An Oxidative Central Metabolism Enables Salmonella to Utilize Microbiota-Derived Succinate

Luisella Spiga, Maria G. Winter, Tatiane Furtado de Carvalho, Wenhan Zhu, Elizabeth R. Hughes, Caroline C. Gillis, Cassie L. Behrendt, Jiwoong Kim, Daniela Chessa, Helene L. Andrews-Polymenis, Daniel P. Beiting, Renato L. Santos, Lora V. Hooper, Sebastian E. Winter

Research output: Contribution to journalArticle

24 Citations (Scopus)

Abstract

The mucosal inflammatory response induced by Salmonella serovar Typhimurium creates a favorable niche for this gut pathogen. Conventional wisdom holds that S. Typhimurium undergoes an incomplete tricarboxylic acid (TCA) cycle in the anaerobic mammalian gut. One change during S. Typhimurium-induced inflammation is the production of oxidized compounds by infiltrating neutrophils. We show that inflammation-derived electron acceptors induce a complete, oxidative TCA cycle in S. Typhimurium, allowing the bacteria to compete with the microbiota for colonization. A complete TCA cycle facilitates utilization of the microbiota-derived fermentation product succinate as a carbon source. S. Typhimurium succinate utilization genes contribute to efficient colonization in conventionally raised mice, but provide no growth advantage in germ-free mice. Mono-association of gnotobiotic mice with Bacteroides, a major succinate producer, restores succinate utilization in S. Typhimurium. Thus, oxidative central metabolism enables S. Typhimurium to utilize a variety of carbon sources, including microbiota-derived succinate. Spiga et al. show that during colonization of the intestinal lumen, the enteric pathogen S. Typhimurium performs a complete TCA cycle. This oxidative central metabolism enables S. Typhimurium to utilize the microbiota-derived fermentation product succinate as a nutrient and to compete with the microbiota for colonization of the intestinal tract.

Original languageEnglish (US)
JournalCell Host and Microbe
DOIs
StateAccepted/In press - 2017

Fingerprint

Microbiota
Succinic Acid
Salmonella
Citric Acid Cycle
Fermentation
Carbon
Germ-Free Life
Inflammation
Bacteroides
Salmonella typhimurium
Neutrophils
Electrons
Bacteria
Food
Growth
Genes

Keywords

  • Bacterial metabolism
  • Gut microbiota
  • Salmonella

ASJC Scopus subject areas

  • Molecular Biology
  • Immunology and Microbiology(all)
  • Cancer Research

Cite this

An Oxidative Central Metabolism Enables Salmonella to Utilize Microbiota-Derived Succinate. / Spiga, Luisella; Winter, Maria G.; Furtado de Carvalho, Tatiane; Zhu, Wenhan; Hughes, Elizabeth R.; Gillis, Caroline C.; Behrendt, Cassie L.; Kim, Jiwoong; Chessa, Daniela; Andrews-Polymenis, Helene L.; Beiting, Daniel P.; Santos, Renato L.; Hooper, Lora V.; Winter, Sebastian E.

In: Cell Host and Microbe, 2017.

Research output: Contribution to journalArticle

Spiga, L, Winter, MG, Furtado de Carvalho, T, Zhu, W, Hughes, ER, Gillis, CC, Behrendt, CL, Kim, J, Chessa, D, Andrews-Polymenis, HL, Beiting, DP, Santos, RL, Hooper, LV & Winter, SE 2017, 'An Oxidative Central Metabolism Enables Salmonella to Utilize Microbiota-Derived Succinate', Cell Host and Microbe. https://doi.org/10.1016/j.chom.2017.07.018
Spiga, Luisella ; Winter, Maria G. ; Furtado de Carvalho, Tatiane ; Zhu, Wenhan ; Hughes, Elizabeth R. ; Gillis, Caroline C. ; Behrendt, Cassie L. ; Kim, Jiwoong ; Chessa, Daniela ; Andrews-Polymenis, Helene L. ; Beiting, Daniel P. ; Santos, Renato L. ; Hooper, Lora V. ; Winter, Sebastian E. / An Oxidative Central Metabolism Enables Salmonella to Utilize Microbiota-Derived Succinate. In: Cell Host and Microbe. 2017.
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