Skip to main content
Biophysical Journal logoLink to Biophysical Journal
. 2001 Dec;81(6):3377–3386. doi: 10.1016/S0006-3495(01)75970-X

Hydration and molecular motions in synthetic phytanyl-chained glycolipid vesicle membranes.

T Baba 1, H Minamikawa 1, M Hato 1, T Handa 1
PMCID: PMC1301794  PMID: 11721000

Abstract

Proton permeation rates across membranes of a synthetic branch-chained glycolipid, 1,3-di-O-phytanyl-2-O-(beta-D-maltotriosyl)glycerol (Mal3(Phyt)2) as well as a branch-chained phospholipid, diphytanoylphosphatidylcholine (DPhPC) were lower than those of straight-chained lipids such as egg yolk phosphatidylcholine (EPC) by a factor of approximately 4 at pH 7.0 and 25 degrees C. To examine whether degrees of water penetration and molecular motions in Mal3(Phyt)2 membranes can account for the lower permeability, nanosecond time-resolved fluorescence spectroscopy was applied to various membranes of branch-chained lipids (Mal3(Phyt)2, DPhPC, and a tetraether lipid from an extremely thermoacidophilic archaeon Thermoplasma acidophilum), as well as straight-chained lipids (EPC, 1-palmitoyl-2-oleoyl-phosphatidylcholine (POPC), and digalactosyldiacylglycerol (DGDG)) using several fluorescent lipids. Degrees of hydration of glycolipids, Mal3(Phyt)2, and DGDG were lower than those of phospholipids, EPC, POPC, and DPhPC at the membrane-water interfaces. DPhPC showed the highest hydration among the lipids examined. Meanwhile, rotational and lateral diffusive motions of the fluorescent phospholipid in branch-chained lipid membranes were more restricted than those in straight-chained ones. The results suggest that the restricted motion of chain segments rather than the lower hydration accounts for the lower proton permeability of branch-chained lipid membranes.

Full Text

The Full Text of this article is available as a PDF (138.0 KB).

