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Cell Host Microbe. 2017 Sep 13;22(3):291-301.e6. doi: 10.1016/j.chom.2017.07.018. Epub 2017 Aug 24.

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

Author information

1
Department of Microbiology, UT Southwestern Medical Center, Dallas, TX 75390, USA.
2
Departamento de Clínica e Cirurgia Veterinárias, Escola de Veterinária, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil.
3
Department of Immunology, UT Southwestern Medical Center, Dallas, TX 75390, USA.
4
Department of Clinical Science, Quantitative Biomedical Research Center, UT Southwestern Medical Center, Dallas, TX 75390, USA.
5
Department of Biomedical Science, School of Medicine, University of Sassari, Sassari, Italy.
6
Department of Microbial Pathogenesis and Immunology, College of Medicine, Texas A&M University System Health Science Center, Bryan, TX 77807, USA.
7
Department of Pathobiology, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.
8
Department of Immunology, UT Southwestern Medical Center, Dallas, TX 75390, USA; Howard Hughes Medical Institute, UT Southwestern Medical Center, Dallas, TX 75390, USA.
9
Department of Microbiology, UT Southwestern Medical Center, Dallas, TX 75390, USA. Electronic address: sebastian.winter@utsouthwestern.edu.

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.

KEYWORDS:

Salmonella; bacterial metabolism; gut microbiota

PMID:
28844888
PMCID:
PMC5599368
DOI:
10.1016/j.chom.2017.07.018
[Indexed for MEDLINE]
Free PMC Article

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