Salmonella Uses Energy Taxis to Benefit From Intestinal Inflammation

PLoS Pathog. 2013;9(4):e1003267. doi: 10.1371/journal.ppat.1003267. Epub 2013 Apr 18.

Abstract

Chemotaxis enhances the fitness of Salmonella enterica serotype Typhimurium (S. Typhimurium) during colitis. However, the chemotaxis receptors conferring this fitness advantage and their cognate signals generated during inflammation remain unknown. Here we identify respiratory electron acceptors that are generated in the intestinal lumen as by-products of the host inflammatory response as in vivo signals for methyl-accepting chemotaxis proteins (MCPs). Three MCPs, including Trg, Tsr and Aer, enhanced the fitness of S. Typhimurium in a mouse colitis model. Aer mediated chemotaxis towards electron acceptors (energy taxis) in vitro and required tetrathionate respiration to confer a fitness advantage in vivo. Tsr mediated energy taxis towards nitrate but not towards tetrathionate in vitro and required nitrate respiration to confer a fitness advantage in vivo. These data suggest that the energy taxis receptors Tsr and Aer respond to distinct in vivo signals to confer a fitness advantage upon S. Typhimurium during inflammation by enabling this facultative anaerobic pathogen to seek out favorable spatial niches containing host-derived electron acceptors that boost its luminal growth.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Bacterial Proteins / metabolism*
  • Carrier Proteins / metabolism
  • Chemotaxis*
  • Colitis / immunology
  • Colitis / microbiology*
  • Electron Transport
  • Energy Metabolism*
  • Female
  • Inflammation
  • Intestinal Mucosa / metabolism
  • Intestines / microbiology
  • Membrane Proteins / metabolism*
  • Methyl-Accepting Chemotaxis Proteins
  • Mice
  • Mice, Inbred C57BL
  • Mice, Inbred CBA
  • Neutrophils / immunology
  • Nitrates / metabolism
  • Reactive Oxygen Species / metabolism
  • Receptors, Cell Surface / metabolism
  • Salmonella Infections, Animal / immunology
  • Salmonella Infections, Animal / microbiology*
  • Salmonella typhimurium / immunology
  • Salmonella typhimurium / pathogenicity*
  • Salmonella typhimurium / physiology
  • Tetrathionic Acid / metabolism

Substances

  • Bacterial Proteins
  • Carrier Proteins
  • Membrane Proteins
  • Methyl-Accepting Chemotaxis Proteins
  • Nitrates
  • Reactive Oxygen Species
  • Receptors, Cell Surface
  • Tsr protein, Bacteria
  • Tetrathionic Acid