Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Distribution, formation and regulation of gas vesicles

Nature Reviews Microbiology volume 10, pages 705–715 (2012)Cite this article

Subjects

Key Points

  • Many bacteria and archaea synthesize intracellular gas-filled proteinaceous structures known as gas vesicles to act as flotation devices in aqueous environments.

  • Gas vesicles provide buoyancy to cells and might help cells survive under stress conditions. Large amounts of gas vesicles reduce the size of the cytoplasm and thereby increase the cell surface-to-volume ratio. Gas vesicles add hollow spaces to the cells, and these spaces are filled, by diffusion, with gases that are dissolved in the surrounding medium; no storage of gas occurs. Gas vesicles of cyanobacteria are permeable to oxygen, nitrogen, hydrogen, carbon dioxide, carbon monoxide, methane and even perfluorocyclobutane.

  • The archaeal gas vesicle wall is formed solely of protein, and the small hydrophobic protein gas vesicle protein A (GvpA) is the main constituent. Another structural protein is GvpC, which stabilizes the wall by attaching to the outside. In the halophilic archaeon Halobacterium salinarum, 12 additional Gvp proteins are required for gas vesicle formation, two of which, GvpD and GvpE, are involved in the regulation of gvp gene expression. GvpE increases transcription by 60–100-fold, whereas GvpD acts as a sink for GvpE. High salt concentrations, high cell densities or growth at low temperatures increase the formation of archaeal gas vesicles, whereas low salt concentrations, anoxic conditions or high light intensities decrease the production of these vesicles.

  • Bacterial gvp gene clusters share many of the essential gvp genes with haloarchaea, but also contain genes with no haloarchaeal homologues. The formation of bacterial gas vesicles is influenced by cell density and light intensities.

  • The formation of the gas vesicle wall is not yet fully understood. Initial information on the structure of GvpA came from solid-NMR studies and suggests a coil–α-helix–β-strand–β-strand–α-helix–coil peptide backbone. The GvpA monomer contains an antiparallel β-sheet (formed by the two β-strands), which might be extended by antiparallel associations with the β-sheets in adjacent monomers.

Abstract

A range of bacteria and archaea produce intracellular gas-filled proteinaceous structures that function as flotation devices in order to maintain a suitable depth in the aqueous environment. The wall of these gas vesicles is freely permeable to gas molecules and is composed of a small hydrophobic protein, GvpA, which forms a single-layer wall. In addition, several minor structural, accessory or regulatory proteins are required for gas vesicle formation. In different organisms, 8–14 genes encoding gas vesicle proteins have been identified, and their expression has been shown to be regulated by environmental factors. In this Review, I describe the basic properties of gas vesicles, the genes that encode them and how their production is regulated. I also discuss the function of these vesicles and the initial attempts to exploit them for biotechnological purposes.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Learn more

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Gas vesicles: the basics.
Figure 2: Regulation of haloarchaeal gene clusters encoding gas vesicle proteins.
Figure 3: Gas vesicle protein-encoding gene clusters.
Figure 4: The sequence and structure of gas vesicle protein A.

Similar content being viewed by others

References

  1. Klebahn, H. Gasvakuolen, ein Bestandteil der Zellen der wasserblütenbildenden Phycochromaceen. Flora (Jena) 80, 241–282 (1895).

    Google Scholar 

  2. Bowen, C. C. & Jensen, T. E. Blue-green algae: fine structure of the gas vacuoles. Science 147, 1460–1461 (1965).

    Article  CAS  PubMed  Google Scholar 

  3. Petter, H. On bacteria of salted fish. Proc. Natl Acad. Sci. Amsterdam 34, 1417–1423 (1931).

    CAS  Google Scholar 

  4. Houwink, A. L. Flagella, gas vacuoles and cell wall structure in Halobacterium halobium; an electron microscope study. J. Gen. Microbiol. 15, 146–150 (1956).

