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Distinct Roles of Shewanella oneidensis Thioredoxin in Regulation of Cellular Responses to Hydrogen and Organic Peroxides.

Identifieur interne : 000175 ( Main/Exploration ); précédent : 000174; suivant : 000176

Distinct Roles of Shewanella oneidensis Thioredoxin in Regulation of Cellular Responses to Hydrogen and Organic Peroxides.

Auteurs : Xue Feng [République populaire de Chine] ; Weining Sun [République populaire de Chine] ; Linggen Kong [République populaire de Chine] ; Haichun Gao [République populaire de Chine]

Source :

RBID : pubmed:31444207

Descripteurs français

English descriptors

Abstract

The thioredoxin (Trx) and glutaredoxin (Grx) antioxidant systems are deeply involved in bacterial response to oxidative stress, but to date, we know surprisingly little about the roles of these systems in response to reactive oxygen species (ROS) other than hydrogen peroxide (H2O2). In this study, we used Shewanella oneidensis, an environmental bacterium, as a research model to investigate the roles of Trx and Grx in oxidative stress response because it has functionally intertwined ROS responsive regulators OxyR and OhrR. We found that Trx1 is the major thiol/disulfide redox system and that in its absence a Grx system becomes essential under normal conditions. Although overshadowed by Trx1 in the wild type, Trx2 can fully replace Trx1 in physiology when overproduced. Trx1 is required for OxyR to function as a repressor but, more importantly, plays a critical role in the cellular response to organic peroxide (OP) by mediating the redox status of OhrR but not OP scavenger OhrA. While none of the trx and grx genes are OxyR dependent, trxA and trxC are affected by OhrR indirectly. Additional data suggest that depletion of glutathione is likely the cue to trigger induced expression of trxA and trxC These findings underscore the particular importance of Trx in the bacterial OP stress response.IMPORTANCE The Trx and Grx systems are deeply involved in bacterial responses to H2O2-induced oxidative stress. However, little is known about their roles in response to other ROS, such as organic peroxides (OPs). In this study, we used S. oneidensis as a research model to investigate the interplay between Trx/Grx and OxyR/OhrR. We show that Trxs mediate the redox status of transcriptional OP-responding regulator OhrR. Although none of the trx or grx genes are directly controlled by OxyR or OhrR, expression of trxA and trxC is induced by tert-butyl hydroperoxide (t-BHP). We further show that the trxA and trxC genes respond to effects of glutathione (GSH) depletion rather than oxidation. These findings underscore the particular importance of Trx in the bacterial OP stress response.

DOI: 10.1128/AEM.01700-19
PubMed: 31444207
PubMed Central: PMC6803319


Affiliations:


