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Glycine betaine is the main organic osmotic solute in a stratified microbial community in a hypersaline evaporitic gypsum crust

Extremophiles volume 17, pages 445–451 (2013)Cite this article

Abstract

We have examined the organic osmotic solutes content within the stratified microbial communities in an evaporitic gypsum crust found in an evaporation pond (~194 g/l total dissolved salts) of the salterns of the Israel Salt Company, Eilat. We extracted intracellular solutes from the upper three pigmented layers of the crust: a yellow-orange layer dominated by unicellular cyanobacteria, a green layer with filamentous cyanobacteria, and a layer colored red-purple by purple sulfur bacteria; dense communities of heterotrophic bacteria were present in all layers. The solutes were analyzed by Raman spectroscopy, 1H and 13C nuclear magnetic resonance, and HPLC. All layers contained glycine betaine as the only detectable osmotic solute; ectoine and other solutes known to be produced by many halophilic and halotolerant prokaryotes were not found. In this first attempt to assess the osmotic solute content within complex natural communities of halophilic microorganisms, the predominant role of glycine betaine as an osmolyte was established. Most heterotrophic bacteria cannot produce glycine betaine but preferentially use it when it is supplied. Presence of glycine betaine produced by the photoautotrophic members of the community, therefore, may relieve the heterotrophs from the need to synthesize other compounds at a high-energy cost.

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References

  • Borowitzka LJ, Demmerle S, Mackay MA, Norton RS (1980) Carbon-13 nuclear magnetic resonance study of osmoregulation in a blue-green alga. Science 210:650–651

    PubMed  Article  CAS  Google Scholar 

  • Brown AD (1990) Microbial water stress physiology. Principles and perspectives. Wiley, Chichester

    Google Scholar 

  • Canfield DE, Sørensen KB, Oren A (2004) Biogeochemistry of a gypsum-encrusted microbial ecosystem. Geobiology 2:133–150

    Article  CAS  Google Scholar 

  • Galinski EA (1993) Compatible solutes of halophilic eubacteria-molecular principles, water–solute interaction, stress protection. Experientia 49:487–496

    Article  CAS  Google Scholar 

  • Galinski EA (1995) Osmoadaptation in bacteria. Adv Microb Physiol 37:273–328

    Article  CAS  Google Scholar 

  • Galinski EA, Oren A (1991) Isolation and structure determination of a novel compatible solute from the moderately halophilic purple sulfur bacterium Ectothiorhodospira marismortui. Eur J Biochem 198:593–598

    PubMed  Article  CAS  Google Scholar 

  • Galinski EA, Trüper HG (1982) Betaine, a compatible solute in the extremely halophilic phototrophic bacterium Ectothiorhodospira halochloris. FEMS Microbiol Lett 13:357–360

    Article  CAS  Google Scholar 

  • Galinski EA, Pfeiffer H-P, Trüper HG (1985) 1,4,5,6-Tetrahydro-2-methyl-4-pyrimidinecarboxylic acid. A novel cyclic amino acid from halophilic phototrophic bacteria of the genus Ectothiorhodospira. Eur J Biochem 149:135–139

    PubMed  Article  CAS  Google Scholar 

  • Hagemann M (2011) Molecular biology of cyanobacterial salt acclimation. FEMS Microbiol Rev 35:87–123

    PubMed  Article  CAS  Google Scholar 

  • Imhoff JF, Rodriguez-Valera F (1984) Betaine is the main compatible solute of halophilic eubacteria. J Bacteriol 160:478–479

    PubMed  CAS  Google Scholar 

  • Jehlička J, Oren A, Edwards HGM (2012a) Raman spectra of compatible osmotic solutes of halophiles. J Raman Spectrosc 43:1134–1140

    Article  Google Scholar 

  • Jehlička J, Oren A, Vítek P (2012b) Use of Raman spectroscopy for identification of compatible solutes in halophilic bacteria. Extremophiles 16:507–514

    PubMed  Article  Google Scholar 

  • Kedar L, Kashman Y, Oren A (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 Microbiol Lett 208:233–237

    PubMed  Article  CAS  Google Scholar 

  • Mackay MA, Norton RS, Borowitzka LJ (1984) Organic osmoregulatory solutes in cyanobacteria. J Gen Microbiol 130:2177–2191

    CAS  Google Scholar 

  • Oren A (1997) Mycosporine-like amino acids as osmotic solutes in a community of halophilic cyanobacteria. Geomicrobiol J 14:233–242

    Article  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, Oren A, Plemenitaš A (eds) Adaptation to life at high salt concentrations in Archaea, Bacteria, and Eukarya. Springer, Dordrecht, pp 41–57

    Chapter  Google Scholar 

  • Oren A (2006) Life at high salt concentrations. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds) The Prokaryotes. A handbook on the biology of bacteria: ecophysiology and biochemistry, vol 2. Springer, New York, pp 263–282

    Google Scholar 

  • Oren A (2012) Salts and brines. In: Whitton BA (ed) Ecology of cyanobacteria II. Their diversity in time and space, 2nd edn. Springer, Dordrecht, pp 401–426

    Chapter  Google Scholar 

  • Oren A, Fischel U, Aizenshtat Z, Krein EB, Reed RH (1994) Osmotic adaptation of microbial communities in hypersaline microbial mats. In: Stal LJ, Caumette P (eds) Microbial mats. Structure, development and environmental significance. Springer, Berlin, pp 125–130

