Depletion of Butyrate-Producing Clostridia from the Gut Microbiota Drives an Aerobic Luminal Expansion of Salmonella

Fabian Rivera-Chávez; Lillian F Zhang; Franziska Faber; Christopher A Lopez; Mariana X Byndloss; Erin E Olsan; Gege Xu; Eric M Velazquez; Carlito B Lebrilla; Sebastian E Winter; Andreas J Bäumler

doi:10.1016/j.chom.2016.03.004

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Depletion of Butyrate-Producing Clostridia from the Gut Microbiota Drives an Aerobic Luminal Expansion of Salmonella

Journal article

Open access

Peer reviewed

Depletion of Butyrate-Producing Clostridia from the Gut Microbiota Drives an Aerobic Luminal Expansion of Salmonella

Fabian Rivera-Chávez, Lillian F Zhang, Franziska Faber, Christopher A Lopez, Mariana X Byndloss, Erin E Olsan, Gege Xu, Eric M Velazquez, Carlito B Lebrilla, Sebastian E Winter, …

Cell host & microbe, Vol.19(4), pp.443-454

04/13/2016

DOI: https://doi.org/10.1016/j.chom.2016.03.004

Handle:

https://hdl.handle.net/20.500.12741/rep:6644

PMCID: PMC4832419

PMID: 27078066

Abstract

Aerobiosis

Virulence Factors - genetics

Salmonella typhimurium - genetics

Streptomycin - pharmacology

Salmonella typhimurium - growth & development

Mice, Inbred C57BL

Bacterial Proteins - genetics

Oxygen - metabolism

Salmonella typhimurium - metabolism

Animals

Gastrointestinal Microbiome - drug effects

Intestines - microbiology

Butyric Acid - metabolism

Mice, Inbred CBA

Bacterial Proteins - metabolism

Female

Virulence Factors - metabolism

Anti-Bacterial Agents - pharmacology

Clostridium - metabolism

Mice

Clostridium - drug effects

The mammalian intestine is host to a microbial community that prevents pathogen expansion through unknown mechanisms, while antibiotic treatment can increase susceptibility to enteric pathogens. Here we show that streptomycin treatment depleted commensal, butyrate-producing Clostridia from the mouse intestinal lumen, leading to decreased butyrate levels, increased epithelial oxygenation, and aerobic expansion of Salmonella enterica serovar Typhimurium. Epithelial hypoxia and Salmonella restriction could be restored by tributyrin treatment. Clostridia depletion and aerobic Salmonella expansion were also observed in the absence of streptomycin treatment in genetically resistant mice but proceeded with slower kinetics and required the presence of functional Salmonella type III secretion systems. The Salmonella cytochrome bd-II oxidase synergized with nitrate reductases to drive luminal expansion, and both were required for fecal-oral transmission. We conclude that Salmonella virulence factors and antibiotic treatment promote pathogen expansion through the same mechanism: depletion of butyrate-producing Clostridia to elevate epithelial oxygenation, allowing aerobic Salmonella growth.

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Title: Depletion of Butyrate-Producing Clostridia from the Gut Microbiota Drives an Aerobic Luminal Expansion of Salmonella
Creators: Fabian Rivera-Chávez - Department of Medical Microbiology and Immunology, School of Medicine, University of California at Davis, One Shields Avenue, Davis, CA 95616, USA
Lillian F Zhang - Department of Medical Microbiology and Immunology, School of Medicine, University of California at Davis, One Shields Avenue, Davis, CA 95616, USA
Franziska Faber - Department of Medical Microbiology and Immunology, School of Medicine, University of California at Davis, One Shields Avenue, Davis, CA 95616, USA
Christopher A Lopez - Department of Medical Microbiology and Immunology, School of Medicine, University of California at Davis, One Shields Avenue, Davis, CA 95616, USA
Mariana X Byndloss - Department of Medical Microbiology and Immunology, School of Medicine, University of California at Davis, One Shields Avenue, Davis, CA 95616, USA
Erin E Olsan - Department of Medical Microbiology and Immunology, School of Medicine, University of California at Davis, One Shields Avenue, Davis, CA 95616, USA
Gege Xu - Department of Chemistry, College of Letters and Sciences, University of California at Davis, One Shields Avenue, Davis, CA 95616, USA
Eric M Velazquez - Department of Medical Microbiology and Immunology, School of Medicine, University of California at Davis, One Shields Avenue, Davis, CA 95616, USA
Carlito B Lebrilla - Department of Chemistry, College of Letters and Sciences, University of California at Davis, One Shields Avenue, Davis, CA 95616, USA
Sebastian E Winter - Department of Microbiology, University of Texas Southwestern Medical Center, 5323 Harry Hines Boulevard, Dallas, TX 75390, USA
Andreas J Bäumler - Department of Medical Microbiology and Immunology, School of Medicine, University of California at Davis, One Shields Avenue, Davis, CA 95616, USA. Electronic address: ajbaumler@ucdavis.edu
Academic Unit: Department of Biological Sciences
Publication Details: 04/13/2016
Grant note: R56 AI112949 / NIAID NIH HHS T32 AI060555 / NIAID NIH HHS R25 GM056765 / NIGMS NIH HHS AI112241 / NIAID NIH HHS F31 AI112241 / NIAID NIH HHS OD010931 / NIH HHS T35 OD010956 / NIH HHS R21 AI103248 / NIAID NIH HHS R01 AI076246 / NIAID NIH HHS T32 OD010931 / NIH HHS AI103248 / NIAID NIH HHS R01 AI076278 / NIAID NIH HHS R21 AI117303 / NIAID NIH HHS AI060555 / NIAID NIH HHS R01 AI044170 / NIAID NIH HHS R01 AI112949 / NIAID NIH HHS R01 AI096528 / NIAID NIH HHS AI112949 / NIAID NIH HHS AI096528 / NIAID NIH HHS
Identifiers: 99257882369401671; https://hdl.handle.net/20.500.12741/rep:6644; https://doi.org/10.1016/j.chom.2016.03.004
Language: English