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<term>Bacterial Proteins (genetics)</term>
<term>Gene Expression Regulation, Bacterial (MeSH)</term>
<term>Genes, Bacterial (genetics)</term>
<term>Glutaredoxins (metabolism)</term>
<term>Hydrogen (metabolism)</term>
<term>Hydrogen Peroxide (metabolism)</term>
<term>Hydrogen Peroxide (pharmacology)</term>
<term>Microbial Sensitivity Tests (MeSH)</term>
<term>Mutagenesis (MeSH)</term>
<term>Mutation (MeSH)</term>
<term>Oxidation-Reduction (MeSH)</term>
<term>Oxidative Stress (MeSH)</term>
<term>Peroxides (metabolism)</term>
<term>Reactive Oxygen Species (metabolism)</term>
<term>Shewanella (drug effects)</term>
<term>Shewanella (genetics)</term>
<term>Shewanella (metabolism)</term>
<term>Thioredoxins (genetics)</term>
<term>Thioredoxins (metabolism)</term>
<term>tert-Butylhydroperoxide (metabolism)</term>
<term>tert-Butylhydroperoxide (pharmacology)</term>
</keywords>
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<term>Espèces réactives de l'oxygène (métabolisme)</term>
<term>Glutarédoxines (métabolisme)</term>
<term>Gènes bactériens (génétique)</term>
<term>Hydrogène (métabolisme)</term>
<term>Mutagenèse (MeSH)</term>
<term>Mutation (MeSH)</term>
<term>Oxydoréduction (MeSH)</term>
<term>Peroxyde d'hydrogène (métabolisme)</term>
<term>Peroxyde d'hydrogène (pharmacologie)</term>
<term>Peroxydes (métabolisme)</term>
<term>Protéines bactériennes (génétique)</term>
<term>Régulation de l'expression des gènes bactériens (MeSH)</term>
<term>Shewanella (effets des médicaments et des substances chimiques)</term>
<term>Shewanella (génétique)</term>
<term>Shewanella (métabolisme)</term>
<term>Stress oxydatif (MeSH)</term>
<term>Tests de sensibilité microbienne (MeSH)</term>
<term>Thiorédoxines (génétique)</term>
<term>Thiorédoxines (métabolisme)</term>
</keywords>
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<term>Bacterial Proteins</term>
<term>Thioredoxins</term>
</keywords>
<keywords scheme="MESH" qualifier="drug effects" xml:lang="en">
<term>Shewanella</term>
</keywords>
<keywords scheme="MESH" qualifier="effets des médicaments et des substances chimiques" xml:lang="fr">
<term>Shewanella</term>
</keywords>
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<term>Genes, Bacterial</term>
<term>Shewanella</term>
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<term>Gènes bactériens</term>
<term>Protéines bactériennes</term>
<term>Shewanella</term>
<term>Thiorédoxines</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en">
<term>Glutaredoxins</term>
<term>Hydrogen</term>
<term>Hydrogen Peroxide</term>
<term>Peroxides</term>
<term>Reactive Oxygen Species</term>
<term>Shewanella</term>
<term>Thioredoxins</term>
<term>tert-Butylhydroperoxide</term>
</keywords>
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<term>2-Hydroperoxy-2-méthyl-propane</term>
<term>Espèces réactives de l'oxygène</term>
<term>Glutarédoxines</term>
<term>Hydrogène</term>
<term>Peroxyde d'hydrogène</term>
<term>Peroxydes</term>
<term>Shewanella</term>
<term>Thiorédoxines</term>
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<keywords scheme="MESH" qualifier="pharmacologie" xml:lang="fr">
<term>2-Hydroperoxy-2-méthyl-propane</term>
<term>Peroxyde d'hydrogène</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="pharmacology" xml:lang="en">
<term>Hydrogen Peroxide</term>
<term>tert-Butylhydroperoxide</term>
</keywords>
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<term>Gene Expression Regulation, Bacterial</term>
<term>Microbial Sensitivity Tests</term>
<term>Mutagenesis</term>
<term>Mutation</term>
<term>Oxidation-Reduction</term>
<term>Oxidative Stress</term>
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<term>Mutagenèse</term>
<term>Mutation</term>
<term>Oxydoréduction</term>
<term>Régulation de l'expression des gènes bactériens</term>
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<front>
<div type="abstract" xml:lang="en">The thioredoxin (Trx) and glutaredoxin (Grx) antioxidant systems are deeply involved in bacterial response to oxidative stress, but to date, we know surprisingly little about the roles of these systems in response to reactive oxygen species (ROS) other than hydrogen peroxide (H
<sub>2</sub>
O
<sub>2</sub>
). In this study, we used
<i>Shewanella oneidensis</i>
