Influence of the fluidity of the membrane on the response of microorganisms to environmental stresses

Abstract. The aim of this mini-review is to relate membrane physical properties to the adaptation and resistance of microorganisms to environmental stresses. In the first part, the effects of various stresses on the structure and dynamic properties of phospholipid and biological membranes are presented. The compensation of these effects, i.e., change in membrane fluidity, phase transitions, by the active cellular control of the membrane chemical composition, is then described. In this natural process, the change in membrane fluidity is viewed as the detecting "input" signal that initiates the regulation, activating proteic effectors that in turn may influence the chemical composition of the membrane (feedback). This adaptation system allows the maintenance of the physical characteristics of membranes and, thereby, of their functionality. When environmental stresses are extreme and occur abruptly, the regulation process may not compensate for the changes in the membrane physical characteristics. In such cases, important variations in the membrane fluidity and structure may induce cellular damages and cell death. However, the lethal consequences are not systematically observed because protective effects of changes in the membrane physical state on the resistance to stresses are also reported.

[1]  W. Brandt,et al.  The LEA-like protein HSP 12 in Saccharomyces cerevisiae has a plasma membrane location and protects membranes against desiccation and ethanol-induced stress. , 2000, Biochimica et biophysica acta.

[2]  J. Crowe,et al.  Membrane Integrity in Anhydrobiotic Organisms: Toward a Mechanism for Stabilizing Dry Cells , 1992 .

[3]  S. Ladha Lipid Heterogeneity and Membrane Fluidity in a Highly Polarized Cell, the Mammalian Spermatozoon , 1998, The Journal of Membrane Biology.

[4]  A. Keith,et al.  The effect of fluidity of membrane lipids on freeze-thaw survival of yeast. , 1978, Cryobiology.

[5]  D S Reid,et al.  Is trehalose special for preserving dry biomaterials? , 1996, Biophysical journal.

[6]  V. Luzzati,et al.  Biological significance of lipid polymorphism: the cubic phases. , 1997, Current opinion in structural biology.

[7]  J. Kingma,et al.  The effect of toluene on the structure and permeability of the outer and cytoplasmic membranes of Escherichia coli. , 1978, Biochimica et biophysica acta.

[8]  G. Lindblom,et al.  Cubic phases and isotropic structures formed by membrane lipids — possible biological relevance , 1989 .

[9]  J. Overstreet,et al.  Cold shock damage is due to lipid phase transitions in cell membranes: a demonstration using sperm as a model. , 1993, The Journal of experimental zoology.

[10]  I. Horváth,et al.  The temperature‐dependent expression of the desaturase gene desA in Synechocystis PCC6803 , 1993, FEBS letters.

[11]  M. Giraud,et al.  Membrane fluidity predicts the outcome of cryopreservation of human spermatozoa. , 2000, Human reproduction.

[12]  Y. Barenholz,et al.  Fluidity parameters of lipid regions determined by fluorescence polarization. , 1978, Biochimica et biophysica acta.

[13]  B. Kruijff Lipid polymorphism and biomembrane function , 1997 .

[14]  T M Swan,et al.  Stress tolerance in a yeast sterol auxotroph: role of ergosterol, heat shock proteins and trehalose. , 1998, FEMS microbiology letters.

[15]  A. Rapoport,et al.  Conservation of Yeasts by Dehydration , 1987, Biotechnology Methods.

[16]  E. Shechter,et al.  Lipid and protein segregation in Escherichia coli membrane: morphological and structural study of different cytoplasmic membrane fractions. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[17]  P. Gervais,et al.  Coupling effects of osmotic pressure and temperature on the viability of Saccharomyces cerevisiae , 2001, Applied Microbiology and Biotechnology.

[18]  J H Crowe,et al.  Trehalose and sucrose protect both membranes and proteins in intact bacteria during drying , 1995, Applied and environmental microbiology.

[19]  Nedwell,et al.  Effect of low temperature on microbial growth: lowered affinity for substrates limits growth at low temperature. , 1999, FEMS microbiology ecology.

