A few extremely halophilic Archaea ( Halobacterium salinarum, Haloquadratum walsbyi, Haloferax mediterranei, Halorubrum vacuolatum, Halogeometricum borinquense, Haloplanus spp.) possess gas vesicles that bestow buoyancy on the cells. Gas vesicles are also produced by the anaerobic endospore-forming halophilic Bacteria Sporohalobacter lortetii and Orenia sivashensis. We have extensive information on the properties of gas vesicles in Hbt. salinarum and Hfx. mediterranei and the regulation of their formation. Different functions were suggested for gas vesicle synthesis: buoying cells towards oxygen-rich surface layers in hypersaline water bodies to prevent oxygen limitation, reaching higher light intensities for the light-driven proton pump bacteriorhodopsin, positioning the cells optimally for light absorption, light shielding, reducing the cytoplasmic volume leading to a higher surface-area-to-volume ratio (for the Archaea) and dispersal of endospores (for the anaerobic spore-forming Bacteria). Except for Hqr. walsbyi which abounds in saltern crystallizer brines, gas-vacuolate halophiles are not among the dominant life forms in hypersaline environments. There only has been little research on gas vesicles in natural communities of halophilic microorganisms, and the few existing studies failed to provide clear evidence for their possible function. This paper summarizes the current status of the different theories why gas vesicles may provide a selective advantage to some halophilic microorganisms.
References
[1]
Oren, A. Family Halobacteriaceae. In The Prokaryotes. A Handbook on the Biology of Bacteria: Ecophysiology and Biochemistry, 4th ed.; Rosenberg, E., DeLong, E.F., Thompson, F., Lory, S., Stackebrandt, E., Eds.; Springer: New York, NY, USA, 2013. in press.
[2]
Petter, H.F.M. On bacteria of salted fish. Proc. Kon. Akad. Wetensch. Ser. B？1931, 34, 1417–1423.
[3]
Petter, H.F.M. Over Roode en Andere Bacteri？n van Gezouten Visch (in Dutch). Ph.D. thesis, University of Utrecht, Utrecht, The Netherlands, 1932.
[4]
Sherwood, J.E.; Stagnitti, F.; Kokkinn, M.J.; Williams, W.D. A standard table for predicting equilibrium dissolved oxygen concentrations in salt lakes dominated by sodium chloride. Int. J. Salt Lake Res.？1992, 1, 1–6.
[5]
Hof, T. Investigations concerning bacterial life in strong brines. Rec. Trav. Bot. Neerl.？1935, 32, 92–173.
[6]
Houwink, A.L. Flagella, gas vacuoles and cell-wall structure in Halobacterium. halobium: An electron microscope study. J. Gen. Microbiol.？1956, 15, 146–150, doi:10.1099/00221287-15-1-146.
[7]
Larsen, H.; Omang, S.; Steensland, H. On the gas vacuoles of the halobacteria. Arch. Mikrobiol.？1967, 59, 197–203, doi:10.1007/BF00406332.
[8]
Pfeifer, F. Distribution, formation and regulation of gas vesicles. Nature Rev. Microbiol.？2012, 10, 705–715, doi:10.1038/nrmicro2834.
[9]
Walsby, A.E. Gas vesicles. Microbiol. Rev.？1994, 58, 94–144.
[10]
Walsby, A.E. The pressure relationships of gas vacuoles. Proc. R. Soc. London B？1971, 178, 301–326, doi:10.1098/rspb.1971.0067.
[11]
DasSarma, S.; Damerval, T.; Jones, J.G.; Tandeau de Marsac, N. A plasmid-encoded gas vesicle protein gene in a halophilic archaebacterium. Mol. Microbiol.？1987, 1, 365–370, doi:10.1111/j.1365-2958.1987.tb01943.x.
[12]
Pfeifer, F.; Weidinger, G.; Goebel, W. Genetic variability in Halobacterium halobium. J. Bacteriol.？1981, 145, 371–381.
