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Ultrastructure of cell wall and thylakoid membranes of the thermophilic cyanobacterium Synechococcus lividus under the influence of temperature shifts

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Abstract

The ultrastructure of the cell wall and the thylakoid membranes of the thermophilic cyanobacterium Synechococcus lividus was studied by freezefracture electron microscopy after temperature shifts. Different fracture faces of the outer, the cytoplasmic and the thylakoid membranes were demonstrated when the preparation-temperature was in the range of the optimal growth temperature at 52°C or after fixation at 52°C. In the outer membrane of the cell wall two fracture faces with holes and 7.5 nm intramembrane particles were detected. On both the outer (EF) and inner (PF) leaflet of the cytoplasmic membrane randomly distributed particles were demonstrated. The particle density on the PF-face was approx. three times that of the EF-face. The EF-face of the thylakoid membrane exposed rows of particles with an average diameter of 10 nm. The spacing between the particle rows was 35–50 nm. This regular particle arrangement on the EF-face was demonstrated only in a few cases. Mostly the intramembrane particles were distributed randomly on the thylakoid fracture faces. The particle density of thylakoids with a random distribution was approx. in the same range both on the EF-and PF-face. The EF-particles fall into four groups of 9,10,11, and 12.5 nm. The main particle class was the 10 nm class. The PF-face exposed smaller particles with two maxima at 8.5–9 nm and 10 nm. When Synechococcus lividus OH-53s was chilled to temperatures below 30–35°C before the freeze-etch preparation a phase transition took place after the temperature shift. On the fracture faces of the thylakoid and cytoplasmic membranes particle depleted areas occurred. The size of the areas were different in both membranes and dependent on the velocity of cooling. Contrary to Synechococcus lividus OH-53s in the mesophilic Synechococcus strain 6910 the phase transition point was 15°C. The lower phase transition point may be due to a higher content of unsaturated fatty acids.

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References

  • Allen, M. M.: Photosynthetic membrane system in Anacystis nidulans. J. Bact. 96, 836–841 (1968)

    Google Scholar 

  • Armond, P. A., Staehelin, L. A., Arntzen, C. J.: Spatial relationship of photosystem I, photosystem II and the light harvesting complex in chloroplast membranes. J. Cell Biol. 73, 400–418 (1977)

    Google Scholar 

  • Arntzen, C. J., Dilley, R. A., Crane, F. L.: A comparison of chloroplast membrane surfaces by freeze-etch and negative staining techniques; and ultrastructural characterization of membrane fractions obtained from digitonin-treated spinach chloroplasts. J. Cell Biol. 43, 16–31 (1969)

    Google Scholar 

  • Bourdu, R., Lefort, M.: Structure fine, observées endosymbiotiques: Glaucocystis nostochinearum Itzigs, et Cyanophora paradoxa Korschikoff. C. R. Acad. Sc. Paris 265, 37–40 (1967)

    Google Scholar 

  • Branton, R., Bullivant, S., Gilula, N. B., Karnovsky, M. J., Moor, H., Mühlethaler, K., Northcote, D. H., Packer, L., Satir, B., Satir, P., Speth, V., Staehelin, L. A., Steere, R. L., Weinstein, R. S.: Freezeetching nomenclature. Science 190, 54–56 (1975)

    Google Scholar 

  • Castenholz, R. W.: Thermophilic blue-green algae and the thermal environment. Bacteriol. Rev. 33, 476–504 (1969)

    Google Scholar 

  • Castenholz, R. W.: Ecology of blue-green algae in hot springs. In: The biology of blue-green algae (N. G. Carr and B. A. Whitton, eds.), Oxford: 1973 Blackwell Scientific Publications

    Google Scholar 

  • Cohen-Bazire, G., Lefort-Tran, M.: Fixation of phycobiliproteis to photosynthetic membrane by glutaraldehyde. Arch. Mikrobiol. 71, 245–257 (1970)

    Google Scholar 

  • Drews, G.: Structure and development of the membrane system of photosynthetic bacteria. Current Topics in Bioenergetics 8B, 161–207 (1978)

    Google Scholar 

  • Edwards, M. R., Berns, D. S., Ghiorse, W. C., Holt, S. C.: Ultrastructure of the thermophilic blue-green alga Synechococcus lividus Copeland. J. Phycol. 4, 283–298 (1968)

