Gut microbiome ADP-ribosyltransferases are widespread phage-encoded fitness factors

Cell Host Microbe. 2021 Sep 8;29(9):1351-1365.e11. doi: 10.1016/j.chom.2021.07.011. Epub 2021 Aug 16.

Abstract

Bacterial ADP-ribosyltransferases (ADPRTs) have been described as toxins involved in pathogenesis through the modification of host proteins. Here, we report that ADPRTs are not pathogen restricted but widely prevalent in the human gut microbiome and often associated with phage elements. We validated their biochemical activity in a large clinical isolate collection and further examined Bxa, a highly abundant ADPRT in Bacteroides. Bxa is expressed, secreted, and enzymatically active in Bacteroides and can ADP-ribosylate non-muscle myosin II proteins. Addition of Bxa to epithelial cells remodeled the actin cytoskeleton and induced secretion of inosine. Bxa-encoding B. stercoris can use inosine as a carbon source and colonizes the gut to significantly greater numbers than a bxa-deleted strain in germ-free and altered Schaedler flora (ASF) mice. Colonization correlated with increased inosine concentrations in the feces and tissues. Altogether, our results show that ADPRTs are abundant in the microbiome and act as bacterial fitness factors.

Keywords: ADP-ribosylation; ADP-ribosyltransferases; Bacteriophages; Bacteroides; Microbiome; biofilms; cytoskeleton; fitness factor; gut colonization; inosine.

Publication types

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

MeSH terms

  • ADP Ribose Transferases / genetics
  • ADP Ribose Transferases / metabolism*
  • Actin Cytoskeleton / metabolism*
  • Animals
  • Bacteriophages / genetics
  • Bacteroides / metabolism*
  • Bacteroides thetaiotaomicron / metabolism*
  • Caco-2 Cells
  • Cell Line, Tumor
  • Epithelial Cells / metabolism*
  • Feces / chemistry
  • Feces / microbiology
  • Female
  • Gastrointestinal Microbiome / genetics
  • Germ-Free Life
  • HT29 Cells
  • Humans
  • Inosine / metabolism*
  • Intestinal Mucosa / metabolism
  • Intestinal Mucosa / microbiology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Myosin Heavy Chains / metabolism

Substances

  • Inosine
  • ADP Ribose Transferases
  • Myosin Heavy Chains

Supplementary concepts

  • Bacteroides stercoris