[13]
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.？1991, 5, 1159–1174, doi:10.1111/j.1365-2958.1991.tb01889.x.
[14]
Englert, C.; Krüger, K.; Offner, S.; Pfeifer, F. Three different but related gene clusters encoding gas vesicles in halophilic archaea. J. Mol. Biol.？1992, 227, 586–592.
[15]
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.？2000, 182, 4328–4336, doi:10.1128/JB.182.15.4328-4336.2000.
[16]
Englert, C.; Wanner, G.; Pfeifer, F. Functional analysis of the gas vesicle gene cluster of the halophilic Archaea Haloferax mediterranei defines the vac-region boundary and suggests a regulatory role for the gvpD gene or its product. Mol. Microbiol.？1992, 6, 3543–3550, doi:10.1111/j.1365-2958.1992.tb01789.x.
[17]
Offner, S.; Ziese, U.; Wanner, G.; Typke, D.; Pfeifer, F. Structural characteristics of halobacterial gas vesicles. Microbiology UK？1998, 144, 1331–1342, doi:10.1099/00221287-144-5-1331.
[18]
Pfeifer, F.; Krüger, K.; R？der, R.; Mayr, A.; Ziesche, S.; Offner, S. Gas vesicle formation in halophilic Archaea. Arch. Microbiol.？1997, 167, 259–268, doi:10.1007/s002030050441.
[19]
Pfeifer, F.; Gregor, D.; Hofacker, A.; Plo？er, P.; Zimmermann, P. Regulation of gas vesicle formation in halophilic archaea. J. Mol. Microbiol. Biotechnol.？2002, 4, 175–181.
Montalvo-Rodríguez, R.; Vreeland, R.H.; Oren, A.; Kessel, M.; Betancourt, C.; López-Garriga, J. Halogeometricum borinquense gen. nov., sp. nov., a novel halophilic archaeon from Puerto Rico. Int. J. Syst. Bacteriol.？1998, 48, 1305–1312, doi:10.1099/00207713-48-4-1305.
[22]
Elevi Bardavid, R.; Mana, L.; Oren, A. Haloplanus natans gen. nov., sp. nov., an extremely halophilic gas-vacuolate archaeon from Dead Sea–Red Sea water mixtures in experimental mesocosms. Int. J. Syst. Evol. Microbiol.？2007, 57, 780–783, doi:10.1099/ijs.0.64648-0.
[23]
Cui, H.-L.; Gao, X.; Li, X.-Y.; Xu, X.-W.; Zhou, Y.-G.; Liu, H.-C.; Zhou, P.-J. Haloplanus vescus sp. nov., an extremely halophilic Archaea from a marine solar saltern, and emended description of the genus Haloplanus. Int. J. Syst. Evol. Microbiol.？2010, 60, 1824–1827.
[24]
Cui, H.-L.; Gao, X.; Yang, X.; Xu, X.-W. Haloplanus aerogenes sp. nov., an extremely halophilic archaeon from a marine solar saltern. Int. J. Syst. Evol. Microbiol.？2011, 61, 965–968, doi:10.1099/ijs.0.025023-0.
[25]
Burns, D.G.; Janssen, P.H.; Itoh, T.; Kamekura, M.; Li, Z.; Jensen, G.; Rodríguez-Valera, F.; Bolhuis, H.; Dyall-Smith, M.L. Haloquadratum walsbyi gen. nov., sp. nov., the square haloarchaeon of Walsby, isolated from saltern crystallizers in Australia and Spain. Int. J. Syst. Evol. Microbiol.？2007, 57, 387–392.
[26]
Mwatha, W.E.; Grant, W.D. Natronobacterium vacuolata, a haloalkaliphilic archaeon isolated from Lake Magadi, Kenya. Int. J. Syst. Bacteriol.？1993, 43, 401–404, doi:10.1099/00207713-43-3-401.
