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Title: An extracytoplasmic function sigma factor-dependent periplasmic glutathione peroxidase is involved in oxidative stress response of Shewanella oneidensis

Abstract

Background: Bacteria use alternative sigma factors (σs) to regulate condition-specific gene expression for survival and Shewanella harbors multiple ECF (extracytoplasmic function) σ genes and cognate anti-sigma factor genes. Here we comparatively analyzed two of the rpoE-like operons in the strain MR-1: rpoE-rseA-rseB-rseC and rpoE2-chrR. Results: RpoE was important for bacterial growth at low and high temperatures, in the minimal medium, and high salinity. The degP/htrA orthologue, required for growth of Escherichia coli and Pseudomonas aeruginosa at high temperature, is absent in Shewanella, while the degQ gene is RpoE-regulated and is required for bacterial growth at high temperature. RpoE2 was essential for the optimal growth in oxidative stress conditions because the rpoE2 mutant was sensitive to hydrogen peroxide and paraquat. The operon encoding a ferrochelatase paralogue (HemH2) and a periplasmic glutathione peroxidase (PgpD) was identified as RpoE2-dependent. PgpD exhibited higher activities and played a more important role in the oxidative stress responses than the cytoplasmic glutathione peroxidase CgpD under tested conditions. The rpoE2-chrR operon and the identified regulon genes, including pgpD and hemH2, are coincidently absent in several psychrophilic and/or deep-sea Shewanella strains. Conclusion: In S. oneidensis MR-1, the RpoE-dependent degQ gene is required for optimal growth under high temperature. Themore » rpoE2 and RpoE2-dependent pgpD gene encoding a periplasmic glutathione peroxidase are involved in oxidative stress responses. But rpoE2 is not required for bacterial growth at low temperature and it even affected bacterial growth under salt stress, indicating that there is a tradeoff between the salt resistance and RpoE2-mediated oxidative stress responses.« less

Authors:
 [1];  [1];  [2];  [3];  [4];  [1]
  1. Chinese Academy of Sciences, Wuhan (China); Univ. of Chinese Academy of Sciences, Beijing (China)
  2. Hubei Univ. of Engineering, Xiaogan (China)
  3. Univ. of Virginia, Charlottesville, VA (United States)
  4. Univ. of Oklahoma, Norman, OK (United States)
Publication Date:
Research Org.:
Univ. of Oklahoma, Norman, OK (United States)
Sponsoring Org.:
USDOE; Chinese Academy of Science, Beijing (China)
OSTI Identifier:
1204353
Grant/Contract Number:  
FG02-07ER64383; Y15103-1-401
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
BMC Microbiology
Additional Journal Information:
Journal Volume: 15; Journal Issue: 1; Journal ID: ISSN 1471-2180
Publisher:
BioMed Central
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Periplasmic glutathione peroxidase; Shewanella; ECF sigma factor; Oxidative stress response

Citation Formats

Dai, Jingcheng, Wei, Hehong, Tian, Chunyuan, Damron, Fredrick, Zhou, Jizhong, and Qiu, Dongru. An extracytoplasmic function sigma factor-dependent periplasmic glutathione peroxidase is involved in oxidative stress response of Shewanella oneidensis. United States: N. p., 2015. Web. doi:10.1186/s12866-015-0357-0.
Dai, Jingcheng, Wei, Hehong, Tian, Chunyuan, Damron, Fredrick, Zhou, Jizhong, & Qiu, Dongru. An extracytoplasmic function sigma factor-dependent periplasmic glutathione peroxidase is involved in oxidative stress response of Shewanella oneidensis. United States. doi:10.1186/s12866-015-0357-0.
Dai, Jingcheng, Wei, Hehong, Tian, Chunyuan, Damron, Fredrick, Zhou, Jizhong, and Qiu, Dongru. Thu . "An extracytoplasmic function sigma factor-dependent periplasmic glutathione peroxidase is involved in oxidative stress response of Shewanella oneidensis". United States. doi:10.1186/s12866-015-0357-0. https://www.osti.gov/servlets/purl/1204353.
@article{osti_1204353,
title = {An extracytoplasmic function sigma factor-dependent periplasmic glutathione peroxidase is involved in oxidative stress response of Shewanella oneidensis},
author = {Dai, Jingcheng and Wei, Hehong and Tian, Chunyuan and Damron, Fredrick and Zhou, Jizhong and Qiu, Dongru},
abstractNote = {Background: Bacteria use alternative sigma factors (σs) to regulate condition-specific gene expression for survival and Shewanella harbors multiple ECF (extracytoplasmic function) σ genes and cognate anti-sigma factor genes. Here we comparatively analyzed two of the rpoE-like operons in the strain MR-1: rpoE-rseA-rseB-rseC and rpoE2-chrR. Results: RpoE was important for bacterial growth at low and high temperatures, in the minimal medium, and high salinity. The degP/htrA orthologue, required for growth of Escherichia coli and Pseudomonas aeruginosa at high temperature, is absent in Shewanella, while the degQ gene is RpoE-regulated and is required for bacterial growth at high temperature. RpoE2 was essential for the optimal growth in oxidative stress conditions because the rpoE2 mutant was sensitive to hydrogen peroxide and paraquat. The operon encoding a ferrochelatase paralogue (HemH2) and a periplasmic glutathione peroxidase (PgpD) was identified as RpoE2-dependent. PgpD exhibited higher activities and played a more important role in the oxidative stress responses than the cytoplasmic glutathione peroxidase CgpD under tested conditions. The rpoE2-chrR operon and the identified regulon genes, including pgpD and hemH2, are coincidently absent in several psychrophilic and/or deep-sea Shewanella strains. Conclusion: In S. oneidensis MR-1, the RpoE-dependent degQ gene is required for optimal growth under high temperature. The rpoE2 and RpoE2-dependent pgpD gene encoding a periplasmic glutathione peroxidase are involved in oxidative stress responses. But rpoE2 is not required for bacterial growth at low temperature and it even affected bacterial growth under salt stress, indicating that there is a tradeoff between the salt resistance and RpoE2-mediated oxidative stress responses.},
doi = {10.1186/s12866-015-0357-0},
journal = {BMC Microbiology},
issn = {1471-2180},
number = 1,
volume = 15,
place = {United States},
year = {2015},
month = {1}
}

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