Blue light promotes zero-valent sulfur production in a deep-sea bacterium.

Ruining Cai, Wanying He, Jing Zhang, Rui Liu, Ziyu Yin, Xin Zhang, Chaomin Sun

Journal: The EMBO journal 2023;42(12):e112514

PMID: 36946144

Abstract

Increasing evidence has shown that light exists in a diverse range of deep-sea environments. We unexpectedly found that blue light is necessary to produce excess zero-valent sulfur (ZVS) in Erythrobacter flavus 21-3, a bacterium that has been recently isolated from a deep-sea cold seep. E. flavus 21-3 is able to convert thiosulfate to ZVS using a novel thiosulfate oxidation pathway comprising a thiosulfate dehydrogenase (TsdA) and a thiosulfohydrolase (SoxB). Using proteomic, bacterial two-hybrid and heterologous expression assays, we found that the light-oxygen-voltage histidine kinase LOV-1477 responds to blue light and activates the diguanylate cyclase DGC-2902 to produce c-di-GMP. Subsequently, the PilZ domain-containing protein mPilZ-1753 binds to c-di-GMP and activates TsdA through direct interaction. Finally, Raman spectroscopy and gene knockout results verified that TsdA and two SoxB homologs cooperate to regulate ZVS production. As ZVS is an energy source for E. flavus 21-3, we propose that deep-sea blue light provides E. flavus 21-3 with a selective advantage in the cold seep, suggesting a previously unappreciated relationship between light-sensing pathways and sulfur metabolism in a deep-sea microorganism.

© 2023 The Authors.

Address: CAS Key Laboratory of Experimental Marine Biology & Center of Deep Sea Research, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, China.; Laboratory for Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, Qingdao, China.; College of Earth Science, University of Chinese Academy of Sciences, Beijing, China.; Center of Ocean Mega-Science, Chinese Academy of Sciences, Qingdao, China.; College of Earth Science, University of Chinese Academy of Sciences, Beijing, China.; Center of Ocean Mega-Science, Chinese Academy of Sciences, Qingdao, China.; CAS Key Laboratory of Marine Geology and Environment & Center of Deep Sea Research, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, China.; School of Life Sciences, Hebei University, Baoding, China.; CAS Key Laboratory of Experimental Marine Biology & Center of Deep Sea Research, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, China.; Laboratory for Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, Qingdao, China.; Center of Ocean Mega-Science, Chinese Academy of Sciences, Qingdao, China.
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