Light-induced carotenogenesis enhances growth and high hydrostatic pressure tolerance in a deep-sea bacterium by...

Deep-sea hydrothermal vents emit geothermal light, yet its ecological role in shaping microbial adaptation remains largely unexplored. To investigate this, we designed a custom cultivation system that simultaneously applies high hydrostatic pressure (HHP) and light and used it to isolate 12 bacterial strains from active chimney fragments collected at the Kairei hydrothermal field. All 12 isolates exhibited enhanced growth under light exposure. Among them, strain SY138, identified as a novel Microbacterium species, was selected for mechanistic investigation. Our results demonstrate that light exposure directly induces carotenoid biosynthesis in SY138, which in turn reduces intracellular reactive oxygen species (ROS) levels. Inhibition of carotenoid synthesis using fosmidomycin abolished both the ROS-lowering effect and the light-dependent growth promotion, confirming that carotenoids are essential for this physiological response. Notably, while HHP severely inhibited growth by elevating intracellular ROS, light-induced carotenogenesis effectively counteracted this oxidative stress and alleviated HHP-induced growth inhibition. Collectively, these findings uncover a previously unrecognized adaptive strategy, wherein deep-sea hydrothermal vent bacteria exploit geothermal light as an environmental signal to activate carotenoid-based antioxidant defenses, thereby enhancing their survival under HHP conditions. This study highlights a previously underappreciated role of light in microbial stress tolerance in extreme deep-sea ecosystems.IMPORTANCEDeep-sea hydrothermal vents harbor thriving ecosystems under extreme pressure and perpetual darkness, yet they have long been considered to be driven solely by chemosynthesis. The discovery of geothermal light has raised fundamental questions regarding its ecological role. Using a specialized cultivation system that simulates in situ high pressure and illumination, we isolated multiple light-responsive bacterial strains from a deep-sea vent, substantially expanding the known diversity of such microorganisms. Using Microbacterium sp. SY138 as a model, we uncovered a previously unrecognized adaptive strategy: these bacteria exploit light not as an energy source but as an environmental cue to preemptively activate carotenoid-based antioxidant defenses. This light-induced mechanism counteracts oxidative stress imposed by high pressure, a ubiquitous deep-sea stressor. Our findings reveal an unexpected interplay between light and pressure in the deep-sea environment, suggesting that light sensing could represent a more widespread and ecologically significant adaptive trait than previously recognized.