Advertisement

Extremophiles

, Volume 12, Issue 1, pp 5–14 | Cite as

Interrelationships between Dunaliella and halophilic prokaryotes in saltern crystallizer ponds

  • Rahel Elevi Bardavid
  • Polina Khristo
  • Aharon OrenEmail author
Review

Abstract

Thanks to their often very high population densities and their simple community structure, saltern crystallizer ponds form ideal sites to study the behavior of halophilic microorganisms in their natural environment at saturating salt concentrations. The microbial community is dominated by square red halophilic Archaea, recently isolated and described as Haloquadratum walsbyi, extremely halophilic red rod-shaped Bacteria of the genus Salinibacter, and the unicellular green alga Dunaliella as the primary producer. We review here, the information available on the microbial community structure of the saltern crystallizer brines and the interrelationships between the main components of their biota. As Dunaliella produces massive amounts of glycerol to provide osmotic stabilization, glycerol is often postulated to be the most important source of organic carbon for the heterotrophic prokaryotes in hypersaline ecosystems. We assess here, the current evidence for the possible importance of glycerol and other carbon sources in the nutrition of the Archaea and the Bacteria, the relative contribution of halophilic Bacteria and Archaea to the heterotrophic activity in the brines, and other factors that determine the nature of the microbial communities that thrive in the salt-saturated brines of saltern crystallizer ponds.

Keywords

Hypersaline Salterns Dunaliella Haloquadratum Salinibacter 

Abbreviations

FISH

Fluorescent in situ hybridization

PHA

Poly-β-hydroxyalkanoate

Notes

Acknowledgments

Our work on the salterns in Eilat has been supported by the Israel Science Foundation (grant no. 504/03). We thank the Israel Salt Company in Eilat, Israel, for allowing access to the salterns, and the staff of the Interuniversity Institute for Marine Sciences of Eilat, for logistic support.

