1887

Abstract

SUMMARY: Previous studies have shown that gas vesicles isolated from the cyanobacterium contain two types of protein, GvpA, a small hydrophobic protein that forms the main ribbed structure, and GvpC, a protein comprising five repeats of a 33-amino-acid-residue motif, which is located on the outer surface of the GvpA shell. GvpC was shown to increase the critical collapse pressure of the gas vesicles; it was thought to do this by forming a series of molecular ties that bind the ribs together. We now show that antibodies raised against GvpC label both the central cylinders and the conical end caps of native gas vesicles but fail to bind to gas vesicles that have been stripped of GvpC. The molar ratio of GvpA to GvpC has been calculated from amino acid analyses of gas vesicle hydrolysates by reference to the abundance of amino acids that occur predominantly or exclusively in one protein or the other; the molar ratio was found to be 25:1 in freshly isolated gas vesicles and 23:1 in gas vesicles saturated with GvpC. We have considered three ways in which the 33-residue repeats of GvpC might interact with the crystallographic unit cell of GvpA molecules in the ribs. The GvpC will bind to and restore the strength of gas vesicles isolated from and that lack their native GvpC.

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1993-10-01
2021-05-09
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References

  1. ARMSTRONG R.E., HAYES P.K., WALSBY A.E. 1983; Gas vacuole formation in hormogonia of Nostoc muscorum.. Journal of General Microbiology 128:263–170
    [Google Scholar]
  2. BLAUROCK A.E., WALSBY A.E. 1976; Crystalline structure of the gas vesicle wall from Anabaena flos-aquae.. Journal of Molecular Biology 105:183–199
    [Google Scholar]
  3. BLAUROCK A.E., WOBER W. 1976; Structure of the wall of Halobacterium halobium gas vesicles.. Journal of Molecular Biology 106:871–888
    [Google Scholar]
  4. BOWEN C.C., JENSEN T.E. 1965; Blue-green algae: fine structure of the gas vacuoles.. Science 147:1460–1462
    [Google Scholar]
  5. DAMERVAL T., HOUMARD J., GUGLIELMI G., CSISZÀR K., TANDEAU DE MARSAC N. 1987; A developmentally regulated gvpABC operonis involved in the formation of gas vesicles in the cyanobacterium Calothrix 7601.. Gene 54:83–92
    [Google Scholar]
  6. DAMERVAL T., CASTETS A.-M., GUGLIELMI G., HOUMARD J., TANDEAU DE MARSAC N. 1989; Occurrence and distribution of gas vesicle genes among cyanobacteria.. Journal of Bacteriology 171:1445–1452
    [Google Scholar]
  7. DAMERVAL T., CASTETS A.-M., HOUMARD J., TANDEAU DE MARSAC N. 1991; Gas vesicle synthesis in the cyanobacterium Pseudanabaena sp.: occurrence of a single photoregulated gene.. Molecular Microbiology 5:657–664
    [Google Scholar]
  8. DEVEREUX J., HAEBERLI P., SMITHIES O. 1984; A comprehensive set of sequence analysis programs for the VAX.. Nucleic Acids Research 12:387–395
    [Google Scholar]
  9. ENGLERT C., HORNE M., PFEIFER F. 1990; Expression of the major gas vesicle protein gene in the halophilic archaebacterium Haloferax mediterranei is modulated by salt.. Molecular and General Genetics 222:225–232
    [Google Scholar]
  10. FLYNN K.J. 1988; Some practical aspects of the analysis of dissolved free amino acids in natural waters and within microalgae by the use of HPLC.. Chemical Ecology 3:269–293
    [Google Scholar]
  11. GRIFFITHS A.E., WALSBY A.E., HAYES P.K. 1992; The homologies of gas vesicle proteins.. Journal of General Microbiology 138:1243–1250
    [Google Scholar]
  12. HARLOW E., LANE D. 1988 Antibodies. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  13. HAYAT M.A. 1989 Principles and Techniques of Electron Microscopy. London: Macmillan;
    [Google Scholar]
  14. HAYES P.K., WALSBY A.E. 1986; The inverse correlation between width and strength of gas vesicles in cyanobacteria.. British Phycological Journal 21:191–197
    [Google Scholar]
  15. HAYES P.K., WALSBY A.E., WALKER J.E. 1986; Complete amino acid sequence of cyanobacterial gas-vesicle protein indicates a 70-residue molecule that corresponds in size to the crystallographic unit cell.. Biochemical Journal 236:31–36
    [Google Scholar]
  16. HAYES P.K., LAZARUS C.M., BEES A., WALKER J.E., WALSBY A.E. 1988; The protein encoded by gvpC is a minor component of gas vesicles isolated from the cyanobacteria Anabaena flos-aquae and Microcystis sp.. Molecular Microbiology 2:545–552
    [Google Scholar]
  17. HAYES P.K., BUCHHOLZ B., WALSBY A.E. 1992; Gas vesicles are strengthened by the outer-surface protein, GvpC.. Archives of Microbiology 157:229–234
    [Google Scholar]
  18. HORNE M., ENGLERT C., PFEIFER F. 1988; Two genes encoding gas vacuole proteins in Halobacterium halobium.. Molecular and General Genetics 213:459–464
    [Google Scholar]
