Skip to main content
PMC home page
Biophysical Journal logoLink to Biophysical Journal
. 1998 Dec;75(6):2877–2887. doi: 10.1016/S0006-3495(98)77730-6

Total lipids with short and long acyl chains from Acholeplasma form nonlamellar phases.

A S Andersson 1, L Rilfors 1, G Orädd 1, G Lindblom 1
PMCID: PMC1299960  PMID: 9826609

Abstract

The cell-wall-less bacterium Acholeplasma laidlawii A-EF22 synthesizes eight glycerolipids. Some of them form lamellar phases, whereas others are able to form normal or reversed nonlamellar phases. In this study we examined the phase properties of total lipid extracts with limiting average acyl chain lengths of 15 and 19 carbon atoms. The temperature at which these extracts formed reversed hexagonal (HII) phases differed by 5-10 degreesC when the water contents were 20-30 wt%. Thus the cells adjust the ratio between lamellar-forming and nonlamellar-forming lipids to the acyl chain lengths. Because short acyl chains generally increase the potential of lipids to form bilayers, it was judged interesting to determine which of the A. laidlawii A lipids are able to form reversed nonlamellar phases with short acyl chains. The two candidates with this ability are monoacyldiglucosyldiacylglycerol (MADGlcDAG) and monoglucosyldiacylglycerol. The average acyl chain lengths were 14.7 and 15.1 carbon atoms, and the degrees of acyl chain unsaturation were 32 and 46 mol%, respectively. The only liquid crystalline phase formed by MADGlcDAG is an HII phase. Monoglucosyldiacylglycerol forms reversed cubic (Ia3d) and HII phases at high temperatures. Thus, even when the organism is grown with short fatty acids, it synthesizes two lipids that have the capacity to maintain the nonlamellar tendency of the lipid bilayer. MADGlcDAG in particular contributes very powerfully to this tendency.

