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

Abstract

In Thermococcus barophilus, a piezophilic hyperthermophilic archaeon, the expression of several gene clusters, including those of energy metabolism, is modulated by hydrostatic pressure. In Thermococcales, SurR, a redox-sensitive transcriptional regulator that responds to sulfur availability, regulates genes involved in energy metabolism. To better understand how high hydrostatic pressure (HHP) influences the expression of energy metabolism genes, several gene deletion mutants including surR partial knockout, were constructed and analyzed under various culture conditions, including different hydrostatic pressures and the presence or absence of sulfur. Phenotypic analysis of the surR mutant revealed that SurR affects both growth and gene expression, independently of sulfur availability. This regulatory behavior differs from that observed in non-piezophilic Thermococcales species such as Pyrococcus furiosus and Thermococcus kodakarensis. These findings suggest that hydrostatic pressure influences the physiological role or functional state of SurR in T. barophilus, highlighting its adaptive versatility in extreme environments. IMPORTANCEThis 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 microbial life under extreme conditions and may have implications for biotechnology, particularly in designing pressure-resistant enzymes or metabolic pathways.