Salmonella enterica serovar typhimurium exploits inflammation to compete with the intestinal microbiota
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Most mucosal surfaces of the mammalian body are colonized by microbial communities ("microbiota"). A high density of commensal microbiota inhabits the intestine and shields from infection ("colonization resistance"). The virulence strategies allowing enteropathogenic bacteria to successfully compete with the microbiota and overcome colonization resistance are poorly understood. Here, we investigated manipulation of the intestinal microbiota by the enteropathogenic bacterium Salmonella enterica subspecies 1 serovar Typhimurium (S. Tm) in a mouse colitis model: we found that inflammatory host responses induced by S. Tm changed microbiota composition and suppressed its growth. In contrast to wild-type S. Tm, an avirulent invGsseD mutant failing to trigger colitis was outcompeted by the microbiota. This competitive defect was reverted if inflammation was provided concomitantly by mixed infection with wild-type S. Tm or in mice (IL10(-/-), VILLIN-HA(CL4-CD8)) with inflammatory bowel disease. Thus, inflammation is necessary and sufficient for overcoming colonization resistance. This reveals a new concept in infectious disease: in contrast to current thinking, inflammation is not always detrimental for the pathogen. Triggering the host's immune defence can shift the balance between the protective microbiota and the pathogen in favour of the pathogen.
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The typically low-abundance Enterobacteraceae expand in concert with inflammation and degree of dysbiosis of the Firmicutes:Bacteroidetes ratio.
“The typically low-abundance Enterobacteraceae expand in concert with inflammation[336] and degree of dysbiosis of the Firmicutes:Bacteroidetes ratio[333,337,338].”
From Enterosalivary nitrate metabolism and the microbiome: Intersection of microbial metabolism, nitric oxide and diet in cardiac and pulmonary vascular health (2017) · cites this paper as [338]
In inflammatory bowel disease, massive blooms of pathogenic, nitrate-reducing Salmonella and Escherichia coli are seen in response to inflammation.
“This shift is particularly notable in the context of inflammatory bowel disease, where massive blooms of pathogenic, nitrate-reducing Salmonella and Escherichia coli are seen in response to inflammation[333,334,338,339].”
From Enterosalivary nitrate metabolism and the microbiome: Intersection of microbial metabolism, nitric oxide and diet in cardiac and pulmonary vascular health (2017) · cites this paper as [338]
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- Authors
- Stecher, B., Robbiani, R., Walker, A. W., Westendorf, A. M., Barthel, M., Kremer, M., Chaffron, S., Macpherson, A. J., Buer, J., Parkhill, J., Dougan, G., von Mering, C., & Hardt, W.-D.
- Affiliations
- Institute of Microbiology (CH)
- Wellcome Sanger Institute (GB)
- Helmholtz Centre for Infection Research (DE)
- Technical University of Munich (DE)
- University of Zurich (CH)
- McMaster University (CA)
- Corresponding author
- Hardt, Wolf-Dietrich
- ORCID
- Venue
- PLoS Biology
- Publisher
- Public Library of Science (PLoS)
- Published
- 2007-08-28
- Volume
- 5
- Issue
- 10
- Pages
- e244
- ISSN
- 1544-9173 (ISSN-L)
- 1545-7885
- PMC
- PMC1951780
- OpenAlex
- W2084120324
- Cited by
- 1,048
- References
- 64
- Citations by year
- 2026: 24 · 2025: 43 · 2024: 60 · 2023: 51 · 2022: 49 · 2021: 62 · 2020: 62 · 2019: 55 · 2018: 47 · 2017: 63 · 2016: 70 · 2015: 74 · 2014: 65 · 2013: 79 · 2012: 55
- FWCI
- 14.72
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS Biology (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Zurich Open Repository and Archive (University of Zurich) (acceptedVersion, cc-by)
- Aberdeen University Research Archive (Aberdeen University) (submittedVersion)
- HAL (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- HZI (Helmholtz Centre for Infection Research) (submittedVersion)
- Minerva Access (University of Melbourne) (submittedVersion, cc-by)
- mediaTUM – the media and publications repository of the Technical University Munich (Technical University Munich) (submittedVersion)
- Repository for Publications and Research Data (ETH Zurich) (submittedVersion, cc-by)
- Zurich Open Repository and Archive (University of Zurich) (submittedVersion, cc-by)
- ETH Zürich Research Collection (cc-by)
- Zurich Open Repository and Archive (University of Zurich)
- Funders
- National Science Foundation
- Wellcome Trust
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (100175, 3100A0)
- 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
- Salmonella typhimurium, gut microbiota, colonization resistance, inflammation, competitive fitness, colitis, IL-10 deficiency, inflammatory bowel disease, host-pathogen interaction, commensal bacteria
- MeSH terms
- Animals, Bacteria, Colitis, Female, Genotype, Intestines, Male, Mice, Inbred C3H, Mice, Inbred C57BL, Mice, Inbred Strains, Microscopy, Fluorescence, Molecular Sequence Data, Mutation, Phylogeny, RNA, Ribosomal, 16S, Salmonella Infections, Salmonella typhimurium, In Situ Hybridization, Fluorescence, Sequence Analysis, DNA, Models, Animal, Mice
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