[27]
Gruber, C.; Legat, A.; Pfaffenhuemer, M.; Radax, C.; Weidler, G.; Busse, H.-J.; Stan-Lotter, H. Halobacterium noricense sp. nov., an archaeal isolate from a bore core of an alpine Permian salt deposit, classification of Halobacterium sp. NRC-1 as a strain of H. salinarum and emended description of H. salinarum. Extremophiles？2004, 8, 431–439, doi:10.1007/s00792-004-0403-6.
[28]
Walsby, A.E. A square bacterium. Nature？1980, 283, 69–71, doi:10.1038/283069a0.
[29]
Bolhuis, H. Walsby's square archaeon. It's hip to be square, but even more hip to be culturable. In Adaptation to Life at High Salt Concentrations in Archaea, Bacteria, and Eukarya; Gunde-Cimerman, N., Oren, A., Plemenita？, A., Eds.; Springer: Dordrecht, The Netherlands, 2005; pp. 187–199.
[30]
Bolhuis, H.; te Poele, E.M.; Rodríguez-Valera, F. Isolation and cultivation of Walsby's square archaeon. Environ. Microbiol.？2004, 6, 1287–1291, doi:10.1111/j.1462-2920.2004.00692.x.
Sublimi-Saponetti, M.; Bobba, F.; Salerno, G.; Scarfato, A.; Corcelli, A.; Cucolo, A.M. Morphological and structural aspects of the extremely halophilic archaeon Haloquadratum walsbyi. PLoS One？2011, doi:10.1371/journal.pone.0018653.
[33]
Bolhuis, H.; Palm, P.; Wende, A.; Falb, M.; Rampp, M.; Rodriguez-Valera, F.; Pfeiffer, F.; Oesterhelt, D. The genome of the square archaeon Haloquadratum walsbyi: life at the limits of water activity. BMC Genomics？2006, 7, 169, doi:10.1186/1471-2164-7-169.
[34]
Mayr, A.; Pfeifer, F. The characterization of the nv-gpvACNOFGH gene cluster involved in gas vesicle formation in Natronobacterium vacuolatum. Arch. Microbiol.？1997, 168, 24–32, doi:10.1007/s002030050465.
Beard, S.J.; Hayes, P.K.; Walsby, A.E. Growth competition between Halobacterium salinarum strain PHH1 and mutants affected in gas vesicle synthesis. Microbiology UK？1997, 143, 467–473, doi:10.1099/00221287-143-2-467.
[37]
Sundararajan, A.; Ju, L.-K. Use of cyanobacterial gas vesicles as oxygen carriers. Cytotechnology？2006, 52, 139–149.
[38]
Richard, T. Calculating the oxygen diffusion coefficient in water. Available online: http://compost.css.cornell.edu/oxygen/oxygen.diff.water.html (accessed on 27 November 2012).
[39]
Oren, A.; Trüper, H.G. Anaerobic growth of halophilic archaeobacteria by reduction of dimethylsulfoxide and trimethylamine N-oxide. FEMS Microbiol. Lett.？1990, 70, 33–36, doi:10.1111/j.1574-6968.1990.tb03772.x.
[40]
Hartmann, R.; Sickinger, H.-D.; Oesterhelt, D. Anaerobic growth of halobacteria. Proc. Natl. Acad. Sci. USA？1980, 77, 3821–3825, doi:10.1073/pnas.77.7.3821.
[41]
Oesterhelt, D. Anaerobic growth of halobacteria. Meth. Enzymol.？1982, 88, 417–420.
[42]
Oren, A.; Litchfield, C.D. A procedure for the enrichment and isolation of Halobacterium species. FEMS Microbiol. Lett.？1999, 173, 353–358, doi:10.1111/j.1574-6968.1999.tb13525.x.
[43]
Hechler, T.; Pfeifer, F. Anaerobiosis inhibits gas vesicle formation in halophilic Archaea. Mol. Microbiol.？2009, 71, 132–145, doi:10.1111/j.1365-2958.2008.06517.x.
