Inactivation of the dlt operon in Staphylococcus aureus confers sensitivity to defensins, protegrins, and other antimicrobial peptides

J Biol Chem. 1999 Mar 26;274(13):8405-10. doi: 10.1074/jbc.274.13.8405.

Abstract

Positively charged antimicrobial peptides with membrane-damaging activity are produced by animals and humans as components of their innate immunity against bacterial infections and also by many bacteria to inhibit competing microorganisms. Staphylococcus aureus and Staphylococcus xylosus, which tolerate high concentrations of several antimicrobial peptides, were mutagenized to identify genes responsible for this insensitivity. Several mutants with increased sensitivity were obtained, which exhibited an altered structure of teichoic acids, major components of the Gram-positive cell wall. The mutant teichoic acids lacked D-alanine, as a result of which the cells carried an increased negative surface charge. The mutant cells bound fewer anionic, but more positively charged proteins. They were sensitive to human defensin HNP1-3, animal-derived protegrins, tachyplesins, and magainin II, and to the bacteria-derived peptides gallidermin and nisin. The mutated genes shared sequence similarity with the dlt genes involved in the transfer of D-alanine into teichoic acids from other Gram-positive bacteria. Wild-type strains bearing additional copies of the dlt operon produced teichoic acids with higher amounts of D-alanine esters, bound cationic proteins less effectively and were less sensitive to antimicrobial peptides. We propose a role of the D-alanine-esterified teichoic acids which occur in many pathogenic bacteria in the protection against human and animal defense systems.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alanine / analysis
  • Amino Acid Sequence
  • Anti-Bacterial Agents / pharmacology*
  • Antimicrobial Cationic Peptides*
  • Bacterial Proteins*
  • Bacteriocins
  • Carrier Proteins / genetics*
  • DNA-Binding Proteins / pharmacology
  • Defensins
  • Genes, Bacterial / drug effects
  • Genes, Bacterial / genetics
  • Membrane Transport Proteins*
  • Molecular Sequence Data
  • Mutagenesis
  • Nisin / pharmacology
  • Operon / genetics*
  • Peptides*
  • Peptides, Cyclic / pharmacology
  • Proteins / pharmacology
  • Sequence Alignment
  • Staphylococcus aureus / drug effects
  • Staphylococcus aureus / genetics*
  • Teichoic Acids / chemistry
  • Teichoic Acids / genetics
  • alpha-Defensins*

Substances

  • Anti-Bacterial Agents
  • Antimicrobial Cationic Peptides
  • Bacterial Proteins
  • Bacteriocins
  • Carrier Proteins
  • DNA-Binding Proteins
  • Defensins
  • DltB protein, Staphylococcus
  • Membrane Transport Proteins
  • Peptides
  • Peptides, Cyclic
  • Proteins
  • Teichoic Acids
  • alpha-Defensins
  • human neutrophil peptide 1
  • protegrin-1
  • gallidermin
  • tachyplesin peptide, Tachypleus tridentatus
  • Nisin
  • Alanine

Associated data

  • GENBANK/AF032440
  • GENBANK/AF101234