Transcriptome Analysis of Cyclooctasulfur Oxidation and Reduction by the Neutrophilic Chemolithoautotrophic Sulfurovum indicum from Deep-Sea Hydrothermal Ecosystems

Abstract

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.