Full Text

The Full Text of this article is available as a PDF (119.8 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Andersson A. S., Demel R. A., Rilfors L., Lindblom G. Lipids in total extracts from Acholeplasma laidlawii A pack more closely than the individual lipids. Monolayers studied at the air-water interface. Biochim Biophys Acta. 1998 Feb 2;1369(1):94–102. doi: 10.1016/s0005-2736(97)00212-5. [DOI] [PubMed] [Google Scholar]
  2. Andersson A. S., Rilfors L., Bergqvist M., Persson S., Lindblom G. New aspects on membrane lipid regulation in Acholeplasma laidlawii A and phase equilibria of monoacyldiglucosyldiacylglycerol. Biochemistry. 1996 Aug 27;35(34):11119–11130. doi: 10.1021/bi960561w. [DOI] [PubMed] [Google Scholar]
  3. Christiansson A., Eriksson L. E., Westman J., Demel R., Wieslander A. Involvement of surface potential in regulation of polar membrane lipids in Acholeplasma laidlawii. J Biol Chem. 1985 Apr 10;260(7):3984–3990. [PubMed] [Google Scholar]
  4. Danino D., Kaplun A., Lindblom G., Rilfors L., Orädd G., Hauksson J. B., Talmon Y. Cryo-TEM and NMR studies of a micelle-forming phosphoglucolipid from membranes of Acholeplasma laidlawii A and B. Chem Phys Lipids. 1997 Jan 17;85(1):75–89. doi: 10.1016/s0009-3084(96)02640-0. [DOI] [PubMed] [Google Scholar]
  5. Di L., Small D. M. Physical behavior of the mixed chain diacylglycerol, 1-stearoyl-2-oleoyl-sn-glycerol: difficulties in chain packing produced marked polymorphism. J Lipid Res. 1993 Sep;34(9):1611–1623. [PubMed] [Google Scholar]
  6. Epand R. M. Diacylglycerols, lysolecithin, or hydrocarbons markedly alter the bilayer to hexagonal phase transition temperature of phosphatidylethanolamines. Biochemistry. 1985 Dec 3;24(25):7092–7095. doi: 10.1021/bi00346a011. [DOI] [PubMed] [Google Scholar]
  7. Gruner S. M. Intrinsic curvature hypothesis for biomembrane lipid composition: a role for nonbilayer lipids. Proc Natl Acad Sci U S A. 1985 Jun;82(11):3665–3669. doi: 10.1073/pnas.82.11.3665. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Gulik-Krzywicki T., Rivas E., Luzzati V. Structure et polymorphisme des lipides: étude par diffraction des rayons X du systéme formé de lipides de mitochondries de coeur de boeuf et d'eau. J Mol Biol. 1967 Jul 28;27(2):303–322. doi: 10.1016/0022-2836(67)90022-8. [DOI] [PubMed] [Google Scholar]
  9. Gulik A., Luzzati V., De Rosa M., Gambacorta A. Structure and polymorphism of bipolar isopranyl ether lipids from archaebacteria. J Mol Biol. 1985 Mar 5;182(1):131–149. doi: 10.1016/0022-2836(85)90032-4. [DOI] [PubMed] [Google Scholar]
  10. Gulik A., Luzzati V., DeRosa M., Gambacorta A. Tetraether lipid components from a thermoacidophilic archaebacterium. Chemical structure and physical polymorphism. J Mol Biol. 1988 May 20;201(2):429–435. doi: 10.1016/0022-2836(88)90149-0. [DOI] [PubMed] [Google Scholar]
  11. Hauksson J. B., Lindblom G., Rilfors L. Structures of glucolipids from the membrane of Acholeplasma laidlawii strain A-EF22. I. Glycerophosphoryldiglucosyldiacylglycerol and monoacylbisglycerophosphoryldiglucosyldiacylglycerol. Biochim Biophys Acta. 1994 Sep 15;1214(2):124–130. doi: 10.1016/0005-2760(94)90035-3. [DOI] [PubMed] [Google Scholar]
  12. Hauksson J. B., Lindblom G., Rilfors L. Structures of glucolipids from the membrane of Acholeplasma laidlawii strain A-EF22. II. Monoacylmonoglucosyldiacylglycerol. Biochim Biophys Acta. 1994 Dec 8;1215(3):341–345. doi: 10.1016/0005-2760(94)90063-9. [DOI] [PubMed] [Google Scholar]
  13. Hauksson J. B., Rilfors L., Lindblom G., Arvidson G. Structures of glucolipids from the membrane of Acholeplasma laidlawii strain A-EF22. III. Monoglucosyldiacylglycerol, diglucosyldiacylglycerol, and monoacyldiglucosyldiacylglycerol. Biochim Biophys Acta. 1995 Aug 24;1258(1):1–9. doi: 10.1016/0005-2760(95)00074-m. [DOI] [PubMed] [Google Scholar]
