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Title: Conserved ABC Transport System Regulated by the General Stress Response Pathways of Alpha- and Gammaproteobacteria

Abstract

Brucella abortus σ E1 is an EcfG family sigma factor that regulates the transcription of dozens of genes in response to diverse stress conditions and is required for maintenance of chronic infection in a mouse model. A putative ATP-binding cassette transporter operon, bab1_0223-bab1_0226, is among the most highly activated gene sets in the σ E1 regulon. The proteins encoded by the operon resemble quaternary ammonium-compatible solute importers but are most similar in sequence to the broadly conserved YehZYXW system, which remains largely uncharacterized. Transcription of yehZYXW is activated by the general stress sigma factor σ S in Enterobacteriaceae, which suggests a functional role for this transport system in bacterial stress response across the classes Alphaproteobacteria and Gammaproteobacteria. Here, we present evidence that B. abortus YehZYXW does not function as an importer of known compatible solutes under physiological conditions and does not contribute to the virulence defect of a σ E1-null strain. The sole in vitro phenotype associated with genetic disruption of this putative transport system is reduced growth in the presence of high Li + ion concentrations. A crystal structure of B. abortus YehZ revealed a class II periplasmic binding protein fold with significant structural homology to Archaeoglobus fulgidus ProX,more » which binds glycine betaine. However, the structure of the YehZ ligand-binding pocket is incompatible with high-affinity binding to glycine betaine. This is consistent with weak measured binding of YehZ to glycine betaine and related compatible solutes. We conclude that YehZYXW is a conserved, stress-regulated transport system that is phylogenetically and functionally distinct from quaternary ammonium-compatible solute importers.« less

Authors:
 [1];  [1];  [1];  [2];  [2];  [1]
  1. Univ. of Chicago, IL (United States)
  2. Argonne National Lab. (ANL), Argonne, IL (United States)
Publication Date:
Research Org.:
Argonne National Lab. (ANL), Argonne, IL (United States). Advanced Photon Source (APS)
Sponsoring Org.:
National Institutes of Health (NIH); National Institute of Allergy and Infectious Diseases (NIAID); Ruth Kirschstein Postdoctoral Fellowship
OSTI Identifier:
1356416
Grant/Contract Number:  
U19AI107792; R01AI107159; F32 GM109661
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Journal of Bacteriology
Additional Journal Information:
Journal Volume: 199; Journal Issue: 5; Journal ID: ISSN 0021-9193
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
ENGLISH
Subject:
59 BASIC BIOLOGICAL SCIENCES; Alphaproteobacteria; general stress response; EcfG; lithium; sigma factor; ABC transporter; RpoS; YehZ; YehZYXW

Citation Formats

Herrou, Julien, Willett, Jonathan W., Czyż, Daniel M., Babnigg, Gyorgy, Kim, Youngchang, and Crosson, Sean. Conserved ABC Transport System Regulated by the General Stress Response Pathways of Alpha- and Gammaproteobacteria. United States: N. p., 2016. Web. doi:10.1128/JB.00746-16.
Herrou, Julien, Willett, Jonathan W., Czyż, Daniel M., Babnigg, Gyorgy, Kim, Youngchang, & Crosson, Sean. Conserved ABC Transport System Regulated by the General Stress Response Pathways of Alpha- and Gammaproteobacteria. United States. doi:10.1128/JB.00746-16.
Herrou, Julien, Willett, Jonathan W., Czyż, Daniel M., Babnigg, Gyorgy, Kim, Youngchang, and Crosson, Sean. Mon . "Conserved ABC Transport System Regulated by the General Stress Response Pathways of Alpha- and Gammaproteobacteria". United States. doi:10.1128/JB.00746-16. https://www.osti.gov/servlets/purl/1356416.
@article{osti_1356416,
title = {Conserved ABC Transport System Regulated by the General Stress Response Pathways of Alpha- and Gammaproteobacteria},
author = {Herrou, Julien and Willett, Jonathan W. and Czyż, Daniel M. and Babnigg, Gyorgy and Kim, Youngchang and Crosson, Sean},
abstractNote = {Brucella abortus σE1 is an EcfG family sigma factor that regulates the transcription of dozens of genes in response to diverse stress conditions and is required for maintenance of chronic infection in a mouse model. A putative ATP-binding cassette transporter operon, bab1_0223-bab1_0226, is among the most highly activated gene sets in the σE1 regulon. The proteins encoded by the operon resemble quaternary ammonium-compatible solute importers but are most similar in sequence to the broadly conserved YehZYXW system, which remains largely uncharacterized. Transcription of yehZYXW is activated by the general stress sigma factor σS in Enterobacteriaceae, which suggests a functional role for this transport system in bacterial stress response across the classes Alphaproteobacteria and Gammaproteobacteria. Here, we present evidence that B. abortus YehZYXW does not function as an importer of known compatible solutes under physiological conditions and does not contribute to the virulence defect of a σE1-null strain. The sole in vitro phenotype associated with genetic disruption of this putative transport system is reduced growth in the presence of high Li+ ion concentrations. A crystal structure of B. abortus YehZ revealed a class II periplasmic binding protein fold with significant structural homology to Archaeoglobus fulgidus ProX, which binds glycine betaine. However, the structure of the YehZ ligand-binding pocket is incompatible with high-affinity binding to glycine betaine. This is consistent with weak measured binding of YehZ to glycine betaine and related compatible solutes. We conclude that YehZYXW is a conserved, stress-regulated transport system that is phylogenetically and functionally distinct from quaternary ammonium-compatible solute importers.},
doi = {10.1128/JB.00746-16},
journal = {Journal of Bacteriology},
issn = {0021-9193},
number = 5,
volume = 199,
place = {United States},
year = {2016},
month = {12}
}

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