[20]  G. Balogh,et al.  Evidence for a lipochaperonin: association of active protein-folding GroESL oligomers with lipids can stabilize membranes under heat shock conditions. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[21]  N J Russell,et al.  Cold adaptation of microorganisms. , 1990, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[22]  M. Jobin,et al.  Molecular characterization of the gene encoding an 18-kilodalton small heat shock protein associated with the membrane of Leuconostoc oenos , 1997, Applied and environmental microbiology.

[23]  N. Morita,et al.  Evidence for cis-trans isomerization of a double bond in the fatty acids of the psychrophilic bacterium Vibrio sp. strain ABE-1 , 1993, Journal of bacteriology.

[24]  J. Killian,et al.  Polymorphic regulation of membrane phospholipid composition in Escherichia coli. , 1993, The Journal of biological chemistry.

[25]  S. Lindquist,et al.  Thermotolerance in Saccharomyces cerevisiae: the Yin and Yang of trehalose. , 1998, Trends in biotechnology.

[26]  M. Sinensky Homeoviscous adaptation--a homeostatic process that regulates the viscosity of membrane lipids in Escherichia coli. , 1974, Proceedings of the National Academy of Sciences of the United States of America.

[27]  D. Los,et al.  Structure and expression of fatty acid desaturases. , 1998, Biochimica et biophysica acta.

[28]  R. McElhaney The structure and function of the Acholeplasma laidlawii plasma membrane. , 1984, Biochimica et biophysica acta.

[29]  K. Watson,et al.  Membrane fatty acid composition and membrane fluidity as parameters of stress tolerance in yeast. , 1997, Canadian journal of microbiology.

[30]  J. D. de Bont,et al.  Bacteria tolerant to organic solvents , 1998, Extremophiles.

[31]  A. Nakano,et al.  The plasma membrane of Saccharomyces cerevisiae: structure, function, and biogenesis. , 1995, Microbiological reviews.

[32]  A. Panek,et al.  Trehalose inhibits ethanol effects on intact yeast cells and liposomes. , 1994, Biochimica et biophysica acta.

[33]  P. Yeagle Regulation of Membrane Function Through Composition, Structure, and Dynamics , 1989, Annals of the New York Academy of Sciences.

[34]  P. Quinn Effects of temperature on cell membranes. , 1988, Symposia of the Society for Experimental Biology.

[35]  L. W. Parks,et al.  Role of sterol structure in the thermotropic behavior of plasma membranes of Saccharomyces cerevisiae , 1983 .

[36]  P. Mazur,et al.  Hyperosmotic tolerance of human spermatozoa: separate effects of glycerol, sodium chloride, and sucrose on spermolysis. , 1993, Biology of reproduction.

[37]  S. Gruner,et al.  Solute-induced shift of phase transition temperature in Di-saturated PC liposomes: adoption of ripple phase creates osmotic stress. , 1997, Biochimica et biophysica acta.

[38]  L. Beney,et al.  Membrane fluidity of stressed cells of Oenococcus oeni. , 2000, International journal of food microbiology.

[39]  C. le Grimellec,et al.  In situ determination of intracellular membrane physical state heterogeneity in renal epithelial cells using fluorescence ratio microscopy , 1998, European Biophysics Journal.

[40]  P. Gervais,et al.  Influence of the shape of phospholipid vesicles on the measurement of their size by photon correlation spectroscopy , 1998, European Biophysics Journal.

[41]  B. de Kruijff Lipid polymorphism and biomembrane function. , 1997, Current opinion in chemical biology.

[42]  B. Curran,et al.  Cellular lipid composition influences stress activation of the yeast general stress response element (STRE). , 2000, Microbiology.

[43]  J. Crowe,et al.  Trehalose lowers membrane phase transitions in dry yeast cells. , 1994, Biochimica et biophysica acta.

