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. 1977 Mar;129(3):1563–1573. doi: 10.1128/jb.129.3.1563-1573.1977

Effects of lipid phase transition of the freeze-cleaved envelope of Escherichia coli.

M E Bayer, M Dolack, E Houser
PMCID: PMC235136  PMID: 321432

Abstract

We studied the fine structure of the envelope of Escherichia coli auxotroph K1060 after the cells were grown in the presence of one of the following fatty acids; oleic, palmitelaidic, or elidic acid. The cells were freeze-fractured after exposure to temperatures above and below the lipid phase transition range. As judged by freeze-etching methods, we observed that below the transition range the fracture plane of the inner membrane showed the typical aggregation of intramembranous particles (IMP) and concomitant development of areas devoid of IMP. In these areas we found a regular arrangement of equally spaced ridges, often intersected at 90 degrees by arrays of similar ridges. The ridges were composed of spherical particles measuring 4 to 5 nm in diameter. Formation and melting of these arrays took place within 15 to 30s after temperature shift-down or shift-up, respectively. Fixation in glutaraldehyde prevented these changes. The outer-membrane fracture plane revealed ordered areas to a lesser degree; these were discernible only by the regular arrangement of the IMP of the concave fracture plane. We interpret the data by suggesting that the pattern of ridges in E. coli K1060 is analogous to the band patterns described for artificial liposomes, and that the particles, possibly proteins, are lined up or extruded along the ridges during membrane lipid crystallization.

