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Dihydroxyacetone metabolism in Salinibacter ruber and in Haloquadratum walsbyi

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Abstract

The extremely halophilic bacterium Salinibacter ruber inhabits saltern crystallizer ponds worldwide, together with the square archaeon Haloquadratum walsbyi. Cultures of Salinibacter have been shown to convert up to 20% of the glycerol added to a not previously characterized overflow product. We here identify this product of incomplete glycerol oxidation by Salinibacter as dihydroxyacetone. Genomic information suggests that H. walsbyi possesses an efficient uptake system for dihydroxyacetone, and we show here that dihydroxyacetone is indeed metabolized by Haloquadratum cultures, as well as by the heterotrophic prokaryotic community of the saltern crystallizer ponds in Eilat, Israel, dominated by Haloquadratum-like cells. In the absence of glycerol, Salinibacter also takes up dihydroxyacetone. Degradation of glycerol, produced in hypersaline lakes as an osmotic solute by the green alga Dunaliella salina may thus involve dihydroxyacetone as an intermediate, which can then be taken up by different types of heterotrophs present in the environment.

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Abbreviations

DHA:

dihydroxyacetone

PQQ:

pyrroloquinoline quinone

References

  • Antón J, Rosselló-Mora R, Rodríguez-Valera F, Amann R (2000) Extremely halophilic Bacteria in crystallizer ponds from solar salterns. Appl Environ Microbiol 66:3052–3057

    Article  PubMed  Google Scholar 

  • Antón J, Oren A, Benlloch S, Rodríguez-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 52:485–491

    PubMed  Google Scholar 

  • Ben-Amotz A, Avron M (1978) On the mechanism of osmoregulation in Dunaliella. In: Caplan SR, Ginzburg M (eds) Energetics and structure of halophilic microorganisms. Elsevier—North Holland Biomedical, Amsterdam, pp 529–541

    Google Scholar 

  • Bolhuis H, te Poele EM, Rodríguez-Valera F (2004) Isolation and cultivation of Walsby’s square archaeon. Environ Microbiol 6:1287–1291

    Article  PubMed  Google Scholar 

  • 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 7:169

    Article  PubMed  CAS  Google Scholar 

  • Brown AD, Lilley RM, Marengo T (1982) Osmoregulation in Dunaliella. Intracellular distribution of enzymes of glycerol metabolism. Z Naturforsch 37:1115–1123

    Google Scholar 

  • Burns DG, Camakaris HM, Janssen PH, Dyall-Smith ML (2004) Cultivation of Walsby’s square haloarchaeon. FEMS Microbiol Lett 238:469–473

    PubMed  CAS  Google Scholar 

  • Burns DG, Janssen PH, Itoh T, Kamekura M, Li Z, Jensen G, Rodríguez-Valera FE, Bolhuis H, Dyall-Smith ML (2007) Haloquadratum walsbyi gen. nov., sp. nov., the square haloarchaeon of Walsby, isolated from saltern crystallizers in Australia and Spain. Int J Syst Evol Microbiol 57:387–392

    Article  PubMed  CAS  Google Scholar 

  • Burton RM (1955) Glycerol dehydrogenase from Aerobacter aerogenes. Meth Enzymol 1:397–400

    Article  CAS  Google Scholar 

  • Burton RM (1957) The determination of glycerol and dihydroxyacetone. Meth Enzymol 3:246–249

    Article  Google Scholar 

  • Elevi Bardavid R, Ionescu D, Oren A, Rainey FA, Hollen BJ, Bagaley DR, Small AM, McKay CM (2007a) Selective enrichment, isolation, and molecular detection of Salinibacter and related extremely halophilic Bacteria from hypersaline environments. Hydrobiologia 576:3–13

    Article  CAS  Google Scholar 

  • Elevi Bardavid R, Khristo P, Oren A (2007b) Interrelationships between Dunaliella and halophilic prokaryotes in saltern crystallizer ponds. Extremophiles, published online 22nd December 2006; DOI 10.1007/s00792-006-0053-y

  • Gimmler H, Lotter G (1982) The intracellular distribution of enzymes of the glycerol cycle in the unicellular alga Dunaliella parva. Z Naturforsch 37:1107–1114