    Google Scholar 

  • Edwards, M. R., Gantt, E.: Phycobilisomes of the thermophilic bluegreen alga Synechococcus lividus. J. Cell Biol. 50, 896–900 (1971)

    Google Scholar 

  • Esfahani, M., Limbrick, A. R., Knutton, S., Oka, T., Wakil, S. J.: The molecular organization of lipids in the membrane of Escherichia coli: Phase transitions. Proc. Nat. Acad. Sci. U.S.A. 68, 3180–3184 (1971)

    Google Scholar 

  • Farrell, J., Jose, A.: Temperature effects on microorganisms. Ann. Rev. Microbiol. 21, 101–120 (1967)

    Google Scholar 

  • Gantt, E., Conti, S. F.: Granules associated with the chloroplast lamellae of Porphyridium cruentum. J. Cell Biol. 29, 423–434 (1966)

    Google Scholar 

  • Giddings, Th. H., Jr., Staehelin, L. A.: Plasma membrane architecture of Anabaena cylindrica: occurrence of microplasmodesmata and changes associated with heterocyst development and the cell cycle. Cytobiologie 16, 235–249 (1978)

    Google Scholar 

  • Gill, C. O., Suisted, J. R.: The effects of temperature and growth rate on the proportion of unsaturated fatty acids in bacterial lipids. J. Gen. Microbiol. 104, 31–36 (1978)

    Google Scholar 

  • Golecki, J. R.: Studies on ultrastructure and composition of cell walls of the cyanobacterium Anacystis nidulans. Arch. Microbiol. 114, 35–41 (1977)

    Google Scholar 

  • Golecki, J. R., Drews, G.: Zur Struktur der Blaualgen-Zellwand. Gefrierätzuntersuchungen an normalen und extrahierten Zellwänden von Anabaena variabilis. Cytobiologie 8, 213–227 (1974)

    Google Scholar 

  • Haest, C. W. M., DeGier, J., Van Es, A., Verkleij, A. J., Van Deenen, L. L. M.: Fragility of the permeability barrier of Escherichia coli. Biochim. Biophys. Acta 288, 43–53 (1972)

    Google Scholar 

  • Haest, C. W. M., Verkleij, A. J., DeGier, J., Scheek, R., Ververgaert, P. H. J.: The effect of lipid phase transitions on the architecture of bacterial membranes. Biochim. Biophys. Acta 356, 17–26 (1974)

    Google Scholar 

  • Holt, S. C., Edwards, M. R.: Fine structure of the thermophilic bluegreen alga Synechococcus lividus Copeland. A study of froeenfractured-etched cells. Can. J. Microbiol. 18, 175–181 (1972)

    Google Scholar 

  • Jost, M.: Die Ultrastruktur von Oscillatoria rubescens D. C., Arch. Mikrobiol. 50, 211–245 (1965)

    Google Scholar 

  • Jüttner, F., Victor, H., Metzner, H.: Massenanzucht phototropher Organismen in einer automatischen Kulturanlage. Arch. Mikrobiol. 77, 275–280 (1971)

    Google Scholar 

  • Kenyon, C. N.: Fatty acid composition of unicellular strains of bluegreen algae. J. Bact. 109, 827–834 (1972)

    Google Scholar 

  • Krogmann, D. W.: Photosynthetic reactions and components of thylakoids. The biology of blue-green algae (N. J. Carr, B. A. Whitton, eds.) pp. 80–98, Oxford: Blackwell Scientific Publications 1973

    Google Scholar 

  • Lefort-Tran, M., Cohen-Bazire, G., Pouphile, M.: Les membranes photosynthétiques des algues à biliproteines observées apres cryodécapage. J. Ultrastruct. Res. 44, 199–209 (1973)

    Google Scholar 

  • Lichtlé, C., Thomas, J. C.: Etude ultrastructurale des thylakoides des algues à phycobiliproteines, comparaison des résultats obtenus par fixation classique et cryodécapage. Phycologia 15, 393–404 (1976)

    Google Scholar 

  • Marr, A. G., Ingraham, J. L.: Effect of temperature on the composition of fatty acids in Escherichia coli. J. Bact. 84, 1260–1267 (1962)

