Deep-sea in situ and laboratory proteomics provide insights into the sulfur metabolism of a novel deep-sea bacterium, Pseudodesulfovibrio serpens sp. nov.

Sulfate-reducing bacteria (SRB) are ubiquitously distributed across various biospheres and play key roles in global sulfur cycles. However, few deep-sea SRB have been cultivated and studied in situ, limiting our understanding of the true metabolism of SRB in the deep biosphere. Here, we firstly clarified the high abundance of SRB in deep-sea cold seep sediments and successfully isolated a sulfate-reducing bacterium (strain zrk46). Our genomic, physiological and phylogenetic analyses indicate that strain zrk46 is a novel species, which we propose as Pseudodesulfovibrio serpens. Based on the combined results from growth assays and proteomic analyses, we found that supplementation with sulfate (SO42-), thiosulfate (S2O32-), or sulfite (SO32-) promoted the growth of strain zrk46 by facilitating energy production through the dissimilatory sulfate reduction with the auxiliary functions of heterodisulfide reductases, ferredoxins, and nitrate reduction associated proteins, which were coupled with the oxidation of environmental organic matter in both laboratory and deep-sea in situ conditions. Moreover, metatranscriptomic results confirmed the dissimilatory sulfate reduction of deep-sea SRB in deep-sea environment, which might be coupled to the methane oxidation of anaerobic methanotrophic archaea (ANME-2) through direct interspecies electron transfer via cytochromes. IMPORTANCEThe deep-sea cold seep sediments were ideal habitats for uncovering diverse metabolisms of SRB. Unfortunately, the paucity of SRB isolates has limited further insights into their physiological and metabolic features as well as ecological roles. In the present study, we demonstrated the high abundance of SRB in the deep-sea cold seep sediments and isolated a sulfate-reducing bacterium. Our results demonstrate that the existence of dissimilatory sulfate reduction of strain zrk46 in both laboratory and deep-sea in situ environments, accompanied by the auxiliary effect of heterodisulfide reductases, ferredoxins, and nitrate reduction associated proteins. Our findings also unravel that the sulfate reduction of deep-sea SRB in in situ environment might be coupled to the methane oxidation of ANME-2. Overall, these findings expand our understanding of deep-sea SRB, while highlighting their importance for deep-sea elemental cycles.