Regulation of gene expression under high hydrostatic pressure: the versatile role of the master regulator SurR in energy metabolism

Yann Moalic^1,2*Toan Bao Hung NGUYEN²Jordan Hartunians²Tiphaine Birien²Axel Thiel²Mohamed Jebbar^1*

• ¹ISEN Yncréa Ouest, Brest, France
• ²Université de Bretagne Occidentale, Brest, Brittany, France

In Thermococcales, energy metabolism genes are regulated by the sulfur-responsive transcriptional regulator SurR. In the piezophilic archaeon Thermococcus barophilus, these genes are also influenced by hydrostatic pressure. To explore the interaction between pressure, sulfur availability, and gene regulation, we constructed and analyzed several deletion mutants, including a partial surR knockout, under varying conditions.Our results show that hydrostatic pressure modulates the expression of energy metabolism genes and that SurR is essential for activating the hydrogenogenic gene cluster, even in sulfur-rich environments. Under sulfur limitation, the membrane-bound sulfur-reducing complex (MBS) is required for normal growth. These regulatory patterns expand current models derived from non-piezophilic species such as Pyrococcus furiosus and Thermococcus kodakarensis.Overall, our findings indicate that hydrostatic pressure shapes SurR function in T. barophilus, reflecting its adaptive plasticity in extreme environments.Extremophiles possess a range of evolved adaptation mechanisms that enable their survival under diverse stress conditions in unique environments (high temperature, high salinity, low pH…). This study provides new insights into the adaptive mechanisms of hyperthermophilic archaea to high hydrostatic pressure, a key factor in deep-sea environments. By demonstrating that SurR regulation differs in T. barophilus compared to non-piezophilic species, it suggests that pressure can modify transcriptional control mechanisms, potentially reshaping energy metabolism strategies in deep-sea archaea. Understanding these regulatory adaptations contributes to our broader knowledge of metabolic flexibility under extreme conditions and may have implications for biotechnology, particularly in designing pressure-resistant enzymes or for performance optimization of cell factories.