4.5 Article

Inflammation-associated nitrate facilitates ectopic colonization of oral bacterium Veillonella parvula in the intestine

Journal

NATURE MICROBIOLOGY
Volume 7, Issue 10, Pages 1673-+

Publisher

NATURE PORTFOLIO
DOI: 10.1038/s41564-022-01224-7

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Funding

  1. National Institutes of Health [P30 DK043351]
  2. Center for Microbiome Informatics and Therapeutics
  3. Crohn's and Colitis Foundation
  4. Deutsche Forschungsgemeinschaft (German Research Foundation) [426120468]

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Veillonella parvula utilizes nitrate produced during inflammation to facilitate colonization in the intestine, which has significant implications for understanding the pathogenesis and treatment of inflammatory bowel disease.
Colonization of the intestine by oral microbes has been linked to multiple diseases such as inflammatory bowel disease and colon cancer, yet mechanisms allowing expansion in this niche remain largely unknown. Veillonella parvula, an asaccharolytic, anaerobic, oral microbe that derives energy from organic acids, increases in abundance in the intestine of patients with inflammatory bowel disease. Here we show that nitrate, a signature metabolite of inflammation, allows V. parvula to transition from fermentation to anaerobic respiration. Nitrate respiration, through the narGHJI operon, boosted Veillonella growth on organic acids and also modulated its metabolic repertoire, allowing it to use amino acids and peptides as carbon sources. This metabolic shift was accompanied by changes in carbon metabolism and ATP production pathways. Nitrate respiration was fundamental for ectopic colonization in a mouse model of colitis, because a V. parvula narG deletion mutant colonized significantly less than a wild-type strain during inflammation. These results suggest that V. parvula harness conditions present during inflammation to colonize in the intestine. The oral bacterium Veillonella parvula utilizes inflammation-associated nitrate to facilitate colonization of the intestinal tract, which is observed in a mouse model of colitis and patients with inflammatory bowel disease.

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