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Microbial communities and processes within a hypersaline gypsum crust in a saltern evaporation pond (Eilat, Israel)

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Abstract

Gypsum crusts containing multicolored, stratified microbial communities develop in the evaporation ponds of a commercial saltern in Eilat, Israel at salt concentrations between 190 and 240 g l−1. The upper 0.5–2 cm of the crust is densely populated by orange-brown unicellular cyanobacteria. Below, a layer of green-colored filamentous cyanobacteria is found. Underneath, a bright purple layer of anoxygenic phototrophs is present, below which a reduced black layer is found. We have investigated the biological properties of this crust using a wide variety of techniques, and we here review the results of these interdisciplinary studies. The tests performed included microscopic examination of the biota, phylogenetic analyses based on 16S rRNA gene clone libraries and denaturing gradient gel electrophoresis, fatty acid analysis, light intensity and light quality measurements, microelectrode studies of oxygen profiles and oxygen evolution, determination of sulfate reduction using radioisotope methods, and measurement of methane evolution. The stable vertical stratification in the system enabled separate analyses of the different layers with a high spatial resolution. It was therefore possible to combine the different approaches and obtain information on the activities of the different types of oxygenic and anoxygenic phototrophs, dissimilatory sulfate reducers and methanogens in the different layers, as well as phylogenetic information on the nature of the microorganisms responsible for these processes. The gypsum crust thus becomes a paradigm for the study of a wide variety of microbial processes and their interrelationships in the presence of high salt concentrations.

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References

  • Airs, R. L. & B. J. Keely, 2003. A high resolution study of the chlorophyll and bacteriochlorophyll pigment distributions in a calcite/gypsum microbial mat. Organic Geochemistry 34: 539–551.

    Article  CAS  Google Scholar 

  • Antón, J., A. Oren, S. Benlloch, F. Rodríguez-Valera, R. Amann & R. Rosselló-Mora, 2002. Salinibacter ruber gen. nov., sp. nov., a novel extremely halophilic member of the Bacteria from saltern crystallizer ponds. International Journal of Systematic and Evolutionary Microbiology 52: 485–491.

    PubMed  Google Scholar 

  • Bolhuis, H., E. M. te Poele & F. Rodríguez-Valera, 2004. Isolation and cultivation of Walsby’s square archaeon. Environmental Microbiology 6: 1287–1291.

    Article  PubMed  Google Scholar 

  • Boone, D. R., 2001. Genus IV: Methanohalophilus. In Boone, D. R. & R. W. Castenholz (eds), Bergey’s Manual of Systematic Bacteriology, 2nd Edition. Volume 1. The Archaea and the Deeply Branching and Phototrophic Bacteria. Springer, New York: 281–283.

    Google Scholar 

  • Brandt, K. K. & K. Ingvorsen, 1997. Desulfobacter halotolerans sp. nov., a halotolerant acetate-oxidizing sulfate-reducing bacterium isolated from sediments of Great Salt Lake, Utah. Systematic and Applied Microbiology 20: 366–373.

    Google Scholar 

  • Brandt, K. K., F. Vester, A. N. Jensen & K. Ingvorsen, 2001. Sulfate reduction dynamics and enumeration of sulfate-reducing bacteria in hypersaline sediments of the Great Salt Lake. Microbial Ecology 41: 1–11.

    PubMed  CAS  Google Scholar 

  • Burns, D. G., H. M. Camakaris, P. H. Janssen & M. L. Dyall-Smith, 2004. Cultivation of Walsby’s square haloarchaeon. FEMS Microbiology Letters 238: 469–473.

    PubMed  CAS  Google Scholar 

  • Burns, D. G., P. H. Janssen, T. Itoh, M. Kamekura, Z. Li, G. Jensen, F. Rodríguez-Valera, H. Bolhuis & M. L. Dyall-Smith, 2007. Haloquadratum walsbyi gen nov., sp. nov., the square haloarchaeon of Walsby, isolated from saltern crystallizers in Australia and Spain. International Journal of Systematic and Evolutionary Microbiology 57: 387–392.

    Article  PubMed  CAS  Google Scholar 

  • Canfield, D. E., K. B. Sørensen & A. Oren, 2004. Biogeochemistry of a gypsum-encrusted microbial ecosystem. Geobiology 2: 133–150.

