Synthesis and release of the bacterial compatible solute 5-hydroxyectoine in Hansenula polymorpha

Journal of Biotechnology

Volumn 167, Issue 2, 2013, Pages 85-93

  Eilert, Eva ^a,b   Kranz, Andreas ^a   Hollenberg, Cornelis P ^a,b   Piontek, Michael ^a   Suckow, Manfred ^a  

^a ARTES Biotechnology GmbH   (Germany)

^b HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

5 Hydroxyectoine; Compatible solute; Ectoine; Halomonas elongata; Hansenula polymorpha; Whole cell biocatalysis

Indexed keywords

5-HYDROXYECTOINE; COMPATIBLE SOLUTES; ECTOINE; HALOMONAS ELONGATA; HANSENULA POLYMORPHA; WHOLE-CELL BIOCATALYSIS;

BIOTECHNOLOGY;

BIOCHEMISTRY;

5 HYDROXYECTOINE; ECTOINE; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; GENE INSERTION; GENOME; NONHUMAN; PICHIA ANGUSTA; PRIORITY JOURNAL; SOLUTE; SYNTHESIS;

5-HYDROXYECTOINE; ASD; ASK; ASPARTATE KINASE; ASPARTATE SEMIALDEHYDE DEHYDROGENASE; COMPATIBLE SOLUTE; DABA; DABA ACYLTRANSFERASE; DABA-2-OXOGLUTARATE TRANSAMINASE; DCW; DIAMINOBUTYRATE; DRY CELL WEIGHT; ECTA; ECTB; ECTC; ECTD; ECTOINE; ECTOINE HYDROXYLASE; ECTOINE SYNTHASE; FMD; FORMATE DEHYDROGENASE; HALOMONAS ELONGATA; HANSENULA POLYMORPHA; MEOH; METHANOL; METHANOL OXIDASE; MOX; WHOLE-CELL BIOCATALYSIS;

AMINO ACIDS, DIAMINO; BACTERIAL PROTEINS; CARBON; GENES, BACTERIAL; HALOMONAS; HYDROGEN-ION CONCENTRATION; PICHIA; SALINITY;

BACTERIA (MICROORGANISMS); HALOMONAS ELONGATA; PICHIA ANGUSTA;

EID: 84881031085     PISSN: 01681656     EISSN: 18734863     Source Type: Journal    
DOI: 10.1016/j.jbiotec.2013.02.005     Document Type: Article

References (48)