[44]
DasSarma, P.; Zamora, R.C.; Müller, J.A.; DasSarma, S. Genome-wide responses of the model archaeon Halobacterium sp. strain NRC-1 to oxygen limitation. J. Bacteriol.？2012, 194, 5530–5537, doi:10.1128/JB.01153-12.
[45]
Müller, J.A.; DasSarma, S. Genomic analysis of anaerobic respiration in the archaeon Halobacterium sp. strain NRC-1: Dimethyl sulfoxide and trimethylamine N-oxide as terminal electron acceptors. J. Bacteriol.？2005, 187, 1659–1667, doi:10.1128/JB.187.5.1659-1667.2005.
[46]
Englert, C.; Horne, M.; Pfeifer, F. Expression of the major gas vesicle protein in the halophilic archaebacterium Haloferax mediterranei is modulated by salt. Mol. Gen. Genet.？1990, 222, 225–232, doi:10.1007/BF00633822.
[47]
R？der, R.; Pfeifer, F. Influence of salt on the transcription of the gas-vesicle gene of Haloferax mediterranei and identification of the endogeneous transcriptional activator. Microbiology UK？1996, 142, 1715–1723, doi:10.1099/13500872-142-7-1715.
[48]
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.？2012, 194, 269–279, doi:10.1007/s00203-011-0756-z.
[49]
Coker, J.; DasSarma, P.; Kumar, J.; Müller, J.; DasSarma, S. Transcriptional profiling of the model archaeon Halobacterium sp. NRC-1: Responses to changes in salinity and temperature. Saline Syst.？2007, 3, 6, doi:10.1186/1746-1448-3-6.
[50]
Bickel-Sandk？tter, S.; G？rtner, W.; Dane, M. Conversion of energy in halobacteria: ATP synthesis and phototaxis. Arch. Microbiol.？1996, 166, 1–11, doi:10.1007/s002030050349.
[51]
Lobasso, S.; Lopalco, P.; Vitale, R.; Sublimi Saponetti, M.; Capitanio, G.; Mangini, V.; Milano, F.; Trotta, M.; Corcelli, A. The light-activated proton pump BopI of the archaeon Haloquadratum walsbyi. Photochem. Photobiol.？2012, 88, 690–700, doi:10.1111/j.1751-1097.2012.01089.x.
[52]
Kessel, M.; Cohen, Y.; Walsby, A.E. Structure and physiology of square-shaped and other halophilic bacteria from the Gavish Sabkha. In Hypersaline Ecosystems. The Gavish Sabkha; Friedman, G.M., Krumbein, W.E., Eds.; Springer-Verlag: Berlin, Germany, 1985; pp. 267–287.
[53]
Simon, R.D. Interactions between light and gas vacuoles in Halobacterium salinarium strain 5: effect of ultraviolet light. Appl. Environ. Microbiol.？1980, 40, 984–987.
[54]
Oren, A. Halophilic Microorganisms and Their Environments; Kluwer Scientific Publishers: Dordrecht, The Netherlands, 2002.
[55]
Lopalco, P.; Lobasso, S.; Baronio, M.; Angelini, R.; Corcelli, A. Chapter 6. In Halophiles and Hypersaline Environments; Ventosa, A., Ed.; Springer-Verlag: Berlin, Germany, 2011; pp. 123–135.
[56]
Bodaker, I.; Sharon, I.; Suzuki, M.T.; Reingersch, R.; Shmoish, M.; Andreishcheva, E.; Sogin, M.L.; Rosenberg, M.; Belkin, S.; Oren, A.; Béjà, O. Comparative community genomics in the Dead Sea: an increasingly extreme environment. ISME J.？2010, 4, 399–407, doi:10.1038/ismej.2009.141.
[57]
Antón, J.; Llobet-Brossa, E.; Rodríguez-Valera, F.; Amann, R. Fluorescence in situ hybridization analysis of the prokaryotic community inhabiting crystallizer ponds. Environ. Microbiol.？1999, 1, 517–523, doi:10.1046/j.1462-2920.1999.00065.x.