    Article  CAS  PubMed  Google Scholar 

  5. Walsby, A. E. Gas vesicles. Microbiol. Rev. 58, 94–144 (1994). An excellent review on the physical properties of gas vesicles and their functions in bacteria.

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Englert, C. & Pfeifer, F. Analysis of gas vesicle gene expression in Haloferax mediterranei reveals that GvpA and GvpC are both gas vesicle structural proteins. J. Biol. Chem. 268, 9329–9336 (1993).

    CAS  PubMed  Google Scholar 

  7. Halladay, J. T., Jones, J. G., Lin, F., MacDonald, A. B. & DasSarma, S. The rightward gas vesicle operon in Halobacterium plasmid pNRC100: identification of the gvpA and gvpC gene products by use of antibody probes and genetic analysis of the region downstream of gvpC. J. Bacteriol. 175, 684–692 (1993).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Hayes, P. K., Buchholz, B. & Walsby, A. E. Gas vesicles are strengthened by the outer-surface protein, GvpC. Arch. Microbiol. 157, 229–234 (1992).

    Article  CAS  PubMed  Google Scholar 

  9. Hayes, P. K., Lazarus, C. M., Bees, A., Walker, J. E. & Walsby, A. E. The protein encoded by gvpC is a minor component of gas vesicles isolated from the cyanobacteria Anabaena flos-aquae and Microcystis sp. Mol. Microbiol. 2, 545–552 (1988).

    Article  CAS  PubMed  Google Scholar 

  10. Walsby, A. E. & Hayes, P. K. The minor cyanobacterial gas vesicle protein, GvpC, is attached to the outer surface of the gas vesicle. J. Gen. Microbiol. 134, 2647–2657 (1988).

    CAS  Google Scholar 

  11. Stoeckenius, W. & Kunau, W. H. Further characterization of particulate fractions from lysed cell envelopes of Halobacterium halobium and isolation of gas vacuole membranes. J. Cell Biol. 38, 337–357 (1968).

    Article  PubMed Central  Google Scholar 

  12. Oesterhelt, D. The structure and mechanism of the family of retinal proteins from halophilic archaea. Curr. Opin. Struct. Biol. 8, 489–500 (1998).

    Article  CAS  PubMed  Google Scholar 

  13. Hechler, T. & Pfeifer, F. Anaerobiosis inhibits gas vesicle formation in halophilic Archaea. Mol. Microbiol. 71, 132–145 (2009).

    Article  CAS  PubMed  Google Scholar 

  14. Bleiholder, A., Frommherz, R., Teufel, K. & Pfeifer, F. Expression of multiple tfb genes in different Halobacterium salinarum strains and interaction of TFB with transcriptional activator GvpE. Arch. Microbiol. 194, 269–279 (2012).

    Article  CAS  PubMed  Google Scholar 

  15. Coker, J. A. & DasSarma, S. Genetic and transcriptomic analysis of transcription factor genes in the model halophilic Archaeon: coordinate action of TbpD and TfbA. BMC Genet. 8, 61 (2007).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  16. Englert, C., Horne, M. & Pfeifer, F. Expression of the major gas vesicle protein gene in the halophilic archaebacterium Haloferax mediterranei is modulated by salt. Mol. Gen. Genet. 222, 225–232 (1990).

    Article  CAS  PubMed  Google Scholar 

  17. Mayr, A. & Pfeifer, F. The characterization of the nv-gvpACNOFGH gene cluster involved in gas vesicle formation in Natronobacterium vacuolatum. Arch. Microbiol. 168, 24–32 (1997).

    Article  CAS  PubMed  Google Scholar 

  18. Mwatha, W. E. & Grant, W. D. Natronobacterium vacuolata sp. nov, a haloalkaliphilic archaeon isolated from Lake Magadi, Kenya. Int. J. System Bacteriol. 43, 401–404 (1993).

