Dataset Information

Nitric oxide regulates perylenequinones biosynthesis in Shiraia bambusicola S4201 induced by hydrogen peroxide.

ABSTRACT: Shiraia bambusicola has been used as a traditional Chinese medicine for a long history. Its major medicinal active metabolites are perylenequinones, including hypocrellin A, elsinochrome A and so on. At present, the fermentation yield of perylenequinones is low, and its complex biosynthesis and regulatory pathways are still unclear. In this study, nitric oxide, as a downstream signal molecule of hydrogen peroxide, regulates the biosynthesis of perylenequinones. Exogenous addition of 0.01 mM sodium nitroprusside (nitric oxide donor) can promote perylenequinones production by 156% compared with the control. Further research found that hydrogen peroxide and nitric oxide increased the transcriptional level of the biosynthetic genes of hypocrellin A. The results showed that nitric oxide is involved in the biosynthesis and regulation of perylenequinones in Shiraia bambusicola as a signal molecule. In the future, the yield of perylenequinones can be increased by adding exogenous nitric oxide in fermentation.

SUBMITTER: Zhao N

PROVIDER: S-EPMC7840948 | biostudies-literature | 2021 Jan

REPOSITORIES: biostudies-literature

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Nitric oxide regulates perylenequinones biosynthesis in Shiraia bambusicola S4201 induced by hydrogen peroxide.

Zhao Ning N Yu Yingying Y Yue Yunxia Y Dou Mingzhu M Guo Bingjing B Yan Shuzhen S Chen Shuanglin S

Scientific reports 20210127 1

Shiraia bambusicola has been used as a traditional Chinese medicine for a long history. Its major medicinal active metabolites are perylenequinones, including hypocrellin A, elsinochrome A and so on. At present, the fermentation yield of perylenequinones is low, and its complex biosynthesis and regulatory pathways are still unclear. In this study, nitric oxide, as a downstream signal molecule of hydrogen peroxide, regulates the biosynthesis of perylenequinones. Exogenous addition of 0.01 mM sodi ...[more]

PMID: 33504905

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Project description:Hydrogen peroxide (H2O2) and nitric oxide (NO·) are toxic metabolites that immune cells use to attack pathogens. These antimicrobials can be present at the same time in phagosomes, and it remains unclear how bacteria deal with these insults when simultaneously present. Here, using Escherichia coli, we observed that simultaneous exposure to H2O2 and NO· leads to prioritized detoxification, where enzymatic removal of NO· is impeded until H2O2 has been eliminated. This phenomenon is reminiscent of carbon catabolite repression (CCR), where preferred carbon sources are catabolized prior to less desirable substrates; however, H2O2 and NO· are toxic, growth-inhibitory compounds rather than growth-promoting nutrients. To understand how NO· detoxification is delayed by H2O2 whereas H2O2 detoxification proceeds unimpeded, we confirmed that the effect depended on Hmp, which is the main NO· detoxification enzyme, and used an approach that integrated computational modeling and experimentation to delineate and test potential mechanisms. Plausible interactions included H2O2-dependent inhibition of hmp transcription and translation, direct inhibition of Hmp catalysis, and competition for reducing equivalents between Hmp and H2O2-degrading enzymes. Experiments illustrated that Hmp catalysis and NAD(P)H supply were not impaired by H2O2, whereas hmp transcription and translation were diminished. A dependence of this phenomenon on transcriptional regulation parallels CCR, and we found it to involve the transcriptional repressor NsrR. Collectively, these data suggest that bacterial regulation of growth inhibitor detoxification has similarities to the regulation of growth substrate consumption, which could have ramifications for infectious disease, bioremediation, and biocatalysis from inhibitor-containing feedstocks.IMPORTANCE Bacteria can be exposed to H2O2 and NO· concurrently within phagosomes. In such multistress situations, bacteria could have evolved to simultaneously degrade both toxic metabolites or preferentially detoxify one over the other. Here, we found that simultaneous exposure to H2O2 and NO· leads to prioritized detoxification, where detoxification of NO· is hampered until H2O2 has been eliminated. This phenomenon resembles CCR, where bacteria consume one substrate over others in carbon source mixtures. Further experimentation revealed a central role for transcriptional regulation in the prioritization of H2O2 over NO·, which is also important to CCR. This study suggests that regulatory scenarios observed in bacterial consumption of growth-promoting compound mixtures can be conserved in bacterial detoxification of toxic metabolite mixtures.

Dataset Information

Nitric oxide regulates perylenequinones biosynthesis in Shiraia bambusicola S4201 induced by hydrogen peroxide.

Publications

Nitric oxide regulates perylenequinones biosynthesis in Shiraia bambusicola S4201 induced by hydrogen peroxide.

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