    Article  CAS  Google Scholar 

  • Caumette, P., 1993. Ecology and physiology of phototrophic bacteria and sulfate-reducing bacteria in marine salterns. Experientia 49: 473–486.

    Article  CAS  Google Scholar 

  • Caumette, P., R. Baulaigue & R. Matheron, 1988. Characterization of Chromatium salexigens sp. nov., a halophilic Chromatiaceae isolated from Mediterranean salterns. Systematic and Applied Microbiology 10: 284–292.

    Google Scholar 

  • Caumette, P., R. Matheron, N. Raymond & J.-C. Relexans, 1994. Microbial mats in the hypersaline ponds of Mediterranean salterns (Salins-de-Giraud, France). FEMS Microbiology Ecology 13: 273–286.

    Article  CAS  Google Scholar 

  • Cohen, Y., E. Padan & M. Shilo, 1975. Facultative anoxygenic photosynthesis in the cyanobacterium Oscillatoria limnetica. Journal of Bacteriology 123: 855–861.

    PubMed  CAS  Google Scholar 

  • Conrad, R., P. Frenzel & Y. Cohen, 1995. Methane emission from hypersaline microbial mats: lack of aerobic methane oxidation activity. FEMS Microbiology Ecology 16: 297–306.

    Article  CAS  Google Scholar 

  • Cornée, A., 1984. Étude préliminaire des bactéries des saumures et des sédiments des salins de Santa Pola (Espagne). Comparison avec les marais salants de Salin-de-Giraud (Sud de la France). Revista d’Investigacions Geologiques 38/39: 109–122.

    Google Scholar 

  • Elevi Bardavid, R., D. Ionescu, A. Oren, F. A. Rainey, B. J. Hollen, D. R. Bagaley, A. M. Small & C. M. McKay, 2007. Selective enrichment, isolation and molecular detection of Salinibacter and related extremely halophilic Bacteria from hypersaline environments. Hydrobiologia 576: 3–13.

    Article  CAS  Google Scholar 

  • Fossing, H. & B. B. Jørgensen, 1989. Measurement of bacterial sulfate reduction in sediments. Evaluation of a single-step chromium reduction method. Biogeochemistry 8: 205–222.

    Article  CAS  Google Scholar 

  • Garcia-Pichel, F., U. Nübel & G. Muyzer, 1998. The phylogeny of unicellular, extremely halotolerant cyanobacteria. Archives of Microbiology 169: 469–482.

    Article  PubMed  CAS  Google Scholar 

  • Grimalt, J. O., R. de Wit, P. Teixidor & J. Albaiges, 1992. Lipid biogeochemistry of Phormidium and Microcoleus mats. Organic Geochemistry 19: 509–530.

    Article  CAS  Google Scholar 

  • Ionescu, D., A. Lipski, K. Altendorf & A. Oren, 2007. Characterization of the endoevaporitic microbial communities in a hypersaline gypsum crust by fatty acid analysis. Hydrobiologia 576: 15–26.

    Article  CAS  Google Scholar 

  • Jahnke, L. L., B. Lee, M. J. Sweeney & H. P. Klein, 1989. Anaerobic biosynthesis of unsaturated fatty acids in the cyanobacterium, Oscillatoria limnetica. Archives of Microbiology 152: 215–217.

    Article  PubMed  CAS  Google Scholar 

  • Javor, B., 1989. Hypersaline Environments. Microbiology and Biogeochemistry. Springer-Verlag, Berlin.

    Google Scholar 

  • Jonkers, H. M., R. Ludwig, R. de Wit, O. Pringault, G. Muyzer, H. Niemann, N. Finke & D. de Beer, 2003. Structural and functional analysis of a microbial mat ecosystem from a unique permanent hypersaline inland lake: ‘La Salada de Chiprana’ (NE Spain). FEMS Microbiology Ecology 44: 175–189.

    Article  CAS  PubMed  Google Scholar 

  • Kedar, L., Y. Kashman & A. Oren, 2002. Mycosporine-2-glycine is the major mycosporine-like amino acid in a unicellular cyanobacterium (Euhalothece sp.) isolated from a gypsum crust in a hypersaline saltern pond. FEMS Microbiology Letters 208: 233–237.

    Article  PubMed  CAS  Google Scholar 

  • Klappenbach, J. A. & B. K. Pierson, 2004. Phylogenetic and physiological characterization of a filamentous anoxygenic photoautotrophic bacterium ‘Candidatus Chlorothrix halophila’ gen. nov., sp. nov., recovered from hypersaline microbial mats. Archives of Microbiology 181: 17–25.

