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Loss of OxyR reduces efficacy of oxygen respiration in Shewanella oneidensis.

ABSTRACT: In many bacteria, OxyR is the major regulator controlling cellular response to H₂O₂. A common phenotype resulting from OxyR loss is reduced growth rate, but the underlying mechanism is unknown. We demonstrated in Shewanella oneidensis, an important research model for applied and environmental microbes, that the defect is primarily due to an electron shortage to major terminal oxidase cytochrome cbb₃. The loss of OxyR leads to enhanced production of electron carriers that compete for electrons against cytochrome cbb₃, cytochrome bd in particular. We further showed that the oxyR mutation also results in increased production of menaquinone, an additional means to lessen electrons to cytochrome cbb₃. Although regulation of OxyR on these biological processes appears to be indirect, these data indicate that the regulator plays a previously underappreciated role in mediating respiration.

SUBMITTER: Wan F

PROVIDER: S-EPMC5307378 | biostudies-literature | 2017 Feb

REPOSITORIES: biostudies-literature

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Loss of OxyR reduces efficacy of oxygen respiration in Shewanella oneidensis.

Wan Fen F Shi Miaomiao M Gao Haichun H

Scientific reports 20170214

In many bacteria, OxyR is the major regulator controlling cellular response to H2O2. A common phenotype resulting from OxyR loss is reduced growth rate, but the underlying mechanism is unknown. We demonstrated in Shewanella oneidensis, an important research model for applied and environmental microbes, that the defect is primarily due to an electron shortage to major terminal oxidase cytochrome cbb3. The loss of OxyR leads to enhanced production of electron carri ...[more]

PMID: 28195212

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Project description:UnlabelledOxidative stresses triggered by reactive oxygen species (ROS) that damage various cellular components are unavoidable for virtually all living organisms. In defense, microorganisms have evolved sophisticated mechanisms to sense, respond to, and battle against ROS. Shewanella oneidensis, an important research model for applied and environmental microbes, employs OxyR to mediate the response to H2O2 by derepressing the production of the major H2O2 scavenger KatB as a major means toward these goals. Surprisingly, despite enhanced H2O2 degradation, the oxyR mutant carries a viability deficiency phenotype (plating defect), which can be suppressed by the addition of exogenous iron species. Experiments showed that the defect was not due to iron starvation. Rather, multiple lines of evidence suggested that H2O2 generated abiotically in lysogeny broth (LB) is responsible for the defect by quickly killing mutant cells. We then showed that the iron species suppressed the plating defect by two distinct mechanisms, either as an H2O2 scavenger without involving living cells or as an environmental cue to stimulate an OxyR-independent response to help cells cope with oxidative stress. Based on the suppression of the plating defect by overproduction of H2O2 scavengers in vivo, we propose that cellular components that are vulnerable to H2O2 and responsible for the defect may reside outside the cytoplasm.ImportanceIn bacteria, OxyR is the major regulator controlling the cellular response to H2O2. The loss of OxyR results in reduced viability in many species, but the underlying mechanism is unknown. We showed in S. oneidensis that this defect was due to H2O2 generated abiotically in LB. We then showed that this defect could be corrected by the addition of Fe(2+) or catalase to the LB or increased intracellular production of catalase. Further analyses revealed that Fe(2+) was able not only to decompose H2O2 directly but also to stimulate the activity of OxyR-independent H2O2-scavenging enzymes. Our data indicate that iron species play a previously underappreciated role in protecting cells from H2O2 in environments.

Dataset Information

Loss of OxyR reduces efficacy of oxygen respiration in Shewanella oneidensis.

Publications

Loss of OxyR reduces efficacy of oxygen respiration in Shewanella oneidensis.

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