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Selected References

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  1. Bachmann L., Schmitt W. W. Improved cryofixation applicable to freeze etching. Proc Natl Acad Sci U S A. 1971 Sep;68(9):2149–2152. doi: 10.1073/pnas.68.9.2149. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bayer M. E., Koplow J., Goldfine H. Alterations in envelope structure of heptose-deficient mutants of Escherichia coli as revealed by freeze-etching. Proc Natl Acad Sci U S A. 1975 Dec;72(12):5145–5149. doi: 10.1073/pnas.72.12.5145. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bayer M. E., Remsen C. C. Structure of Escherichia coli after freeze-etching. J Bacteriol. 1970 Jan;101(1):304–313. doi: 10.1128/jb.101.1.304-313.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Branton D. Fracture faces of frozen membranes. Proc Natl Acad Sci U S A. 1966 May;55(5):1048–1056. doi: 10.1073/pnas.55.5.1048. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Chapman D., Urbina J. Biomembrane phase transitions. Studies of lipid-water systems using differential scanning calorimetry. J Biol Chem. 1974 Apr 25;249(8):2512–2521. [PubMed] [Google Scholar]
  6. Copps T. P., Chelack W. S., Petkau A. Variation in distribution of membrane particles in Acholeplasma laidlawii B with pH. J Ultrastruct Res. 1976 Apr;55(1):1–3. doi: 10.1016/s0022-5320(76)80076-7. [DOI] [PubMed] [Google Scholar]
  7. Gulik-Krzywicki T. Structural studies of the associations between biological membrane components. Biochim Biophys Acta. 1975 Mar 25;415(1):1–28. doi: 10.1016/0304-4157(75)90015-5. [DOI] [PubMed] [Google Scholar]
  8. Haest C. W., Verkleij A. J., De Gier J., Scheek R., Ververgaert P. H., Van Deenen L. L. The effect of lipid phase transitions on the architecture of bacterial membranes. Biochim Biophys Acta. 1974 Jul 12;356(1):17–26. doi: 10.1016/0005-2736(74)90290-9. [DOI] [PubMed] [Google Scholar]
  9. James R., Branton D. Lipid- and temperature-dependent structural changes in Acholeplasma laidlawii cell membranes. Biochim Biophys Acta. 1973 Oct 25;323(3):378–390. doi: 10.1016/0005-2736(73)90183-1. [DOI] [PubMed] [Google Scholar]
  10. Kleemann W., McConnell H. M. Lateral phase separations in Escherichia coli membranes. Biochim Biophys Acta. 1974 Apr 29;345(2):220–230. doi: 10.1016/0005-2736(74)90260-0. [DOI] [PubMed] [Google Scholar]
  11. Kwok-Kwong LI J., Fox C. F. Ultrastructural studies on the inner and outer membranes of an unsaturated fatty acid auxotroph of Escherichia coli. J Ultrastruct Res. 1975 Jul;52(1):120–133. doi: 10.1016/s0022-5320(75)80027-x. [DOI] [PubMed] [Google Scholar]
  12. Meyer H. W., Winkelmann H. Uber die Anordnung der Membranproteine nach Untersuchungen mit der Gefrierätzung an isolierten Erythozytenmembranen. Protoplasma. 1972;75(3):255–284. doi: 10.1007/BF01279819. [DOI] [PubMed] [Google Scholar]
  13. Mizushima S., Yamada H. Isolation and characterization of two outer membrane preparations from Escherichia coli. Biochim Biophys Acta. 1975 Jan 14;375(1):44–53. doi: 10.1016/0005-2736(75)90071-1. [DOI] [PubMed] [Google Scholar]
  14. Osborn M. J., Gander J. E., Parisi E., Carson J. Mechanism of assembly of the outer membrane of Salmonella typhimurium. Isolation and characterization of cytoplasmic and outer membrane. J Biol Chem. 1972 Jun 25;247(12):3962–3972. [PubMed] [Google Scholar]
  15. Overath P., Brenner M., Gulik-Krzywicki T., Shechter E., Letellier L. Lipid phase transitions in cytoplasmic and outer membranes of Escherichia coli. Biochim Biophys Acta. 1975 May 6;389(2):358–369. doi: 10.1016/0005-2736(75)90328-4. [DOI] [PubMed] [Google Scholar]
  16. Overath P., Raufuss E. M. The induction of the enzymes of fatty acid degradation in Escherichia coli. Biochem Biophys Res Commun. 1967 Oct 11;29(1):28–33. doi: 10.1016/0006-291x(67)90535-9. [DOI] [PubMed] [Google Scholar]
  17. Overath P., Schairer H. U., Stoffel W. Correlation of in vivo and in vitro phase transitions of membrane lipids in Escherichia coli. Proc Natl Acad Sci U S A. 1970 Oct;67(2):606–612. doi: 10.1073/pnas.67.2.606. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Overath P., Träuble H. Phase transitions in cells, membranes, and lipids of Escherichia coli. Detection by fluorescent probes, light scattering, and dilatometry. Biochemistry. 1973 Jul 3;12(14):2625–2634. doi: 10.1021/bi00738a012. [DOI] [PubMed] [Google Scholar]
  19. Pinto da Silva P., Douglas S. D., Branton D. Localization of A antigen sites on human erythrocyte ghosts. Nature. 1971 Jul 16;232(5307):194–196. doi: 10.1038/232194a0. [DOI] [PubMed] [Google Scholar]
  20. Rosen B. P., Hackette S. L. Effects of fatty acid substitution on the release of enzymes by osmotic shock. J Bacteriol. 1972 Jun;110(3):1181–1189. doi: 10.1128/jb.110.3.1181-1189.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Salton M. R. Bacterial membranes. CRC Crit Rev Microbiol. 1971 May;1(1):161–197. doi: 10.3109/10408417109104480. [DOI] [PubMed] [Google Scholar]
  22. Shechter E., Letellier L., Gulik-Krzywicki G. Relations between structure and function in cytoplasmic membrane vesicles isolated from an Escherichia coli fatty-acid auxotroph. High-angle x-ray diffraction, freeze-etch electron microscopy and transport studies. Eur J Biochem. 1974 Nov 1;49(1):61–76. doi: 10.1111/j.1432-1033.1974.tb03811.x. [DOI] [PubMed] [Google Scholar]
  23. Silbert D. F., Vagelos P. R. Fatty acid mutant of E. coli lacking a beta-hydroxydecanoyl thioester dehydrase. Proc Natl Acad Sci U S A. 1967 Oct;58(4):1579–1586. doi: 10.1073/pnas.58.4.1579. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Speth V., Wunderlich F. Membranes of Tetrahymena. II. Direct visualization of reversible transitions in biomembrane structure induced by temperature. Biochim Biophys Acta. 1973 Feb 16;291(3):621–628. doi: 10.1016/0005-2736(73)90467-7. [DOI] [PubMed] [Google Scholar]
  25. Tardieu A., Luzzati V., Reman F. C. Structure and polymorphism of the hydrocarbon chains of lipids: a study of lecithin-water phases. J Mol Biol. 1973 Apr 25;75(4):711–733. doi: 10.1016/0022-2836(73)90303-3. [DOI] [PubMed] [Google Scholar]
  26. Tsien H. C., Higgins M. L. Effect of temperature on the distribution of membrane particles in Streptococcus faecalis as seen by the freeze-fracture technique. J Bacteriol. 1974 May;118(2):725–734. doi: 10.1128/jb.118.2.725-734.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Verkleij A. J., Lugtenberg E. J., Ververgaert P. H. Freeze etch morphology of outer membrane mutants of Escherichia coli K12. Biochim Biophys Acta. 1976 Mar 19;426(3):581–586. doi: 10.1016/0005-2736(76)90401-6. [DOI] [PubMed] [Google Scholar]
  28. Verkleij A. J., Ververgaert P. H., van Deenen L. L., Elbers P. F. Phase transitions of phospholipid bilayers and membranes of Acholeplasma laidlawii B visualized by freeze fracturing electron microscopy. Biochim Biophys Acta. 1972 Nov 2;288(2):326–332. doi: 10.1016/0005-2736(72)90253-2. [DOI] [PubMed] [Google Scholar]
  29. Ververgaert P. H., Verkleij A. J., Elbers P. F., van Deenen L. L. Analysis of the crystallization process in lecithin liposomes: a freeze-etch study. Biochim Biophys Acta. 1973 Jul 6;311(3):320–329. doi: 10.1016/0005-2736(73)90313-1. [DOI] [PubMed] [Google Scholar]
  30. Zingsheim H. P. Membrane structure and electron microscopy. The significance of physical problems and techniques (freeze etching). Biochim Biophys Acta. 1972 Aug 4;265(3):339–366. doi: 10.1016/0304-4157(72)90013-5. [DOI] [PubMed] [Google Scholar]
  31. van Heerikhuizen H., Kwak E., van Bruggen E. F., Witholt B. Characterization of a low density cytoplasmic membrane subfraction isolated from Escherichia coli. Biochim Biophys Acta. 1975 Dec 1;413(2):177–191. doi: 10.1016/0005-2736(75)90102-9. [DOI] [PubMed] [Google Scholar]

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