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

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

doi:10.1016/j.chom.2016.03.004

Cited by 867Gut microbiota and healthSalmonella and Campylobacter epidemiologyEscherichia coli research studies

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

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Rivera-Chávez, Fabian, Zhang, Lillian F., Faber, Franziska, Lopez, Christopher A., Byndloss, Mariana X., Olsan, Erin E., Xu, Gege, Velazquez, Eric M. +3 more·2016·Cell Host & Microbe

DOI 10.1016/j.chom.2016.03.004PMC PMC4832419

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Abstract

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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When butyrate is reduced with antibiotic treatment, oxygen availability increases, which promotes the growth of facultatively anaerobic pathogens.
“When butyrate is reduced with antibiotic treatment oxygen availability increases, which promotes the growth of facultatively anaerobic pathogens [50].”
From Role of the gut microbiota in nutrient competition and protection against intestinal pathogen colonization (2023) · cites this paper as [50]

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Microbiota-liberated host sugars facilitate post-antibiotic expansion of enteric pathogens
Ng, K. M., Ferreyra, J. A., Higginbottom, S. K., Lynch, J. B., Kashyap, P. C., Gopinath, S., Naidu, N., Choudhury, B., Weimer, B. C., Monack, D. M., et al. (2013) · Nature · doi:10.1038/nature12503 · Cited by 1,035 · see citing works

Authors: Rivera-Chávez, F., Zhang, L. F., Faber, F., Lopez, C. A., Byndloss, M. X., Olsan, E. E., Xu, G., Velazquez, E. M., Lebrilla, C. B., Winter, S. E., & Bäumler, A. J.
Affiliations: University of California, Davis (US)
The University of Texas Southwestern Medical Center (US)
Corresponding author: Bäumler, Andreas J.
ORCID: Rivera-Chávez, Fabian
Faber, Franziska
Lopez, Christopher A.
Byndloss, Mariana X.
Olsan, Erin E.
Xu, Gege
Velazquez, Eric M.
Lebrilla, Carlito B.
Winter, Sebastian E.
Bäumler, Andreas J.
Venue: Cell Host & Microbe
Publisher: Elsevier BV
Published: 2016-04
Volume: 19
Issue: 4
Pages: 443-454
ISSN: 1931-3128 (ISSN-L)
DOI: 10.1016/j.chom.2016.03.004
PMC: PMC4832419
OpenAlex: W2338773685
Cited by: 864
References: 50
Citations by year: 2026: 75 · 2025: 93 · 2024: 93 · 2023: 90 · 2022: 115 · 2021: 127 · 2020: 74 · 2019: 70 · 2018: 60 · 2017: 46 · 2016: 18
FWCI: 33.77
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 377 d)
Locations: Cell Host & Microbe (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
eScholarship (California Digital Library) (submittedVersion)
Funders: National Institutes of Health (T32OD010931, T35OD010956)
National Institute of General Medical Sciences (R25GM056765)
National Institute of Allergy and Infectious Diseases (R01AI044170, AI112949, AI103248, R01AI076278, R21AI103248, AI060555, R01AI076246, F31AI112241, AI096528, AI112241, R56AI112949, R21AI117303, R37AI044170, T32AI060555, R01AI112949, R01AI096528)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
Life Sciences › Agricultural and Biological Sciences › Food Science › Salmonella and Campylobacter epidemiology
Life Sciences › Biochemistry, Genetics and Molecular Biology › Endocrinology › Escherichia coli research studies
Keywords: gut microbiota depletion, Salmonella typhimurium, streptomycin, antibiotic-induced dysbiosis, tributyrin, type III secretion system, nitrate reductase, fecal-oral transmission, host-pathogen interaction, commensal bacteria
MeSH terms: Gastrointestinal Microbiome, Aerobiosis, Animals, Anti-Bacterial Agents, Bacterial Proteins, Clostridium, Female, Intestines, Mice, Inbred CBA, Mice, Inbred C57BL, Oxygen, Salmonella typhimurium, Streptomycin, Butyric Acid, Virulence Factors, Mice

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

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