    Chapter  Google Scholar 

  • Oren A, Kühl M, Karsten U (1995) An endoevaporitic microbial mat within a gypsum crust: zonation of phototrophs, photopigments, and light penetration. Mar Ecol Prog Ser 128:151–159

    Article  Google Scholar 

  • Oren A, Ionescu D, Lipski A, Altendorf K (2005) Fatty acid analysis of a layered community of cyanobacteria developing in a hypersaline gypsum crust. Algol Stud 117:339–347

    Article  Google Scholar 

  • Oren A, Sørensen KB, Canfield DE, Teske AP, Ionescu D, Lipski A, Altendorf K (2009) Microbial communities and processes within a hypersaline gypsum crust in a saltern evaporation pond (Eilat, Israel). Hydrobiologia 626:15–26

    Article  CAS  Google Scholar 

  • Prášil O, Bina D, Medová H, Řeháková K, Zapomělová E, Veselá J, Oren A (2009) Emission spectroscopy and kinetic fluorimetry studies of the phototrophic microbial communities along the salinity gradient in the solar saltern evaporation ponds of Eilat, Israel. Aquat Microb Ecol 56:285–296

    Article  Google Scholar 

  • Reed RH, Chudek JA, Foster R, Stewart WDP (1984) Osmotic adjustment in cyanobacteria from hypersaline environments. Arch Microbiol 138:333–337

    Article  CAS  Google Scholar 

  • Řeháková K, Zapomělová E, Prášil O, Veselá J, Medová H, Oren A (2009) Composition changes of phototrophic microbial communities along the salinity gradient in the solar saltern evaporation ponds of Eilat, Israel. Hydrobiologia 636:77–88

    Article  Google Scholar 

  • Roberts MF (2005) Organic compatible solutes of halotolerant and halophilic microorganisms. Saline Syst 1:5

    PubMed  Article  Google Scholar 

  • Roberts MF (2006) Characterization of organic compatible solutes of halotolerant and halophilic microorganisms. In: Rainey FA, Oren A (eds) Extremophiles—Methods in microbiology, vol 35. Elsevier/Academic Press, Amsterdam, pp 615–647

    Chapter  Google Scholar 

  • Severin J, Wohlfarth A, Galinski EA (1992) The predominant role of recently discovered tetrahydropyrimidines for the osmoadaptation of halophilic eubacteria. J Gen Microbiol 138:1629–1638

    CAS  Google Scholar 

  • Sørensen KB, Canfield DE, Oren A (2004) Salinity responses of benthic microbial communities in a solar saltern (Eilat, Israel). Appl Environ Microbiol 70:1608–1616

    PubMed  Article  Google Scholar 

  • Sørensen KB, Canfield DE, Teske AP, Oren A (2005) Community composition of a hypersaline endoevaporitic microbial mat. Appl Environ Microbiol 71:7352–7365

    PubMed  Article  Google Scholar 

  • Sørensen K, Řeháková K, Zapomělová E, Oren A (2009) Distribution of benthic phototrophs, sulfate reducers, and methanogens in two adjacent salt ponds in Eilat, Israel. Aquat Microb Ecol 56:275–284

    Article  Google Scholar 

  • Ventosa A, Nieto JJ, Oren A (1998) Biology of aerobic moderately halophilic bacteria. Microbiol Mol Biol Rev 62:504–544

    PubMed  CAS  Google Scholar 

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

    PubMed  Article  CAS  Google Scholar 

  • Welsh DT (2000) Ecological significance of compatible solute accumulation by micro-organisms: from single cells to global climate. FEMS Microbiol Rev 24:263–290

    PubMed  Article  CAS  Google Scholar 

  • Wohlfarth A, Severin J, Galinski EA (1990) The spectrum of compatible solutes in heterotrophic halophilic eubacteria of the family Halomonadaceae. J Gen Microbiol 136:705–712

    CAS  Google Scholar 

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Acknowledgments

We thank Lily Mana for her assistance during the experiments, 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. This study was supported by Grant No. 1103/10 from the Israel Science Foundation (to AO and ZA) and by Grant No. P210/10/0467 from the Grant Agency of the Czech Republic and institutional support MSM0021620855 from the Ministry of Education of the Czech Republic (to JJ).

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Affiliations

  1. Department of Plant and Environmental Sciences, The Alexander Silberman Institute of Life Sciences, The Hebrew University of Jerusalem, 91904, Jerusalem, Israel

    Aharon Oren & Rahel Elevi Bardavid

  2. The Institute of Chemistry and Casali Institute of Applied Chemistry, The Hebrew University of Jerusalem, 91904, Jerusalem, Israel

    Nesya Kandel & Zeev Aizenshtat

  3. Institute of Geochemistry, Mineralogy and Mineral Resources, Charles University, Prague, Czech Republic

    Jan Jehlička

Authors
  1. Aharon Oren
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  2. Rahel Elevi Bardavid
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  3. Nesya Kandel
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  4. Zeev Aizenshtat
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  5. Jan Jehlička
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Correspondence to Aharon Oren.

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Communicated by L. Huang.

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Oren, A., Elevi Bardavid, R., Kandel, N. et al. Glycine betaine is the main organic osmotic solute in a stratified microbial community in a hypersaline evaporitic gypsum crust. Extremophiles 17, 445–451 (2013). https://doi.org/10.1007/s00792-013-0522-z

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  • DOI: https://doi.org/10.1007/s00792-013-0522-z

Keywords

  • Compatible solutes
  • Raman spectroscopy
  • Gypsum
  • Hypersaline
  • Halophilic