1887

Abstract

Gas vesicle formation in halophilic archaea is encoded by a DNA region (the vac region) containing 14 different genes: and In PHH1 (which expresses the p-vac region from plasmid pHH1), gas vesicles are spindle shaped, whereas predominantly cylindrical gas vesicles are synthesized by the chromosomal c-vac region of PHH4 and the single chromosomal mc-vac region of Homologous complementation of gene clusters derived from the chromosomal c-vac region led to cylindrical gas vesicles in transformants and proved that the activity of the c- promoter depended on a gene product from the c- DNA region. Heterologous complementation experiments with transcription units of different vac regions demonstrated that the formation of chimeric gas vesicles was possible. Comparison of micrographs of wild-type and chimeric gas vesicles indicated that the shape was not exclusively determined by GvpA, the major structural protein of the gas vesicle wall. More likely, a dynamic equilibrium of several gene products was responsible for determination of the shape. Transmission electron microscopy of frozen hydrated, wild-type gas vesicles showed moiré patterns due to the superposition of the front and back parts of the ribbed gas vesicle envelope. Comparison of projections of model helices with the moiré pattern seen on the cylindrical part of the gas vesicles provided evidence that the ribs formed a helix of low pitch and not a stack of hoops.

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1998-05-01
2021-05-10
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References

  1. Blaseio, U., Pfeifer, F. (1990); Transformation of Halobacterium halobium: development of vectors and investigation of gas vesicle synthesis.. Proc Natl Acad Sci USA 87:(17)6772–6776 [CrossRef]
    [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:(2)183–199 [CrossRef]
    [Google Scholar]
  3. Cline, S. W., Schalkwyk, L., Doolittle, W. F. (1989); Transformation of the archaebacterium Halobacterium volcanii with genomic DNA.. Journal of Bacteriology 171:(9)4987–4991 [CrossRef]
    [Google Scholar]
  4. Damerval, T., Houmard, J., Guglielmi, G., Csiszar, K., Tandeau de Marsac, N. (1987); A developmentally regulated gvp ABC operon is involved in the formation of gas vesicles in the cyanobacterium Calothrix 7601.. Gene 54:(1)83–92 [CrossRef]
    [Google Scholar]
  5. Englert, C., Pfeifer, F. (1993); Analysis of gas-vesicle gene expression in Haloferax mediterranei reveals that GvpA and GvpC are both gas-vesicle structural proteins.. Journal of Biological Chemistry 268:(13)9329–9336 [CrossRef]
    [Google Scholar]
  6. Englert, C., Horne, M., Pfeifer, F. (1990); Expression of the major gas vesicle protein in the halophilic archaebacterium Haloferax mediterranei is modulated by salt.. Molecular & General Genetics 222:(2–3)225–232 [CrossRef]
    [Google Scholar]
  7. Englert, C., Krüger, K., Offner, S., Pfeifer, F. (1992a); Three different but related gene clusters encoding gas vesicles in halophilic archaea.. ] Mol Biol 227:(2)586–592 [CrossRef]
    [Google Scholar]
  8. Englert, C., Wanner, G., Pfeifer, F. (1992b); Functional analysis of the gas-vesicle gene cluster of the halophilic archaeon Haloferax mediterranei defines the vac-region boundary and suggests a regulatory role for the gvpD gene or its product.. Molecular Microbiology 6:(23)3543–3550 [CrossRef]
    [Google Scholar]
  9. Hain, J., Reiter, W.-D., HUdepohl, U., Zillig, W. (1992); Elements of an archaeal promoter defined by mutational analysis.. Nucleic Acids Research 20:(20)5423–5428 [CrossRef]