    Article  Google Scholar 

  19. Bolhuis, H., te Poele, E. M. & Rodriguez-Valera, F. Isolation and cultivation of Walsby's square archaeon. Environ. Microbiol. 6, 1287–1291 (2004).

    Article  PubMed  Google Scholar 

  20. Burns, D. G., Camakaris, H. M., Janssen, P. H. & Dyall-Smith, M. L. Cultivation of Walsby's square haloarchaeon. FEMS Microbiol. Lett. 238, 469–473 (2004).

    CAS  PubMed  Google Scholar 

  21. Parkes, K. & Walsby, A. E. Ultrastructure of a gas-vacuolate square bacterium. J. Gen. Microbiol. 126, 503–506 (1981).

    Google Scholar 

  22. Oren, A., Pri-El, N., Shapiro, O. & Siboni, N. Buoyancy studies in natural communities of square gas-vacuolate archaea in saltern crystallizer ponds. Saline Systems 2, 4 (2006).

    Article  PubMed  PubMed Central  Google Scholar 

  23. Oliver, R. L. & Walsby, A. E. Direct evidence for the role of light-mediated gas vesicle collapse in the buoyancy regulation of Anabaena flos-aquae (Cyanobacteria). Limnol. Oceanogr. 29, 879–886 (1984).

    Article  Google Scholar 

  24. Thomas, R. H. & Walsby, A. E. Buoyancy regulation in a strain of Microcystis. J. Gen. Microbiol. 131, 799–809 (1985).

    Google Scholar 

  25. Overmann, J., Lehmann, S. & Pfennig, N. Gas vesicle formation and buoyancy regulation in Pelodictyon phaeoclathratiforme (Green sulfur bacteria). Arch. Microbiol. 157, 29–37 (1991).

    Article  CAS  Google Scholar 

  26. Clark, A. E. & Walsby, A. E. Development and vertical distribution of populations of gas-vacuolate bacteria in an eutrophic, monomictic lake. Arch. Microbiol. 118, 229–233 (1978).

    Article  Google Scholar 

  27. Walsby, A. E. & Hayes, P. K. Gas vesicle proteins. Biochem. J. 264, 313–322 (1989).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Gosink, J. J., Herwig, R. P. & Staley, J. T. Octadecabacter arcticus gen. nov., sp. nov., and O. antarcticus, sp. nov., nonpigmented, psychrophilic gas vacuolate bacteria from polar sea ice and water. Syst. Appl. Microbiol. 20, 512–512 (1997).

    Article  Google Scholar 

  29. Jung, D. O., Achenbach, L. A., Karr, E. A., Takaichi, S. & Madigan, M. T. A gas vesiculate planktonic strain of the purple non-sulfur bacterium Rhodoferax antarcticus isolated from Lake Fryxell, Dry Valleys, Antarctica. Arch. Microbiol. 182, 236–243 (2004).

    Article  CAS  PubMed  Google Scholar 

  30. Staley, J. T., Irgens, R. L. & Herwig, R. P. Gas vacuolate bacteria from the sea ice of Antarctica. Appl. Environ. Microbiol. 55, 1033–1036 (1989).

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Isaksen, M. F. & Teske, A. Desulforhopalus vacuolatus gen nov, sp nov, a new moderately psychrophilic sulfate-reducing bacterium with gas vacuoles isolated from a temperate estuary. Arch. Microbiol. 166, 160–168 (1996).

    Article  CAS  Google Scholar 

  32. Irgens, R. L., Suzuki, I. & Staley, J. T. Gas vacuolate bacteria obtained from marine waters of Antarctica. Curr. Microbiol. 18, 261–265 (1989).

    Article  Google Scholar 

  33. Konopka, A. E., Lara, J. C. & Staley, J. T. Isolation and characterization of gas vesicles from Microcyclus aquaticus. Arch. Microbiol. 112, 133–140 (1977).

