The existence of light in various deep-sea environments has been well established. Our previous research found blue light promotes zero-valent sulfur (ZVS) production in Erythrobacter flavus 21-3, a bacterium isolated from the deep-sea cold seep. E. flavus 21-3 can convert thiosulfate to ZVS through a novel thiosulfate oxidation pathway comprising a thiosulfate dehydrogenase (TsdA) and two thiosulfohydrolases (SoxB). Using proteomic analysis, bacterial two-hybrid system and heterologous expression assays, we found that infrared light also promotes zero-valent sulfur (ZVS) production in E. flavus 21-3. The bacteriophytochrome (bphp) Ef2bphp-15570 autophosphorylated and activated GGDEF domain-containing protein D0Y83_RS00450 to produce c-di-GMP. Subsequently, the PilZ protein mPilZ-1753 bound to c-di-GMP and activated downstream sulfur oxidation pathways. During this process, polyphosphate kinase 2 (PPK2) affects the content of c-di-GMP by competing for GTP, thereby together c-di-GMP regulating ZVS production, as well as other metabolic processes in E. flavus 21-3. This study provides a novel insight into a deep-sea non-photosynthetic bacterium which sensing infrared light to regulate sulfur metabolism through a bacteriophytochrome photoreceptor, thus offering new understandings perspectives on microbial utilization of light energy.