Gut inflammation provides a respiratory electron acceptor for Salmonella

Sebastian E. Winter, Parameth Thiennimitr, Maria G. Winter, Brian P. Butler, Douglas L. Huseby, Robert W. Crawford, Joseph M. Russell, Charles L. Bevins, L. Garry Adams, Renãe M. Tsolis, John R. Roth, Andreas J. Bäumler

Research output: Contribution to journalArticle

583 Citations (Scopus)

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.

Original languageEnglish (US)
Pages (from-to)426-429
Number of pages4
JournalNature
Volume467
Issue number7314
DOIs
StatePublished - Sep 23 2010

Fingerprint

Salmonella
Electrons
Inflammation
Virulence Factors
Sulfur Compounds
Thiosulfates
Salmonella enterica
Microbiota
Intestinal Mucosa
Reactive Oxygen Species
Respiration
Macrophages
Serogroup
Growth
Genes

ASJC Scopus subject areas

  • General
  • Medicine(all)

Cite this

Winter, S. E., Thiennimitr, P., Winter, M. G., Butler, B. P., Huseby, D. L., Crawford, R. W., ... Bäumler, A. J. (2010). Gut inflammation provides a respiratory electron acceptor for Salmonella. Nature, 467(7314), 426-429. https://doi.org/10.1038/nature09415

Gut inflammation provides a respiratory electron acceptor for Salmonella. / Winter, Sebastian E.; Thiennimitr, Parameth; Winter, Maria G.; Butler, Brian P.; Huseby, Douglas L.; Crawford, Robert W.; Russell, Joseph M.; Bevins, Charles L.; Adams, L. Garry; Tsolis, Renãe M.; Roth, John R.; Bäumler, Andreas J.

In: Nature, Vol. 467, No. 7314, 23.09.2010, p. 426-429.

Research output: Contribution to journalArticle

Winter, SE, Thiennimitr, P, Winter, MG, Butler, BP, Huseby, DL, Crawford, RW, Russell, JM, Bevins, CL, Adams, LG, Tsolis, RM, Roth, JR & Bäumler, AJ 2010, 'Gut inflammation provides a respiratory electron acceptor for Salmonella', Nature, vol. 467, no. 7314, pp. 426-429. https://doi.org/10.1038/nature09415
Winter SE, Thiennimitr P, Winter MG, Butler BP, Huseby DL, Crawford RW et al. Gut inflammation provides a respiratory electron acceptor for Salmonella. Nature. 2010 Sep 23;467(7314):426-429. https://doi.org/10.1038/nature09415
Winter, Sebastian E. ; Thiennimitr, Parameth ; Winter, Maria G. ; Butler, Brian P. ; Huseby, Douglas L. ; Crawford, Robert W. ; Russell, Joseph M. ; Bevins, Charles L. ; Adams, L. Garry ; Tsolis, Renãe M. ; Roth, John R. ; Bäumler, Andreas J. / Gut inflammation provides a respiratory electron acceptor for Salmonella. In: Nature. 2010 ; Vol. 467, No. 7314. pp. 426-429.
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