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Distinct H(2)O(2)-Scavenging System in Yersinia pseudotuberculosis: KatG and AhpC Act Together to Scavenge Endogenous Hydrogen Peroxide

To colonize in the digestive tract of animals and humans, Yersinia pseudotuberculosis has to deal with reactive oxygen species (ROS) produced by host cells and microbiota. However, an understanding of the ROS-scavenging systems and their regulation in this bacterium remains largely elusive. In this...

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Autores principales: Wan, Fen, Feng, Xue, Yin, Jianhua, Gao, Haichun
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8139631/
https://www.ncbi.nlm.nih.gov/pubmed/34025596
http://dx.doi.org/10.3389/fmicb.2021.626874
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author Wan, Fen
Feng, Xue
Yin, Jianhua
Gao, Haichun
author_facet Wan, Fen
Feng, Xue
Yin, Jianhua
Gao, Haichun
author_sort Wan, Fen
collection PubMed
description To colonize in the digestive tract of animals and humans, Yersinia pseudotuberculosis has to deal with reactive oxygen species (ROS) produced by host cells and microbiota. However, an understanding of the ROS-scavenging systems and their regulation in this bacterium remains largely elusive. In this study, we identified OxyR as the master transcriptional regulator mediating cellular responses to hydrogen peroxide (H(2)O(2)) in Y. pseudotuberculosis through genomics and transcriptomics analyses. OxyR activates transcription of diverse genes, especially the core members of its regulon, including those encoding catalases, peroxidases, and thiol reductases. The data also suggest that sulfur species and manganese may play a particular role in the oxidative stress response of Y. pseudotuberculosis. Among the three H(2)O(2)-scavenging systems in Y. pseudotuberculosis, catalase/peroxidase KatE functions as the primary scavenger for high levels of H(2)O(2); NADH peroxidase alkyl hydroperoxide reductase (AhpR) and catalase KatG together are responsible for removing low levels of H(2)O(2). The simultaneous loss of both AhpC (the peroxidatic component of AhpR) and KatG results in activation of OxyR. Moreover, we found that AhpC, unlike its well-characterized Escherichia coli counterpart, has little effect on protecting cells against toxicity of organic peroxides. These findings provide not only novel insights into the structural and functional diversity of bacterial H(2)O(2)-scavenging systems but also a basic understanding of how Y. pseudotuberculosis copes with oxidative stress.
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spelling pubmed-81396312021-05-22 Distinct H(2)O(2)-Scavenging System in Yersinia pseudotuberculosis: KatG and AhpC Act Together to Scavenge Endogenous Hydrogen Peroxide Wan, Fen Feng, Xue Yin, Jianhua Gao, Haichun Front Microbiol Microbiology To colonize in the digestive tract of animals and humans, Yersinia pseudotuberculosis has to deal with reactive oxygen species (ROS) produced by host cells and microbiota. However, an understanding of the ROS-scavenging systems and their regulation in this bacterium remains largely elusive. In this study, we identified OxyR as the master transcriptional regulator mediating cellular responses to hydrogen peroxide (H(2)O(2)) in Y. pseudotuberculosis through genomics and transcriptomics analyses. OxyR activates transcription of diverse genes, especially the core members of its regulon, including those encoding catalases, peroxidases, and thiol reductases. The data also suggest that sulfur species and manganese may play a particular role in the oxidative stress response of Y. pseudotuberculosis. Among the three H(2)O(2)-scavenging systems in Y. pseudotuberculosis, catalase/peroxidase KatE functions as the primary scavenger for high levels of H(2)O(2); NADH peroxidase alkyl hydroperoxide reductase (AhpR) and catalase KatG together are responsible for removing low levels of H(2)O(2). The simultaneous loss of both AhpC (the peroxidatic component of AhpR) and KatG results in activation of OxyR. Moreover, we found that AhpC, unlike its well-characterized Escherichia coli counterpart, has little effect on protecting cells against toxicity of organic peroxides. These findings provide not only novel insights into the structural and functional diversity of bacterial H(2)O(2)-scavenging systems but also a basic understanding of how Y. pseudotuberculosis copes with oxidative stress. Frontiers Media S.A. 2021-05-07 /pmc/articles/PMC8139631/ /pubmed/34025596 http://dx.doi.org/10.3389/fmicb.2021.626874 Text en Copyright © 2021 Wan, Feng, Yin and Gao. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Wan, Fen
Feng, Xue
Yin, Jianhua
Gao, Haichun
Distinct H(2)O(2)-Scavenging System in Yersinia pseudotuberculosis: KatG and AhpC Act Together to Scavenge Endogenous Hydrogen Peroxide
title Distinct H(2)O(2)-Scavenging System in Yersinia pseudotuberculosis: KatG and AhpC Act Together to Scavenge Endogenous Hydrogen Peroxide
title_full Distinct H(2)O(2)-Scavenging System in Yersinia pseudotuberculosis: KatG and AhpC Act Together to Scavenge Endogenous Hydrogen Peroxide
title_fullStr Distinct H(2)O(2)-Scavenging System in Yersinia pseudotuberculosis: KatG and AhpC Act Together to Scavenge Endogenous Hydrogen Peroxide
title_full_unstemmed Distinct H(2)O(2)-Scavenging System in Yersinia pseudotuberculosis: KatG and AhpC Act Together to Scavenge Endogenous Hydrogen Peroxide
title_short Distinct H(2)O(2)-Scavenging System in Yersinia pseudotuberculosis: KatG and AhpC Act Together to Scavenge Endogenous Hydrogen Peroxide
title_sort distinct h(2)o(2)-scavenging system in yersinia pseudotuberculosis: katg and ahpc act together to scavenge endogenous hydrogen peroxide
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8139631/
https://www.ncbi.nlm.nih.gov/pubmed/34025596
http://dx.doi.org/10.3389/fmicb.2021.626874
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