    Article  PubMed  CAS  Google Scholar 

  • Lassen, C., H. Plough & B. B. Jørgensen, 1992. A fibre-optic scalar irradiance microsensor: application for spectral light measurements in sediments. FEMS Microbiology Ecology 86: 247–254.

    Article  Google Scholar 

  • Margheri, M. C., M. R. Tredici, L. Barsanti & W. Balloni, 1987. The photosynthetic community of the Trapani saline lagoons: an alternative option for the exploitation of an extreme environment. Annali di Microbiologia ed Enzimologia 37: 203–215.

    CAS  Google Scholar 

  • Mouné, S., P. Caumette, R. Matheron & J. Willison, 2003. Molecular sequence analysis of prokaryotic diversity in the anoxic sediments underlying cyanobacterial mats of two hypersaline ponds in Mediterranean salterns. FEMS Microbiology Ecology 44: 117–130.

    Article  CAS  PubMed  Google Scholar 

  • Nübel, U., F. Garcia-Pichel & G. Muyzer, 2000a. The halotolerance and phylogeny of cyanobacteria with tightly coiled trichomes (Spirulina Turpin) and the description of Halospirulina tapeticola gen. nov., sp. nov. International Journal of Systematic and Evolutionary Microbiology 50: 1265–1277.

    PubMed  Google Scholar 

  • Nübel, U., F. Garcia-Pichel, E. Clavero & G. Muyzer, 2000b. Matching molecular diversity and ecophysiology of benthic cyanobacteria and diatoms in communities along a salinity gradient. Environmental Microbiology 2: 217–226.

    Article  PubMed  Google Scholar 

  • Nübel, U., M. M. Bateson, M. T. Madigan, M. Kühl & D. M. Ward, 2001. Diversity and distribution in hypersaline microbial mats of bacteria related to Chloroflexus spp. Applied and Environmental Microbiology 67: 4365–4371.

    Article  PubMed  Google Scholar 

  • Ollivier, B., M.-L. Fardeau, J.-L. Cayol, M. Magot, B. K. C. Patel, G. Prensier & J.-L. Garcia, 1998. Methanocalculus halotolerans gen. nov., sp. nov., isolated from an oil-producing well. International Journal of Systematic Bacteriology 48: 821–828.

    Article  PubMed  Google Scholar 

  • Oren, A., 1997. Mycosporine-like amino acids as osmotic solutes in a community of halophilic cyanobacteria. Geomicrobiology Journal 14: 233–242.

    Article  Google Scholar 

  • Oren, A., 1999. Bioenergetic aspects of halophilism. Microbiology and Molecular Biology Reviews 63: 334–348.

    PubMed  CAS  Google Scholar 

  • Oren, A., 2000. Salts and brines. In Whitton, B. A. & M. Potts (eds), Ecology of Cyanobacteria: Their Diversity in Time and Space. Kluwer, Dordrecht: 281–306.

    Google Scholar 

  • Oren, A., 2002. Halophilic Microorganisms and their Environments. Kluwer, Dordrecht.

    Google Scholar 

  • Oren, A., 2005. Microscopic examination of microbial communities along a salinity gradient in saltern evaporation ponds: a ‘halophilic safari’. In Gunde-Cimerman, N., A. Oren & A. Plemenitaš (eds), Adaptation to Life at High Salt Concentrations in Archaea, Bacteria. and Eukarya. Springer, Dordrecht: 41–57.

    Chapter  Google Scholar 

  • Oren, A., 2006. Life at high salt concentrations. In Dworkin, M., S. Falkow, E. Rosenberg, K.-H. Schleifer & E. Stackebrandt (eds), The Prokaryotes: A handbook on the Biology of Bacteria: Ecophysiology and Biochemistry, Vol. 2. Springer, New York: 263–282.

    Google Scholar 

  • Oren, A., M. Kühl & U. Karsten, 1995. An endevaporitic microbial mat within a gypsum crust: zonation of phototrophs, photopigments, and light penetration. Marine Ecology Progress Series 128: 151–159.

    Article  Google Scholar 

  • Oren, A., D. Ionescu, A. Lipski & K. Altendorf, 2005. Fatty acid analysis of a layered community of cyanobacteria developing in a hypersaline gypsum crust. Algological Studies 117: 1–9.