    Article  CAS  PubMed  Google Scholar 

  34. Staley, J. T. Prosthecomicrobium and Ancalomicrobium: new prosthecate freshwater bacteria. J. Bacteriol. 95, 1921–1942 (1968).

    CAS  PubMed  PubMed Central  Google Scholar 

  35. Staley, J. T., Irgens, R. L. & Brenner, D. J. Enhydrobacter aerosaccus gen. nov., sp. nov, a gas-vacuolated, facultatively anaerobic, heterotrophic rod. Int. J. Syst. Bacteriol. 37, 289–291 (1987).

    Article  Google Scholar 

  36. van Ert, M. & Staley, J. T. New gas vacuolated heterotrophic rod from freshwaters. Arch. Mikrobiol. 80, 70–77 (1971).

    Article  CAS  PubMed  Google Scholar 

  37. Oren, A. Clostridium lortetii sp. nov., a halophilic obligatory anaerobic bacterium producing endospores with attached gas vacuoles. Arch. Microbiol. 136, 42–48 (1983).

    Article  Google Scholar 

  38. Widdel, F. & Pfennig, N. A new anaerobic, sporing, acetate-oxidizing, sulfate-reducing bacterium, Desulfotomaculum (emend.) acetoxidans. Arch. Microbiol. 112, 119–122 (1977).

    Article  CAS  PubMed  Google Scholar 

  39. Li, N. & Cannon, M. C. Gas vesicle genes identified in Bacillus megaterium and functional expression in Escherichia coli. J. Bacteriol. 180, 2450–2458 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  40. Ramsay, J. P., Williamson, N. R., Spring, D. R. & Salmond, G. P. A quorum-sensing molecule acts as a morphogen controlling gas vesicle organelle biogenesis and adaptive flotation in an enterobacterium. Proc. Natl Acad. Sci. USA 108, 14932–14937 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Damerval, T., Houmard, J., Guglielmi, G., Csiszar, K. & Tandeau de Marsac, N. A developmentally regulated gvpABC operon is involved in the formation of gas vesicles in the cyanobacterium Calothrix 7601. Gene 54, 83–92 (1987).

    Article  CAS  PubMed  Google Scholar 

  42. Tandeau de Marsac, N., Mazel, D., Bryant, D. A. & Houmard, J. Molecular cloning and nucleotide sequence of a developmentally regulated gene from the cyanobacterium Calothrix PCC 7601: a gas vesicle protein gene. Nucleic Acids Res. 13, 7223–7236 (1985).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Walker, J. E. & Walsby, A. E. Molecular weight of gas vesicle protein from the planktonic cyanobacterium Anabaena flos-aquae and implications for structure of the vesicle. Biochem. J. 209, 809–815 (1983).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. DasSarma, S., Damerval, T., Jones, J. G. & Tandeau de Marsac, N. A plasmid-encoded gas vesicle protein gene in a halophilic archaebacterium. Mol. Microbiol. 1, 365–370 (1987).

    Article  CAS  PubMed  Google Scholar 

  45. Horne, M., Englert, C. & Pfeifer, F. Two genes encoding gas vacuole proteins in Halobacterium halobium. Mol. Gen. Genet. 213, 459–464 (1988).

    Article  CAS  PubMed  Google Scholar 

  46. Horne, M. & Pfeifer, F. Expression of two gas vacuole protein genes in Halobacterium halobium and other related species. Mol. Gen. Genet. 218, 437–444 (1989).

    Article  CAS  PubMed  Google Scholar 

  47. Englert, C., Krüger, K., Offner, S. & Pfeifer, F. Three different but related gene clusters encoding gas vesicles in halophilic archaea. J. Mol. Biol. 227, 586–592 (1992).

    Article  CAS  PubMed  Google Scholar 

  48. Ng, W. V. et al. Genome sequence of Halobacterium species NRC-1. Proc. Natl Acad. Sci. USA 97, 12176–12181 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Krüger, K. & Pfeifer, F. Transcript analysis of the c-vac region and differential synthesis of the two regulatory gas vesicle proteins GvpD and GvpE in Halobacterium salinarium PHH4. J. Bacteriol. 178, 4012–4019 (1996).