References

  1. Al Harbi N, Gilmour DJ (2006) A comparion of glycerol production and leakage by three strains of the unicellular green alga Dunaliella (Volvocales, Chlorophyceae). Poster and Abstract, The 6th International Congress on Extremophiles, BrestGoogle Scholar
  2. Antón J, Llobet Brossa E, Rodriguez-Valera F, Amann R (1999) Fluorescence in situ hybridization analysis of the prokaryotic community inhabiting crystallizer ponds. Environ Microbiol 1:517–523PubMedCrossRefGoogle Scholar
  3. Antón J, Rosselló-Mora R, Rodriguez-Valera F, Amann R (2000) Extremely halophilic Bacteria in crystallizer ponds from solar salterns. Appl Environ Microbiol 66:3052–3057PubMedCrossRefGoogle Scholar
  4. Antón J, Oren A, Benlloch S, Rodriguez-Valera F, Amann R, Rosselló-Mora R (2002) Salinibacter ruber gen. nov., sp. nov., a novel extreme halophilic member of the Bacteria from saltern crystallizer ponds. Int J Syst Evol Microbiol 52:485–491PubMedGoogle Scholar
  5. Benlloch S, Martínez-Murcia AJ, Rodriguez-Valera F (1995) Sequencing of bacterial and archaeal 16S rRNA genes directly amplified from a hypersaline environment. Syst Appl Microbiol 18:574–581Google Scholar
  6. Benlloch S, Acinas SG, López-López A, Luz SP, Rodriguez-Valera F (2001) Archaeal biodiversity in crystallizer ponds from a solar saltern: culture versus PCR. Microb Ecol 41:12–19PubMedGoogle Scholar
  7. Bolhuis H (2005) Walsby’s square archaeon. It’s hip to be square, but even more hip to be culturable. In: Gunde-Cimerman N, Oren A, Plemenitaš A (eds) Adaptation to life at high salt concentrations in Archaea, Bacteria, and Eukarya. Springer, Dordrecht, pp 185–199CrossRefGoogle Scholar
  8. Bolhuis H, te Poele EM, Rodriguez-Valera F (2004) Isolation and cultivation of Walsby’s square archaeon. Environ Microbiol 6:1287–1291PubMedCrossRefGoogle Scholar
  9. Bolhuis H, Palm P, Wende A, Farb M, Rampp M, Rodriguez-Valera F, Pfeiffer F, Oesterhelt D (2006) The genome of the square archaeon “Haloquadratum walsbyi”: life at the limits of water activity. BMC Genomics 7:169PubMedCrossRefGoogle Scholar
  10. Borowitzka LJ (1981) The microflora. Adaptation to life in extremely saline lakes. Hydrobiologia 81:33–46CrossRefGoogle Scholar
  11. Brown AD, Lilley RM, Marengo T (1982a) Osmoregulation in Dunaliella. Intracellular distribution of enzymes of glycerol metabolism. Z Naturforsch 37:1115–1123Google Scholar
  12. Brown FF, Sussman I, Avron M, Degani H (1982b) NMR studies of glycerol permeability in lipid vesicles, erythrocytes, and the alga Dunaliella. Biochim Biophys Acta 690:165–173CrossRefGoogle Scholar
  13. Burns DG, Camakaris HM, Janssen PH, Dyall-Smith ML (2004a) Cultivation of Walsby’s square haloarchaeon. FEMS Microbiol Lett 238:469–473Google Scholar
  14. Burns DG, Camakaris HM, Janssen PH, Dyall-Smith ML (2004b) Combined use of cultivation-dependent and cultivation-independent methods indicates that members of most haloarchaeal groups in an Australian crystallizer pond are cultivable. Appl Environ Microbiol 70:5258–5265CrossRefGoogle Scholar
  15. Burns DG, Janssen PH, Itoh T, Kamekura M, Li Z, Jensen G, Rodriguez-Valera FE, Bolhuis H, Dyall-Smith ML (2006) Haloquadratum walsbyi gen. nov., sp. nov., the square haloarchaeon of Walsby, isolated from saltern crystallizers in Australia and Spain. Int J Syst Evol Microbiol (in press)Google Scholar
  16. Burton RM (1957) The determination of glycerol and dihydroxyacetone. Meth Enzymol 3:246–249Google Scholar
  17. Cho BC (2005) Heterotrophic flagellates in hypersaline waters. In: Gunde-Cimerman N, Oren A, Plemenitaš A (eds) Adaptation to life at high salt concentrations in Archaea, Bacteria, and Eukarya. Springer, Dordrecht, pp 543–549Google Scholar
  18. Corcelli A, Lattanzio VMT, Mascolo G, Babudri F, Oren A, Kates M (2004) Novel sulfonolipid in the extremely halophilic bacterium Salinibacter ruber. Appl Environ Microbiol 70:6678–6685PubMedCrossRefGoogle Scholar
  19. Elevi Bardavid R, Ionescu D, Oren A, Rainey FA, Hollen BJ, Bagaley DR, Small AM, McKay CM (2006) Selective enrichment, isolation and molecular detection of Salinibacter and related extremely halophilic Bacteria from hypersaline environments. Hydrobiologia (in press)Google Scholar
  20. Fernandez-Castillo R, Rodriguez-Valera F, Gonzalez-Ramos J, Ruiz-Berraquero F (1986) Accumulation of poly-β-hydroxybutyrate) by halobacteria. Appl Environ Microbiol 51:214–216PubMedGoogle Scholar
  21. Fujii S, Hellebust JA (1992) Release of intracellular glycerol and pore formation in Dunaliella tertiolecta exposed to hypertonic stress. Can J Bot 70:1313–1318Google Scholar
