High hydrostatic pressure enhanced the growth of deep-sea Thermococcus aciditolerans by promoting the reduction of elemental sulfur
Thermococcus 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 n...
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Frontiers Media S.A.
2025-08-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2025.1643593/full |
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| author | Ze-Xi Jiao Ze-Xi Jiao Xue-Gong Li Xue-Gong Li Xue-Gong Li Wei-Jia Zhang Wei-Jia Zhang Wei-Jia Zhang Guan-Yuan Zhang Guan-Yuan Zhang Shi-Jie Bai Ling Fu Long-Fei Wu Long-Fei Wu |
| author_facet | Ze-Xi Jiao Ze-Xi Jiao Xue-Gong Li Xue-Gong Li Xue-Gong Li Wei-Jia Zhang Wei-Jia Zhang Wei-Jia Zhang Guan-Yuan Zhang Guan-Yuan Zhang Shi-Jie Bai Ling Fu Long-Fei Wu Long-Fei Wu |
| author_sort | Ze-Xi Jiao |
| collection | DOAJ |
| description | Thermococcus 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 Thermococcus 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 mbs and mbh expression. Our results demonstrate that HHP enhances both S° reduction and growth in SY113 strain, independent of the general regulator SurR. Genetic disruption of mbsL significantly impaired H2S production and growth under HHP conditions, establishing the essential role of S° reduction in HHP adaptation. Furthermore, disrupted mbhL1 gene confirmed that a single MBS complex is sufficient to maintain pressure-stimulated growth. The gene expression analysis revealed that the expression of mbsL gene is primarily promoted by S°, while the expression of mbhL1 gene is induced by HHP. Moreover, the expression of these genes exhibits correlation. Additionally, we found that the expression of mbsL gene, mbhL1 gene, and mbhL2 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 Thermococcus species used to dwell in the deep-sea hydrothermal vent. |
| format | Article |
| id | doaj-art-7ecb05adfeb84ad1b04141a4811c09d0 |
| institution | DOAJ |
| issn | 1664-302X |
| language | English |
| publishDate | 2025-08-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj-art-7ecb05adfeb84ad1b04141a4811c09d02025-08-20T03:06:58ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2025-08-011610.3389/fmicb.2025.16435931643593High hydrostatic pressure enhanced the growth of deep-sea Thermococcus aciditolerans by promoting the reduction of elemental sulfurZe-Xi Jiao0Ze-Xi Jiao1Xue-Gong Li2Xue-Gong Li3Xue-Gong Li4Wei-Jia Zhang5Wei-Jia Zhang6Wei-Jia Zhang7Guan-Yuan Zhang8Guan-Yuan Zhang9Shi-Jie Bai10Ling Fu11Long-Fei Wu12Long-Fei Wu13Laboratory of Deep-Sea Microbial Cell Biology, Institute of Deep-Sea Science and Engineering, Chinese Academy of Sciences, Sanya, ChinaCollege of Marine Sciences, University of Chinese Academy of Sciences, Beijing, ChinaLaboratory of Deep-Sea Microbial Cell Biology, Institute of Deep-Sea Science and Engineering, Chinese Academy of Sciences, Sanya, ChinaInternational Associated Laboratory of Evolution and Development of Magnetotactic Multicellular Organisms, CNRS-Marseille/CAS, Sanya, ChinaHainan Deep-Sea Technology Laboratory, Institution of Deep-Sea Life Sciences, IDSSE-BGI, Sanya, Hainan, ChinaLaboratory of Deep-Sea Microbial Cell Biology, Institute of Deep-Sea Science and Engineering, Chinese Academy of Sciences, Sanya, ChinaInternational Associated Laboratory of Evolution and Development of Magnetotactic Multicellular Organisms, CNRS-Marseille/CAS, Sanya, ChinaHainan Deep-Sea Technology Laboratory, Institution of Deep-Sea Life Sciences, IDSSE-BGI, Sanya, Hainan, ChinaLaboratory of Deep-Sea Microbial Cell Biology, Institute of Deep-Sea Science and Engineering, Chinese Academy of Sciences, Sanya, ChinaCollege of Marine Sciences, University of Chinese Academy of Sciences, Beijing, ChinaLaboratory of Marine Viruses and Molecular Biology, Institute of Deep-Sea Science and Engineering, Chinese Academy of Sciences, Sanya, ChinaState Key Laboratory of Proteomics, Beijing Proteome Research Center, National Center for Protein Sciences Beijing, Beijing Institute of Lifeomics, Beijing, ChinaInternational Associated Laboratory of Evolution and Development of Magnetotactic Multicellular Organisms, CNRS-Marseille/CAS, Sanya, ChinaCNRS, LCB, IMM, IM2B, Aix Marseille University, Marseille, FranceThermococcus 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 Thermococcus 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 mbs and mbh expression. Our results demonstrate that HHP enhances both S° reduction and growth in SY113 strain, independent of the general regulator SurR. Genetic disruption of mbsL significantly impaired H2S production and growth under HHP conditions, establishing the essential role of S° reduction in HHP adaptation. Furthermore, disrupted mbhL1 gene confirmed that a single MBS complex is sufficient to maintain pressure-stimulated growth. The gene expression analysis revealed that the expression of mbsL gene is primarily promoted by S°, while the expression of mbhL1 gene is induced by HHP. Moreover, the expression of these genes exhibits correlation. Additionally, we found that the expression of mbsL gene, mbhL1 gene, and mbhL2 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 Thermococcus species used to dwell in the deep-sea hydrothermal vent.https://www.frontiersin.org/articles/10.3389/fmicb.2025.1643593/fullThermococcus aciditolerans SY113high hydrostatic pressureelemental sulfur reductionmembrane-bound sulfane reductasemembrane-bound hydrogenaseSurR |
| spellingShingle | Ze-Xi Jiao Ze-Xi Jiao Xue-Gong Li Xue-Gong Li Xue-Gong Li Wei-Jia Zhang Wei-Jia Zhang Wei-Jia Zhang Guan-Yuan Zhang Guan-Yuan Zhang Shi-Jie Bai Ling Fu Long-Fei Wu Long-Fei Wu High hydrostatic pressure enhanced the growth of deep-sea Thermococcus aciditolerans by promoting the reduction of elemental sulfur Frontiers in Microbiology Thermococcus aciditolerans SY113 high hydrostatic pressure elemental sulfur reduction membrane-bound sulfane reductase membrane-bound hydrogenase SurR |
| title | High hydrostatic pressure enhanced the growth of deep-sea Thermococcus aciditolerans by promoting the reduction of elemental sulfur |
| title_full | High hydrostatic pressure enhanced the growth of deep-sea Thermococcus aciditolerans by promoting the reduction of elemental sulfur |
| title_fullStr | High hydrostatic pressure enhanced the growth of deep-sea Thermococcus aciditolerans by promoting the reduction of elemental sulfur |
| title_full_unstemmed | High hydrostatic pressure enhanced the growth of deep-sea Thermococcus aciditolerans by promoting the reduction of elemental sulfur |
| title_short | High hydrostatic pressure enhanced the growth of deep-sea Thermococcus aciditolerans by promoting the reduction of elemental sulfur |
| title_sort | high hydrostatic pressure enhanced the growth of deep sea thermococcus aciditolerans by promoting the reduction of elemental sulfur |
| topic | Thermococcus aciditolerans SY113 high hydrostatic pressure elemental sulfur reduction membrane-bound sulfane reductase membrane-bound hydrogenase SurR |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2025.1643593/full |
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