Systematic reconstruction of an effector-gene network reveals determinants of Salmonella cellular and tissue tropism

Cell Host Microbe. 2021 Oct 13;29(10):1531-1544.e9. doi: 10.1016/j.chom.2021.08.012. Epub 2021 Sep 17.

Abstract

The minimal genetic requirements for microbes to survive within multiorganism communities, including host-pathogen interactions, remain poorly understood. Here, we combined targeted gene mutagenesis with phenotype-guided genetic reassembly to identify a cooperative network of SPI-2 T3SS effector genes that are sufficient for Salmonella Typhimurium (STm) to cause disease in a natural host organism. Five SPI-2 effector genes support pathogen survival within the host cell cytoplasm by coordinating bacterial replication with Salmonella-containing vacuole (SCV) division. Unexpectedly, this minimal genetic repertoire does not support STm systemic infection of mice. In vivo screening revealed a second effector-gene network, encoded by the spv operon, that expands the life cycle of STm from growth in cells to deep-tissue colonization in a murine model of typhoid fever. Comparison between Salmonella infection models suggests how cooperation between effector genes drives tissue tropism in a pathogen group.

Keywords: SPI-2 T3SS; Salmonella Typhimurium; bacterial pathogenesis; effector proteins; sifA; sopD2; spv locus; sseF; sseG; steA.

MeSH terms

  • Animals
  • Bacterial Proteins / genetics*
  • Bacterial Proteins / metabolism
  • Cytoplasm / microbiology
  • Female
  • Gene Regulatory Networks*
  • Genomic Islands
  • Host-Pathogen Interactions
  • Humans
  • Mice
  • Mice, Inbred C57BL
  • Microbial Viability
  • Operon
  • Salmonella Infections / microbiology*
  • Salmonella typhimurium / genetics*
  • Salmonella typhimurium / growth & development
  • Salmonella typhimurium / pathogenicity
  • Salmonella typhimurium / physiology
  • Tropism
  • Type III Secretion Systems / genetics
  • Type III Secretion Systems / metabolism
  • Virulence

Substances

  • Bacterial Proteins
  • Type III Secretion Systems