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Gut inflammation provides a respiratory electron acceptor for Salmonella

Author

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  • Sebastian E. Winter

    (School of Medicine, University of California, Davis, One Shields Avenue, Davis, California 95616, USA)

  • Parameth Thiennimitr

    (School of Medicine, University of California, Davis, One Shields Avenue, Davis, California 95616, USA
    Faculty of Medicine, Chiang Mai University)

  • Maria G. Winter

    (School of Medicine, University of California, Davis, One Shields Avenue, Davis, California 95616, USA)

  • Brian P. Butler

    (School of Medicine, University of California, Davis, One Shields Avenue, Davis, California 95616, USA)

  • Douglas L. Huseby

    (University of California, Davis, One Shields Avenue, Davis, California 95616, USA)

  • Robert W. Crawford

    (School of Medicine, University of California, Davis, One Shields Avenue, Davis, California 95616, USA)

  • Joseph M. Russell

    (School of Medicine, University of California, Davis, One Shields Avenue, Davis, California 95616, USA)

  • Charles L. Bevins

    (School of Medicine, University of California, Davis, One Shields Avenue, Davis, California 95616, USA)

  • L. Garry Adams

    (College of Veterinary Medicine, Texas A&M University)

  • Renée M. Tsolis

    (School of Medicine, University of California, Davis, One Shields Avenue, Davis, California 95616, USA)

  • John R. Roth

    (University of California, Davis, One Shields Avenue, Davis, California 95616, USA)

  • Andreas J. Bäumler

    (School of Medicine, University of California, Davis, One Shields Avenue, Davis, California 95616, USA)

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.

Suggested Citation

  • 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 & Renée M. Tsolis & Joh, 2010. "Gut inflammation provides a respiratory electron acceptor for Salmonella," Nature, Nature, vol. 467(7314), pages 426-429, September.
  • Handle: RePEc:nat:nature:v:467:y:2010:i:7314:d:10.1038_nature09415
    DOI: 10.1038/nature09415
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    Cited by:

    1. Gina Paola Rodriguez-Castaño & Federico E Rey & Alejandro Caro-Quintero & Alejandro Acosta-González, 2020. "Gut-derived Flavonifractor species variants are differentially enriched during in vitro incubation with quercetin," PLOS ONE, Public Library of Science, vol. 15(12), pages 1-21, December.
    2. Patrick A McLaughlin & Julie A Bettke & Jason W Tam & Jesse Leeds & James B Bliska & Brian P Butler & Adrianus W M van der Velden, 2019. "Inflammatory monocytes provide a niche for Salmonella expansion in the lumen of the inflamed intestine," PLOS Pathogens, Public Library of Science, vol. 15(7), pages 1-17, July.

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