Elemental sulfur reduction by a deep‐sea hydrothermal vent CampylobacteriumSulfurimonassp.NW10

Abstract

Summary Sulfurimonas species (class Campylobacteria, phylum Campylobacterota) were globally distributed and especially predominant in deep‐sea hydrothermal environments. They were previously identified as chemolithoautotrophic sulfur‐oxidizing bacteria (SOB), whereas little is known about their potential in sulfur reduction. In this report, we found that the elemental sulfur reduction is quite common in different species of genus Sulfurimonas. To gain insights into the sulfur reduction mechanism, growth tests, morphology observation, as well as genomic and transcriptomic analyses were performed on a deep‐sea hydrothermal vent bacterium Sulfurimonas sp. NW10. Scanning electron micrographs and dialysis tubing tests confirmed that elemental sulfur reduction occurred without direct contact of cells with sulfur particles while direct access strongly promoted bacterial growth. Furthermore, we demonstrated that most species of Sulfurimonas probably employ both periplasmic and cytoplasmic polysulfide reductases, encoded by genes psrA1B1CDE and psrA2B2, respectively, to accomplish cyclooctasulfur reduction. This is the first report showing two different sulfur reduction pathways coupled to different energy conservations could coexist in one sulfur‐reducing microorganism, and demonstrates that most bacteria of Sulfurimonas could employ both periplasmic and cytoplasmic polysulfide reductases to perform cyclooctasulfur reduction. The capability of sulfur reduction coupling with hydrogen oxidation may partially explain the prevalenceof Sulfurimonas in deep‐sea hydrothermal vent environments.

Characterization of Sulfurimonas hydrogeniphila sp. nov., a Novel Bacterium Predominant in Deep-Sea Hydrothermal Vents and Comparative Genomic Analyses of the Genus Sulfurimonas

“…Across the 274,621 deep-sea hydrothermal vent samples gathered in the IMNGS platform, the relative abundance of Sulfurimonas sp. NW10-like sequences (>97% similarity of 16S rRNA gene in length 1,447 bps) was more than 1% total sequence reads in 49% of the vent samples and more than 0.1-1% in 39% of the vent samples (Wang et al, 2020a). The highest relative abundance was found in a deep-sea hydrothermal vent fluid sample from the Pacific Ocean, accounting for 22.4% of the total 16S sequences (Wang et al, 2020a).…”

“…NW10-like sequences (>97% similarity of 16S rRNA gene in length 1,447 bps) was more than 1% total sequence reads in 49% of the vent samples and more than 0.1-1% in 39% of the vent samples (Wang et al, 2020a). The highest relative abundance was found in a deep-sea hydrothermal vent fluid sample from the Pacific Ocean, accounting for 22.4% of the total 16S sequences (Wang et al, 2020a). The relative high abundance and wide distribution of the new species highlight its importance in the biogeochemical cycles of sulfur in in situ hydrothermal environments.…”

“…When hydrogen was used as the energy source, strain NW10 T could respire element sulfur. The product of sulfur reduction was sulfide, which reached up to 42 µM at the late exponential phase in the medium (Wang et al, 2020a). As a chemolithoautotroph, strain NW10 T could not grow using any of the tested organic compounds as the carbon source.…”

“…To define the ecological roles of Sulfurimonas in deep-sea hydrothermal environments, culturable bacteria representing the predominant member in situ are required. Six potential novel species of genus Sulfurimonas were recently isolated from different marine environments, including three from deepsea hydrothermal vents, one from deep-sea sediment and two from coastal marine sediments (Wang et al, 2020a). Two isolates from coastal environments, S. xiamenensis 1-1N T and S. lithotrophica GYSZ_1 T , have been just assigned as novel species (Wang et al, 2020b).…”

“…Two isolates from coastal environments, S. xiamenensis 1-1N T and S. lithotrophica GYSZ_1 T , have been just assigned as novel species (Wang et al, 2020b). Bacteria of novel species, represented by strain NW10, were recently reported to predominate the bacterial population in in situ deep-sea hydrothermal vents globally (Wang et al, 2020a). To understand its environment adaptation and ecological role in hydrothermal ecosystems, we firstly characterized it via a polyphasic taxonomic approach as a novel species.…”