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Title: Analysis of the Salmonella regulatory network suggests involvement of SsrB and H-NS in σ E-regulated SPI-2 gene expression

Abstract

The extracytoplasmic functioning sigma factor σ E is known to play an essential role for Salmonella enterica serovar Typhimurium to survive and proliferate in macrophages and mice. However, its regulatory network is not well characterized, especially during infection. Here we used microarray to identify genes regulated by σ E in Salmonella grown in three conditions: a nutrient-rich condition and two others that mimic early and late intracellular infection. We found that in each condition σ E regulated different sets of genes, and notably, several global regulators. When comparing nutrient-rich and infection-like conditions, large changes were observed in the expression of genes involved in Salmonella pathogenesis island (SPI)-1 type-three secretion system (TTSS), SPI-2 TTSS, protein synthesis, and stress responses. In total, the expression of 58% of Salmonella genes was affected by σ E in at least one of the three conditions. An important finding is that σ E up-regulates SPI-2 genes, which are essential for Salmonella intracellular survival, by up-regulating SPI-2 activator ssrB expression at the early stage of infection and down-regulating SPI-2 repressor hns expression at a later stage. Moreover, σ E is capable of countering the silencing of H-NS, releasing the expression of SPI-2 genes. This connection between σmore » E and SPI-2 genes, combined with the global regulatory effect of σ E, may account for the lethality of rpoE-deficient Salmonella in murine infection.« less

Authors:
; ; ; ; ; ; ; ; ; ; ;
Publication Date:
Research Org.:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1184934
Report Number(s):
PNNL-SA-101010
Journal ID: ISSN 1664-302X
Grant/Contract Number:  
AC05-76RL01830
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Volume: 6; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Salmonella Typhimurium; bacterial pathogenesis; systems biology; transcriptomics; regulatory network; bioinformatics; computational biology

Citation Formats

Li, Jie, Overall, Christopher C., Nakayasu, Ernesto S., Kidwai, Afshan S., Jones, Marcus B., Johnson, Rudd, Nguyen, Nhu T., McDermott, Jason E., Ansong, Charles, Heffron, Fred, Cambronne, Eric, and Adkins, Joshua N. Analysis of the Salmonella regulatory network suggests involvement of SsrB and H-NS in σE-regulated SPI-2 gene expression. United States: N. p., 2015. Web. doi:10.3389/fmicb.2015.00027.
Li, Jie, Overall, Christopher C., Nakayasu, Ernesto S., Kidwai, Afshan S., Jones, Marcus B., Johnson, Rudd, Nguyen, Nhu T., McDermott, Jason E., Ansong, Charles, Heffron, Fred, Cambronne, Eric, & Adkins, Joshua N. Analysis of the Salmonella regulatory network suggests involvement of SsrB and H-NS in σE-regulated SPI-2 gene expression. United States. doi:10.3389/fmicb.2015.00027.
Li, Jie, Overall, Christopher C., Nakayasu, Ernesto S., Kidwai, Afshan S., Jones, Marcus B., Johnson, Rudd, Nguyen, Nhu T., McDermott, Jason E., Ansong, Charles, Heffron, Fred, Cambronne, Eric, and Adkins, Joshua N. Tue . "Analysis of the Salmonella regulatory network suggests involvement of SsrB and H-NS in σE-regulated SPI-2 gene expression". United States. doi:10.3389/fmicb.2015.00027. https://www.osti.gov/servlets/purl/1184934.
@article{osti_1184934,
title = {Analysis of the Salmonella regulatory network suggests involvement of SsrB and H-NS in σE-regulated SPI-2 gene expression},
author = {Li, Jie and Overall, Christopher C. and Nakayasu, Ernesto S. and Kidwai, Afshan S. and Jones, Marcus B. and Johnson, Rudd and Nguyen, Nhu T. and McDermott, Jason E. and Ansong, Charles and Heffron, Fred and Cambronne, Eric and Adkins, Joshua N.},
abstractNote = {The extracytoplasmic functioning sigma factor σE is known to play an essential role for Salmonella enterica serovar Typhimurium to survive and proliferate in macrophages and mice. However, its regulatory network is not well characterized, especially during infection. Here we used microarray to identify genes regulated by σE in Salmonella grown in three conditions: a nutrient-rich condition and two others that mimic early and late intracellular infection. We found that in each condition σE regulated different sets of genes, and notably, several global regulators. When comparing nutrient-rich and infection-like conditions, large changes were observed in the expression of genes involved in Salmonella pathogenesis island (SPI)-1 type-three secretion system (TTSS), SPI-2 TTSS, protein synthesis, and stress responses. In total, the expression of 58% of Salmonella genes was affected by σE in at least one of the three conditions. An important finding is that σE up-regulates SPI-2 genes, which are essential for Salmonella intracellular survival, by up-regulating SPI-2 activator ssrB expression at the early stage of infection and down-regulating SPI-2 repressor hns expression at a later stage. Moreover, σE is capable of countering the silencing of H-NS, releasing the expression of SPI-2 genes. This connection between σE and SPI-2 genes, combined with the global regulatory effect of σE, may account for the lethality of rpoE-deficient Salmonella in murine infection.},
doi = {10.3389/fmicb.2015.00027},
journal = {Frontiers in Microbiology},
number = ,
volume = 6,
place = {United States},
year = {2015},
month = {2}
}

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