The Stringent Response Regulator DksA Is Required for Salmonella enterica Serovar Typhimurium Growth in Minimal Medium, Motility, Biofilm Formation, and Intestinal Colonization

Infect Immun. 2015 Nov 9;84(1):375-84. doi: 10.1128/IAI.01135-15. Print 2016 Jan.

Abstract

Salmonella enterica serovar Typhimurium is a facultative intracellular human and animal bacterial pathogen posing a major threat to public health worldwide. Salmonella pathogenicity requires complex coordination of multiple physiological and virulence pathways. DksA is a conserved Gram-negative regulator that belongs to a distinct group of transcription factors that bind directly to the RNA polymerase secondary channel, potentiating the effect of the signaling molecule ppGpp during a stringent response. Here, we established that in S. Typhimurium, dksA is induced during the logarithmic phase and DksA is essential for growth in minimal defined medium and plays an important role in motility and biofilm formation. Furthermore, we determined that DksA positively regulates the Salmonella pathogenicity island 1 and motility-chemotaxis genes and is necessary for S. Typhimurium invasion of human epithelial cells and uptake by macrophages. In contrast, DksA was found to be dispensable for S. Typhimurium host cell adhesion. Finally, using the colitis mouse model, we found that dksA is spatially induced at the midcecum during the early stage of the infection and required for gastrointestinal colonization and systemic infection in vivo. Taken together, these data indicate that the ancestral stringent response regulator DksA coordinates various physiological and virulence S. Typhimurium programs and therefore is a key virulence regulator of Salmonella.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bacterial Adhesion
  • Bacterial Proteins / genetics*
  • Bacterial Proteins / metabolism
  • Biofilms / growth & development
  • Caco-2 Cells
  • Cell Line
  • Chemotaxis / genetics
  • Colitis / immunology
  • Colitis / microbiology
  • Colitis / pathology*
  • Culture Media / chemistry
  • Epithelial Cells / microbiology
  • Female
  • Gene Expression Regulation, Bacterial
  • Humans
  • Intestines / microbiology*
  • Macrophages / immunology
  • Macrophages / microbiology
  • Mice
  • Mice, Inbred C57BL
  • Salmonella Infections, Animal / immunology
  • Salmonella Infections, Animal / microbiology
  • Salmonella Infections, Animal / pathology*
  • Salmonella typhimurium / genetics
  • Salmonella typhimurium / growth & development*
  • Salmonella typhimurium / pathogenicity
  • Transcription Factors / genetics
  • Virulence Factors / genetics*

Substances

  • Bacterial Proteins
  • Culture Media
  • DksA protein, Salmonella typhimurium
  • Spi1 protein, Salmonella
  • Transcription Factors
  • Virulence Factors

Grants and funding

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.