A CGTase with high coupling activity using γ-cyclodextrin isolated from a novel strain clustering under the genus Carboxydocella

Glycobiology

Volumn 25, Issue 5, 2015, Pages 514-523

  Ara, Kazi Z G ^a,b   Lundemo, Pontus ^b   Fridjonsson, Olafur H ^c   Hreggvidsson, Gudmundur O ^c   Adlercreutz, Patrick ^b   Karlsson, Eva Nordberg ^b  

^a Biotechnology ^*  (Sweden)

^b Matis ohf Iceland   (Iceland)

^c UNIVERSITY OF ICELAND   (Iceland)

Author keywords

CODEHOP; Coupling; Cyclodextrin glucanotransferase; cyclodextrin

Indexed keywords

CYCLOMALTODEXTRIN GLUCANOTRANSFERASE; DNA 16S; GAMMA CYCLODEXTRIN; BACTERIAL PROTEIN; GAMMA CYCLODEXTRIN DERIVATIVE; GLUCOSYLTRANSFERASE; PROTEIN BINDING;

AMINO ACID SEQUENCE; ARTICLE; CARBOXYDOCELLA; COMPARATIVE STUDY; CYCLIZATION; DEGRADATION; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME ISOLATION; ENZYME PURIFICATION; GENE AMPLIFICATION; GENE ISOLATION; GENE SEQUENCE; GENETIC SCREENING; GLYCOSYLATION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HYDROLYSIS; IMMOBILIZED METAL AFFINITY CHROMATOGRAPHY; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PH; PHYLOGENY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEQUENCE ANALYSIS; TEMPERATURE SENSITIVITY; THERMOPHILIC BACTERIUM; ANAEROBIC BACTERIUM; CHEMISTRY; ENZYMOLOGY; GENETICS; METABOLISM; MOLECULAR GENETICS;

AMINO ACID SEQUENCE; BACTERIA, ANAEROBIC; BACTERIAL PROTEINS; BASE SEQUENCE; GAMMA-CYCLODEXTRINS; GLUCOSYLTRANSFERASES; MOLECULAR SEQUENCE DATA; PROTEIN BINDING;

EID: 84942243886     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cwu182     Document Type: Article

References (90)

1. Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, Miller W, Lipman DJ. 1997. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res. 25: 3389-3402.
2. Atanasova N, Kitayska T, Bojadjieva I, Yankov D, Tonkova A. 2011. A novel cyclodextrin glucanotransferase from alkaliphilic Bacillus pseudalcaliphilus 20RF: Purification and properties. Process Biochem. 46: 116-122.
3. Cao XZ, Jin ZY, Wang X, Chen F. 2005. A novel cyclodextrin glycosyltransferase from an alkalophilic Bacillus species: Purification and characterization. Food Res Int. 38: 309-314.
4. Chotipanang K, Bhunthumnavin W, Prousoontorn MH. 2011. Synthesis of alkyl glycosides from cyclodextrin using cyclodextrin glycosyltransferase from Paenibacillus sp RB01. J Incl Phenom Macro. 70: 359-368.
5. Elias Meezan BAL, Dennis J, Pillion BAL. 1997. Absorption enhancers for drug administration. US: US 4868289 (Sep, 1989) Magnusson et al. 36/4.1; US 5182258 (Jan, 1993) Chiou 514/3; US 5369095 (Nov, 1994) Kee et al. 514/24. Patent US4868289.
6. Felsenstein J. 1985. Confidence-limits on phylogenies - An approach using the bootstrap. Evolution. 39: 783-791.
7. Geer LY, Domrachev M, Lipman DJ, Bryant SH. 2002. CDART: Protein homology by domain architecture. Genome Res. 12: 1619-1623.
8. Hashimoto Y, Yamamoto T, Fujiwara S, Takagi M, Imanaka T. 2001. Extracellular synthesis, specific recognition, and intracellular degradation of cyclomaltodextrins by the hyperthermophilic archaeon Thermococcus sp strain B1001. J Bacteriol. 183: 5050-5057.
9. Ibrahim ASS, Al-Salamah AA, Bahl H. 2011. An alkaliphilic cyclodextrin glycosyltransferase from a new Bacillus agaradhaerens WN-I strain isolated from an Egyptian soda lake: Purification and properties. Afr J Biotechnol. 10: 6107-6119.
10. Ibrahim ASS, Al-Salamah AA, El-Tayeb MA, El-Badawi YB, Antranikian G. 2012. A novel cyclodextrin glycosyltransferase from alkaliphilic Amphibacillus sp NPST-10: Purification and properties. Int J Mol Sci. 13: 10505-10522.
11. Janecek Š, Svensson B, MacGregor EA. 2003. Relation between domain evolution, specificity, and taxonomy of the α-amylase family members containing a C-terminal starch-binding domain. Eur J Biochem. 270: 635-645.
12. Kelly RM, Dijkhuizen L, Leemhuis H. 2009. The evolution of cyclodextrin glucanotransferase product specificity. Appl Microbiol Biot. 84: 119-133.
13. Kim YH, Bae KH, Kim TJ, Park KH, Lee HS, Byun SM. 1997. Effect on product specificity of cyclodextrin glycosyltransferase by site-directed mutagenesis. Biochem Mol Biol Int. 41: 227-234.
14. Kitayska T, Petrova P, Ivanova V, Tonkova AI. 2011. Purification and properties of a new thermostable cyclodextrin glucanotransferase from Bacillus pseudalcaliphilus 8SB. Appl Biochem Biotech. 165: 1285-1295.
15. Krieger E, Koraimann G, Vriend G. 2002. Increasing the precision of comparative models with YASARA NOVA - A self-parameterizing force field. Proteins Struct Funct Bioinf. 47: 393-402.
16. Labes A, Karlsson EN, Fridjonsson OH, Turner P, Hreggvidson GO, Kristjansson JK, Holst O, Schonheit P. 2008. Novel members of glycoside hydrolase family 13 derived from environmental DNA. Appl Environ Microb. 74: 1914-1921.
17. Laemmli UK 1970. Cleavage of structural proteins during assembly of head of bacteriophage-T4. Nature. 227: 680.
18. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, et al. 2007. Clustal W and clustal X version 2.0. Bioinformatics. 23: 2947-2948.
19. le Maire M, Champeil P, Moller JV. 2000. Interaction of membrane proteins and lipids with solubilizing detergents. Biochim Biophys Acta. 1508: 86-111.
20. Leemhuis H, Kelly RM, Dijkhuizen L. 2009. Directed evolution of enzymes: Library screening strategies. IUBMB Life. 61: 222-228.
21. MacGregor EA, Janecek S, Svensson B. 2001. Relationship of sequence and structure to specificity in the alpha-amylase family of enzymes. Biochim Biophys Acta. 1546: 1-20.
22. Martins RF, Hatti-Kaul R. 2002. A new cyclodextrin glycosyltransferase from an alkaliphilic Bacillus agaradhaerens isolate: Purification and characterisation. Enzyme Microb Technol. 30: 116-124.
