Variations in carotenoid content and acyl chain composition in exponential, stationary and biofilm states of Staphylococcus aureus, and their influence on membrane biophysical properties

Biochim Biophys Acta Biomembr. 2019 May 1;1861(5):978-987. doi: 10.1016/j.bbamem.2019.02.001. Epub 2019 Feb 13.

Abstract

Bacteria are often found in close association with surfaces, resulting in the formation of biofilms. In Staphylococcus aureus (S. aureus), biofilms are implicated in the resilience of chronic infections, presenting a serious clinical problem world-wide. Here, S. aureus biofilms are grown under flow within clinical catheters at 37 °C. The lipid composition and biophysical properties of lipid extracts from these biofilms are compared with those from exponential growth and stationary phase cells. Biofilms show a reduction in iso and anteiso branching compensated by an increase in saturated fatty acids compared to stationary phase. A drastic reduction in carotenoid levels is also observed during biofilm formation. Thermotropic measurements of Laurdan GP and DPH polarization, show a reduction of lipid packing at 37 °C for biofilms compared to stationary phase. We studied the effects of carotenoid content on DMPG and DPPG model membranes showing trends in thermotropic behavior consistent with those observed in bacterial isolates, indicating that carotenoids participate in modulating lipid packing. Additionally, bending elastic constant (kc) measurements using vesicle fluctuation analysis (VFA) show that the presence of carotenoids can increase membrane bending rigidity. The antimicrobial peptide Magainin H2 was less activity on liposomes composed of stationary phase compared to biofilms or exponential growth isolates. This study contributes to an understanding of how Staphylococcus aureus modulates the composition of its membrane lipids, and how those changes affect the biophysical properties of membranes, which in turn may play a role in its virulence and its resistance to different membrane-active antimicrobial agents.

Keywords: Antimicrobial peptides; Biofilm; Carotenoids; Lipid composition; Membrane mechanical properties; Staphylococcus aureus.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Anti-Bacterial Agents / chemistry
  • Anti-Bacterial Agents / pharmacology
  • Antimicrobial Cationic Peptides / chemistry
  • Antimicrobial Cationic Peptides / pharmacology
  • Biofilms / drug effects
  • Biofilms / growth & development*
  • Carotenoids / chemistry
  • Carotenoids / metabolism*
  • Microbial Sensitivity Tests
  • Particle Size
  • Phosphatidylglycerols / chemistry
  • Phosphatidylglycerols / metabolism*
  • Staphylococcus aureus / chemistry
  • Staphylococcus aureus / drug effects
  • Staphylococcus aureus / isolation & purification
  • Staphylococcus aureus / metabolism*
  • Surface Properties
  • Temperature

Substances

  • Anti-Bacterial Agents
  • Antimicrobial Cationic Peptides
  • Phosphatidylglycerols
  • Carotenoids
  • dimyristoylphosphatidylglycerol
  • 1,2-dipalmitoylphosphatidylglycerol