Fusobacteriumnucleatum Adheres to Clostridioides difficile via the RadD Adhesin to Enhance Biofilm Formation in Intestinal Mucus

Gastroenterology. 2021 Mar;160(4):1301-1314.e8. doi: 10.1053/j.gastro.2020.11.034. Epub 2020 Nov 21.

Abstract

Background & aims: Although Clostridioides difficile infection (CDI) is known to involve the disruption of the gut microbiota, little is understood regarding how mucus-associated microbes interact with C difficile. We hypothesized that select mucus-associated bacteria would promote C difficile colonization and biofilm formation.

Methods: To create a model of the human intestinal mucus layer and gut microbiota, we used bioreactors inoculated with healthy human feces, treated with clindamycin and infected with C difficile with the addition of human MUC2-coated coverslips.

Results: C difficile was found to colonize and form biofilms on MUC2-coated coverslips, and 16S rRNA sequencing showed a unique biofilm profile with substantial cocolonization with Fusobacterium species. Consistent with our bioreactor data, publicly available data sets and patient stool samples showed that a subset of patients with C difficile infection harbored high levels of Fusobacterium species. We observed colocalization of C difficile and F nucleatum in an aggregation assay using adult patients and stool of pediatric patients with inflammatory bowel disease and in tissue sections of patients with CDI. C difficile strains were found to coaggregate with F nucleatum subspecies in vitro; an effect that was inhibited by blocking or mutating the adhesin RadD on Fusobacterium and removal of flagella on C difficile. Aggregation was shown to be unique between F nucleatum and C difficile, because other gut commensals did not aggregate with C difficile. Addition of F nucleatum also enhanced C difficile biofilm formation and extracellular polysaccharide production.

Conclusions: Collectively, these data show a unique interaction of between pathogenic C difficile and F nucleatum in the intestinal mucus layer.

Keywords: Biofilm; Clostridioides difficile; MUC2; Mucus.

Publication types

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

MeSH terms

  • Adhesins, Bacterial / genetics
  • Adhesins, Bacterial / metabolism*
  • Bacterial Adhesion / immunology
  • Biofilms
  • Bioreactors / microbiology
  • Clostridioides difficile / genetics
  • Clostridioides difficile / immunology
  • Clostridioides difficile / metabolism
  • Clostridioides difficile / pathogenicity*
  • Clostridium Infections / immunology*
  • Clostridium Infections / microbiology
  • Feces / microbiology
  • Flagella / genetics
  • Flagella / metabolism
  • Fusobacterium nucleatum / immunology*
  • Fusobacterium nucleatum / metabolism
  • Gastrointestinal Microbiome / immunology*
  • HT29 Cells
  • Humans
  • Intestinal Mucosa / immunology
  • Intestinal Mucosa / metabolism
  • Intestinal Mucosa / microbiology
  • Intestinal Mucosa / pathology
  • Mucin-2 / metabolism

Substances

  • Adhesins, Bacterial
  • MUC2 protein, human
  • Mucin-2