Growth of Staphylococcus aureus in the presence of oleic acid shifts the glycolipid fatty acid profile and increases resistance to antimicrobial peptides

Biochim Biophys Acta Biomembr. 2025 Jan;1867(1):184395. doi: 10.1016/j.bbamem.2024.184395. Epub 2024 Nov 3.

Abstract

Staphylococcus aureus readily adapts to various environments and quickly develops antibiotic resistance, which has led to an increase in multidrug-resistant infections. Hence, S. aureus presents a significant global health issue and its adaptations to the host environment are crucial for understanding pathogenesis and antibiotic susceptibility. When S. aureus is grown conventionally, its membrane lipids contain a mix of branched-chain and straight-chain saturated fatty acids. However, when unsaturated fatty acids are present in the growth medium, they become a major part of the total fatty acid composition. This study explores the biophysical effects of incorporating straight-chain unsaturated fatty acids into S. aureus membrane lipids. Membrane preparations from cultures supplemented with oleic acid showed more complex differential scanning calorimetry scans than those grown in tryptic soy broth alone. When grown in the presence of oleic acid, the cultures exhibited a transition significantly above the growth temperature, attributed to the presence of glycolipids with long-chain fatty acids causing acyl chain packing frustration within the bilayer. Functional aspects of the membrane were assessed by studying the kinetics of dye release from unilamellar vesicles induced by the antimicrobial peptide mastoparan X. Dye release was slower from liposomes prepared from cells grown in oleic acid-supplemented cultures, suggesting that changes in membrane lipid composition and biophysics protect the cell membrane against peptide-induced lysis. These findings underscore the intricate relationship between the growth environment, membrane lipid composition, and the physical properties of the bacterial membrane, which should be considered when developing new strategies against S. aureus infections.

Keywords: Antimicrobial peptides; Inverted lipid phases; Lipid adaptation; Lipid bilayer; Membranes; S. aureus.

MeSH terms

  • Anti-Bacterial Agents / chemistry
  • Anti-Bacterial Agents / pharmacology
  • Antimicrobial Peptides / chemistry
  • Antimicrobial Peptides / metabolism
  • Antimicrobial Peptides / pharmacology
  • Cell Membrane / chemistry
  • Cell Membrane / drug effects
  • Cell Membrane / metabolism
  • Drug Resistance, Bacterial / drug effects
  • Fatty Acids* / chemistry
  • Fatty Acids* / metabolism
  • Glycolipids* / chemistry
  • Glycolipids* / metabolism
  • Glycolipids* / pharmacology
  • Membrane Lipids / chemistry
  • Membrane Lipids / metabolism
  • Microbial Sensitivity Tests
  • Oleic Acid* / chemistry
  • Oleic Acid* / metabolism
  • Oleic Acid* / pharmacology
  • Staphylococcus aureus* / drug effects
  • Staphylococcus aureus* / growth & development
  • Staphylococcus aureus* / metabolism

Substances

  • Oleic Acid
  • Glycolipids
  • Fatty Acids
  • Antimicrobial Peptides
  • Membrane Lipids
  • Anti-Bacterial Agents