Discrete and overlapping functions of peptidoglycan synthases in growth, cell division and virulence of Listeria monocytogenes

Mol Microbiol. 2015 Jan;95(2):332-51. doi: 10.1111/mmi.12873. Epub 2014 Dec 19.

Abstract

Upon ingestion of contaminated food, Listeria monocytogenes can cause serious infections in humans that are normally treated with β-lactam antibiotics. These target Listeria's five high molecular weight penicillin-binding proteins (HMW PBPs), which are required for peptidoglycan biosynthesis. The two bi-functional class A HMW PBPs PBP A1 and PBP A2 have transglycosylase and transpeptidase domains catalyzing glycan chain polymerization and peptide cross-linking, respectively, whereas the three class B HMW PBPs B1, B2 and B3 are monofunctional transpeptidases. The precise roles of these PBPs in the cell cycle are unknown. Here we show that green fluorescent protein (GFP)-PBP fusions localized either at the septum, the lateral wall or both, suggesting distinct and overlapping functions. Genetic data confirmed this view: PBP A1 and PBP A2 could not be inactivated simultaneously, and a conditional double mutant strain is largely inducer dependent. PBP B1 is required for rod-shape and PBP B2 for cross-wall biosynthesis and viability, whereas PBP B3 is dispensable for growth and cell division. PBP B1 depletion dramatically increased β-lactam susceptibilities and stimulated spontaneous autolysis but had no effect on peptidoglycan cross-linkage. Our in vitro virulence assays indicated that the complete set of all HMW PBPs is required for maximal virulence.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 3T3 Cells
  • Animals
  • Anti-Bacterial Agents / pharmacology
  • Bacterial Proteins / metabolism
  • Cell Wall / chemistry
  • Cell Wall / physiology
  • HeLa Cells
  • Humans
  • Listeria monocytogenes / cytology
  • Listeria monocytogenes / drug effects
  • Listeria monocytogenes / pathogenicity*
  • Listeria monocytogenes / physiology*
  • Mice
  • Microbial Sensitivity Tests
  • Mutation
  • Penicillin-Binding Proteins / genetics*
  • Penicillin-Binding Proteins / metabolism*
  • Peptidoglycan / metabolism
  • Virulence / genetics
  • beta-Lactams / pharmacology

Substances

  • Anti-Bacterial Agents
  • Bacterial Proteins
  • Penicillin-Binding Proteins
  • Peptidoglycan
  • beta-Lactams