Role of lipid-bound peptidoglycan precursors in the formation of pores by nisin, epidermin and other lantibiotics

Mol Microbiol. 1998 Oct;30(2):317-27. doi: 10.1046/j.1365-2958.1998.01065.x.

Abstract

It is generally assumed that type A lantibiotics primarily kill bacteria by permeabilization of the cytoplasmic membrane. As previous studies had demonstrated that nisin interacts with the membrane-bound peptidoglycan precursors lipid I and lipid II, we presumed that this interaction could play a role in the pore formation process of lantibiotics. Using a thin-layer chromatography system, we found that only nisin and epidermin, but not Pep5, can form a complex with [14C]-lipid II. Lipid II was then purified from Micrococcus luteus and incorporated into carboxyfluorescein-loaded liposomes made of phosphatidylcholine and cholesterol (1:1). Liposomes supplemented with 0.05 or 0.1 mol% of lipid II did not release any marker when treated with Pep5 or epilancin K7 (peptide concentrations of up to 5 mol% were tested). In contrast, as little as 0.01 mol% of epidermin and 0.1 mol% of nisin were sufficient to induce rapid marker release; phosphatidylglycerol-containing liposomes were even more susceptible. Controls with moenomycin-, undecaprenol- or dodecaprenolphosphate-doped liposomes demonstrated the specificity of the lantibiotics for lipid II. These results were correlated with intact cells in an in vivo model. M. luteus and Staphylococcus simulans were depleted of lipid II by preincubation with the lipopeptide ramoplanin and then tested for pore formation. When applied in concentrations below the minimal inhibitory concentration (MIC) and up to 5-10 times the MIC, the pore formation by nisin and epidermin was blocked; at higher concentrations of the lantibiotics the protective effect of ramoplanin disappeared. These results demonstrate that, in vitro and in vivo, lipid II serves as a docking molecule for nisin and epidermin, but not for Pep5 and epilancin K7, and thereby facilitates the formation of pores in the cytoplasmic membrane.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Anti-Bacterial Agents / metabolism
  • Anti-Bacterial Agents / pharmacology*
  • Bacteriocins
  • Depsipeptides*
  • Liposomes / metabolism
  • Micrococcus luteus / drug effects
  • Micrococcus luteus / metabolism
  • Nisin / metabolism
  • Nisin / pharmacology*
  • Peptides*
  • Peptides, Cyclic*
  • Peptidoglycan / drug effects
  • Peptidoglycan / metabolism*
  • Polyisoprenyl Phosphate Oligosaccharides / metabolism
  • Staphylococcus / drug effects
  • Staphylococcus / metabolism

Substances

  • Anti-Bacterial Agents
  • Bacteriocins
  • Depsipeptides
  • Liposomes
  • Peptides
  • Peptides, Cyclic
  • Peptidoglycan
  • Polyisoprenyl Phosphate Oligosaccharides
  • ramoplanin
  • mersacidin
  • Nisin
  • undecaprenyl diphosphate-(N-acetylglucosaminyl)(1-4)-N-acetylmuramoyl pentapeptide
  • epidermin