[58]
Oren, A.; Duker, S.; Ritter, S. The polar lipid composition of Walsby's square bacterium. FEMS Microbiol. Lett.？1996, 138, 135–140, doi:10.1111/j.1574-6968.1996.tb08146.x.
[59]
Romanenko, V.I. Square microcolonies in the surface water film of the Saxkoye lake (in Russian). Mikrobiologiya (USSR)？1981, 50, 571–574.
[60]
Rodriguez-Valera, F.; Ventosa, A.; Juez, G.; Imhoff, J.F. Variation of environmental features and microbial populations with salt concentrations in a multi-pond saltern. Microb. Ecol.？1985, 11, 107–115, doi:10.1007/BF02010483.
[61]
Warkentin, M.; Schumann, R.; Oren, A. Community respiration studies in saltern crystallizer ponds. Aquat. Microb. Ecol.？2009, 56, 255–261, doi:10.3354/ame01298.
[62]
Stoeckenius, W. Walsby's square bacterium: Fine structure of an orthogonal prokaryote. J. Bacteriol.？1981, 148, 352–360.
[63]
Kessel, M.; Cohen, Y. Ultrastructure of square bacteria from a brine pool in southern Sinai. J. Bacteriol.？1982, 150, 851–860.
[64]
Parkes, K.; Walsby, A.E. Ultrastructure of a gas-vacuolate square bacterium. J. Gen. Microbiol.？1981, 126, 503–506.
[65]
Oren, A.; Priel, N.; Shapiro, O.; Siboni, N. Buoyancy studies in natural communities of square gas-vacuolate archaea in saltern crystallizer ponds. Saline Syst.？2006, 2, 4, doi:10.1186/1746-1448-2-4.
[66]
Denny, M.W. Air and Water: The Biology and Physics of Life's Media; Princeton University Press: Princeton, New Jersey, USA, 1993.
[67]
McNown, J.S.; Malaika, J. Effect of particle shape on settling velocity at low Reynolds numbers. Trans. Amer. Geophys. Union？1950, 31, 74–82, doi:10.1029/TR031i001p00074.
[68]
Purcell, E.M. Life at low Reynolds number. Amer. J. Phys.？1977, 45, 3–11, doi:10.1119/1.10903.
[69]
Coker, J.A.; DasSarma, P.; Kumar, J.; Müller, J.A.; DasSarma, S. Transcriptional profiling of the model archaeon Halobacterium sp. NRC-1: Responses to changes in salinity and temperature. Saline Syst.？2007, 3, 6, doi:10.1186/1746-1448-3-6.
[70]
Oren, A. Clostridium lortetii sp. nov., a halophilic obligately anaerobic bacterium producing endospores with attached gas vacuoles. Arch. Microbiol.？1983, 136, 42–48, doi:10.1007/BF00415608.
[71]
Oren, A.; Pohla, H.; Stackebrandt, E. Transfer of Clostridium lortetii to a new genus Sporohalobacter gen. nov. as Sporohalobacter lortetii comb. nov., and description of Sporohalobacter marismortui sp. nov. System. Appl. Microbiol.？1987, 9, 239–246, doi:10.1016/S0723-2020(87)80028-0.
[72]
Zhilina, T.N.; Tourova, T.P.; Kuznetsov, B.B.; Kostrikina, N.A.; Lysenko, A.M. Orenia sivashensis sp. nov., a new moderately halophilic anaerobic bacterium from lake Sivash lagoons. Microbiology (Russia)？1999, 68, 452–459.
[73]
Duda, V.I.; Makar'eva, E.D. Morphogenesis and function of gas caps on spores of anaerobic bacteria of the genus (in Russian). Mikrobiologiya？1978, 70, 689–694.
[74]
Larsen, H. The halobacteria's confusion to biology. Antonie van Leeuwenhoek？1973, 39, 383–396, doi:10.1007/BF02578880.
