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Phylogenetic analysis and characterization of lipolytic activity of halophilic archaeal isolates

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Abstract

Five isolates designated as B45, D83A, A206A, A85 and E49 found to possess lipolytic activities were taxonomically classified on the basis of their phylogenetic, phenotypic and chemotaxonomic characteristics. The isolates were determined to be gram-negative, catalase and oxidase positive, hydrolyzing Tween 80 and 60 but not starch, need 3.5–4 M NaCl for optimal growth and lack of anaerobic growth with arginine or DMSO. All isolates had the highest lipolytic activity at pH 8.5. Lipase and esterase activities increased with salt concentration up to 3–4.5 M NaCl, and decreased at 5 M NaCl. Esterase and lipase showed their maximal activities at 50–55°C and 60–65°C, respectively. The phylogenetic tree constructed by the neighbor-joining method indicated that the strain B45 and A85 were closely related to the members of genera Halovivax and Natrinema, respectively. The closest relative of the strain A206A and D83A were found to be Haloterrigena saccharevitans. The strain E49 displayed a more distant relationship to known strains.

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References

  1. Hanzawa, S., Hoaki, T., Jannasch, H., and Maruyama, T., An Extremely Thermostable Serine Protease from Hyperthermophilic Archaeum, Desulfurococcus SY, Isolated from a Deep Sea Hydrothermal Vent, J. Mar. Biotechnol., 1996, vol. 4, pp. 121–126.

    CAS  Google Scholar 

  2. Holmes, M.L., Scopes, R.K., Moritz, R.L., Simpson, R.J., Englert, C., Pfeifer, F., and Dyall-Smith, M.L., Purification and Analysis of an Extremely Halophilic b-Galactosidase from Haloferax alicantei, Biochim. Biophys. Acta., 1997, vol. 1337, pp. 276–286.

    Article  PubMed  CAS  Google Scholar 

  3. Synowiecki, J., Grzybowska, B., and Zdzieblo, A., Sources, Properties and Suitability of New Thermostable Enzymes in Food Processing, Crit. Rev. Food Sci. Nutrit., 2006, vol. 46, pp. 197–205.

    Article  CAS  Google Scholar 

  4. Adamczak, M. and Krishna, S.H., Strategies for Improving Enzymes for Efficient Biocatalysis, Food Technol. Biotechnol., 2004, vol. 42, pp. 251–264.

    CAS  Google Scholar 

  5. Reetz, M.T. and Jaeger, K.E., Superior Biocatalysts by Directed Evolution, Top. Curr. Chem., 1999, vol. 200, pp. 32–57.

    Google Scholar 

  6. Jaeger, K.E., Eggert, T., Eipper, A., and Reetz, M.T., Directed Evolution and the Creation of Enantioselective Biocatalysts, Appl. Microbiol. Biotechnol., 2001, vol. 55, pp. 519–530.

    Article  PubMed  CAS  Google Scholar 

  7. Madern, D., Ebel, C., and Zaccai, G., Halophilic Adaptation of Enzymes, Extremophiles, 2000, vol. 4, pp. 91–98.

    Article  PubMed  CAS  Google Scholar 

  8. Richard, S.B., Madern, D., Garcin, E., and Zaccai, G., Halophilic Adaptation: Novel Solvent Protein Interactions Observed in the 2.9 and 2.6 A Resolution Structures of the Wild Type and a Mutant of Malate Dehydrogenase from Haloarcula marismortui, Biochemistry, 2000, vol. 39, pp. 992–1000.

    Article  PubMed  CAS  Google Scholar 

  9. Oren, A., Diversty of Halophilic Microorganisms: Environments, Phylogeny, Physiology, and Applications, J. Indust. Microbiol. Biotech., 2002, vol. 28, pp. 56–63.

    CAS  Google Scholar 

  10. Mellado, E. and Ventosa, A. Biotechnological Potential of Moderately and Extremely Halophilic Microorganisms. Barredo, J.L., Ed., Kerala: Research Signpost, 2003.

    Google Scholar 

  11. Jaeger, K.E., Dijkstra, B.W., and Reetz, M.T., Bacterial Biocatalysts: Molecular Biology Three-Dimensional Structures and Biotechnological Applications of Lipases, Ann. Rev. Microbiol., 1999, vol. 53, pp. 315–351.

    Article  CAS  Google Scholar 

  12. Baliga, N.S., Bonneau, R., Facciotti, M.T., Pan, M., Glusman, G., Deutsch, E.W., Shannon, P., Chiu, Y., Weng, R.S., Gan, R.R., Hung, P., Date, S.V., Marcotte, E., Hood, L., and Ng, W.V., Genome Sequence of Haloarcula marismortui: A Halophilic Archaeon from the Dead Sea, Genome Res., 2004, vol. 14, pp. 2221–2234.

    Article  PubMed  CAS  Google Scholar 

  13. Camacho, R.M., Mateos, J.C., Gonzalez-Reynoso, O., Prado, L.A., and Cordova, J., Production and Characterization of Esterase and Lipase from Haloarcula marismortui, J. Ind. Microbiol. Biotechnol., 2009, vol. 36, pp. 901–909.

