Gut inflammation provides a respiratory electron acceptor for Salmonella

Nature. 2010 Sep 23;467(7314):426-9. doi: 10.1038/nature09415.

Abstract

Salmonella enterica serotype Typhimurium (S. Typhimurium) causes acute gut inflammation by using its virulence factors to invade the intestinal epithelium and survive in mucosal macrophages. The inflammatory response enhances the transmission success of S. Typhimurium by promoting its outgrowth in the gut lumen through unknown mechanisms. Here we show that reactive oxygen species generated during inflammation react with endogenous, luminal sulphur compounds (thiosulphate) to form a new respiratory electron acceptor, tetrathionate. The genes conferring the ability to use tetrathionate as an electron acceptor produce a growth advantage for S. Typhimurium over the competing microbiota in the lumen of the inflamed gut. We conclude that S. Typhimurium virulence factors induce host-driven production of a new electron acceptor that allows the pathogen to use respiration to compete with fermenting gut microbes. Thus the ability to trigger intestinal inflammation is crucial for the biology of this diarrhoeal pathogen.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Respiration*
  • Colitis / metabolism
  • Colitis / microbiology
  • Electron Transport
  • Electrons*
  • Female
  • Gastrointestinal Tract / metabolism
  • Gastrointestinal Tract / microbiology*
  • Gastrointestinal Tract / pathology*
  • Inflammation / metabolism
  • Inflammation / microbiology
  • Inflammation / pathology
  • Intestinal Mucosa / metabolism
  • Intestinal Mucosa / microbiology
  • Intestinal Mucosa / pathology
  • Mice
  • Mice, Inbred C57BL
  • Reactive Oxygen Species / metabolism
  • Salmonella typhimurium / growth & development
  • Salmonella typhimurium / metabolism*
  • Tetrathionic Acid / metabolism
  • Thiosulfates / metabolism

Substances

  • Reactive Oxygen Species
  • Thiosulfates
  • Tetrathionic Acid