Salmonella Typhimurium exploits host polyamines for assembly of the type 3 secretion machinery

PLoS Biol. 2024 Aug 5;22(8):e3002731. doi: 10.1371/journal.pbio.3002731. eCollection 2024 Aug.

Abstract

Bacterial pathogens utilize the factors of their hosts to infect them, but which factors they exploit remain poorly defined. Here, we show that a pathogenic Salmonella enterica serovar Typhimurium (STm) exploits host polyamines for the functional expression of virulence factors. An STm mutant strain lacking principal genes required for polyamine synthesis and transport exhibited impaired infectivity in mice. A polyamine uptake-impaired strain of STm was unable to inject effectors of the type 3 secretion system into host cells due to a failure of needle assembly. STm infection stimulated host polyamine production by increasing arginase expression. The decline in polyamine levels caused by difluoromethylornithine, which inhibits host polyamine production, attenuated STm colonization, whereas polyamine supplementation augmented STm pathogenesis. Our work reveals that host polyamines are a key factor promoting STm infection, and therefore a promising therapeutic target for bacterial infection.

MeSH terms

  • Animals
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism
  • Female
  • Host-Pathogen Interactions
  • Humans
  • Mice
  • Polyamines* / metabolism
  • Salmonella Infections / metabolism
  • Salmonella Infections / microbiology
  • Salmonella typhimurium* / genetics
  • Salmonella typhimurium* / metabolism
  • Salmonella typhimurium* / pathogenicity
  • Type III Secretion Systems* / genetics
  • Type III Secretion Systems* / metabolism
  • Virulence Factors* / genetics
  • Virulence Factors* / metabolism

Substances

  • Polyamines
  • Type III Secretion Systems
  • Virulence Factors
  • Bacterial Proteins

Grants and funding

This work was supported in part by Japan society for the promotion of science (JSPS) KAKENHI Grant Number JP21K07030 (to TMiki), JP21K07011 (to NO), JP20K15749 (to MK), JP22K06162 (to MK), JP22K07073 (to TH), JP19H03182 (to TMinamino), JP22H02573 (to TMinamino), JP22K19274 (to TMinamino). YGK is supported by a Fuji Foundation for Protein Research. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.