1. Adler L., Blomber A., Nilsson A. Glycerol Metabolism and osmoregulation in salt-tolerant yeast Debaryomyces hansenii. Journal of Bacteriology 1985, 162(1):300-306.
2. Anbu Rajan L., Joseph T., Thampuran N., James R., Ashok Kumar K., Viswanathan C., Bansal K. Cloning and heterologous expression of ectoine biosynthesis genes from Bacillus halodurans in Escherichia coli. Biotechnology Letters 2008, 30(8):1403-1407.
3. Bestvater T., Louis P., Galinski E. Heterologous ectoine production in Escherichia coli: by-passing the metabolic bottle-neck. Saline Systems 2008, 4:12.
4. Bursy J., Pierik A., Pica N., Bremer E. Osmotically induced synthesis of the compatible solute hydroxyectoine is mediated by an evolutionarily conserved ectoine hydroxylase. Journal of Biological Chemistry 2007, 282(43):31147-31155.
5. Cánovas D., Borges N., Vargas C., Ventosa A., Nieto J., Santos H. Role of Nγ-acetyldiaminobutyrate as an enzyme stabilizer and an intermediate in the biosynthesis of hydroxyectoine. Applied and Environment Microbiology 1999, 65(9):3774-3779.
6. Degelmann A., Müller F., Sieber H., Jenzelewski V., Suckow M., Strasser A., Gellissen G. Strain and process development for the production of human cytokines in Hansenula polymorpha. FEMS Yeast Research 2002, 2(3):349-361.
7. Eilert E., Hollenberg C.P., Piontek M., Suckow M. The use of highly expressed FTH1 as carrier protein for cytosolic targeting in Hansenula polymorpha. Journal of Biotechnology 2012, 159(3):172-176.
8. Faber K.N., Haima P., Harder W., Veenhuis M.A.B.G. Highly-efficient electrotransformation of the yeast Hansenula polymorpha. Current Genetics 1994, 25(4):305-310.
9. Frings E., Sauer T., Galinski E. Production of hydroxyectoine: high cell-density cultivation and osmotic downshock of Marinococcus strain M52. Journal of Biotechnology 1995, 43:53-61.
10. Galinski E., Pfeiffer H.P., Trüper H. 1,4,5,6-Tetrahydro-2-methyl-4-pyrimidinecarboxylic acid. A novel cyclic amino acid from halophilic phototrophic bacteria of the genus Ectothiorhodospira. European Journal of Biochemistry 1985, 149(1):135-139.
11. García-Estepa R., Cánovas D., Iglesias-Guerra F., Ventosa A., Csonka L., Nieto J., Vargas C. Osmoprotection of Salmonella enterica serovar Typhimurium by Nγ-acetyldiaminobutyrate, the precursor of the compatible solute ectoine. Systematic and Applied Microbiology 2006, 29(8):626-633.
12. Gellissen G., Hollenberg C.P. Application of yeasts in gene expression studies: a comparison of Saccharomyces cerevisiae, Hansenula polymorpha and Kluyveromyces lactis-a review. Gene 1997, 190(1):87-97.
13. Gellissen G., Janowicz Z.A., Weydemann U., Melber K., Strasser A.W., Hollenberg C.P. High-level expression of foreign genes in Hansenula polymorpha. Biotechnology Advances 1992, 10(2):179-189.
14. Gellissen G., Piontek M., Dahlems U., Jenzelewski V., Gavagan J.E., DiCosimo R., Anton D.L., Janowicz Z.A. Recombinant Hansenula polymorpha as a biocatalyst: coexpression of the spinach glycolate oxidase (GO) and the S. cerevisiae catalase T (CTT1) gene. Applied Microbiology and Biotechnology 1996, 46(1):46-54.
15. Grammann K., Volke A., Kunte H. New type of osmoregulated solute transporter identified in halophilic members of the bacteria domain: TRAP transporter TeaABC mediates uptake of ectoine and hydroxyectoine in Halomonas elongata DSM 2581(T). Journal of Bacteriology 2002, 184(11):3078-3085.
16. Güldener, Heck U., Fielder S., Beinhauer T., Hegemann J.J.H. A new efficient gene disruption cassette for repeated use in budding yeast. Nucleic Acids Research 1996, 24(13):2519-2524.
17. 15N NMR spectroscopy. Journal of Biological Chemistry 1988, 263(31):16014-16022.
18. Janowicz Z.A., Melber K., Merckelbach A., Jacobs E., Harford N., Comberbach M., Hollenberg C. Simultaneous expression of the S and L surface antigens of hepatitis B, and formation of mixed particles in the methylotrophic yeast, Hansenula polymorpha. Yeast 1991, 7:431-443.
19. Jebbar M., Sohn-Bösser L., Bremer E., Bernard T., Blanco C. Ectoine-induced proteins in Sinorhizobium meliloti include an Ectoine ABC-type transporter involved in osmoprotection and ectoine catabolism. Journal of Bacteriology 2005, 187(4):1293-1304.
20. Kikuchi Y., Kojima H., Tanaka T. Mutational analysis of the feedback sites of lysine-sensitive aspartokinase of Escherichia coli. FEMS Microbiology Letters 1999, 173(1):211-215.
21. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227(5259):680-685.
22. Lages F., Silva-Graça M., Lucas C. Active glycerol uptake is a mechanism underlying halotolerance in yeasts: a study of 42 species. Microbiology 1999, 145:2577-2585.
23. Lahtchev K., Semenova V., Tolstorukov I., van der Klei I., Veenhuis M. Isolation and properties of genetically defined strains of the methylotrophic yeast Hansenula polymorpha CBS4732. Archives of Microbiology 2002, 177(2):150-158.
24. Lentzen G., Schwarz T. Extremolytes: natural compounds from extremophiles for versatile applications. Applied Microbiology and Biotechnology 2006, 72(4):623-634.
25. Lentzen G., Schwarz T. Kompatible Solute: Mikrobielle Herstellung und Anwendung. Angewandte Mikrobiologie 2006, Springer-Verlag, Berlin, Heidelberg. G. Antranikian (Ed.).
