Metabolic diversity in commensal protists regulates intestinal immunity and trans-kingdom competition

The microbiota influences intestinal health and physiology, yet the contributions of commensal protists to the gut environment have been largely overlooked. Here, we discover human- and rodent-associated parabasalid protists, revealing substantial diversity and prevalence in nonindustrialized human...

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Bibliographic Details
Published in:Cell 2024-01, Vol.187 (1), p.62-78.e20
Main Authors: Gerrick, Elias R, Zlitni, Soumaya, West, Patrick T, Carter, Matthew M, Mechler, Claire M, Olm, Matthew R, Caffrey, Elisa B, Li, Jessica A, Higginbottom, Steven K, Severyn, Christopher J, Kracke, Frauke, Spormann, Alfred M, Sonnenburg, Justin L, Bhatt, Ami S, Howitt, Michael R
Format: Article
Language:English
Subjects:
excretion
genomics
humans
immunity
intestines
metabolism
metabolites
metabolomics
mice
microorganisms
mucus
niches
polysaccharides
protists
succinic acid
Tritrichomonas
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Summary:The microbiota influences intestinal health and physiology, yet the contributions of commensal protists to the gut environment have been largely overlooked. Here, we discover human- and rodent-associated parabasalid protists, revealing substantial diversity and prevalence in nonindustrialized human populations. Genomic and metabolomic analyses of murine parabasalids from the genus Tritrichomonas revealed species-level differences in excretion of the metabolite succinate, which results in distinct small intestinal immune responses. Metabolic differences between Tritrichomonas species also determine their ecological niche within the microbiota. By manipulating dietary fibers and developing in vitro protist culture, we show that different Tritrichomonas species prefer dietary polysaccharides or mucus glycans. These polysaccharide preferences drive trans-kingdom competition with specific commensal bacteria, which affects intestinal immunity in a diet-dependent manner. Our findings reveal unappreciated diversity in commensal parabasalids, elucidate differences in commensal protist metabolism, and suggest how dietary interventions could regulate their impact on gut health.
ISSN:0092-8674
1097-4172
1097-4172
DOI:10.1016/j.cell.2023.11.018