Commensal Enterobacteriaceae Protect against Salmonella Colonization through Oxygen Competition

Yael Litvak, Khin K.Z. Mon, Henry Nguyen, Ganrea Chanthavixay, Megan Liou, Eric M. Velazquez, Laura Kutter, Monique A. Alcantara, Mariana X. Byndloss, Connor R. Tiffany, Gregory T. Walker, Franziska Faber, Yuhua Zhu, Denise N. Bronner, Austin J. Byndloss, Renee M Tsolis, Huaijun Zhou, Andreas J Baumler

Research output: Contribution to journalArticle

4 Citations (Scopus)

Abstract

Neonates are highly susceptible to infection with enteric pathogens, but the underlying mechanisms are not resolved. We show that neonatal chick colonization with Salmonella enterica serovar Enteritidis requires a virulence-factor-dependent increase in epithelial oxygenation, which drives pathogen expansion by aerobic respiration. Co-infection experiments with an Escherichia coli strain carrying an oxygen-sensitive reporter suggest that S. Enteritidis competes with commensal Enterobacteriaceae for oxygen. A combination of Enterobacteriaceae and spore-forming bacteria, but not colonization with either community alone, confers colonization resistance against S. Enteritidis in neonatal chicks, phenocopying germ-free mice associated with adult chicken microbiota. Combining spore-forming bacteria with a probiotic E. coli isolate protects germ-free mice from pathogen colonization, but the protection is lost when the ability to respire oxygen under micro-aerophilic conditions is genetically ablated in E. coli. These results suggest that commensal Enterobacteriaceae contribute to colonization resistance by competing with S. Enteritidis for oxygen, a resource critical for pathogen expansion.

Original languageEnglish (US)
Pages (from-to)128-139.e5
JournalCell Host and Microbe
Volume25
Issue number1
DOIs
StatePublished - Jan 9 2019

Fingerprint

Enterobacteriaceae
Salmonella
Oxygen
Escherichia coli
Spores
Bacteria
Salmonella enteritidis
Microbiota
Probiotics
Virulence Factors
Coinfection
Chickens
Respiration
Infection

Keywords

  • colonization resistance
  • Enterobacteriaceae
  • microbiota
  • neonate
  • oxygen
  • Salmonella

ASJC Scopus subject areas

  • Parasitology
  • Microbiology
  • Virology

Cite this

Commensal Enterobacteriaceae Protect against Salmonella Colonization through Oxygen Competition. / Litvak, Yael; Mon, Khin K.Z.; Nguyen, Henry; Chanthavixay, Ganrea; Liou, Megan; Velazquez, Eric M.; Kutter, Laura; Alcantara, Monique A.; Byndloss, Mariana X.; Tiffany, Connor R.; Walker, Gregory T.; Faber, Franziska; Zhu, Yuhua; Bronner, Denise N.; Byndloss, Austin J.; Tsolis, Renee M; Zhou, Huaijun; Baumler, Andreas J.

In: Cell Host and Microbe, Vol. 25, No. 1, 09.01.2019, p. 128-139.e5.

Research output: Contribution to journalArticle

Litvak, Y, Mon, KKZ, Nguyen, H, Chanthavixay, G, Liou, M, Velazquez, EM, Kutter, L, Alcantara, MA, Byndloss, MX, Tiffany, CR, Walker, GT, Faber, F, Zhu, Y, Bronner, DN, Byndloss, AJ, Tsolis, RM, Zhou, H & Baumler, AJ 2019, 'Commensal Enterobacteriaceae Protect against Salmonella Colonization through Oxygen Competition', Cell Host and Microbe, vol. 25, no. 1, pp. 128-139.e5. https://doi.org/10.1016/j.chom.2018.12.003
Litvak Y, Mon KKZ, Nguyen H, Chanthavixay G, Liou M, Velazquez EM et al. Commensal Enterobacteriaceae Protect against Salmonella Colonization through Oxygen Competition. Cell Host and Microbe. 2019 Jan 9;25(1):128-139.e5. https://doi.org/10.1016/j.chom.2018.12.003
Litvak, Yael ; Mon, Khin K.Z. ; Nguyen, Henry ; Chanthavixay, Ganrea ; Liou, Megan ; Velazquez, Eric M. ; Kutter, Laura ; Alcantara, Monique A. ; Byndloss, Mariana X. ; Tiffany, Connor R. ; Walker, Gregory T. ; Faber, Franziska ; Zhu, Yuhua ; Bronner, Denise N. ; Byndloss, Austin J. ; Tsolis, Renee M ; Zhou, Huaijun ; Baumler, Andreas J. / Commensal Enterobacteriaceae Protect against Salmonella Colonization through Oxygen Competition. In: Cell Host and Microbe. 2019 ; Vol. 25, No. 1. pp. 128-139.e5.
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