[44]  S. Ohnishi,et al.  Osmoelastic coupling in biological structures: decrease in membrane fluidity and osmophobic association of phospholipid vesicles in response to osmotic stress. , 1989, Biochemistry.

[45]  U. Jung,et al.  The protein kinase C-activated MAP kinase pathway of Saccharomyces cerevisiae mediates a novel aspect of the heat shock response. , 1995, Genes & development.

[46]  L. W. Parks,et al.  Influence of sterol structure on yeast plasma membrane properties. , 1985, Biochimica et biophysica acta.

[47]  P. Gervais,et al.  Effect of the kinetics of temperature variation on Saccharomyces cerevisiae viability and permeability. , 1995, Biochimica et biophysica acta.

[48]  C. Laroche,et al.  The effect of osmotic pressure on the membrane fluidity of Saccharomyces cerevisiae at different physiological temperatures , 2001, Applied Microbiology and Biotechnology.

[49]  R. Prasad,et al.  High membrane fluidity is related to NaCl stress in Candida membranefaciens. , 1995, Biochemistry and molecular biology international.

[50]  J. Crowe,et al.  Induction of anhydrobiosis: membrane changes during drying. , 1982, Cryobiology.

[51]  P. Gervais,et al.  Influence of thermal and osmotic stresses on the viability of the yeast Saccharomyces cerevisiae. , 2000, International journal of food microbiology.

[52]  J. Ramos,et al.  Mechanisms for Solvent Tolerance in Bacteria* , 1997, The Journal of Biological Chemistry.

[53]  Quinn Pj,et al.  Effects of temperature on cell membranes. , 1988 .

[54]  J. Käs,et al.  Shape transitions and shape stability of giant phospholipid vesicles in pure water induced by area-to-volume changes. , 1991, Biophysical journal.

[55]  Seifert,et al.  Shape transformations of vesicles: Phase diagram for spontaneous- curvature and bilayer-coupling models. , 1991, Physical review. A, Atomic, molecular, and optical physics.

[56]  K. Watson Thermal adaptation in yeasts: correlation of substrate transport with membrane lipid composition in psychrophilic and thermotolerant yeasts [proceedings]. , 1978, Biochemical Society transactions.

[57]  R. Herbert,et al.  Osmotically induced intracellular trehalose, but not glycine betaine accumulation promotes desiccation tolerance in Escherichia coli. , 1999, FEMS microbiology letters.

[58]  D. Chapman The Role of Water in Biomembrane Structures , 1994 .

[59]  I. Horváth,et al.  The primary signal in the biological perception of temperature: Pd-catalyzed hydrogenation of membrane lipids stimulated the expression of the desA gene in Synechocystis PCC6803. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[60]  J. R. Abney,et al.  Fluctuations and membrane heterogeneity. , 1995, Biophysical chemistry.

[61]  V. Luzzati,et al.  THE STRUCTURE OF THE LIQUID-CRYSTALLINE PHASES OF LIPID-WATER SYSTEMS , 1962, The Journal of cell biology.

[62]  R. Helm,et al.  Engineering Desiccation Tolerance inEscherichia coli , 2000, Applied and Environmental Microbiology.

[63]  R. Welti,et al.  Lipid domains in model and biological membranes. , 1994, Chemistry and physics of lipids.

[64]  L. W. Parks,et al.  Multiple functions for sterols in Saccharomyces cerevisiae. , 1985, Biochimica et Biophysica Acta.

[65]  J. Watts,et al.  Identification and Characterization of an Animal Δ12 Fatty Acid Desaturase Gene by Heterologous Expression in Saccharomyces cerevisiae , 2000 .

[66]  U. Seifert,et al.  Thermal shape fluctuations of fluid-phase phospholipid-bilayer membranes and vesicles , 1997 .

[67]  P. Steponkus,et al.  Phase diagram of 1,2-dioleoylphosphatidylethanolamine (DOPE):water system at subzero temperatures and at low water contents. , 1999, Biochimica et biophysica acta.

