Analysis of the Salmonella regulatory network suggests involvement of SsrB and H-NS in σE-regulated SPI-2 gene expression
Abstract
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 themore »
- Authors:
- Publication Date:
- Research Org.:
- Pacific Northwest National Laboratory (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. https://doi.org/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. https://doi.org/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 = {Tue Feb 10 00:00:00 EST 2015},
month = {Tue Feb 10 00:00:00 EST 2015}
}
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Works referencing / citing this record:
ChIP-Seq Analysis of the σE Regulon of Salmonella enterica Serovar Typhimurium Reveals New Genes Implicated in Heat Shock and Oxidative Stress Response
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Preliminary Transcriptome Analysis of Mature Biofilm and Planktonic Cells of Salmonella Enteritidis Exposure to Acid Stress
journal, September 2017
- Jia, Kun; Wang, Guangyu; Liang, Lijiao
- Frontiers in Microbiology, Vol. 8
Combination of berberine and ciprofloxacin reduces multi-resistant Salmonella strain biofilm formation by depressing mRNA expressions of luxS, rpoE, and ompR
journal, January 2018
- Shi, Chenxi; Li, Minmin; Muhammad, Ishfaq
- Journal of Veterinary Science, Vol. 19, Issue 6
Preliminary Transcriptome Analysis of Mature Biofilm and Planktonic Cells of Salmonella Enteritidis Exposure to Acid Stress
journal, September 2017
- Jia, Kun; Wang, Guangyu; Liang, Lijiao
- Frontiers in Microbiology, Vol. 8
HldE Is Important for Virulence Phenotypes in Enterotoxigenic Escherichia coli
journal, August 2018
- Maigaard Hermansen, Grith M.; Boysen, Anders; Krogh, Thøger J.
- Frontiers in Cellular and Infection Microbiology, Vol. 8