    Article  PubMed  CAS  Google Scholar 

  14. Ikeda, M. and Clark, D.S., Molecular Cloning of Extremely Thermostable Esterase Gene from Hyperthermophilic Archaeon Pyrococcus furiosus in Escherichia coli, Biotechnol. Bioeng., 1998, vol. 57, pp. 624–629.

    Article  PubMed  CAS  Google Scholar 

  15. Almeida, R.C, Campbell Alqueres, S.M., Ariane Leites Larentis, A.L., Rossle, S.C., Cardoso, A.M., Almeida, W.I., Bisch, P.M., Moitinho Alves, T.L., and Martins, O.B., Cloning, Expression, Partial Characterization and Structural Modeling of a Novel Esterase from Pyrococcus furiosus, Enzyme Microbial. Technol., 2006, vol. 39, pp. 1128–1136.

    Article  CAS  Google Scholar 

  16. Elevi, R., Assa, P., Birbir, M., Ogan, A., and Oren, A., Characterization of Extremely Halophilic Archaea Isolated from the Ayvalik Saltern, World J. Microbiol. Biotechnol., 2004, vol. 20, pp. 719–725.

    Article  CAS  Google Scholar 

  17. Ozcan, B., Cokmus, C., Coleri, A., and Caliskan, M., Characterization of Extremely Halophilic Archaea Isolated from Saline Environment in Different Parts of Turkey, Microbiology, 2006, vol. 75, pp. 739–746.

    Article  CAS  Google Scholar 

  18. Birbir, M., Calli, B., Mertoglu, B., Elevi Bardavid, R., Oren, A., Ogmen, M.N., and Ogan, A., Extremely Halophilic Archaea from Tuz lake, Turkey, and the Adjacent Kaldirim and Kayacik Salterns, World J. Microbiol. Biotechnol., 2007, vol. 23, pp. 309–316.

    Article  CAS  Google Scholar 

  19. Ozcan, B., Ozyilmaz, G., Cokmus, C., and Caliskan, M., Characterization of Extracellular Esterase and Lipase Activities from Five Halophilic Archaeal Strains, J. Ind. Microbiol. Biotechnol., 2009, vol. 36, pp. 105–110.

    Article  PubMed  CAS  Google Scholar 

  20. Ozcan, B., Ozcengiz, G., Coleri, A., and Cokmus, C., Diversity of Halohilic Archaea from Six Hypersaline Environments in Turkey, J. Microbiol. Biotechnol., 2007, vol. 17, pp. 985–992.

    PubMed  CAS  Google Scholar 

  21. Oren, A., Ventosa, A., and Grant, W.D., Proposed Minimal Standarts for Description of New Taxa in the Order Halobacteriales, Int. J. Syst. Bacteriol., 1997, vol. 47, pp. 233–238.

    Article  Google Scholar 

  22. Dussault, H.P., An Improved Technique for Staining Red Halophilic Bacteria, J. Bacteriol., 1995, vol. 70, pp. 484–485.

    Google Scholar 

  23. Hartmann, R., Sickinger, H.D., and Oesterhelt, D., Anaerobic Growth of Halobacteria, Proc. Natl. Acad. Sci. U.S.A., 1980, vol. 77, pp. 3821–3825.

    Article  PubMed  CAS  Google Scholar 

  24. Stan-Lotter, H., Pfaffenhuemer, M., Legat, A., Busse, H.J., Radax, C., and Gruber, C., Halococcus dombrowskii sp. nov., an Archaeal Isolate from a Permian Alpine Salt Deposit, Int. J. Syst. Evol. Microbiol., 2002, vol. 52, pp. 1807–1814.

    Article  PubMed  CAS  Google Scholar 

  25. Oren, A. and Litchfield, D.C., A Procedure for the Enrichment and Isolation of Halobacterium, FEMS Microbiol. Letters, 1999, vol. 173, pp. 353–358.

    Article  CAS  Google Scholar 

  26. Tamura, K., Dudley, J., Nei, M., and Kumar, S., MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0, Mol. Biol. Evol., 2007, vol. 24, pp. 1596–1599.

    Article  PubMed  CAS  Google Scholar 

  27. Castillo, A.M., Gutierrez, M.C., Kamekura, M., Ma, Y., Cowan, D.A., Jones, B.E., Grant, W.D., and Ventosa, A., Halovivax asiaticus gen. nov., sp. nov., a Novel Extremely Halophilic Archaeon Isolated from Inner Mongolia, Int. J. Syst. Evol. Microbiol., 2006, vol. 56, pp. 765–770.

    Article  PubMed  CAS  Google Scholar 

  28. Castillo, A.M., Gutierrez, M.C., Kamekura, M., Xue, Y., Ma, Y., Cowan, D.A., Jones, B.E., Grant, W.D., and Ventosa, A., Halovivax ruber sp. nov., an Extremely Halophilic Archaeon Isolated from Lake Xilinhot, Inner Mongolia, China, Int. J. Syst. Evol. Microbiol., 2007, vol. 57, pp. 1024–1027.