  19. HORNE M., ENGLERT C., WIMMER C., PFEIFER F. 1991; A DNA region of 9 kbp contains all genes necessary for gas vesicle synthesis in halophilic archaebacteria.. Molecular Microbiology 5:1159–1174
    [Google Scholar]
  20. JONES J.G., YOUNG D.C., DASSARMA S. 1991; Structure and organization of the gas vesicle gene cluster on the Halobacterium halobium plasmid pNCRIOO.. Gene 102:1017–1022
    [Google Scholar]
  21. JOST M. 1965; Die Ultrastruktur von Oscillatoria rubescens D.C.. Archiv für Mikrobiologie 50:211–245
    [Google Scholar]
  22. JOST M., JONES D.D. 1970; Morphological parameters and macromolecular organization of gas vacuole membranes of Micro-cystis aeruginosa Kuetz. emend. Elenkin.. Canadian Journal of Microbiology 16:159–164
    [Google Scholar]
  23. LAEMMLI U.K. 1970; Cleavage of structural proteins during the assembly of the head of bacteriophage T4.. Nature, London 227:680–685
    [Google Scholar]
  24. LEHMANN H., JOST M. 1971; Kinetics of the assembly of gas vacuoles in the blue-green alga Microcystis aeruginosa Kuetz. emend. Elekin.. Archiv für Microbiologie 79:59–68
    [Google Scholar]
  25. POWELL R.S., WALSBY A.E., HAYES P.K., PORTER R. 1991; Antibodies to the N-terminal sequence of GVPa bind to the ends of gas vesicles.. Journal of General Microbiology 137:2395–2400
    [Google Scholar]
  26. RIPPKA R., DERUELLES J., WATERBURY J.B., HERDMAN M., STANIER R.Y. 1979; Generic assignments, strain histories and properties of pure cultures of cyanobacteria.. Journal of General Microbiology 111:1–61
    [Google Scholar]
  27. SCHULZ G.E., SCHIRMER R.H. 1979 Principles of Protein Structure. New York: Springer-Verlag;
    [Google Scholar]
  28. SUREK B., PILLAY B., RDEST U., BEYREUTHER K., GOEBEL W. 1988; Evidence for two different gas vesicle proteins and genes in Halobacterium halobium.. Journal of Bacteriology 70:1746–1751
    [Google Scholar]
  29. TANDEAU DE MARSAC N., HOUMARD J. 1993; Adaptation of cyanobacteria to environmental stimuli: new steps towards molecular mechanisms.. FEMS Microbiology Reviews 104:119–189
    [Google Scholar]
  30. TANDEAU DE MARSAC N., MAZEL D., BRYANT D.A., HOUMARD J. 1985; Molecular cloning and nucleotide sequence of a developmentally regulated gene from the cyanobacterium Calothrix PCC 7601: a gas vesicle protein gene.. Nucleic Acids Research 13:7223–7236
    [Google Scholar]
  31. THOMPSON E.O.P., SANGER F. 1963; Halogenation of tyrosine during acid hydrolysis.. Biochimica et Biophysica Acta 71:468–471
    [Google Scholar]
  32. WAALAND J.R., BRANTON D. 1969; Gas vacuole development in a blue-green alga.. Science 163:1339–1341
    [Google Scholar]
  33. WALKER J.E., WALSBY A.E. 1983; Molecular weight of gas-vesicle protein from the planktonic cyanobacterium Anabaena flos-aquae and implications for structure of the vesicle.. Biochemical Journal 209:809–815
    [Google Scholar]
  34. WALKER J.E., HAYES P.K., WALSBY A.E. 1984; Homology of gas vesicle proteins in cyanobacteria and halobacteria.. Journal of General Microbiology 130:2709–2715
    [Google Scholar]
  35. WALSBY A.E. 1971; The pressure relationships of gas vacuoles.. Proceedings of the Royal Society of London B178301–326
    [Google Scholar]
  36. WALSBY A.E. 1972; Structure and function of gas vacuoles.. Bacteriological Reviews 36:1–32
    [Google Scholar]
  37. WALSBY A.E. 1977; Absence of gas vesicle protein in a mutant of Anabaena flos-aquae.. Archives of Microbiology 114:167–170
    [Google Scholar]
  38. WALSBY A.E. 1978; The gas vesicles of aquatic prokaryotes.. In Relations between Structure and Function in the Prokaryotic Cell (Symposia of the Society for General Microbiology no. 28) pp. 327–358 Edited by Stanier R. Y., Rogers H. J., Ward J. B. Cambridge: Cambridge University Press;
    [Google Scholar]
  39. WALSBY A.E. 1980; The water relations of gas-vacuolate prokaryotes.. Proceedings of the Royal Society of London B20873–102
    [Google Scholar]
  40. WALSBY A.E. 1991; The mechanical properties of the Microcystis gas vesicle.. Journal of General Microbiology 137:2401–2408
    [Google Scholar]
  41. WALSBY A.E., ARMSTRONG R.E. 1979; Average thickness of the gas vesicle wall.. Journal of Molecular Biology 129:279–285
    [Google Scholar]
  42. WALSBY A.E., BLEYTHING A. 1988; The dimensions of cyanobacterial gas vesicles in relation to their efficiency in providing buoyancy and withstanding pressure.. Journal of General Micro-biology 134:2635–2645
    [Google Scholar]
  43. WALSBY A.E., HAYES P.K. 1988; The minor cyanobacterial gas vesicle protein, GVPc, is attached to the outer surface of the gas vesicle.. Journal of General Microbiology 134:2647–2657
    [Google Scholar]
  44. WALSBY A.E., HAYES P.K. 1989; Gas vesicle proteins.. Biochemical Journal 264:313–322
    [Google Scholar]
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