al, 2011), A. ferrooxidans ) and A. thiooxidans A01 (Yin et al, 2014) enables A. thiooxidans to metabolize and access this energy. The identification of its role in sulfur metabolism here, may assist taxonomic classification and facilitate better understanding of the potential for sulfur metabolism across all Acidithiobacilli (Nuñez et al, 2017;Cao et al, 2018;Koch and Dahl, 2018;Wang et al, 2019) and other sulfur oxidizing microbes.…”