Outer membrane barrier impairment by envC deletion reduces gut colonization of Crohn's disease pathobiont Escherichia coli

Microbiology (Reading). 2024 Oct;170(10):001509. doi: 10.1099/mic.0.001509.

Abstract

Adherent-invasive Escherichia coli (AIEC) has been implicated in the aetiology of Crohn's disease (CD), a chronic inflammatory disorder of the gastrointestinal tract. The presence of Enterobacteriaceae, including AIEC, is heightened in the intestines of CD patients. Therefore, inhibiting AIEC colonization in the gastrointestinal tract could be a promising therapeutic intervention for CD. This study aims to assess the potential of EnvC as a novel therapeutic target, examining how disrupting EnvC activity through the deletion of the envC gene decreases AIEC gut colonization levels. EnvC serves as a catalyst for peptidoglycan (also called murein) amidases, facilitating bacterial cell division. An AIEC mutant lacking the envC gene exhibited impaired cell division. Furthermore, envC deletion led to a diminished outer membrane barrier, as seen in our finding that the envC mutant became susceptible to vancomycin. Finally, we found that the envC mutant is impaired in competitive gut colonization in a dysbiotic mouse model. The colonization defects might be attributable to reduced resistance to colonic bile acids, as evidenced by our finding that increased colonic levels of bile acids inhibited the colonization of the gastrointestinal tract by AIEC strains. The present findings suggest that targeting bacterial cell division through the inhibition of EnvC activity could represent a promising intervention for CD.

Keywords: AIEC; Crohn’s disease; bile acids; cell division; gut colonization; outer membrane barrier.

MeSH terms

  • Animals
  • Bacterial Outer Membrane / metabolism
  • Bile Acids and Salts / metabolism
  • Cell Division
  • Crohn Disease* / drug therapy
  • Crohn Disease* / microbiology
  • Crohn Disease* / pathology
  • Disease Models, Animal
  • Dysbiosis / microbiology
  • Dysbiosis / pathology
  • Endopeptidases* / genetics
  • Epithelial Cells / microbiology
  • Escherichia coli Proteins* / genetics
  • Escherichia coli* / drug effects
  • Gastrointestinal Tract / microbiology
  • Mice
  • Mice, Inbred C57BL
  • Mutation
  • Phagocytes / immunology

Substances

  • EnvC protein, E coli
  • Endopeptidases
  • Escherichia coli Proteins
  • Bile Acids and Salts