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

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.

Dynamically Quantifying Intracellular Elemental Sulfur and Predicting Pertinent Gene Transcription by Raman Spectroscopy in Living Cells

“…Remarkably, the thiosulfate group displayed a visible increase of the intracellular elemental sulfur compared to the control group on day 1 (Figure ). However, the relative expression levels of the sox or tsdA genes of no more than 2-fold upregulation during S 0 formation (Figure S6A) are inconsistent with the previous study . In addition, the genomic sequences indicated that T.…”

“…Currently, we cannot rule out the possible factors such as light or oxygen that initiates S 0 production in T. mangrovi. , In addition, T. mangrovi harbors the dsrABEFCHMKLJOP clusters encoding dissimilatory siroheme sulfite reductase and other proteins.…”

“…However, the relative expression levels of the sox or tsdA genes of no more than 2-fold upregulation during S 0 formation (Figure S6A) are inconsistent with the previous study. 36 In addition, the genomic sequences indicated that T. mangrovi is also capable of oxidizing sulfide to intracellular S 0 through the pathway of sulfide/quinone oxidoreductases (sqr). 17,35,37 Unlike previous reports, 38 despite a significant increase in S 0 observed in the sulfide group compared to the control group, the relative expression level of sqr only showed a marginal increase (Figure S6A).…”

Cyclic di‐GMP signaling—Where did you come from and where will you go?

“…Being fundamental and providing a wider perspective, but not often explored yet is the role of cyclic di‐GMP signaling in biogeochemical cycling. Promotion of biofilm formation on sulfur and pyrite, iron disulfide, the regulation of cytochrome c‐type proteins on the transcriptional level, involvement in the regulation of the abiotic sulfur cycle, and enhanced biofilm formation by anaerobic, oceanic ecosystem relevant electron acceptors couples cyclic di‐GMP signaling to the global abiotic sulfur cycle and biogeochemical and ancient energy conservation processes (Cai et al, 2023; Martin‐Rodriguez et al, 2021; Ng et al, 2020; Ruiz et al, 2012). Whether cyclic di‐GMP signaling is involved to a larger extent in the global abiotic or biotic sulfur cycle equally as in the global nitrogen and carbon cycles remains to be shown.…”

Seeing the light brings more food in the deep sea

“…The presence of potential cyclic di-GMP turnover proteins in deepest branching bacteria indicates that cyclic di-GMP is an ancient signaling molecule. In this issue of The EMBO Journal, Cai et al (2023) B ioinformatic analyses pinpoint cyclic di-GMP as the most abundant second messenger in bacteria. Ubiquitously regulating the lifestyle transition between sessility and motility, this signaling molecule has been mainly investigated in animal and plant pathogens, where it not only regulates the trade-off between environmental survival versus acute virulence but also directs the intracellular lifestyle of microbes (Ro ¨mling et al, 2013).…”