    Article  PubMed  CAS  Google Scholar 

  29. Saitou, N. and Nei, M., The Neighbor-Joining Method: A New Method for Reconstructing Phylogenetic Trees, Mol. Biol. Evol., 1987, vol. 4, pp. 406–425.

    PubMed  CAS  Google Scholar 

  30. Xin, H., Itoh, T., Zhou, P., Suzuki, K., Kamekura, M., and Nakase, T., Natrinema versiforme sp. nov., an Halophilic Archaeon from Aibi Salt Lake, Int. J. Syst. Evol. Microbiol., 2000, vol. 50, pp. 1297–1303.

    Article  PubMed  CAS  Google Scholar 

  31. Ventosa, A., Gutierrez, M.C., Kamekura, M., and Dyall-Smith, M., Proposal to Transfer Halococcus turcmenicus, Halobacterium trapanicum JCM 9743 and strain GSL-11 to Haloterrigena turkmenica gen. nov., comb. nov., Int. J. Syst. Bacteriol., 1999, vol. 49, pp. 131–136.

    Article  PubMed  Google Scholar 

  32. Cui, H.L., Tohty, D., Zhou, P.J., and Liu, S.J., Haloterrigena longa sp. nov. and Haloterrigena limicola sp. nov., Extremely Halophilic Archaea Isolated from a Salt Lake, Int. J. Syst. Evol. Microbiol., 2006, vol. 56, pp. 1837–1840.

    Article  PubMed  CAS  Google Scholar 

  33. Gutierrez, M.C., Castillo, A.M., Kamekura, M., and Ventosa, A., Haloterrigena salina sp. nov., an Extremely Halophilic Archaeon Isolated from a Salt Lake, Int. J. Syst. Evol. Microbiol., 2008, vol. 58, pp. 2880–2884.

    Article  PubMed  CAS  Google Scholar 

  34. Montalvo-Rodriguez, R., Lopez-Garriga, J., Vreeland, H., Oren, A., Ventosa, A., and Kamekura, M., Haloterrigena thermotolerans sp. nov., a Halophilic Archaeon from Puerto Rico, Int. J. Syst. Evol. Microbiol., 2000, vol. 50, pp. 1065–1071.

    Article  PubMed  CAS  Google Scholar 

  35. Xu, X.W., Liu, S.J., Tohty, D., Oren, A., Wu, M., Zhou, P.J., Haloterrigena saccharevitans sp. nov., an Extremely Halophilic Archaeon from Xin-Jiang, China, Int. J. Syst. Evol. Microbiol., 2005, vol. 55, pp. 2539–2542.

    Article  PubMed  CAS  Google Scholar 

  36. Fukushima, T., Mizuki, T., Echigo, A., Inoue, A., and Usami, R., Organic Solvent Tolerance of Halophilic α-Amylase from a Haloarchaeon, Haloarcula sp. Strain S-1, Extremophiles, 2005, vol. 9, pp. 85–89.

    Article  PubMed  CAS  Google Scholar 

  37. Boutaiba, S., Bhatnagar, T., Hacene, H., Mitchell, D.A., and Baratti, J.C., Preliminary Characterisation of a Lipolytic Activity from an Extremely Halophilic Archaeon, Natronococcus sp., J. Mol. Catal. B Enzym., 2006, vol. 41, pp. 21–26.

    Article  CAS  Google Scholar 

  38. Bonete, M.J., Pire, C., Lorca, F.I., and Camacho, M.L., Glucose Dehydrogenase from the Halophilic Archaeon Haloferax mediterranei: Enzyme Purification, Characterization and N-Terminal Sequence, FEBS Lett., 1996, vol. 383, pp. 227–229

    Article  PubMed  CAS  Google Scholar 

  39. Bhatnagar, T., Boutaiba, S., Hacene, H., Cayol, J.L., Fardeau, M.L., Olliver, B., and Baratti, J.C., Lipolytic Activity from Halobacteria: Screening and Hydrolyses Production, FEMS Microbiol. Lett., 2005, vol. 248, pp. 133–140.

    Article  PubMed  CAS  Google Scholar 

  40. Krieg, N.R. Prokaryotik Domains. Garrity, G.M. Ed., Bergey’s Manual of Systematic Bacteriology V.I, The Archaea and Deeply Branching and Phototrophic Bacteria, New York: Springer, 2001.

    Google Scholar 

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Authors and Affiliations

  1. Biology Department, Faculty of Sciences and Letters, Mustafa Kemal University, Antakya, Turkey

    B. Ozcan & M. Caliskan

  2. Chemistry Department, Faculty of Sciences and Letters, Mustafa Kemal University, Antakya, Turkey

    G. Ozyilmaz

  3. Biology Department, Faculty of Sciences, Ankara University, Ankara, Turkey

    A. Cihan & C. Cokmus

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Ozcan, B., Ozyilmaz, G., Cihan, A. et al. Phylogenetic analysis and characterization of lipolytic activity of halophilic archaeal isolates. Microbiology 81, 186–194 (2012). https://doi.org/10.1134/S0026261712020105

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