Selected References

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

  1. Abrams F. S., Chattopadhyay A., London E. Determination of the location of fluorescent probes attached to fatty acids using parallax analysis of fluorescence quenching: effect of carboxyl ionization state and environment on depth. Biochemistry. 1992 Jun 16;31(23):5322–5327. doi: 10.1021/bi00138a011. [DOI] [PubMed] [Google Scholar]
  2. Asuncion-Punzalan E., Kachel K., London E. Groups with polar characteristics can locate at both shallow and deep locations in membranes: the behavior of dansyl and related probes. Biochemistry. 1998 Mar 31;37(13):4603–4611. doi: 10.1021/bi9726234. [DOI] [PubMed] [Google Scholar]
  3. BARTLETT G. R. Phosphorus assay in column chromatography. J Biol Chem. 1959 Mar;234(3):466–468. [PubMed] [Google Scholar]
  4. Baba T., Minamikawa H., Hato M., Motoki A., Hirano M., Zhou D., Kawasaki K. Synthetic phytanyl-chained glycolipid vesicle membrane as a novel matrix for functional reconstitution of cyanobacterial photosystem II complex. Biochem Biophys Res Commun. 1999 Nov 30;265(3):734–738. doi: 10.1006/bbrc.1999.1754. [DOI] [PubMed] [Google Scholar]
  5. Baba T., Toshima Y., Minamikawa H., Hato M., Suzuki K., Kamo N. Formation and characterization of planar lipid bilayer membranes from synthetic phytanyl-chained glycolipids. Biochim Biophys Acta. 1999 Sep 21;1421(1):91–102. doi: 10.1016/s0005-2736(99)00114-5. [DOI] [PubMed] [Google Scholar]
  6. Baba T, Zheng LQ, Minamikawa H, Hato M. Interglycolipid Membrane Interactions: pH-Dependent Aggregation of Nonionic Synthetic Glycolipid Vesicles. J Colloid Interface Sci. 2000 Mar 15;223(2):235–243. doi: 10.1006/jcis.1999.6649. [DOI] [PubMed] [Google Scholar]
  7. Choquet C. G., Patel G. B., Beveridge T. J., Sprott G. D. Stability of pressure-extruded liposomes made from archaeobacterial ether lipids. Appl Microbiol Biotechnol. 1994 Nov;42(2-3):375–384. doi: 10.1007/BF00902745. [DOI] [PubMed] [Google Scholar]
  8. Dannenmuller O., Arakawa K., Eguchi T., Kakinuma K., Blanc S., Albrecht A. M., Schmutz M., Nakatani Y., Ourisson G. Membrane properties of archaeal macrocyclic diether phospholipids. Chemistry. 2000 Feb 18;6(4):645–654. doi: 10.1002/(sici)1521-3765(20000218)6:4<645::aid-chem645>3.0.co;2-a. [DOI] [PubMed] [Google Scholar]
  9. Deamer D. W., Nichols J. W. Proton flux mechanisms in model and biological membranes. J Membr Biol. 1989 Feb;107(2):91–103. doi: 10.1007/BF01871715. [DOI] [PubMed] [Google Scholar]
  10. Degani H., Danon A., Caplan S. R. Proton and carbon-13 nuclear magnetic resonance studies of the polar lipids of Halobacterium halobium. Biochemistry. 1980 Apr 15;19(8):1626–1631. doi: 10.1021/bi00549a016. [DOI] [PubMed] [Google Scholar]
  11. Elferink M. G., de Wit J. G., Demel R., Driessen A. J., Konings W. N. Functional reconstitution of membrane proteins in monolayer liposomes from bipolar lipids of Sulfolobus acidocaldarius. J Biol Chem. 1992 Jan 15;267(2):1375–1381. [PubMed] [Google Scholar]
  12. Elferink M. G., de Wit J. G., Driessen A. J., Konings W. N. Stability and proton-permeability of liposomes composed of archaeal tetraether lipids. Biochim Biophys Acta. 1994 Aug 3;1193(2):247–254. doi: 10.1016/0005-2736(94)90160-0. [DOI] [PubMed] [Google Scholar]
  13. Freisleben H. J., Zwicker K., Jezek P., John G., Bettin-Bogutzki A., Ring K., Nawroth T. Reconstitution of bacteriorhodopsin and ATP synthase from Micrococcus luteus into liposomes of the purified main tetraether lipid from Thermoplasma acidophilum: proton conductance and light-driven ATP synthesis. Chem Phys Lipids. 1995 Nov 17;78(2):137–147. doi: 10.1016/0009-3084(95)02491-z. [DOI] [PubMed] [Google Scholar]
  14. Gabriel J. L., Chong P. L. Molecular modeling of archaebacterial bipolar tetraether lipid membranes. Chem Phys Lipids. 2000 Apr;105(2):193–200. doi: 10.1016/s0009-3084(00)00126-2. [DOI] [PubMed] [Google Scholar]
  15. Galla H. J., Hartmann W., Theilen U., Sackmann E. On two-dimensional passive random walk in lipid bilayers and fluid pathways in biomembranes. J Membr Biol. 1979 Jul 31;48(3):215–236. doi: 10.1007/BF01872892. [DOI] [PubMed] [Google Scholar]
  16. Galla H. J., Sackmann E. Lateral diffusion in the hydrophobic region of membranes: use of pyrene excimers as optical probes. Biochim Biophys Acta. 1974 Feb 26;339(1):103–115. doi: 10.1016/0005-2736(74)90336-8. [DOI] [PubMed] [Google Scholar]
  17. Grzesiek S., Dencher N. A. Dependency of delta pH-relaxation across vesicular membranes on the buffering power of bulk solutions and lipids. Biophys J. 1986 Aug;50(2):265–276. doi: 10.1016/S0006-3495(86)83460-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Haines T. H. Water transport across biological membranes. FEBS Lett. 1994 Jun 6;346(1):115–122. doi: 10.1016/0014-5793(94)00470-6. [DOI] [PubMed] [Google Scholar]
  19. Hato M., Minamikawa H., Tamada K., Baba T., Tanabe Y. Self-assembly of synthetic glycolipid/water systems. Adv Colloid Interface Sci. 1999 Apr 30;80(3):233–270. doi: 10.1016/s0001-8686(98)00085-2. [DOI] [PubMed] [Google Scholar]
  20. Ho C., Slater S. J., Stubbs C. D. Hydration and order in lipid bilayers. Biochemistry. 1995 May 9;34(18):6188–6195. doi: 10.1021/bi00018a023. [DOI] [PubMed] [Google Scholar]
