The Regulation of Membrane Fluidity in Bacteria by Acyl Chain Length Changes

  • Nicholas J. Russell
Part of the Biomembranes book series (B, volume 12)


It has been appreciated for many years that certain organisms, notably poikilotherms including bacteria, alter the fatty acyl composition of their lipids in response to changes in environmental temperature. Publication of the “fluid mosaic model” of membrane structure (Singer and Nicolson, 1972) signaled a decade in which our comprehension of the physiological significance of these fatty acyl changes has grown very considerably. The application of physical techniques, such as electron spin resonance (ESR) and nuclear magnetic resonance, to membranes and their lipids has in particular shown how membrane fluidity is modulated by lipid acyl composition. These findings are embodied in the widely accepted “mosaic” model of membrane structure in which intrinsic proteins are embedded in or traverse a lipid bilayer; thus, lipid acyl chains are in contact with polypeptide chains and may regulate the activity of enzyme active sites directly or indirectly. The nature of the phospholipid (or glycolipid) head group may also be important in lipid-protein interactions. But much less is known about the role of head groups in membrane lipid fluidity, and this aspect will not be dealt with in this review (see Keough and Davis, this volume).


Electron Spin Resonance Membrane Fluidity Acyl Chain Fatty Acid Synthesis Desaturase Activity 


