OxyR senses sulfane sulfur and activates the genes for its removal in Escherichia coli

Hou, Ningke; Yan, Zhenzhen; Fan, Kaili; Li, Huanjie; Zhao, Rui; Xia, Yongzhen; Xun, Luying; Liu, Huaiwei

doi:10.1016/j.redox.2019.101293

Cited by 45 publications

(61 citation statements)

References 68 publications

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“…S5) (35). This suggests either that OxyR does not respond directly to sulfane sulfur in A. baumannii as previously observed in E. coli (44) or that the induction of the OxyR regulon under these conditions is weak compared to the robust H 2 O 2 response. As a result, only a few members of the regulon are induced at or above our detection limits.…”

Section: Resultsmentioning

confidence: 55%

The Response of Acinetobacter baumannii to Hydrogen Sulfide Reveals Two Independent Persulfide-Sensing Systems and a Connection to Biofilm Regulation

Walsh

Wang

Edmonds

et al. 2020

mBio

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Acinetobacter baumannii is an opportunistic nosocomial pathogen that is the causative agent of several serious infections in humans, including pneumonia, sepsis, and wound and burn infections. A. baumannii is also capable of forming proteinaceous biofilms on both abiotic and epithelial cell surfaces. Here, we investigate the response of A. baumannii toward sodium sulfide (Na2S), known to be associated with some biofilms at oxic/anoxic interfaces. The addition of exogenous inorganic sulfide reveals that A. baumannii encodes two persulfide-sensing transcriptional regulators, a primary σ54-dependent transcriptional activator (FisR), and a secondary system controlled by the persulfide-sensing biofilm growth-associated repressor (BigR), which is only induced by sulfide in a fisR deletion strain. FisR activates an operon encoding a sulfide oxidation/detoxification system similar to that characterized previously in Staphylococcus aureus, while BigR regulates a secondary persulfide dioxygenase (PDO2) as part of yeeE-yedE-pdo2 sulfur detoxification operon, found previously in Serratia spp. Global S-sulfuration (persulfidation) mapping of the soluble proteome reveals 513 persulfidation targets well beyond FisR-regulated genes and includes five transcriptional regulators, most notably the master biofilm regulator BfmR and a poorly characterized catabolite regulatory protein (Crp). Both BfmR and Crp are well known to impact biofilm formation in A. baumannii and other organisms, respectively, suggesting that persulfidation of these regulators may control their activities. The implications of these findings on bacterial sulfide homeostasis, persulfide signaling, and biofilm formation are discussed. IMPORTANCE Although hydrogen sulfide (H2S) has long been known as a respiratory poison, recent reports in numerous bacterial pathogens reveal that H2S and more downstream oxidized forms of sulfur collectedly termed reactive sulfur species (RSS) function as antioxidants to combat host efforts to clear the infection. Here, we present a comprehensive analysis of the transcriptional and proteomic response of A. baumannii to exogenous sulfide as a model for how this important human pathogen manages sulfide/RSS homeostasis. We show that A. baumannii is unique in that it encodes two independent persulfide sensing and detoxification pathways that govern the speciation of bioactive sulfur in cells. The secondary persulfide sensor, BigR, impacts the expression of biofilm-associated genes; in addition, we identify two other transcriptional regulators known or projected to regulate biofilm formation, BfmR and Crp, as highly persulfidated in sulfide-exposed cells. These findings significantly strengthen the connection between sulfide homeostasis and biofilm formation in an important human pathogen.

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Section: Resultsmentioning

confidence: 55%

The Response of Acinetobacter baumannii to Hydrogen Sulfide Reveals Two Independent Persulfide-Sensing Systems and a Connection to Biofilm Regulation

Walsh

Wang

Edmonds

et al. 2020

mBio

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“…Recently, it was shown that the signaling role of H 2 S is via sulfane sulfur, which is sensed by gene regulators that activate the genes involved in H 2 S oxidation in bacteria (51)(52)(53). OxyR also senses high levels of cellular sulfane sulfur to produce enzymes for its removal (54). Our evidence suggests that sulfane sulfur is likely involved in regulating photosynthetic genes ( Fig.…”