  22. Gimmler H, Lotter G (1982) The intracellular distribution of enzymes of the glycerol cycle in the unicellular alga Dunaliella parva. Z Naturforsch 37:1107–1114Google Scholar
  23. Gimmler H, Hartung W (1988) Low permeability of the plasma membrane of Dunaliella for solutes. J Plant Physiol 133:165–172Google Scholar
  24. Guixa-Boixareu N, Caldéron-Paz JI, Heldal M, Bratbak G, Pedrós-Alió C (1996) Viral lysis and bacterivory as prokaryotic loss factors along a salinity gradient. Aquat Microb Ecol 11:213–227CrossRefGoogle Scholar
  25. Guven K, Mutlu MB, Martinez-Garcia M, Santos F, Antón J (2006) Microbial populations of Camalti saltern in Turkey. Poster and Abstract, 11th International Symposium on Microbial Ecology, ViennaGoogle Scholar
  26. Hart BC, Gilmour DJ (1991) A mutant of Dunaliella parva CCAP 19/9 leaking large amounts of glycerol into the medium. J Appl Phycol 3:367–372Google Scholar
  27. Javor B (1989) Hypersaline environments. Microbiology and biogeochemistry. Springer, Berlin Heidelberg New YorkGoogle Scholar
  28. Kessel M, Cohen Y (1982) Ultrastructure of square bacteria from a brine pool in southern Sinai. J Bacteriol 150:851–860PubMedGoogle Scholar
  29. Kis-Papo T, Oren A (2000) Halocins: are they important in the competition between different types of halobacteria in saltern ponds? Extremophiles 4:35–41PubMedGoogle Scholar
  30. Legault BA, Lopez-Lopez A, Alba-Casado JC, Doolittle WF, Bolhuis H, Rodriguez-Valera F, Papke RT (2006) Environmental genomics of “Haloquadratum walsbyi” in a saltern crystallizer indicates a large pool of accessory genes in an otherwise coherent species. BMC Genomics 7:171PubMedCrossRefGoogle Scholar
  31. Lillo JAG, Rodriguez-Valera F (1990) Effects of culture conditions on poly-β-hydroxybutyric acid) production by Haloferax mediterranei. Appl Environ Microbiol 56:2517–2521PubMedGoogle Scholar
  32. Lutnæs BF, Oren A, Liaaen-Jensen S (2002) New C40-carotenoid acyl glycoside as principal carotenoid of Salinibacter ruber, an extremely halophilic eubacterium. J Nat Prod 65:1340–1343PubMedCrossRefGoogle Scholar
  33. Mongodin EF, Nelson KE, Daugherty S, DeBoy RT, Wister J, Khouri H, Weidman J, Walsh DA, Papke RT, Sanchez Perez G, Sharma AK, Nesbø CL, MacLeod D, Bapteste E, Doolittle WF, Charlebois RL, Legault B, Rodriguez-Valera F (2005) The genome of Salinibacter ruber: convergence and gene exchange among hyperhalophilic bacteria and archaea. Proc Natl Acad Sci USA 102:18147–18152PubMedCrossRefGoogle Scholar
  34. O’Connor EM, Shand RF (2002) Halocins and sulfolobicins: the emerging stody of archaeal protein and peptide antibiotics. J Ind Microbiol Biotechnol 28:23–31PubMedCrossRefGoogle Scholar
  35. Oren A (1983) Halobacterium sodomense sp. nov., a Dead Sea halobacterium with extremely high magnesium requirement and tolerance. Int J Syst Bacteriol 33:381–386Google Scholar
  36. Oren A (1990a) Estimation of the contribution of halobacteria to the bacterial biomass and activity in a solar saltern by the use of bile salts. FEMS Microbiol Ecol 73:41–48CrossRefGoogle Scholar
  37. Oren A (1990b) The use of protein synthesis inhibitors in the estimation of the contribution of halophilic archaebacteria to bacterial activity in hypersaline environments. FEMS Microbiol Ecol 73:187–192CrossRefGoogle Scholar
  38. Oren A (1990c) Thymidine incorporation in saltern ponds of different salinities: estimation of in situ growth rates of halophilic archaeobacteria and eubacteria. Microb Ecol 19:43–51CrossRefGoogle Scholar
  39. Oren A (1991) Estimation of the contribution of archaebacteria and eubacteria to the bacterial biomass and activity in hypersaline ecosystems: novel approaches. In: Rodriguez-Valera F (ed) General and applied aspects of halophilic bacteria. Plenum Publishing Company, New York, pp 25–31Google Scholar
  40. Oren A (1993) Availability, uptake and turnover of glycerol in hypersaline environments. FEMS Microbiol Ecol 12:15–23CrossRefGoogle Scholar
  41. Oren A (1994) Characterization of the halophilic archaeal community in saltern crystallizer ponds by means of polar lipid analysis. Int J Salt Lake Res 3:15–29CrossRefGoogle Scholar
  42. Oren A (1995a) The role of glycerol in the nutrition of halophilic archaeal communities: a study of respiratory electron transport. FEMS Microbiol Ecol 16:281–290CrossRefGoogle Scholar
  43. Oren A (1995b) Uptake and turnover of acetate in hypersaline environments. FEMS Microbiol Ecol 18:75–84CrossRefGoogle Scholar
  44. Oren A (1999) The enigma of square and triangular halophilic Archaea. In: Seckbach J (ed) Enigmatic microorganisms and life in extreme environments. Kluwer, Dordrecht, pp 337–355Google Scholar
  45. Oren A (2002) Halophilic microorganisms and their environments. Kluwer, DordrechtGoogle Scholar