    Article  PubMed  PubMed Central  Google Scholar 

  50. Ng, W. L., Kothakota, S. & DasSarma, S. Structure of the gas vesicle plasmid in Halobacterium halobium: inversion isomers, inverted repeats, and insertion sequences. J. Bacteriol. 173, 1958–1964 (1991).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Bauer, M. et al. Overlapping activator sequences determined for two oppositely oriented promoters in halophilic Archaea. Nucleic Acids Res. 36, 598–606 (2008).

    Article  CAS  PubMed  Google Scholar 

  52. Englert, C., Wanner, G. & Pfeifer, F. 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. Mol. Microbiol. 6, 3543–3550 (1992).

    Article  CAS  PubMed  Google Scholar 

  53. Röder, R. & Pfeifer, F. Influence of salt on the transcription of the gas-vesicle genes of Haloferax mediterranei and identification of the endogenous transcriptional activator gene. Microbiology 142, 1715–1723 (1996).

    Article  PubMed  Google Scholar 

  54. Gregor, D. & Pfeifer, F. Use of a halobacterial bgaH reporter gene to analyse the regulation of gene expression in halophilic archaea. Microbiology 147, 1745–1754 (2001).

    Article  CAS  PubMed  Google Scholar 

  55. Gregor, D. & Pfeifer, F. In vivo analyses of constitutive and regulated promoters in halophilic archaea. Microbiology 151, 25–33 (2005).

    Article  CAS  PubMed  Google Scholar 

  56. Hofacker, A., Schmitz, K. M., Cichonczyk, A., Sartorius-Neef, S. & Pfeifer, F. GvpE- and GvpD-mediated transcription regulation of the p-gvp genes encoding gas vesicles in Halobacterium salinarum. Microbiology 150, 1829–1838 (2004).

    Article  CAS  PubMed  Google Scholar 

  57. Teufel, K. & Pfeifer, F. Interaction of transcription activator GvpE with TATA-box-binding proteins of Halobacterium salinarum. Arch. Microbiol. 192, 143–149 (2010).

    Article  CAS  PubMed  Google Scholar 

  58. Scheuch, S., Marschaus, L., Sartorius-Neef, S. & Pfeifer, F. Regulation of gvp genes encoding gas vesicle proteins in halophilic Archaea. Arch. Microbiol. 190, 333–339 (2008).

    Article  CAS  PubMed  Google Scholar 

  59. Scheuch, S. & Pfeifer, F. GvpD-induced breakdown of the transcriptional activator GvpE of halophilic archaea requires a functional p-loop and an arginine-rich region of GvpD. Microbiology 153, 947–958 (2007).

    Article  CAS  PubMed  Google Scholar 

  60. Zimmermann, P. & Pfeifer, F. Regulation of the expression of gas vesicle genes in Haloferax mediterranei: interaction of the two regulatory proteins GvpD and GvpE. Mol. Microbiol. 49, 783–794 (2003).

    Article  CAS  PubMed  Google Scholar 

  61. Offner, S., Hofacker, A., Wanner, G. & Pfeifer, F. Eight of fourteen gvp genes are sufficient for formation of gas vesicles in halophilic archaea. J. Bacteriol. 182, 4328–4336 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Offner, S., Wanner, G. & Pfeifer, F. Functional studies of the gvpACNO operon of Halobacterium salinarium reveal that the GvpC protein shapes gas vesicles. J. Bacteriol. 178, 2071–2078 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Chu, L. J. et al. New structural proteins of Halobacterium salinarum gas vesicle revealed by comparative proteomics analysis. J. Proteome Res. 10, 1170–1178 (2011).

