Extracellular production of Streptomyces exfoliatus poly(3-hydroxybutyrate) depolymerase in Rhodococcus sp. T104: Determination of optimal biocatalyst conditions

Applied Microbiology and Biotechnology

Volumn 93, Issue 5, 2012, Pages 1975-1988

  García Hidalgo, Javier ^a,b   Hormigo, Daniel ^b   Prieto, María Auxiliadora ^b   Arroyo, Miguel ^a   De La Mata, Isabel ^a  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^b CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

Author keywords

Cloning; Extracellular PHB depolymerase; Rhodococcus sp. T104; Streptomyces exfoliatus

Indexed keywords

3-HYDROXYBUTYRIC ACID; ACTIVE SITE; BIOPLASTICS; CALCIUM IONS; CATALYTIC TRIAD; DEPOLYMERASE; EXTRACELLULAR; HYDROXYALKANOIC ACIDS; MALDI-TOF; NATIVE ENZYMES; POLY(3-HYDROXYBUTYRATE); RANDOM COIL; RECOMBINANT ENZYMES; RHODOCOCCUS SP; SECONDARY STRUCTURES; STREPTOMYCES EXFOLIATUS; THERMOINACTIVATION;

AMINO ACIDS; BACTERIA; BIOCATALYSTS; CARBOXYLIC ACIDS; CHEMICAL MODIFICATION; CHROMATOGRAPHY; CLONING; DIMERS; ENZYMATIC HYDROLYSIS; GENE ENCODING; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; INDUSTRIAL APPLICATIONS; MAGNESIUM; MANGANESE; MASS SPECTROMETRY; MONOMERS; SODIUM CHLORIDE;

ENZYME ACTIVITY;

3 HYDROXYALKANOIC ACID DERIVATIVE; 3 HYDROXYBUTYRIC ACID; CALCIUM ION; CARBOXYLIC ACID; CARBOXYLIC ACID DERIVATIVE; DIMER; HISTIDINE; HYDROLASE; MAGNESIUM ION; METHYL BETA CYCLODEXTRIN; MONOMER; POLY(3 HYDROXYBUTYRATE)DEPOLYMERASE; RECOMBINANT ENZYME; SERINE; SODIUM CHLORIDE; UNCLASSIFIED DRUG;

BACTERIUM; CARBOXYLIC ACID; CATALYSIS; CATALYST; CELL ORGANELLE; CHROMATOGRAPHY; ENZYME ACTIVITY; GENE EXPRESSION; HOMOGENEITY; INHIBITION; MASS SPECTROMETRY; POLYMERASE CHAIN REACTION; RECOMBINATION; TEMPERATURE EFFECT;

ALPHA HELIX; ARTICLE; BETA SHEET; BETA TURN; BIOCATALYSIS; BIOCATALYST; CATALYST SUPPORT; CIRCULAR DICHROISM; CONTROLLED STUDY; ENZYMATIC DEGRADATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME INACTIVATION; ENZYME MODIFICATION; ENZYME PURIFICATION; ENZYME STABILITY; ENZYME SYNTHESIS; FREEZE DRYING; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HYDROLYSIS; HYDROPHOBICITY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MOLECULAR CLONING; NONHUMAN; PH; PROTEIN EXPRESSION; PROTEIN SECONDARY STRUCTURE; RHODOCOCCUS; STREPTOMYCES; STREPTOMYCES EXFOLIATUS; TRANSITION TEMPERATURE;

3-HYDROXYBUTYRIC ACID; CALCIUM; CARBOXYLIC ESTER HYDROLASES; CATIONS, DIVALENT; CHROMATOGRAPHY, LIQUID; CIRCULAR DICHROISM; CLONING, MOLECULAR; ENZYME ACTIVATORS; ENZYME INHIBITORS; ENZYME STABILITY; GENE EXPRESSION; MAGNESIUM; PROTEIN CONFORMATION; RECOMBINANT PROTEINS; RHODOCOCCUS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; STREPTOMYCES; TEMPERATURE; TRANSITION TEMPERATURE;

RHODOCOCCUS SP.; STREPTOMYCES EXFOLIATUS;

EID: 84857917937     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-011-3527-5     Document Type: Article

References (71)