Section: Discussionmentioning

confidence: 64%

Synechococcus sp. Strain PCC7002 Uses Sulfide:Quinone Oxidoreductase To Detoxify Exogenous Sulfide and To Convert Endogenous Sulfide to Cellular Sulfane Sulfur

Liu

Zhang

Lü

et al. 2020

mBio

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Eutrophication and deoxygenation possibly occur in coastal waters due to excessive nutrients from agricultural and aquacultural activities, leading to sulfide accumulation. Cyanobacteria, as photosynthetic prokaryotes, play significant roles in carbon fixation in the ocean. Although some cyanobacteria can use sulfide as the electron donor for photosynthesis under anaerobic conditions, little is known on how they interact with sulfide under aerobic conditions. In this study, we report that Synechococcus sp. strain PCC7002 (PCC7002), harboring an sqr gene encoding sulfide:quinone oxidoreductase (SQR), oxidized self-produced sulfide to S0, present as persulfide and polysulfide in the cell. The Δsqr mutant contained less cellular S0 and had increased expression of key genes involved in photosynthesis, but it was less competitive than the wild type in cocultures. Further, PCC7002 with SQR and persulfide dioxygenase (PDO) oxidized exogenous sulfide to tolerate high sulfide levels. Thus, SQR offers some benefits to cyanobacteria even under aerobic conditions, explaining the common presence of SQR in cyanobacteria. IMPORTANCE Cyanobacteria are a major force for primary production via oxygenic photosynthesis in the ocean. A marine cyanobacterium, PCC7002, is actively involved in sulfide metabolism. It uses SQR to detoxify exogenous sulfide, enabling it to survive better than its Δsqr mutant in sulfide-rich environments. PCC7002 also uses SQR to oxidize endogenously generated sulfide to S0, which is required for the proper expression of key genes involved in photosynthesis. Thus, SQR has at least two physiological functions in PCC7002. The observation provides a new perspective for the interplays of C and S cycles.

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“…Previously, we discovered that deleting OxyR, the redox-sensitive transcriptional factor, in E. coli BL21 leads to a notable increase in its intracellular polysulfide level ( 11 ). On the basis of the conclusion of the report ( 10 ), we speculated that the protein persulfidation level should also be higher in E. coli BL21Δ oxyR than in E. coli BL21 wild type (wt).…”

Section: Resultsmentioning

confidence: 99%

Evidence that the ProPerDP method is inadequate for protein persulfidation detection due to lack of specificity

2020

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Protein persulfidation (protein-SSH) is a previously unidentified type of modification found in both eukaryotic and prokaryotic cells in recent years. Although a few persulfidated proteins have been identified, analyzing protein persulfidation from a proteomic level is still a big challenge. ProPerDP is a persulfidation detection method recently reported in Science Advances. The authors claimed that this method could specifically detect persulfidated proteins of cell lysate with minor false-positive hits; hence, it could be used for proteomic-level analysis of protein persulfidation. However, when using this method for Escherichia coli cell lysate analysis, we found that the percentage of false-positive hit was >90%. We performed a systematic study on this method and discovered that iodoacetyl-PEG2-biotin tag mislabeling is the reason causing this low specificity. We concluded that the ProPerDP method is completely inadequate for persulfidation analysis. The previous findings based on the ProPerDP method need to be reinvestigated.

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OxyR senses sulfane sulfur and activates the genes for its removal in Escherichia coli

Cited by 45 publications

References 68 publications

The Response of Acinetobacter baumannii to Hydrogen Sulfide Reveals Two Independent Persulfide-Sensing Systems and a Connection to Biofilm Regulation

The Response of Acinetobacter baumannii to Hydrogen Sulfide Reveals Two Independent Persulfide-Sensing Systems and a Connection to Biofilm Regulation

Synechococcus sp. Strain PCC7002 Uses Sulfide:Quinone Oxidoreductase To Detoxify Exogenous Sulfide and To Convert Endogenous Sulfide to Cellular Sulfane Sulfur

Evidence that the ProPerDP method is inadequate for protein persulfidation detection due to lack of specificity

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