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  1. Baldassare, J. J., Rhinehart, K. B., and Silbert, D. F., 1976, Modification of membrane lipid: physical properties in relation to fatty acid structure, Biochemistry 15:2986.PubMedCrossRefGoogle Scholar
  2. Cameron, D. G., Gudgin, E. F., and Mantsch, H. H., 1981, Dependence of acyl chain packing of phospholipids on the head group and acyl chain length, Biochemistry 20:4496.PubMedCrossRefGoogle Scholar
  3. Chapman, D., 1975, Phase transitions and fluidity characteristics of lipids and cell membranes, Q. Rev. Biophys. 8:185.PubMedCrossRefGoogle Scholar
  4. Chen, S. C., and Sturtevant, J. M., 1981, Thermotropic behaviour of bilayers formed from mixed-chain phosphatidylcholines, Biochemistry 20:713.PubMedCrossRefGoogle Scholar
  5. Cossins, A. R., and Prosser, C. L., 1978, Evolutionary adaptation of membranes to temperature, Proc. Natl. Acad. Sci. USA 75:2040.PubMedCrossRefGoogle Scholar
  6. Cronan, J. E., Jr., 1978, Molecular biology of bacterial membrane lipids, Annu. Rev. Biochem. 47:163.PubMedCrossRefGoogle Scholar
  7. Cronan, J. E., Jr., and Vagelos, P. R., 1972, Metabolism and function of the membrane phospholipids of Escherichia coli, Biochim. Biophys. Acta 265:25.PubMedGoogle Scholar
  8. Cronan, J. E., Jr., Weisberg, J. L., and Allen, R. G., 1975, Regulation of membrane lipid synthesis in Escherichia coli. Accumulation of free fatty acids of abnormal length during inhibition of phospholipid synthesis, J. Biol. Chem. 250:5835.PubMedGoogle Scholar
  9. Cullis, P. R., and de Kruijff, B., 1979, Lipid polymorphism and the functional roles of lipids in biological membranes, Biochim. Biophys. Acta 559:399.PubMedGoogle Scholar
  10. D’Agnolo, G., Rosenfeld, I. S., Awaya, J., Omura, S., and Vagelos, P. R., 1973, Inhibition of fatty acid synthesis by the antibiotic cerulenin. Specific inactivation of β-ketoacyl acyl carrier protein synthetase, Biochim. Biophys. Acta 326:155.PubMedGoogle Scholar
  11. Davis, J. H., Nichol, C. P., Weeks, G., and Blood, M., 1979, Study of the cytoplasmic and outer membranes of Escherichia coli by deuterium magnetic resonance, Biochemistry 18:2103.PubMedCrossRefGoogle Scholar
  12. Davis, P. J., Fleming, B. D., Coolbear, K. P., and Keough, K. M. W., 1981, Gel to liquid-crystalline transition temperatures of water dispersions of two pairs of positional isomers of unsaturated mixed-acid phosphatidylcholines, Biochemistry 20:3633.PubMedCrossRefGoogle Scholar
  13. Engleman, D. M., 1970, X-ray diffraction studies of phase transitions in the membrane of Mycoplasma laidlawii, J. Mol. Biol. 47:115.CrossRefGoogle Scholar
  14. Fulco, A. J., and Fujii, D. K., 1980, Adaptive regulation of membrane lipid biosynthesis in bacilli by environmental temperatures, in: Membrane Fluidity: Biophysical Techniques and Cellular Regulation (M. Kates and A. Kuksis, eds.), pp. 77–98, Humana Press, Clifton, N.J.Google Scholar
  15. Garwin, J. L., and Cronan, J. E., Jr., 1980, Thermal modulation of fatty acid synthesis in Escherichia coli does not involve de novo enzyme synthesis, J. Bacteriol. 141:1457.PubMedGoogle Scholar
  16. Garwin, J. L., Klages, A. L., and Cronan, J. E., Jr., 1980, β-Ketoacyl-acyl carrier protein synthetase II of Escherichia coli. Evidence for function in the thermal regulation of fatty acid synthesis, J. Biol. Chem. 255:3263.PubMedGoogle Scholar
  17. Gelmann, E. P., and Cronan, J. E., Jr., 1972, Mutant of Escherichia coli deficient in the synthesis of cis-vaccenic acid, J. Bacteriol. 112:381.PubMedGoogle Scholar
  18. Harder, M. E., and Banaszak, L. J., 1979, Small angle X-ray scattering from the inner and outer membranes from Escherichia coli, Biochim. Biophys. Acta 552:89.PubMedCrossRefGoogle Scholar
  19. Hasegawa, Y., Kawada, N., and Nosoh, Y., 1980, Change in chemical composition of membrane of Bacillus caldotenax after shifting the growth temperature, Arch. Microbiol. 126:103.PubMedCrossRefGoogle Scholar
  20. Kainuma-Kuroda, R., Goelz, S., and Cronan, J. E., Jr., 1980, Regulation of membrane phospholipid synthesis in Escherichia coli during temperature up-shift, J. Bacteriol. 142:362.PubMedGoogle Scholar
  21. Kaneda, T., 1977, Fatty acids of the genus Bacillus: an example of branched-chain preference, Bacteriol. Rev. 41:391.PubMedGoogle Scholar
  22. Keough, K. M. W., and Davis, P. J., 1979, Gel to liquid-crystalline phase transitions in water dispersions of saturated mixed-acid phosphatidylcholines, Biochemistry 18:1453.PubMedCrossRefGoogle Scholar