    Article  CAS  PubMed  Google Scholar 

  64. Shukla, H. D. & DasSarma, S. Complexity of gas vesicle biogenesis in Halobacterium sp. strain NRC-1: identification of five new proteins. J. Bacteriol. 186, 3182–3186 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Strunk, T. et al. Structural model of the gas vesicle protein GvpA and analysis of GvpA mutants in vivo. Mol. Microbiol. 81, 56–68 (2011).

    Article  CAS  PubMed  Google Scholar 

  66. Beard, S. J., Davis, P. A., Iglesias-Rodriguez, D., Skulberg, O. M. & Walsby, A. E. Gas vesicle genes in Planktothrix spp. from Nordic lakes: strains with weak gas vesicles possess a longer variant of gvpC. Microbiology 146, 2009–2018 (2000).

    Article  CAS  PubMed  Google Scholar 

  67. Beard, S. J., Handley, B. A. & Walsby, A. E. Spontaneous mutations in gas vesicle genes of Planktothrix spp. affect gas vesicle production and critical pressure. FEMS Microbiol. Lett. 215, 189–195 (2002).

    Article  CAS  PubMed  Google Scholar 

  68. Hayes, P. K. & Powell, R. S. The gvpA/C cluster of Anabaena flos-aquae has multiple copies of a gene encoding GvpA. Arch. Microbiol. 164, 50–57 (1995).

    Article  CAS  PubMed  Google Scholar 

  69. Kinsman, R. & Hayes, P. K. Genes encoding proteins homologous to halobacterial Gvps N, J, K, F & L are located downstream of gvpC in the cyanobacterium Anabaena flos-aquae. DNA Seq. 7, 97–106 (1997).

    Article  CAS  PubMed  Google Scholar 

  70. Mlouka, A., Comte, K., Castets, A. M., Bouchier, C. & Tandeau de Marsac, N. The gas vesicle gene cluster from Microcystis aeruginosa and DNA rearrangements that lead to loss of cell buoyancy. J. Bacteriol. 186, 2355–2365 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. van Keulen, G., Hopwood, D. A., Dijkhuizen, L. & Sawers, R. G. Gas vesicles in actinomycetes: old buoys in novel habitats? Trends Microbiol. 13, 350–354 (2005).

    Article  CAS  PubMed  Google Scholar 

  72. Walsby, A. E. & Dunton, P. G. Gas vesicles in actinomycetes? Trends Microbiol. 14, 99–100 (2006).

    Article  CAS  PubMed  Google Scholar 

  73. Lee, E. J. et al. A master regulator σB governs osmotic and oxidative response as well as differentiation via a network of sigma factors in Streptomyces coelicolor. Mol. Microbiol. 57, 1252–1264 (2005).

    Article  CAS  PubMed  Google Scholar 

  74. Bright, D. I. & Walsby, A. E. The relationship between critical pressure and width of gas vesicles in isolates of Planktothrix rubescens from Lake Zurich. Microbiology 145, 2769–2775 (1999).

    Article  CAS  PubMed  Google Scholar 

  75. Jones, D. D. & Jost, M. Characterization of the protein from gas vesicles membranes of the blue-green algae Microcystis aeruginosa. Planta 100, 277–287 (1971).

    Article  CAS  PubMed  Google Scholar 

  76. Offner, S., Ziese, U., Wanner, G., Typke, D. & Pfeifer, F. Structural characteristics of halobacterial gas vesicles. Microbiology 144, 1331–1342 (1998).

    Article  CAS  PubMed  Google Scholar 

  77. McMaster, T. J., Miles, M. J. & Walsby, A. E. Direct observation of protein secondary structure in gas vesicles by atomic force microscopy. Biophys. J. 70, 2432–2436 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Blaurock, A. E. & Walsby, A. E. Crystalline structure of the gas vesicle wall from Anabaena flos-aquae. J. Mol. Biol. 105, 183–199 (1976).