  14. Helfrich W. Elastic properties of lipid bilayers: theory and possible experiments. Z Naturforsch C. 1973 Nov-Dec;28(11):693–703. doi: 10.1515/znc-1973-11-1209. [DOI] [PubMed] [Google Scholar]
  15. Koynova R., Caffrey M. Phases and phase transitions of the hydrated phosphatidylethanolamines. Chem Phys Lipids. 1994 Jan;69(1):1–34. doi: 10.1016/0009-3084(94)90024-8. [DOI] [PubMed] [Google Scholar]
  16. LUZZATI V., HUSSON F. The structure of the liquid-crystalline phasis of lipid-water systems. J Cell Biol. 1962 Feb;12:207–219. doi: 10.1083/jcb.12.2.207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Lindblom G., Brentel I., Sjölund M., Wikander G., Wieslander A. Phase equilibria of membrane lipids from Acholeplasma laidlawii: importance of a single lipid forming nonlamellar phases. Biochemistry. 1986 Nov 18;25(23):7502–7510. doi: 10.1021/bi00371a037. [DOI] [PubMed] [Google Scholar]
  18. Lindblom G., Hauksson J. B., Rilfors L., Bergenståhl B., Wieslander A., Eriksson P. O. Membrane lipid regulation in Acholeplasma laidlawii grown with saturated fatty acids. Biosynthesis of a triacylglucolipid forming reversed micelles. J Biol Chem. 1993 Aug 5;268(22):16198–16207. [PubMed] [Google Scholar]
  19. Mannock D. A., Lewis R. N., McElhaney R. N. Physical properties of glycosyl diacylglycerols. 1. Calorimetric studies of a homologous series of 1,2-di-O-acyl-3-O-(alpha-D-glucopyranosyl)-sn-glycerols. Biochemistry. 1990 Aug 28;29(34):7790–7799. doi: 10.1021/bi00486a003. [DOI] [PubMed] [Google Scholar]
  20. Mannock D. A., McElhaney R. N. Differential scanning calorimetry and X-ray diffraction studies of a series of synthetic beta-D-galactosyl diacylglycerols. Biochem Cell Biol. 1991 Dec;69(12):863–867. doi: 10.1139/o91-128. [DOI] [PubMed] [Google Scholar]
  21. Monck M. A., Bloom M., Lafleur M., Lewis R. N., McElhaney R. N., Cullis P. R. Influence of lipid composition on the orientational order in Acholeplasma laidlawii strain B membranes: a deuterium NMR study. Biochemistry. 1992 Oct 20;31(41):10037–10043. doi: 10.1021/bi00156a025. [DOI] [PubMed] [Google Scholar]
  22. Morein S., Andersson A., Rilfors L., Lindblom G. Wild-type Escherichia coli cells regulate the membrane lipid composition in a "window" between gel and non-lamellar structures. J Biol Chem. 1996 Mar 22;271(12):6801–6809. doi: 10.1074/jbc.271.12.6801. [DOI] [PubMed] [Google Scholar]
  23. Niemi A. R., Rilfors L., Lindblom G. Influence of monoglucosyldiacylglycerol and monoacylmonoglucosyldiacylglycerol on the lipid bilayer of the membrane from Acholeplasma laidlawii strain A-EF22. Biochim Biophys Acta. 1995 Nov 1;1239(2):186–194. doi: 10.1016/0005-2736(95)00132-m. [DOI] [PubMed] [Google Scholar]
  24. Osterberg F., Rilfors L., Wieslander A., Lindblom G., Gruner S. M. Lipid extracts from membranes of Acholeplasma laidlawii A grown with different fatty acids have a nearly constant spontaneous curvature. Biochim Biophys Acta. 1995 Jun 27;1257(1):18–24. doi: 10.1016/0005-2760(95)00042-b. [DOI] [PubMed] [Google Scholar]
  25. Rietveld A. G., Killian J. A., Dowhan W., de Kruijff B. Polymorphic regulation of membrane phospholipid composition in Escherichia coli. J Biol Chem. 1993 Jun 15;268(17):12427–12433. [PubMed] [Google Scholar]
  26. Rilfors L., Eriksson P. O., Arvidson G., Lindblom G. Relationship between three-dimensional arrays of "lipidic particles" and bicontinuous cubic lipid phases. Biochemistry. 1986 Nov 18;25(23):7702–7711. doi: 10.1021/bi00371a063. [DOI] [PubMed] [Google Scholar]
  27. Rilfors L., Hauksson J. B., Lindblom G. Regulation and phase equilibria of membrane lipids from Bacillus megaterium and Acholeplasma laidlawii strain A containing methyl-branched acyl chains. Biochemistry. 1994 May 24;33(20):6110–6120. doi: 10.1021/bi00186a010. [DOI] [PubMed] [Google Scholar]