    Google Scholar 

  • Neushul, M.: Uniformity of thylakoid structure in red, brown, and two blue-green algae. J. Ultrastruct. Res. 37, 532–543 (1971)

    Google Scholar 

  • Nolan, W. G., Smillie, R. M.: Multi-temperature effects on Hill reaction activity of barley chloroplasts. Biochim. Biophys. Acta 440, 461–475 (1976)

    Google Scholar 

  • Oelze, J., Drews, G.: Membranes of photosynthetic bacteria. Biochim. Biophys. Acta. 265, 209–239 (1972)

    Google Scholar 

  • Ogawa, T., Vernon, L. P., Mollenhauer, H. H.: Properties and structure of fractions prepared from Anabaena variabilis by the action of Triton X-100. Biochim. Biophys. Acta. 172, 216–229 (1969)

    Google Scholar 

  • Ogawa, T., Vernon, L. P.: Properties of partially purified photosynthetic reaction centers from Scenedesmus mutant 6E and Anabaena variabilis grown in the presence of diphenylamine. Biochim. Biophys. Acta. 197, 292–301 (1970)

    Google Scholar 

  • Papahadjopoulos, D., Jacobsen, K., Nir, S., Isac, T.: Phase transitions in phospholipid vesicles. Fluorescence polarization and permeability measurements concerning the effect of temperature and cholesterol. Biochim. Biophys. Acta. 311, 330–348 (1973)

    Google Scholar 

  • Peary, J. A., Castenholz, R. W.: Temperature strains of a thermophilic blue-green alga. Nature 202, 720–721 (1964)

    Google Scholar 

  • Raison, J. K., Lyons, J. M., Thomson, W. W.: The influence of membranes on the temperature-induced changes in the kinetics of some respiratory enzymes of mitochondria. Arch. Biochem. Biophys. 142, 83–90 (1971)

    Google Scholar 

  • Speth, V., Wunderlich, F.: Membranes of Tetrahymena. II. Direct visualization of reversible transitions in biomembrane structure induced by temperature. Biochim. Biophys. Acta. 291, 621–628 (1973)

    Google Scholar 

  • Staehelin, L. A., Armond, P. A., Miller, K. R.: Chloroplast membrane organization at the supramolecular level and its functional implications. Krookhaven Symp. Biol. 28, 278–315 (1976)

    Google Scholar 

  • Stanier, R. Y., Kunisawa, R., Mandel, M., Cohen-Bazire, G.: Purification and properties of unicellular blue-green algae (order Chroococcales). Bact. Rev. 35, 171–205 (1971)

    Google Scholar 

  • Stanier, R. Y., Cohen-Bazire, G.: Phototrophic prokaryotes: The cyanobacteria. Ann. Rev. Microbiol. 31, 225–274 (1977)

    Google Scholar 

  • 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. Bact. 118, 725–734 (1974)

    Google Scholar 

  • Verkleij, A. J., Ververgaert, P. H. J., Van Deenen, L. L. M., Elbers, P. F.: Phase transitions of phospholipid bilayers and membranes of Acholeplasma Laidlawii B visualized by freeze fracturing electron microscopy. Biochim. Biophys. Acta. 288, 326–332 (1972)

    Google Scholar 

  • Wunderlich, F., Speth, V., Batz, W., Kleinig, H.: Membranes of Tetrahymena: III. The effect of temperature on membrane core, structure and fatty acid composition of Tetrahymena cells. Biochim. Biophys. Acta. 298, 39–49 (1973)

    Google Scholar 

  • Wunderlich, F. Ronai, H.: Adaptive lowering of the lipid clustering temperature within Tetrahymena membranes. FEBS Letters 55, 237–241 (1975)

    Google Scholar 

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Dedicated to Prof. D. Peters (Hamburg) on the occasion of the 65th anniversary of his birthday

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Golecki, J.R. Ultrastructure of cell wall and thylakoid membranes of the thermophilic cyanobacterium Synechococcus lividus under the influence of temperature shifts. Arch. Microbiol. 120, 125–133 (1979). https://doi.org/10.1007/BF00409098

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  • DOI: https://doi.org/10.1007/BF00409098

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