    Article  CAS  PubMed  Google Scholar 

  79. Belenky, M., Meyers, R. & Herzfeld, J. Subunit structure of gas vesicles: a MALDI-TOF mass spectrometry study. Biophys. J. 86, 499–505 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Bayro, M. J., Daviso, E., Belenky, M., Griffin, R. G. & Herzfeld, J. An amyloid organelle: solid state NMR evidence for cross-beta assembly of gas vesicles. J. Biol. Chem. 287, 3479–3484 (2011).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  81. Sivertsen, A. C., Bayro, M. J., Belenky, M., Griffin, R. G. & Herzfeld, J. Solid-state NMR evidence for inequivalent GvpA subunits in gas vesicles. J. Mol. Biol. 387, 1032–1039 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Sivertsen, A. C., Bayro, M. J., Belenky, M., Griffin, R. G. & Herzfeld, J. Solid-state NMR characterization of gas vesicle structure. Biophys. J. 99, 1932–1939 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Buchholz, B. E., Hayes, P. K. & Walsby, A. E. The distribution of the outer gas vesicle protein, GvpC, on the Anabaena gas vesicle, and its ratio to GvpA. J. Gen. Microbiol. 139, 2353–2363 (1993).

    Article  CAS  PubMed  Google Scholar 

  84. Kinsman, R., Walsby, A. E. & Hayes, P. K. GvpCs with reduced numbers of repeating sequence elements bind to and strengthen cyanobacterial gas vesicles. Mol. Microbiol. 17, 147–154 (1995).

    Article  CAS  PubMed  Google Scholar 

  85. Dunton, P. G., Mawby, W. J., Shaw, V. A. & Walsby, A. E. Analysis of tryptic digests indicates regions of GvpC that bind to gas vesicles of Anabaena flos-aquae. Microbiology 152, 1661–1669 (2006).

    Article  CAS  PubMed  Google Scholar 

  86. Horne, M., Englert, C., Wimmer, C. & Pfeifer, F. A. DNA region of 9 kbp contains all genes necessary for gas vesicle synthesis in halophilic archaebacteria. Mol. Microbiol. 5, 1159–1174 (1991).

    Article  CAS  PubMed  Google Scholar 

  87. Offner, S. & Pfeifer, F. Complementation studies with the gas vesicle-encoding p-vac region of Halobacterium salinarium PHH1 reveal a regulatory role for the p-gvpDE genes. Mol. Microbiol. 16, 9–19 (1995).

    Article  CAS  PubMed  Google Scholar 

  88. Jäger, A., Samorski, R., Pfeifer, F. & Klug, G. Individual gvp transcript segments in Haloferax mediterranei exhibit varying half-lives, which are differentially affected by salt concentration and growth phase. Nucleic Acids Res. 30, 5436–5443 (2002).

    Article  PubMed  PubMed Central  Google Scholar 

  89. Csiszar, K., Houmard, J., Damerval, T. & Tandeau de Marsac, N. Transcriptional analysis of the cyanobacterial gvpABC operon in differentiated cells: occurrence of an antisense RNA complementary to three overlapping transcripts. Gene 60, 29–37 (1987).

    Article  CAS  PubMed  Google Scholar 

  90. Sremac, M. & Stuart, E. S. Recombinant gas vesicles from Halobacterium sp. displaying SIV peptides demonstrate biotechnology potential as a pathogen peptide delivery vehicle. BMC Biotechnol. 8, 9 (2008).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  91. Sremac, M. & Stuart, E. S. SIVsm Tat, Rev, and Nef1: functional characteristics of r-GV internalization on isotypes, cytokines, and intracellular degradation. BMC Biotechnol. 10, 54 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  92. Stuart, E. S., Morshed, F. Sremac, M. & DasSarma, S. Antigen presentation using novel particulate organelles from halophilic archaea. J. Biotechnol. 88, 119–128 (2001).

    Article  CAS  PubMed  Google Scholar 

  93. Stuart, E. S., Morshed, F. Sremac, M. & DasSarma, S. Cassette-based presentation of SIV epitopes with recombinant gas vesicles from halophilic archaea. J. Biotechnol. 114, 225–237 (2004).

