Adaptation of the wine bacterium Oenococcus oeni to ethanol stress: role of the small heat shock protein Lo18 in membrane integrity

Appl Environ Microbiol. 2014 May;80(10):2973-80. doi: 10.1128/AEM.04178-13. Epub 2014 Feb 28.

Abstract

Malolactic fermentation in wine is often carried out by Oenococcus oeni. Wine is a stressful environment for bacteria because ethanol is a toxic compound that impairs the integrity of bacterial membranes. The small heat shock protein (sHsp) Lo18 is an essential actor of the stress response in O. oeni. Lo18 prevents the thermal aggregation of proteins and plays a crucial role in membrane quality control. Here, we investigated the interaction between Lo18 and four types of liposomes: one was prepared from O. oeni grown under optimal growth conditions (here, control liposomes), one was prepared from O. oeni grown in the presence of 8% ethanol (here, ethanol liposomes), one was prepared from synthetic phospholipids, and one was prepared from phospholipids from Bacillus subtilis or Lactococcus lactis. We observed the strongest interaction between Lo18 and control liposomes. The lipid binding activity of Lo18 required the dissociation of oligomeric structures into dimers. Protein protection experiments carried out in the presence of the liposomes from O. oeni suggested that Lo18 had a higher affinity for control liposomes than for a model protein. In anisotropy experiments, we mimicked ethanol action by temperature-dependent fluidization of the liposomes. Results suggest that the principal determinant of Lo18-membrane interaction is lipid bilayer phase behavior rather than phospholipid composition. We suggest a model to describe the ethanol adaptation of O. oeni. This model highlights the dual role of Lo18 in the protection of proteins from aggregation and membrane stabilization and suggests how modifications of phospholipid content may be a key factor determining the balance between these two functions.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptation, Physiological
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism*
  • Cell Membrane / chemistry
  • Cell Membrane / genetics
  • Cell Membrane / metabolism*
  • Ethanol / metabolism*
  • Fermentation
  • Heat-Shock Proteins, Small / genetics
  • Heat-Shock Proteins, Small / metabolism*
  • Liposomes / chemistry
  • Liposomes / metabolism
  • Oenococcus / chemistry
  • Oenococcus / genetics
  • Oenococcus / physiology*
  • Protein Binding
  • Stress, Physiological
  • Wine / microbiology

Substances

  • Bacterial Proteins
  • Heat-Shock Proteins, Small
  • Liposomes
  • Ethanol