Expression of OXA-type and SFO-1 β-lactamases induces changes in peptidoglycan composition and affects bacterial fitness

Antimicrob Agents Chemother. 2012 Apr;56(4):1877-84. doi: 10.1128/AAC.05402-11. Epub 2012 Jan 30.

Abstract

β-Lactamases and penicillin-binding proteins (PBPs) have evolved from a common ancestor. β-Lactamases are enzymes that degrade β-lactam antibiotics, whereas PBPs are involved in the synthesis and processing of peptidoglycan, which forms an elastic network in the bacterial cell wall. This study analyzed the interaction between β-lactamases and peptidoglycan and the impact on fitness and biofilm production. A representative set of all classes of β-lactamases was cloned in the expression vector pBGS18 under the control of the CTX-M promoter and expressed in Escherichia coli MG1655. The peptidoglycan composition of all clones was evaluated, and quantitative changes were found in E. coli strains expressing OXA-24, OXA-10-like, and SFO-1 (with its upstream regulator AmpR) β-lactamases; the level of cross-linked muropeptides decreased, and their average length increased. These changes were associated with a statistically significant fitness cost, which was demonstrated in both in vitro and in vivo experiments. The observed changes in peptidoglycan may be explained by the presence of residual DD-endopeptidase activity in these β-lactamases, which may result in hydrolysis of the peptide cross bridge. The biological cost associated with these changes provides important data regarding the interaction between β-lactamases and the metabolism of peptidoglycan and may provide an explanation for the epidemiology of these β-lactamases in Enterobacteriaceae.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Biofilms
  • Cloning, Molecular
  • Drug Resistance, Bacterial / genetics
  • Escherichia coli / drug effects*
  • Escherichia coli / genetics
  • Escherichia coli / pathogenicity*
  • Escherichia coli Infections / microbiology
  • Female
  • Mice
  • Microscopy, Electron, Transmission
  • Peptidoglycan / chemistry*
  • Peptidoglycan / metabolism
  • Phenotype
  • Plasmids / genetics
  • beta-Lactamases / biosynthesis*
  • beta-Lactamases / genetics*

Substances

  • Peptidoglycan
  • beta-lactamase OXA-10
  • beta-lactamase SFO-1
  • beta-Lactamases
  • beta-lactamase OXA-24