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

Nat Microbiol. 2022 Oct;7(10):1673-1685. doi: 10.1038/s41564-022-01224-7. Epub 2022 Sep 22.

Abstract

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.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, N.I.H., Extramural

MeSH terms

  • Adenosine Triphosphate / metabolism
  • Amino Acids / metabolism
  • Animals
  • Carbon / metabolism
  • Inflammation
  • Inflammatory Bowel Diseases*
  • Intestines
  • Mice
  • Nitrates / metabolism
  • Veillonella* / genetics
  • Veillonella* / metabolism

Substances

  • Amino Acids
  • Nitrates
  • Carbon
  • Adenosine Triphosphate

Supplementary concepts

  • Veillonella parvula