Analysis of the Salmonella regulatory network suggests involvement of SsrB and H-NS in σE-regulated SPI-2 gene expression

Jie Li, Christopher C. Overall, Ernesto S. Nakayasu, Afshan S. Kidwai, Marcus B. Jones, Rudd C. Johnson, Nhu T. Nguyen, Jason E. McDermott, Charles Ansong, Fred Heffron, Eric Cambronne, Joshua N. Adkins

Research output: Contribution to journalArticle

10 Citations (Scopus)

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 the global regulatory effect of σE, may account for the lethality of rpoE-deficient Salmonella in murine infection.

Original languageEnglish (US)
JournalFrontiers in Microbiology
Volume6
Issue numberFEB
DOIs
StatePublished - 2015

Fingerprint

Islands
Salmonella
Gene Expression
Infection
Genes
Food
Salmonella enterica
Essential Genes
Heat-Shock Proteins
Up-Regulation
Macrophages

Keywords

  • ChIP-seq
  • H-NS
  • Microarray
  • Regulation
  • RpoE
  • Salmonella
  • SPI-2

ASJC Scopus subject areas

  • Microbiology
  • Microbiology (medical)

Cite this

Analysis of the Salmonella regulatory network suggests involvement of SsrB and H-NS in σE-regulated SPI-2 gene expression. / Li, Jie; Overall, Christopher C.; Nakayasu, Ernesto S.; Kidwai, Afshan S.; Jones, Marcus B.; Johnson, Rudd C.; Nguyen, Nhu T.; McDermott, Jason E.; Ansong, Charles; Heffron, Fred; Cambronne, Eric; Adkins, Joshua N.

In: Frontiers in Microbiology, Vol. 6, No. FEB, 2015.

Research output: Contribution to journalArticle

Li, J, Overall, CC, Nakayasu, ES, Kidwai, AS, Jones, MB, Johnson, RC, Nguyen, NT, McDermott, JE, Ansong, C, Heffron, F, Cambronne, E & Adkins, JN 2015, 'Analysis of the Salmonella regulatory network suggests involvement of SsrB and H-NS in σE-regulated SPI-2 gene expression', Frontiers in Microbiology, vol. 6, no. FEB. https://doi.org/10.3389/fmicb.2015.00027
Li, Jie ; Overall, Christopher C. ; Nakayasu, Ernesto S. ; Kidwai, Afshan S. ; Jones, Marcus B. ; Johnson, Rudd C. ; 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. In: Frontiers in Microbiology. 2015 ; Vol. 6, No. FEB.
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AU - Overall, Christopher C.

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AU - Kidwai, Afshan S.

AU - Jones, Marcus B.

AU - Johnson, Rudd C.

AU - Nguyen, Nhu T.

AU - McDermott, Jason E.

AU - Ansong, Charles

AU - Heffron, Fred

AU - Cambronne, Eric

AU - Adkins, Joshua N.

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AB - 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.

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