26. Lippert K., Galinski E. Enzyme stabilization by ectoine-type compatible solutes: protection against heating, freezing and drying. Applied Microbiology and Biotechnology 1992, 37:61-65.
27. Mayer A.F., Hellmuth K., Schlieker H., Lopez-Ulibarri R., Oertel S., Dahlems U., Strasser A.W., van Loon A.P. An expression system matures: a highly efficient and cost-effective process for phytase production by recombinant strains of Hansenula polymorpha. Biotechnology and Bioengineering 1999, 63(3):373-381.
28. Ono H., Sawada K., Khunajakr N., Tao T., Yamamoto M., Hiramoto M., Shinmyo A., Takano M., Murooka Y. Characterization of biosynthetic enzymes for ectoine as a compatible solute in a moderately halophilic eubacterium, Halomonas elongata. Journal of Bacteriology 1999, 181(1):91-99.
29. Pastor J., Salvador M., Argandoña M., Bernal V., Reina-Bueno M., Csonka L., Iborra J., Vargas C., Nieto J., Cánovas M. Ectoines in cell stress protection: uses and biotechnological production. Biotechnology Advances 2010, 28(6):782-801.
30. Peters P., Galinski E., Trüper H. The biosynthesis of ectoine. FEMS Microbiology Letters 1990, 71:157-162.
31. Reshetnikov A., Khmelenina V., Mustakhimov I., Trotsenko Y. Genes and enzymes of ectoine biosynthesis in halotolerant methanotrophs. Methods in Enzymology 2011, 495:15-30.
32. Sauer B. Functional expression of the cre-lox site-specific recombination system in the yeast Saccharomyces cerevisiae. Molecular and Cellular Biology 1987, 7(6):2087-2096.
33. Sauer T., Galinski E. Bacterial milking: a novel bioprocess for production of compatible solutes. Biotechnology and Bioengineering 1998, 57(3):306-313.
34. Schiraldi C., Maresca C., Catapano A., Galinski E., de Rosa M. High-yield cultivation of Marinococcus M52 for production and recovery of hydroxyectoine. Research in Microbiology 2006, 157(7):693-699.
35. Schubert T., Maskow T., Benndorf D., Harms H., Breuer U. Continuous synthesis and excretion of the compatible solute ectoine by a transgenic, nonhalophilic bacterium. Applied and Environment Microbiology 2007, 73(10):3343-3347.
36. Schwibbert K., Marin-Sanguino A., Bagyan I., Heidrich G., Lentzen G., Seitz H., Rampp M., Schuster S.C., Klenk H.-P., Pfeiffer F., Oesterhelt D., Kunte H. A blueprint of ectoine metabolism from the genome of the industrial producer Halomonas elongata DSM 2581. Environmental Microbiology 2010, 13(8):1973-1994.
37. Seip B., Galinski E., Kurz M. Natural and engineered hydroxyectoine production based on the Pseudomonas stutzeri ectABCD-ask gene cluster. Applied and Environment Microbiology 2011, 77(4):1368-1374.
38. Stöveken N., Pittelkow M., Sinner T., Jensen R., Heider J., Bremer E. A specialized aspartokinase enhances the biosynthesis of the osmoprotectants ectoine and hydroxyectoine in Pseudomonas stutzeri A1501. Journal of Bacteriology 2011, 193(17):4456-4468.
39. Tamás M.J., Luyten K., Sutherland C.W., Hernandez A., Albertyn J., Valadi H., Li H., Prior B.A., Kilian S.G., Ramos J., Gustafsson L., Thevelein J.M., Hohmann S. Fps1p controls the accumulation and release of compatible solute glycerol in yeast osmoregulation. Molecular Microbiology 1999, 31(4):1087-1104.
40. van Eck J.H., Prior B.A., Brandt E.V. The water relations of growth and polyhydroxyl alcohol production by ascomycetous yeasts. Journal of General Microbiology 1993, 139:1047-1054.
41. van Zyl P.J., Kilian S.G., Prior B.A. The role of an active transport mechanism in glycerol accumulation during osmoregulation by Zygosaccharomyces rouxii. Applied Microbiology and Biotechnology 1990, 34:231-235.
42. Vargas C., Jebbar M., Carrasco R., Blanco C., Calderón M.I., Iglesias-Guerra F., Nieto J.J. Ectoines as compatible solutes and carbon and energy sources for the halophilic bacterium Chromohalobacter salexigens. Journal of Applied Microbiology 2006, 100(1):98-107.
43. Vargas C., Argandoña M., Reina-Bueno M., Rodríguez-Moya J., Fernández-Aunión C., Nieto J. Unravelling the adaptation responses to osmotic and temperature stress in Chromohalobacter salexigens, a bacterium with broad salinity tolerance. Saline Systems 2008, 4:14.
44. Veenhuis M., van Dijken J.P., Harder W. The significance of peroxisomes in the metabolism of one-carbon compounds in yeasts. Advances in Microbial Physiology 1983, 24:1-82.
45. Vermeulen V., Kunte H.J. Marinococcus halophilus DSM 20408T encodes two transporters for compatible solutes belonging to the betaine-carnitine-choline transporter family: identification and characterization of ectoine transporter EctM and glycine betaine transporter BetM. Extremophiles 2004, 8(3):175-184.
46. Viola R.E. The central enzymes of the aspartate family of amino acid biosynthesis. Accounts of Chemical Research 2001, 34(5):339-349.
47. Weydemann U., Keup P., Piontek M., Strasser A.W., Schweden J., Gellissen G., Janowicz Z.A. High-level secretion of hirudin by Hansenula polymorpha - authentic processing of three different preprohirudins. Applied Microbiology and Biotechnology 1995, 44(3-4):377-385.
48. Wohlfarth A., Severin J., Galinski E.A. The spectrum of compatible solutes in heterotrophic halophilic eubacteria of the family Halomondaceae. Journal of General Microbiology 1990, 136:705-712.