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Chemolithoautotrophic Campylobacterota are widespread and predominant in worldwide hydrothermal vents, and they are key players in the turnover of zero-valence sulfur. However, at present, the mechanism of cyclooctasulfur activation and catabolism in Campylobacterota bacteria is not clearly understood. Here, we investigated these processes in a hydrothermal vent isolate named Sulfurovum indicum ST-419. A transcriptome analysis revealed that multiple genes related to biofilm formation were highly expressed during both sulfur oxidation and reduction. Additionally, biofilms containing cells and EPS coated on sulfur particles were observed by SEM, suggesting that biofilm formation may be involved in S0 activation in Sulfurovum species. Meanwhile, several genes encoding the outer membrane proteins of OprD family were also highly expressed, and among them, gene IMZ28_RS00565 exhibited significantly high expressions by 2.53- and 7.63-fold changes under both conditions, respectively, which may play a role in sulfur uptake. However, other mechanisms could be involved in sulfur activation and uptake, as experiments with dialysis bags showed that direct contact between cells and sulfur particles was not mandatory for sulfur reduction activity, whereas cell growth via sulfur oxidation did require direct contact. This indirect reaction could be ascribed to the role of H2S and/or other thiol-containing compounds, such as cysteine and GSH, which could be produced in the culture medium during sulfur reduction. In the periplasm, the sulfur-oxidation-multienzyme complexes soxABXY1Z1 and soxCDY2Z2 are likely responsible for thiosulfate oxidation and S0 oxidation, respectively. In addition, among the four psr gene clusters encoding polysulfide reductases, only psrA3B3C3 was significantly upregulated under the sulfur reduction condition, implying its essential role in sulfur reduction. These results expand our understanding of the interactions of Campylobacterota with the zero-valence sulfur and their adaptability to deep-sea hydrothermal environments. [ABSTRACT FROM AUTHOR]

The disproportionation of inorganic sulfur compounds could be widespread in natural habitats, and microorganisms could produce energy to support primary productivity through this catabolism. However, the microorganisms that carry this process out and the catabolic pathways at work remain relatively unstudied. Here, we investigated the bacterial diversity involved in sulfur disproportionation in hydrothermal plumes from Carlsberg Ridge in the northwestern Indian Ocean by enrichment cultures. A bacterial community analysis revealed that bacteria of the genera Sulfurimonas and Sulfurovum , belonging to the phylum Campylobacterota and previously having been characterized as chemolithoautotrophic sulfur oxidizers, were the most dominant members in six enrichment cultures. Subsequent bacterial isolation and physiological studies confirmed that five Sulfurimonas and Sulfurovum isolates could disproportionate thiosulfate and elemental sulfur. The ability to disproportionate sulfur was also demonstrated in several strains of Sulfurimonas and Sulfurovum that were isolated from hydrothermal vents or other natural environments. Dialysis membrane experiments showed that S 0 disproportionation did not require the direct contact of cells with bulk sulfur. A comparative genomic analysis showed that Campylobacterota strains did not contain some genes of the Dsr and rDSR pathways ( aprAB , dsrAB , dsrC , dsrMKJOP , and qmoABC ) that are involved in sulfur disproportionation in some other taxa, suggesting the existence of an unrevealed catabolic pathway for sulfur disproportionation. These findings provide evidence for the catabolic versatility of these Campylobacterota genera, which are widely distributed in chemosynthetic environments, and expand our knowledge of the microbial taxa involved in this reaction of the biogeochemical sulfur cycle in hydrothermal vent environments. IMPORTANCE The phylum Campylobacterota , notably represented by the genera Sulfurimonas and Sulfurovum , is ubiquitous and predominant in deep-sea hydrothermal systems. It is well-known to be the major chemolithoautotrophic sulfur-oxidizing group in these habitats. Herein, we show that the mesophilic predominant chemolithoautotrophs of the genera Sulfurimonas and Sulfurovum could grow via sulfur disproportionation to gain energy. This is the first report of the chemolithoautotrophic disproportionation of thiosulfate and elemental sulfur within the genera Sulfurimonas and Sulfurovum , and this comes in addition to their already known role in the chemolithoautotrophic oxidation of sulfur compounds. Sulfur disproportionation via chemolithoautotrophic Campylobacterota may represent a previously unrecognized primary production process in hydrothermal vent ecosystems.

A novel mesophilic, hydrogen-, and sulfur-oxidizing bacterium, designated strain ST-419 T , was isolated from a deep-sea hydrothermal vent plume on the Carlsberg Ridge of the Northwestern Indian Ocean. The isolate was a Gram-staining-negative, non-motile and coccoid to oval-shaped bacterium. Growth was observed at 4-50 °C (optimum 37 °C), pH 5.0-8.6 (optimum pH 6.0) and 1.0-5.0 % (w/v) NaCl (optimum 3.0 %). ST-419 T could grow chemlithoautotrophically with molecular hydrogen, sulfide, elemental sulfur and thiosulfate as energy sources. Molecular oxygen, nitrate and elemental sulfur could be used as electron acceptors. The predominant fatty acids were C 16 : 1 ω7 c , C 18 : 1 ω7 c and C 16 : 0 . The major polar lipids were phosphatidylethanolamine, diphosphatidylglycerol and phosphatidylglycerol. The respiratory quinone was menaquinone MK-6 and the G+C content of the genomic DNA was 42.4 mol%. Phylogenetic analysis based on 16S rRNA gene sequences revealed that ST-419 T represented a member of genus Sulfurovum and was most closely related to Sulfurovum riftiae 1812E T , with 97.6 % sequence similarity. The average nucleotide identity (ANI) and digital DNA-DNA hybridization (dDDH) values between ST-419 T and S. riftiae 1812E T were 74.6 and 19.6 %, respectively. The combined genotypic and phenotypic data indicate that ST-419 T represents a novel species within the genus Sulfurovum , for which the name Sulfurovum indicum sp. nov. is proposed. The type strain is ST-419 T (=MCCC 1A17954 T =KCTC 25164 T ).