Light and polyphosphate kinase 2 cooperatively regulate the production of zero-valent sulfur in a deep-sea bacterium.

It is well established that different wavelengths of light exist in various deep-sea environments, and many deep-sea microorganisms have evolved specialized mechanisms for sensing and utilizing light energy. Our previous research found that blue light promotes zero-valent sulfur (ZVS) production in 21-3, a bacterium isolated from a deep-sea cold seep. Given that long-wavelength light is more prevalent in deep-sea environments, the present study investigates the mechanism by which 21-3 senses infrared light (wavelength 940 nm) and regulates ZVS production. We found that the bacteriophytochrome BPHP-15570 is responsible for sensing infrared light, which induces autophosphorylation of BPHP-15570, activating the diguanylate cyclase DGC-0450 for c-di-GMP biosynthesis. Subsequently, the PilZ domain-containing protein mPilZ-1753 binds to c-di-GMP, triggering a well-established ZVS production pathway involving thiosulfate dehydrogenase (TsdA) and two homologs of thiosulfohydrolases (SoxB). Notably, polyphosphate kinase 2 (PPK2) is recruited to compete for GTP, the direct precursor of c-di-GMP biosynthesis. This competition downregulates ZVS production as well as other important metabolic processes. This negative regulatory pathway helps the bacterium avoid excessive ZVS accumulation, which could be toxic to bacterial growth. Overall, 21-3 has evolved a sophisticated regulatory pathway to sense both blue and infrared light, triggering ZVS production. Our study provides a valuable model for understanding light utilization and its coupling with sulfur cycling in deep-sea environments.IMPORTANCEIt is widely believed that deep-sea ecosystems operate independently of light, relying primarily on chemical energy. However, the discovery of non-photosynthetic bacteria in various deep-sea environments that can sense and utilize light has challenged this assumption. In a recent study, we found that blue light significantly promotes the production of zero-valent sulfur (ZVS) in the deep-sea bacterium 21-3. Given that long-wavelength light is more prevalent in deep-sea environments, we investigated whether infrared light also plays a role in regulating ZVS production in 21-3. Our results indicate that infrared light does promote ZVS formation in this bacterium. We identified PPK2 as a negative regulator, maintaining intracellular ZVS at safe levels to prevent toxicity due to excessive accumulation. Overall, our study offers a valuable model for exploring how light is utilized and its interaction with microbial sulfur cycling in the extreme conditions of the deep sea.