High hydrostatic pressure enhanced the growth of deep-sea Thermococcus aciditolerans by promoting the reduction of elemental sulfur

<i>Thermococcus</i> species are ubiquitously distributed across both shallow and deep-sea hydrothermal vent ecosystems. Elemental sulfur (S°) reduction plays a pivotal role in their energy metabolism. While extensive characterization of the MBS and MBH pathways, along with their SurR-dependent regulatory network, has been established in shallow-water model strains, understanding of the high hydrostatic pressure (HHP) and sulfur-responsive regulation of these pathways in deep-sea <i>Thermococcus</i> lineages remains limited. In this study, we investigated the effects of HHP on both growth and S° reduction in the deep-sea SY113 strain, as well as its regulatory impact on <i>mbs</i> and <i>mbh</i> expression. Our results demonstrate that HHP enhances both S° reduction and growth in SY113 strain, independent of the general regulator SurR. Genetic disruption of <i>mbsL</i> significantly impaired H₂S production and growth under HHP conditions, establishing the essential role of S° reduction in HHP adaptation. Furthermore, disrupted <i>mbhL1</i> gene confirmed that a single MBS complex is sufficient to maintain pressure-stimulated growth. The gene expression analysis revealed that the expression of <i>mbsL</i> gene is primarily promoted by S°, while the expression of <i>mbhL1</i> gene is induced by HHP. Moreover, the expression of these genes exhibits correlation. Additionally, we found that the expression of <i>mbsL</i> gene, <i>mbhL1</i> gene, and <i>mbhL2</i> gene in SY113 strain is not only regulated by SurR, and HHP also plays a role in modulating the expression of these genes. Overall, the sulfur responsive regulation of gene expression in SY113 strain distinguishes from that in the shallow model strains, which implies an adaptive strategy for <i>Thermococcus</i> species used to dwell in the deep-sea hydrothermal vent.