1. Anderson AJ, Dawes EA (1990) Occurrence, metabolism, metabolic role, and industrial uses of bacterial polyhydroxyalkanoates. Microbiol Rev 54:450-472 (Pubitemid 120004382)
2. Asano Y, Watanabe S (2001) Isolation of poly(3-hydroxybutyrate) (PHB)-degrading microorganisms and characterization of PHBdepolymerase from Arthrobacter sp. strain W6. Biosci Biotechnol Biochem 65:1191-1194 (Pubitemid 33665978)
3. Bhatt R, Patel KC, Trivedi U (2010) Purification and properties of extracellular poly(3-hydroxybutyrate) depolymerase produced by Aspergillus fumigatus 202. J Polym Environ 18:141-147
4. Bibb MJ, Janssen GR, Ward JM (1985) Cloning and analysis of the promoter region of the erythromycin resistance gene (ermE) of Streptomyces erythraeus. Gene 38:215-226 (Pubitemid 16169920)
5. Bibb MJ, White J, Ward JM, Janssen GR (1994) The messenger-RNA for the 23S ribosomal-RNA methylase encoded by the ermE gene of Saccharopolyspora erythraea is translated in the absence of a conventional ribosome-binding site. Mol Microbiol 14:533-545 (Pubitemid 24337333)
6. Bohm G, Muhr R, Jaenicke R (1992) Quantitative analysis of protein far UV circular dichroism spectra by neural networks. Protein Eng 5:191-195
7. Bonnet V, Gervaise C, Favrelle A, Sarazin C, Djedaini-Pilard F (2010) Enzymatic catalysis in presence of cyclodextrins. Curr Org Chem 14:1323-1336
8. Bradford MM (1976) Rapid and sensitive method for quantitation of microgram quantities of protein utilizing principle of protein-dye binding. Anal Biochem 72:248-254
9. Brucato CL, Wong SS (1991) Extracellular poly(3-hydroxybutyrate) depolymerase from Penicillium funiculosum: general characteristics and active site studies. Arch Biochem Biophys 290:497-502
10. Calabia BP, Tokiwa Y (2004) Microbial degradation of poly(D-3- hydroxybutyrate) by a new thermophilic Streptomyces isolate. Biotechnol Lett 26:15-19 (Pubitemid 38161951)
11. Calabia BP, Tokiwa Y (2006) A novel PHB depolymerase from a thermophilic Streptomyces sp. Biotechnol Lett 28:383-388
12. Chen GQ, Wu Q (2005) Microbial production and applications of chiral hydroxyalkanoates. Appl Microbiol Biotechnol 67:592-599
13. Chiba K, Hoshino Y, Ishino K, Kogure T, Mikami Y, Uehara Y, Ishikawa J (2007) Construction of a pair of practical Nocardia-Escherichia coli shuttle vectors. Jpn J Infect Dis 60:45-47 (Pubitemid 46443716)
14. Ci SQ, Chen S, Liu DB, Xia HM (2006) An extracellular poly(3- hydroxybutyrate) depolymerase from Penicillium sp. DS9713a-01. World J Microbiol Biotechnol 22:729-735
15. De Eugenio LI, García P, Luengo JM, Sanz JM, Román JS, García JL, Prieto MA (2007) Biochemical evidence that phaZ gene encodes a specific intracellular medium chain length polyhydroxyalkanoate depolymerase in Pseudomonas putida KT2442: characterization of a paradigmatic enzyme. J Biol Chem 282:4951-4962 (Pubitemid 47100956)
16. De Eugenio LI, García JL, García P, Prieto MA, Sanz JM (2008) Physiological, structural and comparative analysis of the medium chain length polyhydroxyalkanoate depolymerase from Pseudomonas putida KT2442. Eng Life Sci 8:1-9
17. De Eugenio LI, Escapa IF, Morales V, Dinjaski N, Galán B, García JL, Prieto MA (2010) The turnover of medium-chain-length polyhydroxyalkanoates in Pseudomonas putida KT2442 and the fundamental role of PhaZ depolymerase for the metabolic balance. Environ Microbiol 12:207-221
18. Ellman GL (1959) Tissue sulfhydryl groups. Arch Biochem Biophys 82:70-77
