An iron-containing dodecameric heptosyltransferase family modifies bacterial autotransporters in pathogenesis

Cell Host Microbe. 2014 Sep 10;16(3):351-63. doi: 10.1016/j.chom.2014.08.008.

Abstract

Autotransporters deliver virulence factors to the bacterial surface by translocating an effector passenger domain through a membrane-anchored barrel structure. Although passenger domains are diverse, those found in enteric bacteria autotransporters, including AIDA-I in diffusely adhering Escherichia coli (DAEC) and TibA in enterotoxigenic E. coli, are commonly glycosylated. We show that AIDA-I is heptosylated within the bacterial cytoplasm by autotransporter adhesin heptosyltransferase (AAH) and its paralogue AAH2. AIDA-I heptosylation determines DAEC adhesion to host cells. AAH/AAH2 define a bacterial autotransporter heptosyltransferase (BAHT) family that contains ferric ion and adopts a dodecamer assembly. Structural analyses of the heptosylated TibA passenger domain reveal 35 heptose conjugates forming patterned and solenoid-like arrays on the surface of a β helix. Additionally, CARC, the AIDA-like autotransporter from Citrobacter rodentium, is essential for colonization in mice and requires heptosylation by its cognate BAHT. Our study establishes a bacterial glycosylation system that regulates virulence and is essential for pathogenesis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adhesins, Escherichia coli / genetics
  • Adhesins, Escherichia coli / metabolism*
  • Amino Acid Sequence
  • Animals
  • Bacterial Adhesion
  • Citrobacter rodentium / enzymology
  • Citrobacter rodentium / genetics
  • Citrobacter rodentium / pathogenicity
  • Citrobacter rodentium / physiology
  • Enterobacteriaceae Infections / microbiology
  • Escherichia coli / enzymology*
  • Escherichia coli / genetics
  • Escherichia coli / pathogenicity
  • Escherichia coli / physiology
  • Escherichia coli Infections / microbiology
  • Glycosylation
  • Glycosyltransferases / chemistry
  • Glycosyltransferases / genetics
  • Glycosyltransferases / metabolism*
  • Humans
  • Iron / metabolism*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Molecular Sequence Data
  • Sequence Alignment
  • Virulence

Substances

  • AIDA-I protein, E coli
  • Adhesins, Escherichia coli
  • Iron
  • Glycosyltransferases
  • heptosyltransferase

Associated data

  • PDB/4Q1Q