Antibodies Set Boundaries Limiting Microbial Metabolite Penetration and the Resultant Mammalian Host Response
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Abstract
Although the mammalian microbiota is well contained within the intestine, it profoundly shapes development and metabolism of almost every host organ. We questioned the range and depth of microbial metabolite penetration into the host, and how this is modulated by intestinal immunity. Chemically identical microbial and host metabolites were distinguished by stable isotope tracing from 13 C-labeled live non-replicating Escherichia coli , differentiating 12 C host isotopes with high-resolution mass spectrometry. Hundreds of endogenous microbial compounds penetrated 23 host tissues and fluids after intestinal exposure: subsequent 12 C host metabolome signatures included lipidemia, reduced glycolysis, and inflammation. Penetrant bacterial metabolites from the small intestine were rapidly cleared into the urine, whereas induced antibodies curtailed microbial metabolite exposure by accelerating intestinal bacterial transit into the colon where metabolite transport mechanisms are limiting. Pervasive penetration of microbial molecules can cause extensive host tissue responses: these are limited by immune and non-immune intestinal mucosal adaptations to the microbiota.
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Bacterial products and metabolites can pass the blood-brain barrier and shape CNS development and functions and the genesis of certain diseases.
“Among the molecules that can pass the BBB are also bacterial products and metabolites shaping not only the CNS development and functions (6, 15) but also the genesis of certain diseases (33–42).”
From The gut-brain axis: how microbiota and host inflammasome influence brain physiology and pathology (2020) · cites this paper as [6]
Under healthy conditions, the microbiota influences numerous physiological processes within the host, including protection against pathogens, nutrient digestion and absorption, development, and education of multiple host organs and the immune system.
“Under healthy conditions, the microbiota influences numerous physiological processes within the host, such as protection against pathogens, nutrient digestion and absorption, development, and education of multiple host organs and the immune system (3–6).”
From The gut-brain axis: how microbiota and host inflammasome influence brain physiology and pathology (2020) · cites this paper as [6]
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Legoux, F., Bellet, D., Daviaud, C., El Morr, Y., Darbois, A., Niort, K., Procopio, E., Salou, M., Gilet, J., Ryffel, B., et al. (2019) · Science · doi:10.1126/science.aaw2719 · Cited by 320 · see citing works
Mining the microbiota for microbial and metabolite-based immunotherapies
Skelly, A. N., Sato, Y., Kearney, S., & Honda, K. (2019) · Nature Reviews Immunology · doi:10.1038/s41577-019-0144-5 · Cited by 306 · see citing works
Gut Microbiota and Iron: The Crucial Actors in Health and Disease
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Self-citationDiversity and dynamism of IgA−microbiota interactions
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Deciphering the Chemical Lexicon of Host–Gut Microbiota Interactions
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Microbiota-gut brain axis involvement in neuropsychiatric disorders
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Microbiota alters the metabolome in an age- and sex- dependent manner in mice
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- Authors
- Uchimura, Y., Fuhrer, T., Li, H., Lawson, M. A., Zimmermann, M., Yilmaz, B., Zindel, J., Ronchi, F., Sorribas, M., Hapfelmeier, S., Ganal-Vonarburg, S. C., Gomez de Agüero, M., McCoy, K. D., Sauer, U., & Macpherson, A. J.
- Affiliations
- University of Bern (CH)
- ETH Zurich (CH)
- Corresponding author
- Sauer, Uwe
- Macpherson, Andrew J.
- ORCID
- Venue
- Immunity
- Publisher
- Elsevier BV
- Published
- 2018-09
- Volume
- 49
- Issue
- 3
- Pages
- 545-559.e5
- ISSN
- 1074-7613 (ISSN-L)
- PMC
- PMC6162337
- OpenAlex
- W2758170246
- Cited by
- 153
- References
- 86
- Citations by year
- 2026: 7 · 2025: 17 · 2024: 18 · 2023: 21 · 2022: 21 · 2021: 21 · 2020: 29 · 2019: 16 · 2018: 3
- FWCI
- 6.14
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Immunity (publishedVersion, cc-by-nc-nd)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
- Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Repository for Publications and Research Data (ETH Zurich) (publishedVersion, cc-by-nc-nd)
- Bern Open Repository and Information System (University of Bern) (submittedVersion, cc-by-nc-nd)
- ETH Zürich Research Collection
- Funders
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (SNSF 310030B_160262, CRSII3_136286, CRSII3_154414)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolomics and Mass Spectrometry Studies
- Keywords
- microbial metabolites, host-microbe interactions, intestinal immunity, antibody-mediated clearance, Escherichia coli, stable isotope tracing, metabolite transport, lipidemia, glycolysis, inflammation, gut microbiota
- MeSH terms
- Gastrointestinal Microbiome, Animals, Antibodies, Carbon Radioisotopes, Glycolysis, Hyperlipidemias, Immunity, Immunoglobulin Heavy Chains, Inflammation, Mammals, Mice, Inbred C57BL, Mass Spectrometry, Mice, Knockout, Mice, Host-Pathogen Interactions
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