19. Gebauer B, Jendrossek D (2006) Assay of poly(3-hydroxybutyrate) depolymerase activity and product determination. Appl Environ Microbiol 72:6094-6100 (Pubitemid 44414641)
20. Griebenow K, Laureano YD, Santos AM, Clemente IM, Rodríguez L, Vidal MW, Barletta G (1999) Improved enzyme activity and enantioselectivity in organic solvents by methyl-beta-cyclodextrin. J Am Chem Soc 121:8157-8163
21. Han JS, Kim MN (2002) Purification and characterization of extracellular poly(3-hydroxybutyrate) depolymerase from Penicillium simplicissimum LAR13. J Microbiol 40:20-25
22. Henley JP, Sadana A (1985) Categorization of enzyme deactivations using a series-type mechanism. Enzyme Microb Technol 7:50-60 (Pubitemid 15066619)
23. Hernández BS, Koh SC, Chial M, Focht DD (1997) Terpene-utilizing isolates and their relevance to enhanced biotransformation of polychlorinated biphenyls in soil. Biodegradation 8:153-158 (Pubitemid 27510250)
24. Hisano T, Kasuya K, Tezuka Y, Ishii N, Kobayashi T, Shiraki M, Oroudjev E, Hansma H, Iwata T, Doi Y, Saito T, Miki K (2006) The crystal structure of polyhydroxybutyrate depolymerase from Penicillium funiculosum provides insights into the recognition and degradation of biopolyesters. J Mol Biol 356:993-1004 (Pubitemid 43145951)
25. Iyer S, Shah R, Sharma A, Jendrossek D, Desai A (2000) Purification of Aspergillus fumigatus (Pdf1) poly(beta-hydroxybutyrate) (PHB) depolymerase using a new, single-step substrate affinity chromatography method: characterization of the PHB depolymerase exhibiting novel self-aggregation behavior. J Polym Environ 8:197-203
26. Jaeger KE, Steinbuchel A, Jendrossek D (1995) Substrate specificities of bacterial polyhydroxyalkanoate depolymerases and lipases: bacterial lipases hydrolyze poly(omega-hydroxyalkanoates). Appl Environ Microbiol 61:3113-3118
27. Jendrossek D (2002) Extracellular polyhydroxyalkanoate depolymerases: the key enzymes of PHA degradation. In: Doi Y, Steinbüchel A (eds) Polyesters II: properties and chemical synthesis, vol 3b. Wiley, Weinheim, pp 41-80
28. Jendrossek D, Handrick R (2002) Microbial degradation of polyhydroxyalkanoates. Annu Rev Microbiol 56:403-432 (Pubitemid 35217461)
29. Jendrossek D, Knoke I, Habibian RB, Steinbüchel A, Schlegel HG (1993) Degradation of poly(3-hydroxybutyrate), PHB, by bacteria and purification of a novel PHB depolymerase from Comamonas sp. J Environ Polym Degrad 1:53-63 (Pubitemid 23606077)
30. Jendrossek D, Backhaus M, Andermann M (1995) Characterization of the extracellular poly(3-hydroxybutyrate) depolymerase of Comamonas sp. and of its structural gene. Can J Microbiol 41:160-169
31. Kasuya K, Inoue Y, Tanaka T, Akehata T, Iwata T, Fukui T, Doi Y (1997) Biochemical and molecular characterization of the polyhydroxybutyrate depolymerase of Comamonas acidovorans YM1609, isolated from freshwater. Appl Environ Microbiol 63:4844-4852 (Pubitemid 27524221)
32. Kasuya K, Ohura T, Masuda K, Doi Y (1999) Substrate and binding specificities of bacterial polyhydroxybutyrate depolymerases. Int J Biol Macromol 24:329-336 (Pubitemid 29268118)
33. Kasuya K, Mitomo H, Nakahara M, Akiba A, Kudo T, Doi Y (2000) Identification of a marine benthic P(3HB)-degrading bacterium isolate and characterization of its P(3HB) depolymerase. Biomacromolecules 1:194-201
34. Kieser T, Bibb MJ, Buttner MJ, Chater KF, Hoopwood DA (2000) Practical Streptomyces genetics. The John Innes Foundation, Norwich
35. Kim DY, Yun JH, Kim HW, Bae KS, Rhee YH (2002) Purification and characterization of poly(3-hydroxybutyrate) depolymerase from a fungal isolate, Emericellopsis minima W2. J Microbiol 40:129-133 (Pubitemid 34969759)