[68]  K. Lohner,et al.  Is the high propensity of ethanolamine plasmalogens to form non-lamellar lipid structures manifested in the properties of biomembranes? , 1996, Chemistry and physics of lipids.

[69]  A. Visser,et al.  Oxidation of unsaturated phospholipids in membrane bilayer mixtures is accompanied by membrane fluidity changes. , 2000, Biochimica et biophysica acta.

[70]  S. Harashima,et al.  Transcriptional co‐regulation of Saccharomyces cerevisiae alcohol acetyltransferase gene, ATF1 and Δ‐9 fatty acid desaturase gene, OLE1 by unsaturated fatty acids , 1998, Yeast.

[71]  P. Gervais,et al.  Passive response of Saccharomyces cerevisiae to osmotic shifts: cell volume variations depending on the physiological state. , 1996, Biochemical and biophysical research communications.

[72]  I. Horváth,et al.  Membrane lipid perturbation modifies the set point of the temperature of heat shock response in yeast. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[73]  D. E. Levin,et al.  Dissecting the protein kinase C/MAP kinase signalling pathway of Saccharomyces cerevisiae. , 1994, Cellular & molecular biology research.

[74]  M. Tate,et al.  Energetics of a hexagonal-lamellar-hexagonal-phase transition sequence in dioleoylphosphatidylethanolamine membranes. , 1992, Biochemistry.

[75]  R. Lawaczeck Defect Structures in Membranes: Routes for the Permeation of Small Molecules , 1988 .

[76]  J. Crowe,et al.  Effects of three stabilizing agents--proline, betaine, and trehalose--on membrane phospholipids. , 1986, Archives of biochemistry and biophysics.

[77]  H. Komatsu,et al.  Increased permeability of phase-separated liposomal membranes with mixtures of ethanol-induced interdigitated and non-interdigitated structures. , 1995, Biochimica et biophysica acta.

[78]  Lipid polymorphism and the functional roles of lipids in biological membranes. , 1979 .

[79]  H. Schwarz,et al.  Phase and electron microscopic observations of osmotically induced wrinkling and the role of endocytotic vesicles in the plasmolysis of the Gram-negative cell wall. , 1995, Microbiology.

[80]  M Edidin,et al.  Lipid microdomains in cell surface membranes. , 1997, Current opinion in structural biology.

[81]  E. Bochkareva,et al.  Targeting of GroEL to SecA on the cytoplasmic membrane of Escherichia coli. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[82]  R. McElhaney The influence of membrane lipid composition and physical properties of membrane structure and function in Acholeplasma laidlawii. , 1989, Critical reviews in microbiology.

[83]  A. Cossins,et al.  Temperature, pressure and cholesterol effects on bilayer fluidity; a comparison of pyrene excimer/monomer ratios with the steady-state fluorescence polarization of diphenylhexatriene in liposomes and microsomes. , 1988, Biochimica et biophysica acta.

[84]  J. Watts,et al.  Identification and characterization of an animal delta(12) fatty acid desaturase gene by heterologous expression in Saccharomyces cerevisiae. , 2000, Archives of biochemistry and biophysics.

[85]  R. McElhaney The use of differential scanning calorimetry and differential thermal analysis in studies of model and biological membranes. , 1982, Chemistry and physics of lipids.

[86]  B. Curran,et al.  Alterations in cellular lipids may be responsible for the transient nature of the yeast heat shock response. , 1997, Microbiology.

[87]  T. Mitsui,et al.  Relation between growth temperature of E. coli and phase transition temperatures of its cytoplasmic and outer membranes. , 1980, Biochimica et biophysica acta.

[88]  K. Watson,et al.  Stress tolerance in a yeast lipid mutant: membrane lipids influence tolerance to heat and ethanol independently of heat shock proteins and trehalose. , 1999, Canadian journal of microbiology.

[89]  David Lloyd,et al.  Effects of growth with ethanol on fermentation and membrane fluidity of Saccharomyces cerevisiae , 1993, Yeast.