    Article  Google Scholar 

  • Pierson, B. K., D. Valdez, M. Larsen, E. Morgan & E. E. Mack, 1994. Chloroflexus-like organisms from marine and hypersaline environments: distribution and diversity. Photosynthesis Research 41: 35–52.

    Article  CAS  Google Scholar 

  • Revsbech, N. P., 1989. An oxygen microsensor with a guard cathode. Limnology and Oceanography 34: 474–478.

    CAS  Google Scholar 

  • Revsbech, N. P., B. B. Jørgensen & O. Brix, 1981. Primary production of microalgae in sediments measured by oxygen microprofile, H14CO3 fixation, and oxygen exchange methods. Limnology and Oceanography 26: 717–730.

    CAS  Google Scholar 

  • Revsbech, N. P., B. B. Jørgensen & T. H. Blackburn, 1983. Microelectrode studies of the photosynthesis and O2, H2S, and pH profiles of a microbial mat. Limnology and Oceanography 28: 1062–1074.

    Google Scholar 

  • Rothschild, L. J., L. J. Giver, M. R. White & R. L. Mancinelli, 1994. Metabolic activity of microorganisms in evaporites. Journal of Phycology 30: 431–438.

    Article  PubMed  CAS  Google Scholar 

  • Sørensen, K. B., D. E. Canfield & A. Oren, 2004. Salt responses of benthic microbial communities in a solar saltern (Eilat, Israel). Applied and Environmental Microbiology 70: 1608–1616.

    Article  PubMed  CAS  Google Scholar 

  • Sørensen, K. B., D. E. Canfield, A. P. Teske & A. Oren, 2005. Community composition of a hypersaline endoevaporitic microbial mat (Israel). Applied and Environmental Microbiology 71: 7352–7365.

    Article  PubMed  CAS  Google Scholar 

  • Spear, J. R., R. E. Ley, A. B. Berger & N. E. Pace, 2003. Complexity in natural microbial ecosystems: the Guerrero Negro experience. Biological Bulletin 204: 168–173.

    Article  PubMed  CAS  Google Scholar 

  • Teske, A., K.-U. Hinrichs, V. Edgcomb, A. de Vera Gomez, D. Kysela, S. P. Sylva, M. L. Sogin & H. W. Jannasch, 2002. Microbial diversity in hydrothermal sediments in the Guaymas Basin: evidence for anaerobic methanotrophic communities. Applied and Environmental Microbiology 68: 1994–2007.

    Article  PubMed  CAS  Google Scholar 

  • van der Wielen, P. W. J. J., H. Bolhuis, S. Borin, D. Daffonchio, C. Corselli, L. Giuliano, G. D’Auria, G. J. de Lange, A. Huebner, S. P. Varnavas, J. Thomson, C. Tamburini, D. Marty, T. J. McGenity, K. N. Timmis & BioDeep Scientific Party, 2005. The enigma of prokaryotic life in deep hypersaline anoxic basins. Science 307: 121–123.

    Article  PubMed  CAS  Google Scholar 

  • Volkmann, M., A. A. Gorbushina, L. Kedar & A. Oren, 2006. The structure of euhalothece-362, a novel red-shifted mycosporine-like amino acid, from a halophilic cyanobacterium (Euhalothece sp.). FEMS Microbiology Letters 258: 50–54.

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

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 and the Moshe Shilo Minerva Center for Marine Biogeochemistry for logistic support. Different aspects of this research project were financially supported by the Danish Basic Research Foundation (Grundforskningsfonden), the Danish Research Agency (Statens Naturvidenskablige Forskningsråd), the Israel Science Foundation founded by the Israel Academy of Sciences and Humanities, the NASA Astrobiology Institutes “Subsurface Biospheres” and “Environmental Genomics”, and the State of Lower-Saxony and the Volkswagen Foundation, Hannover, Germany.

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Correspondence to Aharon Oren.

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Guest Editors: J. John & B. Timms

Salt Lake Research: Biodiversity and Conservation—Selected papers from the 9th Conference of the International Society for Salt Lake Research

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Oren, A., Sørensen, K.B., Canfield, D.E. et al. Microbial communities and processes within a hypersaline gypsum crust in a saltern evaporation pond (Eilat, Israel). Hydrobiologia 626, 15–26 (2009). https://doi.org/10.1007/s10750-009-9734-8

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