    Article  CAS  PubMed  Google Scholar 

  94. Sundararajan, A. & Ju, L. K. Evaluation of oxygen permeability of gas vesicles from cyanobacterium Anabaena flos-aquae. J. Biotechnol. 77, 151–156 (2000).

    Article  CAS  PubMed  Google Scholar 

  95. Sundararajan, A. & Ju, L. K. Use of cyanobacterial gas vesicles as oxygen carriers in cell culture. Cytotechnology 52, 139–149 (2006).

    Article  CAS  PubMed  Google Scholar 

  96. Walsby, A. E. Permeability of gas vesicles to perfluorocyclobutane. J. Gen. Microbiol. 128, 1679–1684 (1982).

    CAS  Google Scholar 

  97. Walsby, A. E., Revsbech, N. P. & Griffel, D. H. The gas permeability coefficient of the cyanobacterial gas vesicle wall. J. Gen. Microbiol. 138, 837–845 (1992).

    Article  CAS  Google Scholar 

  98. Pfeifer, F. & Blaseio, U. Insertion elements and deletion formation in a halophilic archaebacterium. J. Bacteriol. 171, 5135–5140 (1989).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. DasSarma, S. Identification and analysis of the gas vesicle gene cluster on an unstable plasmid of Halobacterium halobium. Experientia 49, 482–486 (1993).

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

Research in the F.P. laboratory is supported by grants from the German Research Foundation (DFG). The author thanks A. Walsby for helpful comments on the manuscript, and A. Kletzin for discussions, help with the comparison of gvp gene clusters and critical reading of the manuscript.

Author information

Authors and Affiliations

  1. Technische Universität Darmstadt, Fachbereich Biologie, Schnittspahnstrasse 10, Darmstadt, D-64287, Germany

    Felicitas Pfeifer

Authors
  1. Felicitas Pfeifer
    View author publications

    You can also search for this author in PubMed Google Scholar

Ethics declarations

Competing interests

The author declares no competing financial interests.

Related links

Related links

FURTHER INFORMATION

Felicitas Pfeifer's homepage

Glossary

Halophilic

Pertaining to microorganisms: salt-loving, living at 2–5 M sodium chloride at neutral pH.

Biconical

Pertaining to a three-dimensional geometric structure: formed by merging two conical ends.

Anoxygenic photosynthetic

Pertaining to microorganisms: unable to form oxygen owing to the lack of photosystem II.

Heterotrophic

Pertaining to microorganisms: using organic carbon sources.

Pellicle

A thin layer of microorganisms at the air–liquid surface.

Anoxic

Without oxygen.

Haloalkaliphilic

Pertaining to microorganisms: high-salt and high-pH loving, living at 2–5 M salt and pH 9–11.

Hypersaline

With a salt concentration surpassing that of the ocean water (>4% weight per volume).

Brackish

With a salt concentration between that of fresh water and ocean water.

Sporulation

The process of endospore formation in microorganisms.

Mini-chromosome

A piece of circular DNA that occurs in addition to the main chromosome and contains essential genes (such as tRNA genes) which are required to survive.

Insertion element

A transposable DNA sequence (0.5–2 kb) that is able to replicate and insert into another position in the chromosome.

Quorum sensing

A chemical communication system that uses small signal molecules to measure cell densities and coordinate the regulation of gene expression in certain bacteria and archaea.

Mycelium

The thread-like cells of Streptomyces spp.; these cells resemble the vegetative hyphae of fungi.

Antigen presentation system

A system of proteins that are engineered to display antigens to the immune system of mice or other animals.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Pfeifer, F. Distribution, formation and regulation of gas vesicles. Nat Rev Microbiol 10, 705–715 (2012). https://doi.org/10.1038/nrmicro2834

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrmicro2834

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing