Intestinal inflammation allows Salmonella to use ethanolamine to compete with the microbiota

Parameth Thiennimitr, Sebastian E. Winter, Maria G. Winter, Mariana N. Xavier, Vladimir Tolstikov, Douglas L. Huseby, Torsten Sterzenbach, Renée M. Tsolis, John R. Roth, Andreas J. Bäumler

Research output: Contribution to journalArticle

286 Citations (Scopus)

Abstract

Conventional wisdom holds that microbes support their growth in vertebrate hosts by exploiting a large variety of nutrients. We show here that use of a specific nutrient (ethanolamine) confers a marked growth advantage on Salmonella enterica serovar Typhimurium (S. Typhimurium) in the lumen of the inflamed intestine. In the anaerobic environment of the gut, ethanolamine supports little or no growth by fermentation. However, S. Typhimurium is able to use this carbon source by inducing the gut to produce a respiratory electron acceptor (tetrathionate), which supports anaerobic growth on ethanolamine. The gut normally converts ambient hydrogen sulfide to thiosulfate, which it then oxidizes further to tetrathionate during inflammation. Evidence is provided that S. Typhimurium's growth advantage in an inflamed gut is because of its ability to respire ethanolamine, which is released from host tissue, but is not utilizable by competing bacteria. By inducing intestinal inflammation, S. Typhimurium sidesteps nutritional competition and gains the ability to use an abundant simple substrate, ethanolamine, which is provided by the host.

Original languageEnglish (US)
Pages (from-to)17480-17485
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume108
Issue number42
DOIs
StatePublished - Oct 18 2011

Fingerprint

Ethanolamine
Microbiota
Salmonella
Inflammation
Growth
Thiosulfates
Food
Hydrogen Sulfide
Salmonella enterica
Fermentation
Intestines
Vertebrates
Carbon
Electrons
Bacteria
Serogroup

Keywords

  • Diarrhea
  • Gastroenteritis
  • Metabolism

ASJC Scopus subject areas

  • General

Cite this

Intestinal inflammation allows Salmonella to use ethanolamine to compete with the microbiota. / Thiennimitr, Parameth; Winter, Sebastian E.; Winter, Maria G.; Xavier, Mariana N.; Tolstikov, Vladimir; Huseby, Douglas L.; Sterzenbach, Torsten; Tsolis, Renée M.; Roth, John R.; Bäumler, Andreas J.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 108, No. 42, 18.10.2011, p. 17480-17485.

Research output: Contribution to journalArticle

Thiennimitr, P, Winter, SE, Winter, MG, Xavier, MN, Tolstikov, V, Huseby, DL, Sterzenbach, T, Tsolis, RM, Roth, JR & Bäumler, AJ 2011, 'Intestinal inflammation allows Salmonella to use ethanolamine to compete with the microbiota', Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 42, pp. 17480-17485. https://doi.org/10.1073/pnas.1107857108
Thiennimitr, Parameth ; Winter, Sebastian E. ; Winter, Maria G. ; Xavier, Mariana N. ; Tolstikov, Vladimir ; Huseby, Douglas L. ; Sterzenbach, Torsten ; Tsolis, Renée M. ; Roth, John R. ; Bäumler, Andreas J. / Intestinal inflammation allows Salmonella to use ethanolamine to compete with the microbiota. In: Proceedings of the National Academy of Sciences of the United States of America. 2011 ; Vol. 108, No. 42. pp. 17480-17485.
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