Crohn's disease-associated adherent-invasive Escherichia coli adhesion is enhanced by exposure to the ubiquitous dietary polysaccharide maltodextrin

PLoS One. 2012;7(12):e52132. doi: 10.1371/journal.pone.0052132. Epub 2012 Dec 12.

Abstract

Crohn's disease (CD) is associated with intestinal dysbiosis evidenced by an altered microbiome forming thick biofilms on the epithelium. Additionally, adherent-invasive E. coli (AIEC) strains are frequently isolated from ileal lesions of CD patients indicating a potential role for these strains in disease pathogenesis. The composition and characteristics of the host microbiome are influenced by environmental factors, particularly diet. Polysaccharides added to food as emulsifiers, stabilizers or bulking agents have been linked to bacteria-associated intestinal disorders. The escalating consumption of polysaccharides in Western diets parallels an increased incidence of CD during the latter 20(th) century. In this study, the effect of a polysaccharide panel on adhesiveness of the CD-associated AIEC strain LF82 was analyzed to determine if these food additives promote disease-associated bacterial phenotypes. Maltodextrin (MDX), a polysaccharide derived from starch hydrolysis, markedly enhanced LF82 specific biofilm formation. Biofilm formation of multiple other E. coli strains was also promoted by MDX. MDX-induced E. coli biofilm formation was independent of polysaccharide chain length indicating a requirement for MDX metabolism. MDX exposure induced type I pili expression, which was required for MDX-enhanced biofilm formation. MDX also increased bacterial adhesion to human intestinal epithelial cell monolayers in a mechanism dependent on type 1 pili and independent of the cellular receptor CEACAM6, suggesting a novel mechanism of epithelial cell adhesion. Analysis of mucosa-associated bacteria from individuals with and without CD showed increased prevalence of malX, a gene essential for MDX metabolism, uniquely in the ileum of CD patients. These findings demonstrate that the ubiquitous dietary component MDX enhances E. coli adhesion and suggests a mechanism by which Western diets rich in specific polysaccharides may promote dysbiosis of gut microbes and contribute to disease susceptibility.

Publication types

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

MeSH terms

  • Animals
  • Antigens, CD / metabolism
  • Bacterial Adhesion / physiology*
  • Biofilms
  • Caco-2 Cells
  • Cell Adhesion / physiology
  • Cell Adhesion Molecules / metabolism
  • Cell Line, Tumor
  • Crohn Disease / metabolism*
  • Crohn Disease / microbiology*
  • Diet / adverse effects
  • Disease Susceptibility / metabolism
  • Disease Susceptibility / microbiology
  • Epithelial Cells / metabolism
  • Epithelial Cells / microbiology
  • Escherichia coli / cytology
  • Escherichia coli / metabolism
  • Escherichia coli / physiology*
  • Escherichia coli Infections / metabolism*
  • Escherichia coli Infections / microbiology
  • Fimbriae, Bacterial / metabolism
  • Food Additives / administration & dosage
  • GPI-Linked Proteins / metabolism
  • HT29 Cells
  • Humans
  • Ileum / metabolism
  • Ileum / microbiology
  • Intestinal Mucosa / metabolism
  • Intestinal Mucosa / microbiology
  • Macrophages / metabolism
  • Macrophages / microbiology
  • Mice
  • Polysaccharides / administration & dosage*

Substances

  • Antigens, CD
  • CEACAM6 protein, human
  • Cell Adhesion Molecules
  • Food Additives
  • GPI-Linked Proteins
  • Polysaccharides
  • maltodextrin