    [Google Scholar]
  10. Halladay, J., Jones, J., Lin, F., MacDonald, B., DasSarma, S. (1993); The rightward gas-vesicle operon in Halobacterium plasmid pNRClOO: identification of the gvp A and gvpC gene products by use of antibody probes and genetic analysis of the region downstream of gvpC.. Journal of Bacteriology 175:(3)684–692 [CrossRef]
    [Google Scholar]
  11. Hanahan, D. (1983); Studies on transformation of Escherichia coli with plasmids.. Journal of Molecular Biology 166:(4)557–580 [CrossRef]
    [Google Scholar]
  12. Hayes, P. K., Powell, R. S. (1995); The gvpA/C cluster of Anabaena flos-aquae has multiple copies of a gene encoding GvpA.. Archives of Microbiology 164:(1)50–57 [CrossRef]
    [Google Scholar]
  13. Hayes, P. K., Buchholz, B., Walsby, A. E. (1992); Gas vesicles are strengthened by the outer-surface protein.. GvpC Archives of Microbiology 157:(3)229–234 [CrossRef]
    [Google Scholar]
  14. Hegerl, R. (1996); The em program package: a platform for image processing in biological electron microscopy.. Journal of Structural Biology 116:(1)30–34 [CrossRef]
    [Google Scholar]
  15. Holmes, M. L., Nuttall, S. D., Dyall-Smith, M. L., Horne, M., Pfeifer, F. (1991); Construction and use of halobacterial shuttle vectors and further studies on Haloferax DNA gyrase, Expression of two gas vacuole protein genes in Halobacterium halobium.. Journal of Bacteriology 12:(12)3807–3813 [CrossRef]
    [Google Scholar]
  16. Horne, M., Englert, C., Pfeifer, F. (1988); Two genes encoding gas vacuole proteins in Halobacterium halobium.. Molecular & General Genetics 213:(2–3)459–464 [CrossRef]
    [Google Scholar]
  17. 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:(5)11591174–1174 [CrossRef]
    [Google Scholar]
  18. Jones, J. G., Young, D. C., DasSarma, S. (1991); Structure and organization of the gas-vesicle gene cluster on the Halobacterium halobium plasmid pNRClOO.. Gene 102:(1)117–122 [CrossRef]
    [Google Scholar]
  19. Kinsman, R., Hayes, P. K., Gvps, N., K., J. (1997); Genes encoding proteins homologous to halobacterial, F and L are located downstream of gvpC in the cyanobacterium Anabaena flos- aquae.. DNA Seq 7:(2)97–106 [CrossRef]
    [Google Scholar]
  20. Kinsman, R., Walsby, A. E., Hayes, P. K. (1995); GvpCs with reduced numbers of repeating sequence elements bind to and strengthen cyanobacterial gas vesicles.. Molecular Microbiology 17:(1)147154–154 [CrossRef]
    [Google Scholar]
  21. Krantz, M. J., Ballou C. E. (1973); Analysis of Halobacterium halobium gas vesicles.. Journal of Bacteriology 3:(3)1058–1067 [CrossRef]
    [Google Scholar]
  22. Krüger, K. (1996) Untersuchungen zur Regulation der Gasvesi- kelsynthese in dem halophilen Archaeon Halobacterium salinarium PHH4. . In Dissertation, LMU Miinchen. Munich:: Shaker Verlag;
    [Google Scholar]
  23. KrUger, K., Pfeifer, F. (1996); Transcript analysis of the c-vac region, and differential synthesis of the two regulatory gas-vesicle proteins GvpD and GvpE in Halobacterium salinarium PHH4.. Journal of Bacteriology 178:(14)4012–019 [CrossRef]
    [Google Scholar]
  24. Lam, W. L., Doolittle, W. F. (1989); Shuttle vectors for the archaebacterium Halobacterium volcanii.. Proc Natl Acad Sci USA 86:(14)5478–5482 [CrossRef]
    [Google Scholar]
  25. McMaster, T. J., Miles, M. J., Walsby, A. E. (1996); Direct observation of protein secondary structure in gas vesicles by atomic force microscopy.. Biophysical Journal 70:(5)2432–2436 [CrossRef]
    [Google Scholar]