  23. Lee, A. G., Birdsall, N. J. M., Metcalfe, J. C, Toon, P. A., and Warren, G. B., 1974, Clusters in lipid bilayers and the interpretation of thermal effects in biological membranes, Biochemistry 13:3699.PubMedCrossRefGoogle Scholar
  24. Martin, C. E., and Foyt, D. C, 1978, Rotational relaxation of 1,6-diphenyl-hexatriene in membrane lipids of cells acclimated to high and low growth temperatures, Biochemistry 17:3587.PubMedCrossRefGoogle Scholar
  25. Nishihara, M., Ishinaga, M., Kato, M., and Kito, M., 1976, Temperature-sensitive formation of the phospholipid molecular species in Escherichia coli membranes, Biochim. Biophys. Acta 431:54.PubMedGoogle Scholar
  26. Odriozola, J. M., Ramos, J. A., and Bloch, K., 1977, Fatty acid synthetase activity in Mycobacterium smegmatis: Characterization of the acyl carrier protein-dependent elongating system, Biochim. Biophys. Acta 488:207.PubMedGoogle Scholar
  27. Okuyama, H., Yamada, K., Kameyama, Y., Ikezawa, H., Akamatsu, Y., and Nojima, S., 1977, Regulation of membrane lipid synthesis in Escherichia coli after shifts in temperature, Biochemistry, 16:2668.PubMedCrossRefGoogle Scholar
  28. Raetz, C. R. H., 1978, Enzymology, genetics and regulation of membrane phospholipid synthesis in Escherichia coli, Microbiol. Rev. 42:614.PubMedGoogle Scholar
  29. Russell, N. J., 1972, Alteration in fatty acid chain length in Micrococcus cryophilus grown at different temperatures, Biochim. Biophys. Acta 231:254.Google Scholar
  30. Russell, N. J., 1978, The positional specificity of a desaturase in the psychrophilic bacterium Micrococcus cryophilus (ATCC 15174), Biochim. Biophys. Acta 531:179.PubMedGoogle Scholar
  31. Russell, M. J., and Volkman, J. K., 1980, The effect of growth temperature on wax ester composition in the psychrophilic bacterium Micrococcus cryophilus ATCC 15174, J. Gen. Microbiol. 118:131.Google Scholar
  32. Sandercock, S. P., and Russell, N. J., 1980, The elongation of exogenous fatty acids and the control of phospholipid acyl chain length in Micrococcus cryophilus, Biochem. J. 188:585.PubMedGoogle Scholar
  33. Shaw, M. K., and Ingraham, J. I., 1965, Fatty acid composition of Escherichia coli as a possible controlling factor of the minimal growth temperature, J. Bacteriol. 90:141.PubMedGoogle Scholar
  34. Silvius, J. R., and McElhaney, R. N., 1980, Membrane lipid physical state and modulation of the Na+, Mg2+-ATPase activity in Acholeplasma laidlawii B, Proc. Natl. Acad. Sci. USA 77:1255.PubMedCrossRefGoogle Scholar
  35. Silvius, J. R., Mak, N., and McElhaney, R. N., 1980, Lipid and protein composition and ther-motropic lipid phase transitions in fatty acid-homogeneous membrane of Acholeplasma laidlawii B, Biochim. Biophys. Acta 597:199.PubMedCrossRefGoogle Scholar
  36. Singer, S. J., and Nicolson, G. L., 1972, The fluid mosaic model of the structure of cell membranes, Science 175:720.PubMedCrossRefGoogle Scholar
  37. Tadayon, R. A., and Carroll, K. K., 1971, Effect of growth conditions on the fatty acid composition of Listeria monocytogenes and comparison with the fatty acids of Erysipelothrix and Corynebacterium, Lipids 6:820.PubMedCrossRefGoogle Scholar
  38. Thilo, L., Traüble, H., and Overath, P., 1977, Mechanistic interpretation of the influence of lipid phase transitions on transport functions, Biochemistry 16:1283.PubMedCrossRefGoogle Scholar
  39. Veerkamp, J. H., 1971, Fatty acid composition of Bifidobacterium and Lactobacillus strains, J. Bacteriol. 108:861.PubMedGoogle Scholar
  40. Weerkamp, A., and Heinen, W., 1972, Effect of temperature on the fatty acid composition of the extreme thermophiles Bacillus caldolyticus and Bacillus caldotenax, J. Bacteriol. 109:443.PubMedGoogle Scholar
  41. Yang, L. L., and Haug, A., 1979, Structure of membrane lipids and physicobiochemical properties of the plasma membrane from Thermoplasma acidophilum, adapted to grow at 37°C, Biochim. Biophys. Acta 573:308.PubMedGoogle Scholar
  42. Zinov’era, M. E., Simakova, I. M., and Kaprel’yants, A. S., 1979, Lateral heterogeneity of the bacterial membrane, Biokhimiya 44:931.Google Scholar

Copyright information

© Plenum Press, New York 1984

Authors and Affiliations

  • Nicholas J. Russell
    • 1
  1. 1.Department of BiochemistryUniversity CollegeCardiff, WalesUK

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