  28. Rilfors L., Wieslander A., Lindblom G. Regulation and physicochemical properties of the polar lipids in Acholeplasma laidlawii. Subcell Biochem. 1993;20:109–166. doi: 10.1007/978-1-4615-2924-8_4. [DOI] [PubMed] [Google Scholar]
  29. Rilfors L., Wieslander A., Ståhl S. Lipid and protein composition of membranes of Bacillus megaterium variants in the temperature range 5 to 70 degrees C. J Bacteriol. 1978 Sep;135(3):1043–1052. doi: 10.1128/jb.135.3.1043-1052.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Rivas E., Luzzati V. Polymorphisme des lipides polaires et des galacto-lipides de chloroplastes de maïs, en présence d'eau. J Mol Biol. 1969 Apr;41(2):261–275. doi: 10.1016/0022-2836(69)90391-x. [DOI] [PubMed] [Google Scholar]
  31. Seddon J. M., Cevc G., Kaye R. D., Marsh D. X-ray diffraction study of the polymorphism of hydrated diacyl- and dialkylphosphatidylethanolamines. Biochemistry. 1984 Jun 5;23(12):2634–2644. doi: 10.1021/bi00307a015. [DOI] [PubMed] [Google Scholar]
  32. Seddon J. M. Structure of the inverted hexagonal (HII) phase, and non-lamellar phase transitions of lipids. Biochim Biophys Acta. 1990 Feb 28;1031(1):1–69. doi: 10.1016/0304-4157(90)90002-t. [DOI] [PubMed] [Google Scholar]
  33. Sen A., Hui S. W., Mannock D. A., Lewis R. N., McElhaney R. N. Physical properties of glycosyl diacylglycerols. 2. X-ray diffraction studies of a homologous series of 1,2-Di-O-acyl-3-O-(alpha-D-glucopyranosyl)-sn-glycerols. Biochemistry. 1990 Aug 28;29(34):7799–7804. doi: 10.1021/bi00486a004. [DOI] [PubMed] [Google Scholar]
  34. Sen A., Williams W. P., Quinn P. J. The structure and thermotropic properties of pure 1,2-diacylgalactosylglycerols in aqueous systems. Biochim Biophys Acta. 1981 Feb 23;663(2):380–389. doi: 10.1016/0005-2760(81)90167-3. [DOI] [PubMed] [Google Scholar]
  35. Shipley G. G., Green J. P., Nichols B. W. The phase behavior of monogalactosyl, digalactosyl, and sulphoquinovosyl diglycerides. Biochim Biophys Acta. 1973 Jul 18;311(4):531–544. doi: 10.1016/0005-2736(73)90128-4. [DOI] [PubMed] [Google Scholar]
  36. Siegel D. P., Banschbach J., Alford D., Ellens H., Lis L. J., Quinn P. J., Yeagle P. L., Bentz J. Physiological levels of diacylglycerols in phospholipid membranes induce membrane fusion and stabilize inverted phases. Biochemistry. 1989 May 2;28(9):3703–3709. doi: 10.1021/bi00435a012. [DOI] [PubMed] [Google Scholar]
  37. Smaal E. B., Romijn D., Geurts van Kessel W. S., de Kruijff B., de Gier J. Isolation and purification of cardiolipin from beef heart. J Lipid Res. 1985 May;26(5):634–637. [PubMed] [Google Scholar]
  38. Thurmond R. L., Niemi A. R., Lindblom G., Wieslander A., Rilfors L. Membrane thickness and molecular ordering in Acholeplasma laidlawii strain A studied by 2H NMR spectroscopy. Biochemistry. 1994 Nov 15;33(45):13178–13188. doi: 10.1021/bi00249a004. [DOI] [PubMed] [Google Scholar]
  39. Tulloch A. P. Preparation of specifically dideuterated octadecanoates and oxooctadecanoates. Lipids. 1977 Jan;12(1):92–98. doi: 10.1007/BF02532978. [DOI] [PubMed] [Google Scholar]
  40. Wieslander A., Christiansson A., Rilfors L., Lindblom G. Lipid bilayer stability in membranes. Regulation of lipid composition in Acholeplasma laidlawii as governed by molecular shape. Biochemistry. 1980 Aug 5;19(16):3650–3655. doi: 10.1021/bi00557a002. [DOI] [PubMed] [Google Scholar]
  41. Wieslander A., Nordström S., Dahlqvist A., Rilfors L., Lindblom G. Membrane lipid composition and cell size of Acholeplasma laidlawii strain A are strongly influenced by lipid acyl chain length. Eur J Biochem. 1995 Feb 1;227(3):734–744. doi: 10.1111/j.1432-1033.1995.tb20196.x. [DOI] [PubMed] [Google Scholar]

Articles from Biophysical Journal are provided here courtesy of The Biophysical Society

RESOURCES