Respiration of Microbiota-Derived 1,2-propanediol Drives Salmonella Expansion during Colitis

Franziska Faber, Parameth Thiennimitr, Luisella Spiga, Mariana X. Byndloss, Yael Litvak, Sara Lawhon, Helene L. Andrews-Polymenis, Sebastian E. Winter, Andreas J Baumler

Research output: Contribution to journalArticle

41 Citations (Scopus)

Abstract

Intestinal inflammation caused by Salmonella enterica serovar Typhimurium increases the availability of electron acceptors that fuel a respiratory growth of the pathogen in the intestinal lumen. Here we show that one of the carbon sources driving this respiratory expansion in the mouse model is 1,2-propanediol, a microbial fermentation product. 1,2-propanediol utilization required intestinal inflammation induced by virulence factors of the pathogen. S. Typhimurium used both aerobic and anaerobic respiration to consume 1,2-propanediol and expand in the murine large intestine. 1,2-propanediol-utilization did not confer a benefit in germ-free mice, but the pdu genes conferred a fitness advantage upon S. Typhimurium in mice mono-associated with Bacteroides fragilis or Bacteroides thetaiotaomicron. Collectively, our data suggest that intestinal inflammation enables S. Typhimurium to sidestep nutritional competition by respiring a microbiota-derived fermentation product.

Original languageEnglish (US)
Article numbere1006129
JournalPLoS Pathogens
Volume13
Issue number1
DOIs
StatePublished - Jan 1 2017

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Propylene Glycol
Microbiota
Colitis
Salmonella
Respiration
Inflammation
Fermentation
Nonoxynol
Bacteroides fragilis
Salmonella enterica
Large Intestine
Virulence Factors
Carbon
Electrons
Growth
Genes

ASJC Scopus subject areas

  • Parasitology
  • Microbiology
  • Immunology
  • Molecular Biology
  • Genetics
  • Virology

Cite this

Respiration of Microbiota-Derived 1,2-propanediol Drives Salmonella Expansion during Colitis. / Faber, Franziska; Thiennimitr, Parameth; Spiga, Luisella; Byndloss, Mariana X.; Litvak, Yael; Lawhon, Sara; Andrews-Polymenis, Helene L.; Winter, Sebastian E.; Baumler, Andreas J.

In: PLoS Pathogens, Vol. 13, No. 1, e1006129, 01.01.2017.

Research output: Contribution to journalArticle

Faber, F, Thiennimitr, P, Spiga, L, Byndloss, MX, Litvak, Y, Lawhon, S, Andrews-Polymenis, HL, Winter, SE & Baumler, AJ 2017, 'Respiration of Microbiota-Derived 1,2-propanediol Drives Salmonella Expansion during Colitis', PLoS Pathogens, vol. 13, no. 1, e1006129. https://doi.org/10.1371/journal.ppat.1006129
Faber F, Thiennimitr P, Spiga L, Byndloss MX, Litvak Y, Lawhon S et al. Respiration of Microbiota-Derived 1,2-propanediol Drives Salmonella Expansion during Colitis. PLoS Pathogens. 2017 Jan 1;13(1). e1006129. https://doi.org/10.1371/journal.ppat.1006129
Faber, Franziska ; Thiennimitr, Parameth ; Spiga, Luisella ; Byndloss, Mariana X. ; Litvak, Yael ; Lawhon, Sara ; Andrews-Polymenis, Helene L. ; Winter, Sebastian E. ; Baumler, Andreas J. / Respiration of Microbiota-Derived 1,2-propanediol Drives Salmonella Expansion during Colitis. In: PLoS Pathogens. 2017 ; Vol. 13, No. 1.
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