Colonocyte-derived lactate promotes E. coli fitness in the context of inflammation-associated gut microbiota dysbiosis

Microbiome. 2022 Nov 26;10(1):200. doi: 10.1186/s40168-022-01389-7.

Abstract

Background: Intestinal inflammation disrupts the microbiota composition leading to an expansion of Enterobacteriaceae family members (dysbiosis). Associated with this shift in microbiota composition is a profound change in the metabolic landscape of the intestine. It is unclear how changes in metabolite availability during gut inflammation impact microbial and host physiology.

Results: We investigated microbial and host lactate metabolism in murine models of infectious and non-infectious colitis. During inflammation-associated dysbiosis, lactate levels in the gut lumen increased. The disease-associated spike in lactate availability was significantly reduced in mice lacking the lactate dehydrogenase A subunit in intestinal epithelial cells. Commensal E. coli and pathogenic Salmonella, representative Enterobacteriaceae family members, utilized lactate via the respiratory L-lactate dehydrogenase LldD to increase fitness. Furthermore, mice lacking the lactate dehydrogenase A subunit in intestinal epithelial cells exhibited lower levels of inflammation in a model of non-infectious colitis.

Conclusions: The release of lactate by intestinal epithelial cells during gut inflammation impacts the metabolism of gut-associated microbial communities. These findings suggest that during intestinal inflammation and dysbiosis, changes in metabolite availability can perpetuate colitis-associated disturbances of microbiota composition. Video Abstract.

Keywords: Gut inflammation; Host-microbe interactions; Lactate metabolism.

Publication types

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

MeSH terms

  • Animals
  • Colitis* / pathology
  • Dysbiosis
  • Enterobacteriaceae / metabolism
  • Escherichia coli / metabolism
  • Gastrointestinal Microbiome*
  • Inflammation / pathology
  • Lactate Dehydrogenase 5
  • Lactic Acid / metabolism
  • Mice
  • Mice, Inbred C57BL

Substances

  • Lactic Acid
  • Lactate Dehydrogenase 5