  26. Mayr, A., Pfeifer, F. (1997); The characterization of the nv- gvpACNOFGH gene cluster involved in gas vesicle formation in Natronobacterium vacuolatum.. Archives of Microbiology 168:(1)24–32 [CrossRef]
    [Google Scholar]
  27. Offner, S., Pfeifer, F. (1995); Complementation studies with the gas vesicle-encoding p-vac region of Halobacterium salinarium PHHl reveal a regulatory role for the p-gvpDE genes.. Molecular Microbiology 16:(1)9–19 [CrossRef]
    [Google Scholar]
  28. Offner, S., Wanner, G., Pfeifer, F. (1996); Functional studies of the gvpACNO operon of Halobacterium salinarium reveal that the GvpC protein shapes gas vesicles.. Journal of Bacteriology 178:(7)2071–2078 [CrossRef]
    [Google Scholar]
  29. Palmer, B., Marinus, M. (1994); The dam and dcm strains of Escherichia coli - a review.. Gene 143:(1)1–12 [CrossRef]
    [Google Scholar]
  30. Pfeifer, F., Ghahraman, P. (1993); Plasmid pHHl of Halobacterium salinarium: characterization of the replicon region, the gas-vesicle gene cluster and insertion elements.. Molecular & General Genetics 238:(1–2)193–200 [CrossRef]
    [Google Scholar]
  31. Pfeifer, F., Offner, S., KrUger, K., Ghahraman, P., Englert, C. (1994); Transformation of halophilic archaea and investigation of gas-vesicle synthesis.. Systematic and Applied Microbiology 16:(4)569–577 [CrossRef]
    [Google Scholar]
  32. Pfeifer, F., Krüger, K., Rbder, R., Mayr, A., Ziesche, S. et al. (1997); Gas vesicle formation in halophilic archaea.. Archives of Microbiology 167:(5)259–268 [CrossRef]
    [Google Scholar]
  33. Rttder, R., Pfeifer, F. (1996); Influence of salt on the transcription of the gas-vesicle genes of Haloferax mediterranei and identification of the endogenous transcriptional activator gene.. Microbiology 142:(7)1715–1723 [CrossRef]
    [Google Scholar]
  34. Sambrook, J., Fritsch, E. F., Maniatis, T. (1989) Molecular Cloning: a Laboratory Manual., 2nd edn.. Cold Spring Harbor, NY:: Cold Spring Harbor Laboratory;
    [Google Scholar]
  35. Schckjger, H., von Jagow, G. (1987); Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for separation of proteins in the range from 1 to 100 kDa.. Analytical Biochemistry 166:(2)368–379 [CrossRef]
    [Google Scholar]
  36. Simon, R. (1981); Morphology and protein composition of gas vesicles from wild type and gas vacuole deficient strains of Halobacterium salinarium strain 5.. Journal of General Microbiology 125:103–111
    [Google Scholar]
  37. Stoeckenius, W., Kunau, W. H. (1968); Further characterization of particulate fractions from lysed cell envelopes of Halobacterium halobium and isolation of gas vacuole membrane.. ] Cell Biol 38:(2)337–357 [CrossRef]
    [Google Scholar]
  38. Surek, B., Pillay, B., Rdest, U., Bayreuther, K., Goebel, W. (1988); Evidence for two different gas vesicle proteins and genes in Halobacterium halobium.. Journal of Bacteriology 170:(4)1746–1751 [CrossRef]
    [Google Scholar]
  39. Ventosa, A., Oren, A. (1996); Halobacterium salinarum nom. corrig., a name to replace Halobacterium salinarium (Elazari- Volcani) and to include Halobacterium halobium and Halobacterium cutirubrum.. International Journal of Systematic Bacteriology 46:(1)347–347 [CrossRef]
    [Google Scholar]
  40. 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]
  41. Walsby, A. E. (1972); Structure and function of gas vacuoles.. Bacteriological Reviews 36:(1)1–32 [CrossRef]
    [Google Scholar]
  42. Walsby, A. E. (1994); Gas vesicles.. Microbiological Reviews 58:(1)94–144 [CrossRef]
    [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]
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