36. Kim HJ, Kim DY, Nam JS, Bae KS, Rhee YH (2003) Characterization of an extracellular medium-chain-length poly(3-hydroxyalkanoate) depolymerase from Streptomyces sp. KJ-72. Antonie Van Leeuwenhoek 83:183-189 (Pubitemid 36592758)
37. Kita K, Ishimaru K, Teraoka M, Yanase H, Kato N (1995) Properties of poly(3-hydroxybutyrate) depolymerase from a marine bacterium, Alcaligenes faecalis AE122. Appl Environ Microbiol 61:1727-1730
38. Klingbeil B, Kroppenstedt RM, Jendrossek D (1996) Taxonomic identification of Streptomyces exfoliatus K10 and characterization of its poly(3-hydroxybutyrate) depolymerase gene. FEMS Microbiol Lett 142:215-221 (Pubitemid 26279148)
39. Kobayashi T, Sugiyama A, Kawase Y, Saito T, Mergaert J, Swings J (1999) Biochemical and genetic characterization of an extracellular poly(3-hydroxybutyrate) depolymerase from Acidovorax sp strain TP4. J Environ Polym Degrad 7:9-18 (Pubitemid 129772951)
40. Kolossvary GJ, Banky-Elod E (1996) Enhancement of enzymatic hydrolysis of triolein in aqueous solution by cyclodextrin derivatives. Biotechnol Tech 10:115-120
41. Laemmli UK (1970) Cleavage of structural proteins during assembly of head of bacteriophage T4. Nature 227:680-685
42. Lee SY, Lee Y, Wang F (1999) Chiral compounds from bacterial polyesters: sugars to plastics to fine chemicals. Biotechnol Bioeng 65:363-368
43. Li J, Toh KC (2002) Formation of inclusion complexes between dimers of (R)-3-hydroxybutanoic acid and beta-cyclodextrin: thermodynamic study of the complexation and conformational analysis of the complexed dimers. J Chem Soc Perkin Trans 2:35-40 (Pubitemid 35188041)
44. Liu HY, Zhang H, Chen S, Liu DB, Xia HM (2006) Purification and properties of a poly (beta-hydroxybutyrate) depolymerase from Penicillium sp. J Polym Environ 14:419-426 (Pubitemid 44830801)
45. Madison LL, Huisman GW (1999) Metabolic engineering of poly(3- hydroxyalkanoates): from DNA to plastic. Microbiol Mol Biol Rev 63:21-53 (Pubitemid 29116086)
46. Mergaert J, Webb A, Anderson C, Wouters A, Swings J (1993) Microbial degradation of poly(3-hydroxybutyrate) and poly(3- hydroxybutyrate-co-3- hydroxyvalerate) in soils. Appl Environ Microbiol 59:3233-3238 (Pubitemid 23296437)
47. Miyazaki K, Takahashi K, Shiraki M, Saito T, Tezuka Y, Kasuya K (2000) Properties of a poly(3-hydroxybutyrate) depolymerase from Penicillium funiculosum. J Polym Environ 8:175-182 (Pubitemid 34635582)
48. Mukai K, Yamada K, Doi Y (1993) Enzymatic degradation of poly (hydroxyalkanoates) by a marine bacterium. Polym Degrad Stabil 41:85-91
49. Nojima S, Mineki S, Iida M (1996) Purification and characterization of extracellular poly(3-hydroxybutyrate) depolymerases produced by Agrobacterium sp. K-03. J Ferment Bioeng 81:72-75
50. Oda Y, Osaka H, Urakami T, Tonomura K (1997) Purification and properties of poly(3-hydroxybutyrate) depolymerase from the fungus Paecilomyces lilacinus D218. Curr Microbiol 34:230-232 (Pubitemid 27150363)
51. Ooe Y, Yamamoto S, Kobayashi M, Kise H (1999) Increase of catalytic activity of alpha-chymotrypsin in organic solvent by colyophilization with cyclodextrins. Biotechnol Lett 21:385-389 (Pubitemid 29299127)
52. Papaneophytou CP, Pantazaki AA, Kyriakidis DA (2009) An extracellular polyhydroxybutyrate depolymerase in Thermus thermophilus HB8. Appl Microbiol Biotechnol 83:659-668