    Google Scholar 

  • Green SR, Whalen EA, Molokie E (2004) Dihydroxyacetone: production and uses. J Biochem Microbiol Technol Eng 3:351–355

    Article  Google Scholar 

  • Hekmat D, Bauer R, Fricke J (2003) Optimization of the microbial synthesis of dihydroxyacetone from glycerol with Gluconobacter oxydans. Bioprocess Biosyst Eng 26:109–116

    Article  PubMed  CAS  Google Scholar 

  • Legault BA, Lopez-Lopez A, Alba-Casado JC, Doolittle WF, Bolhuis H, Rodríguez-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 7:171

    Article  PubMed  CAS  Google Scholar 

  • 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, Rodríguez-Valera F (2005) The genome of Salinibacter ruber: convergence and gene exchange among hyperhalophilic bacteria and archaea. Proc Natl Acad Sci USA 102:18147–18152

    Article  PubMed  CAS  Google Scholar 

  • Oren A (1990) Estimation of the contribution of halobacteria to the bacterial biomass and activity in solar salterns by the use of bile salts. FEMS Microbiol Ecol 73:41–48

    Article  CAS  Google Scholar 

  • Oren A (1993) Availability, uptake, and turnover of glycerol in hypersaline environments. FEMS Microbiol Ecol 12:15–23

    Article  CAS  Google Scholar 

  • 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 14:147–156

    CAS  Google Scholar 

  • Oren A, Rodríguez-Valera F (2001) The contribution of Salinibacter species to the red coloration of saltern crystallizer ponds. FEMS Microbiol Ecol 36:123–130

    PubMed  CAS  Google Scholar 

  • Oren A, Duker S, Ritter S (1996) The polar lipid composition of Walsby’s square bacterium. FEMS Microbiol Lett 138:135–140

    Article  CAS  Google Scholar 

  • Prust C, Hoffmeister M, Liesegang H, Wiezer A, Fricke WF, Ehrenreich A, Gottschalk G, Deppenmeier U (2005) Complete genome sequence of the acetic acid bacterium Gluconobacter oxydans. Nature Biotechnol 23:195–200

    Article  CAS  Google Scholar 

  • 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 7:409–413

    Article  PubMed  CAS  Google Scholar 

  • Sher J, Elevi R, Mana L, Oren A (2004) Glycerol metabolism in the extremely halophilic bacterium Salinibacter ruber. FEMS Microbiol Lett 232:211–215

    Article  PubMed  CAS  Google Scholar 

  • Tomlinson GA, Hochstein LI (1972) Studies on acid production during carbohydrate metabolism by extremely halophilic bacteria. Can J Microbiol 18:1973–1976

    Article  PubMed  CAS  Google Scholar 

  • Tomlinson GA, Koch TK, Hochstein LI (1974) The metabolism of carbohydrates by extremely halophilic bacteria: glucose metabolism via a modified Entner Doudoroff pathway. Can J Microbiol 20:1085–1091

    CAS  Google Scholar 

  • Widdel F, Kohring G-W, Mayer F (1983) Studies on dissimilatory sulfate-reducing bacteria that decompose fatty acids. III. Characterization of the filamentous gliding Desulfonema limicola gen. nov. sp. nov., and Desulfonema magnum sp. nov. Arch Microbiol 134:286–294

    Article  CAS  Google Scholar 

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Acknowledgments

We thank Mike Dyall-Smith and David Burns (Melbourne) for their gift of the Haloquadratum culture, and Lily Mana and Polina Khristo for their assistance in part of the experiments. We are further grateful to the Israel Salt Company in Eilat, Israel for allowing access to the salterns, and to the staff of the Interuniversity Institute for Marine Sciences of Eilat for logistic support. This study was supported by the Israel Science Foundation (grant no. 617/07).

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Correspondence to Aharon Oren.

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Communicated by D. A. Cowan.

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Elevi Bardavid, R., Oren, A. Dihydroxyacetone metabolism in Salinibacter ruber and in Haloquadratum walsbyi . Extremophiles 12, 125–131 (2008). https://doi.org/10.1007/s00792-007-0114-x

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