  46. Oren A, Dubinsky Z (1994) On the red coloration of saltern crystallizer ponds. II. Additional evidence for the contribution of halobacterial pigments. Int J Salt Lake Res 3:9–13CrossRefGoogle Scholar
  47. Oren A, Gurevich P (1994) Production of d-lactate, acetate, and pyruvate from glycerol in communities of halophilic archaea in the Dead Sea and in saltern crystallizer ponds. FEMS Microbiol Ecol 14:147–156Google Scholar
  48. Oren A, Litchfield CD (1999) A procedure for the enrichment and isolation of Halobacterium species. FEMS Microbiol Lett 173:353–358CrossRefGoogle Scholar
  49. Oren A, Mana L (2002) Amino acid composition of bulk protein and salt relationships of selected enzymes of Salinibacter ruber, an extremely halophilic Bacterium. Extremophiles 6:217–223PubMedCrossRefGoogle Scholar
  50. Oren A, Rodriguez-Valera F (2001) The contribution of Salinibacter species to the red coloration of saltern crystallizer ponds. FEMS Microbiol Ecol 36:123–130PubMedGoogle Scholar
  51. Oren A, Stambler N, Dubinsky Z (1992) On the red coloration of saltern crystallizer ponds. Int J Salt Lake Res 1:77–89CrossRefGoogle Scholar
  52. Oren A, Gurevich P, Gemmell RT, Teske A (1995) Halobaculum gomorrense gen. nov., sp. nov., a novel extremely halophilic archaeon from the Dead Sea. Int J Syst Bacteriol 45:747–754PubMedGoogle Scholar
  53. Oren A, Duker S, Ritter S (1996) The polar lipid composition of Walsby’s square bacterium. FEMS Microbiol Lett 138:135–140CrossRefGoogle Scholar
  54. Oren A, Priel N, Shapira O, Siboni N (2005) Gas vesicles in Walsby’s square archaeon—do they provide flotation in saltern crystallizer ponds? Saline Syst 2:4CrossRefGoogle Scholar
  55. Øvreås L, Daae FL, Torsvik V, Rodriguez-Valera F (2003) Characterization of microbial diversity in hypersaline environments by melting profiles and reassociation kinetics in combination with terminal restriction length polymorphism (T-RFLP). Microb Ecol 46:291–301PubMedCrossRefGoogle Scholar
  56. Park JS, Kim HJ, Choi DH, Cho BC (2003) Active flagellates grazing on prokaryotes in high salinity waters of a solar saltern. Aquat Microb Ecol 33:173–179CrossRefGoogle Scholar
  57. Pedrós-Alió C, Calderón-Paz JI, MacLean MH, Medina G, Marasse C, Gasol JM, Guixa-Boixereu N (2000) The microbial food web along salinity gradients. FEMS Microbiol Ecol 32:143–155PubMedGoogle Scholar
  58. Rodriguez-Valera F, Ventosa A, Juez G, Imhoff JF (1985) Variation of environmental features and microbial populations with salt concentrations in a multi-pond saltern. Microb Ecol 11:107–115CrossRefGoogle Scholar
  59. Rodriguez-Valera F, Lillo JAG (1992) Halobacteria as producers of polyhydroxyalkanoates. FEMS Microbiol Rev 103:181–186CrossRefGoogle Scholar
  60. Rodriguez-Valera F, Acinas SG, Antón J (1999) Contribution of molecular techniques to the study of microbial diversity in hypersaline environments. In: Oren A (ed) Microbiology and biogeochemistry of hypersaline environments. CRC Press, Boca Raton, pp 27–38Google Scholar
  61. Rosselló-Mora R, Lee N, Antón J, Wagner M (2003) Substrate uptake in extremely halophilic microbial communities revealed by microautoradiography and fluorescence in situ hybridization. Extremophiles 7:409–413PubMedCrossRefGoogle Scholar
  62. Sher J, Elevi R, Mana L, Oren A (2004) Glycerol metabolism in the extremely halophilic bacterium Salinibacter ruber. FEMS Microbiol Lett 232:211–215PubMedCrossRefGoogle Scholar
  63. Stoeckenius W (1981) Walsby’s square bacterium: fine structure of an orthogonal prokaryote. J Bacteriol 148:352–360PubMedGoogle Scholar
  64. Tomlinson GA, Hochstein LI (1972) Studies on acid production during carbohydrate metabolism by extremely halophilic bacteria. Can J Microbiol 18:1973–1976PubMedCrossRefGoogle Scholar
  65. Walsby AE (1980) A square bacterium. Nature 283:69–71CrossRefGoogle Scholar
  66. Walsby AE (2005) Archaea with square cells. Trends Microbiol 13:193–195PubMedCrossRefGoogle Scholar
  67. Wegmann K, Ben-Amotz A, Avron M (1980) Effect of temperature on glycerol retention in the halotolerant algae Dunaliella and Asteromonas. Plant Physiol 66:1196–1197PubMedCrossRefGoogle Scholar

Copyright information

© Springer 2006

Authors and Affiliations

  • Rahel Elevi Bardavid
    • 1
  • Polina Khristo
    • 1
  • Aharon Oren
    • 1
    • 2
    Email author
  1. 1.The Institute of Life Sciences, and The Moshe Shilo Minerva Center for Marine BiogeochemistryThe Hebrew University of JerusalemJerusalemIsrael
  2. 2.Department of Plant and Environmental Sciences, The Institute of Life SciencesThe Hebrew University of JerusalemJerusalemIsrael

Personalised recommendations