53. Prieto MA, De Eugenio LI, Galán B, Luengo JM, Witholt B (2007) Synthesis and degradation of polyhydroxyalkanoates. In: Ramos JL, Filloux A (eds) Pseudomonas: a model system in biology. Pseudomonas, vol V. Springer, Dordrecht, pp 397-428
54. Quirós LM, Aguirrezabalaga I, Olano C, Mendez C, Salas JA (1998) Two glycosyltransferases and a glycosidase are involved in oleandomycin modification during its biosynthesis by Streptomyces antibioticus. Mol Microbiol 28:1177-1185 (Pubitemid 28293541)
55. Ren Q, Grubelnik A, Hoerler M, Ruth K, Hartmann R, Felber H, Zinn M (2005) Bacterial poly(hydroxyalkanoates) as a source of chiral hydroxyalkanoic acids. Biomacromolecules 6:2290-2298 (Pubitemid 41052228)
56. Ren Q, Ruth K, Thony-Meyer L, Zinn M (2010) Enatiomerically pure hydroxycarboxylic acids: current approaches and future perspectives. Appl Microbiol Biotechnol 87:41-52
57. Romen F, Reinhardt S, Jendrossek D (2004) Thermotolerant poly(3- hydroxybutyrate)-degrading bacteria from hot compost and characterization of the PHB depolymerase of Schlegelella sp. KB1a. Arch Microbiol 182:157-164 (Pubitemid 39361992)
58. Sadocco P, Nocerino S, Dubini-Paglia E, Seves A, Elegir G (1997) Characterization of a poly(3-hydroxybutyrate) depolymerase from Aureobacterium saperdae: active site and kinetics of hydrolysis studies. J Environ Polym Degrad 5:57-65 (Pubitemid 27450021)
59. Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor
60. Sang BI, Lee WK, Hori K, Unno H (2006) Purification and characterization of fungal poly(3-hydroxybutyrate) depolymerase from Paecilomyces lilacinus F4-5 and enzymatic degradation of poly(3-hydroxybutyrate-co-3-hydroxyvalerate) film. World J Microbiol Biotechnol 22:51-57 (Pubitemid 43288289)
61. Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chainterminating inhibitors. Proc Natl Acad Sci USA 74:5463-5467
62. Segel IH (1993) Enzyme kinetics: behavior and analysis of rapid equilibrium and steady state enzyme systems. Wiley, New York
63. Shinohe T, Nojiri M, Saito T, Stanislawski T, Jendrossek D (1996) Determination of the active sites serine of the poly (3-hydroxybutyrate) depolymerases of Pseudomonas lemoignei (PhaZ5) and of Alcaligenes faecalis. FEMS Microbiol Lett 141:103-109 (Pubitemid 26228722)
64. Shinomiya M, Iwata T, Kasuya K, Doi Y (1997) Cloning of the gene for poly(3-hydroxybutyric acid) depolymerase of Comamonas testosteroni and functional analysis of its substrate binding domain. FEMS Microbiol Lett 154:89-94 (Pubitemid 27376741)
65. Speicher DW (1994) Methods and strategies for the sequence analysis of proteins on PVDF membranes. Methods 6:262-273
66. Steinbüchel A, Valentin HE (1995) Diversity of bacterial polyhydroxyalkanoic acids. FEMS Microbiol Lett 128:219-228
67. Tanio T, Fukui T, Shirakura Y, Saito T, Tomita K, Kaiho T, Masamune S (1982) An extracellular poly(3-hydroxybutyrate) depolymerase from Alcaligenes faecalis. Eur J Biochem 124:71-77
68. Tokiwa Y, Calabia BP (2004) Degradation of microbial polyesters. Biotechnol Lett 26:1181-1189 (Pubitemid 40938268)
69. Villalonga R, Cao R, Fragoso A (2007) Supramolecular chemistry of cyclodextrins in enzyme technology. Chem Rev 107:3088-3116 (Pubitemid 47162905)
70. Yamada K, Mukai K, Doi Y (1993) Enzymatic degradation of poly (hydroxyalkanoates) by Pseudomonas pickettii. Int J Biol Macromol 15:215-220 (Pubitemid 23226613)
71. Zhou HL, Wang ZY, Chen S, Liu DB, Xia HM (2009) Purification and characterization of extracellular poly(3-hydroxybutyrate) depolymerase from Penicillium sp. DS9701-D2. Polym Plast Technol Eng 48:58-63