, an environmental bacterium, as a research model to investigate the roles of Trx and Grx in oxidative stress response because it has functionally intertwined ROS responsive regulators OxyR and OhrR. We found that Trx1 is the major thiol/disulfide redox system and that in its absence a Grx system becomes essential under normal conditions. Although overshadowed by Trx1 in the wild type, Trx2 can fully replace Trx1 in physiology when overproduced. Trx1 is required for OxyR to function as a repressor but, more importantly, plays a critical role in the cellular response to organic peroxide (OP) by mediating the redox status of OhrR but not OP scavenger OhrA. While none of the
<i>trx</i>
and
<i>grx</i>
genes are OxyR dependent,
<i>trxA</i>
and
<i>trxC</i>
are affected by OhrR indirectly. Additional data suggest that depletion of glutathione is likely the cue to trigger induced expression of
<i>trxA</i>
and
<i>trxC</i>
These findings underscore the particular importance of Trx in the bacterial OP stress response.
<b>IMPORTANCE</b>
The Trx and Grx systems are deeply involved in bacterial responses to H
<sub>2</sub>
O
<sub>2</sub>
-induced oxidative stress. However, little is known about their roles in response to other ROS, such as organic peroxides (OPs). In this study, we used
<i>S. oneidensis</i>
as a research model to investigate the interplay between Trx/Grx and OxyR/OhrR. We show that Trxs mediate the redox status of transcriptional OP-responding regulator OhrR. Although none of the
<i>trx</i>
or
<i>grx</i>
genes are directly controlled by OxyR or OhrR, expression of
<i>trxA</i>
and
<i>trxC</i>
is induced by
<i>tert</i>
-butyl hydroperoxide (
<i>t</i>
-BHP). We further show that the
<i>trxA</i>
and
<i>trxC</i>
genes respond to effects of glutathione (GSH) depletion rather than oxidation. These findings underscore the particular importance of Trx in the bacterial OP stress response.</div>
</front>
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<Abstract>
<AbstractText>The thioredoxin (Trx) and glutaredoxin (Grx) antioxidant systems are deeply involved in bacterial response to oxidative stress, but to date, we know surprisingly little about the roles of these systems in response to reactive oxygen species (ROS) other than hydrogen peroxide (H
<sub>2</sub>
O
<sub>2</sub>
). In this study, we used
<i>Shewanella oneidensis</i>
, an environmental bacterium, as a research model to investigate the roles of Trx and Grx in oxidative stress response because it has functionally intertwined ROS responsive regulators OxyR and OhrR. We found that Trx1 is the major thiol/disulfide redox system and that in its absence a Grx system becomes essential under normal conditions. Although overshadowed by Trx1 in the wild type, Trx2 can fully replace Trx1 in physiology when overproduced. Trx1 is required for OxyR to function as a repressor but, more importantly, plays a critical role in the cellular response to organic peroxide (OP) by mediating the redox status of OhrR but not OP scavenger OhrA. While none of the
<i>trx</i>
and
<i>grx</i>
genes are OxyR dependent,
<i>trxA</i>
and
<i>trxC</i>
are affected by OhrR indirectly. Additional data suggest that depletion of glutathione is likely the cue to trigger induced expression of
<i>trxA</i>
and
<i>trxC</i>
These findings underscore the particular importance of Trx in the bacterial OP stress response.
<b>IMPORTANCE</b>
The Trx and Grx systems are deeply involved in bacterial responses to H
<sub>2</sub>
O
<sub>2</sub>
-induced oxidative stress. However, little is known about their roles in response to other ROS, such as organic peroxides (OPs). In this study, we used
<i>S. oneidensis</i>
as a research model to investigate the interplay between Trx/Grx and OxyR/OhrR. We show that Trxs mediate the redox status of transcriptional OP-responding regulator OhrR. Although none of the
<i>trx</i>
or
<i>grx</i>
genes are directly controlled by OxyR or OhrR, expression of
<i>trxA</i>
and
<i>trxC</i>
is induced by
<i>tert</i>
-butyl hydroperoxide (
<i>t</i>
-BHP). We further show that the
<i>trxA</i>
and
<i>trxC</i>
genes respond to effects of glutathione (GSH) depletion rather than oxidation. These findings underscore the particular importance of Trx in the bacterial OP stress response.</AbstractText>
<CopyrightInformation>Copyright © 2019 American Society for Microbiology.</CopyrightInformation>
</Abstract>
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<AffiliationInfo>
<Affiliation>Research Center of Siyuan Natural Pharmacy and Biotoxicology, College of Life Sciences, Zhejiang University, Hangzhou, Zhejiang, China.</Affiliation>
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</AffiliationInfo>
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<Affiliation>Research Center of Siyuan Natural Pharmacy and Biotoxicology, College of Life Sciences, Zhejiang University, Hangzhou, Zhejiang, China.</Affiliation>
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