  21. Hsieh C. H., Sue S. C., Lyu P. C., Wu W. G. Membrane packing geometry of diphytanoylphosphatidylcholine is highly sensitive to hydration: phospholipid polymorphism induced by molecular rearrangement in the headgroup region. Biophys J. 1997 Aug;73(2):870–877. doi: 10.1016/S0006-3495(97)78120-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Jarrell H. C., Zukotynski K. A., Sprott G. D. Lateral diffusion of the total polar lipids from Thermoplasma acidophilum in multilamellar liposomes. Biochim Biophys Acta. 1998 Mar 2;1369(2):259–266. doi: 10.1016/s0005-2736(97)00228-9. [DOI] [PubMed] [Google Scholar]
  23. Kao Y. L., Chang E. L., Chong P. L. Unusual pressure dependence of the lateral motion of pyrene-labeled phosphatidylcholine in bipolar lipid vesicles. Biochem Biophys Res Commun. 1992 Nov 16;188(3):1241–1246. doi: 10.1016/0006-291x(92)91364-v. [DOI] [PubMed] [Google Scholar]
  24. Kawato S., Kinosita K., Jr, Ikegami A. Dynamic structure of lipid bilayers studied by nanosecond fluorescence techniques. Biochemistry. 1977 May 31;16(11):2319–2324. doi: 10.1021/bi00630a002. [DOI] [PubMed] [Google Scholar]
  25. Khan T. K., Chong P. L. Studies of archaebacterial bipolar tetraether liposomes by perylene fluorescence. Biophys J. 2000 Mar;78(3):1390–1399. doi: 10.1016/S0006-3495(00)76692-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Komatsu H., Chong P. L. Low permeability of liposomal membranes composed of bipolar tetraether lipids from thermoacidophilic archaebacterium Sulfolobus acidocaldarius. Biochemistry. 1998 Jan 6;37(1):107–115. doi: 10.1021/bi972163e. [DOI] [PubMed] [Google Scholar]
  27. Lipari G., Szabo A. Effect of librational motion on fluorescence depolarization and nuclear magnetic resonance relaxation in macromolecules and membranes. Biophys J. 1980 Jun;30(3):489–506. doi: 10.1016/S0006-3495(80)85109-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Lis L. J., McAlister M., Fuller N., Rand R. P., Parsegian V. A. Interactions between neutral phospholipid bilayer membranes. Biophys J. 1982 Mar;37(3):657–665. [PMC free article] [PubMed] [Google Scholar]
  29. Marrink S. J., Jähnig F., Berendsen H. J. Proton transport across transient single-file water pores in a lipid membrane studied by molecular dynamics simulations. Biophys J. 1996 Aug;71(2):632–647. doi: 10.1016/S0006-3495(96)79264-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. McDaniel R. V. Neutron diffraction studies of digalactosyldiacylglycerol. Biochim Biophys Acta. 1988 May 9;940(1):158–164. doi: 10.1016/0005-2736(88)90020-x. [DOI] [PubMed] [Google Scholar]
  31. Nagle J. F. Theory of passive proton conductance in lipid bilayers. J Bioenerg Biomembr. 1987 Oct;19(5):413–426. doi: 10.1007/BF00770027. [DOI] [PubMed] [Google Scholar]
  32. Parente R. A., Lentz B. R. Fusion and phase separation monitored by lifetime changes of a fluorescent phospholipid probe. Biochemistry. 1986 Mar 11;25(5):1021–1026. doi: 10.1021/bi00353a011. [DOI] [PubMed] [Google Scholar]
  33. Paula S., Volkov A. G., Van Hoek A. N., Haines T. H., Deamer D. W. Permeation of protons, potassium ions, and small polar molecules through phospholipid bilayers as a function of membrane thickness. Biophys J. 1996 Jan;70(1):339–348. doi: 10.1016/S0006-3495(96)79575-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Pomès R., Roux B. Free energy profiles for H+ conduction along hydrogen-bonded chains of water molecules. Biophys J. 1998 Jul;75(1):33–40. doi: 10.1016/S0006-3495(98)77492-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. ROSENBERG A. A COMPARISON OF LIPID PATTERNS IN PHOTOSYNTHESIZING AND NONPHOTOSYNTHESIZING CELLS OF EUGLENA GRACILIS. Biochemistry. 1963 Sep-Oct;2:1148–1154. doi: 10.1021/bi00905a042. [DOI] [PubMed] [Google Scholar]
  36. 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]
  37. Swain M., Brisson J. R., Sprott G. D., Cooper F. P., Patel G. B. Identification of beta-L-gulose as the sugar moiety of the main polar lipid Thermoplasma acidophilum. Biochim Biophys Acta. 1997 Mar 10;1345(1):56–64. doi: 10.1016/s0005-2760(96)00163-4. [DOI] [PubMed] [Google Scholar]
  38. Tocanne J. F., Dupou-Cézanne L., Lopez A. Lateral diffusion of lipids in model and natural membranes. Prog Lipid Res. 1994;33(3):203–237. doi: 10.1016/0163-7827(94)90027-2. [DOI] [PubMed] [Google Scholar]
  39. Yamauchi K., Doi K., Kinoshita M., Kii F., Fukuda H. Archaebacterial lipid models: highly salt-tolerant membranes from 1,2-diphytanylglycero-3-phosphocholine. Biochim Biophys Acta. 1992 Oct 5;1110(2):171–177. doi: 10.1016/0005-2736(92)90355-p. [DOI] [PubMed] [Google Scholar]
  40. Yamauchi K., Doi K., Yoshida Y., Kinoshita M. Archaebacterial lipids: highly proton-impermeable membranes from 1,2-diphytanyl-sn-glycero-3-phosphocholine. Biochim Biophys Acta. 1993 Mar 14;1146(2):178–182. doi: 10.1016/0005-2736(93)90353-2. [DOI] [PubMed] [Google Scholar]
  41. Yeagle P. L. Cholesterol and the cell membrane. Biochim Biophys Acta. 1985 Dec 9;822(3-4):267–287. doi: 10.1016/0304-4157(85)90011-5. [DOI] [PubMed] [Google Scholar]
  42. van de Vossenberg J. L., Driessen A. J., Konings W. N. The essence of being extremophilic: the role of the unique archaeal membrane lipids. Extremophiles. 1998 Aug;2(3):163–170. doi: 10.1007/s007920050056. [DOI] [PubMed] [Google Scholar]

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

RESOURCES