23. Matsumura S, Imai K, Yoshikawa S, Kawada K, Uchibor T. 1990. Surface activities, biodegradability and antimicrobial properties of N-alkyl glucosides, mannosides and galactosides. J Am Oil Chem Soc. 67: 996-1001.
24. Miller GL 1959. Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem. 31: 426-428.
25. More SS, Niraja R, Evelyn C, Byadgi AM, Shwetha V, Das Mangaraj S. 2012. Isolation, purification and biochemical characterization of CGTase from Bacillus halodurans. Croatian J Food Technol Biotech Nutr. 7: 90-97.
26. Moriwaki C, Ferreira LR, Rodella JRT, Matioli G. 2009. A novel cyclodextrin glycosyltransferase from Bacillus sphaericus strain 41: Production, characterization and catalytic properties. Biochem Eng J. 48: 124-131.
27. Nakagawa Y, Saburi W, Yamamoto T, Takada M, Ogawa K, Yamamoto M, Hatada Y, Nakamura N, Horikoshi K. 2010. Characterization of two γ-cyclodextrin-specific enzymes from Bacillus clarkii 7364. J Appl Glycosci. 57: 121-129.
28. Nakano H, Kiso T, Okamoto K, Tomita T, Manan MBA, Kitahata S. 2003. Synthesis of glycosyl glycerol by cyclodextrin glucanotransferases. J Biosci Bioeng. 95: 583-588.
29. Penninga D, Strokopytov B, Rozeboom HJ, Lawson CL, Dijkstra BW, Bergsma J, Dijkhuizen L. 1995. Site-directed mutations in tyrosine-195 of cyclodextrin glycosyltransferase from Bacillus-circulans strain-251 affect activity and product specificity. Biochemistry. 34: 3368-3376.
30. Penninga D, van der Veen BA, Knegtel RMA, van Hijum SAFT, Rozeboom HJ, Kalk KH, Dijkstra BW, Dijkhuizen L. 1996. The raw starch binding domain of cyclodextrin glycosyltransferase from Bacillus circulans strain 251. J Biol Chem. 271: 32777-32784.
31. Petersen TN, Brunak S, von Heijne G, Nielsen H. 2011. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Meth. 8(10): 785-786.
32. Rose TM, Henikoff JG, Henikoff S. 2003. CODEHOP (consensus-degenerate hybrid oligonucleotide primer) PCR primer design. Nucleic Acids Res. 31: 3763-3766.
33. Saitou N, Nei M. 1987. The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol Biol EVol. 4: 406-425.
34. Saw JH, Mountain BW, Feng L, Omelchenko MV, Hou S, Saito JA, Stott MB, Li D, Zhao G, Wu J, et al. 2008. Encapsulated in silica: Genome, proteome and physiology of the thermophilic bacterium Anoxybacillus flavithermus WK1. Genome Biol. 9: R161.
35. Slobodkina GB, Panteleeva AN, Sokolova TG, Bonch-Osmolovskaya EA, Slobodkin AI. 2012. Carboxydocella manganica sp nov., a thermophilic, dissimilatory Mn(IV)- and Fe(III)-reducing bacterium from a Kamchatka hot spring. Int J Syst Evol Micr. 62: 890-894.
36. Sokolova TG, Kostrikina NA, Chernyh NA, Tourova TP, Kolganova TV, Bonch-Osmolovskaya EA. 2002. Carboxydocella thermautotrophica vgen. nov., sp. nov., a novel anaerobic, CO-utilizing thermophile from a Kamchatkan hot spring. Int J Syst Evol Micr. 52: 1961-1967.
37. Svensson D, Ulvenlund S, Adlercreutz P. 2009a. Efficient synthesis of a long carbohydrate chain alkyl glycoside catalyzed by cyclodextrin glycosyltransferase (CGTase). Biotechnol Bioeng. 104: 854-861.
38. Svensson D, Ulvenlund S, Adlercreutz P. 2009b. Enzymatic route to alkyl glycosides having oligomeric head groups. Green Chemistry. 11: 1222-1226.
39. Szejtli J. 1982. Cyclodextrins in food, cosmetics and toiletries. Starch (Weinheim, Fed. Repub. Ger.). 34: 379-385.
40. Tamura K, Nei M, Kumar S. 2004. Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci USA. 101: 11030-11035.
41. van der Veen BA, Uitdehaag JCM, Penninga D, van Alebeek GJWM, Smith LM, Dijkstra BW, Dijkhuizen L. 2000. Rational design of cyclodextrin glycosyltransferase from Bacillus circulans strain 251 to increase alpha-cyclodextrin production. J Mol Biol. 296: 1027-1038.
42. Vikmon M. 1982. Rapid and simple spectrophotometric method for determination of microamounts of cyclodextrins. Proc First Int Symp Cyclodextrins. J. Szejtli, Springer Netherlands. 1: 69-74.
43. von Rybinski W, Hill K. 1998. Alkyl polyglycosides - Properties and applications of a new class of surfactants. Angew Chem Int Ed Engl. 37: 1328-1345.
44. Wegerer A, Sun TQ, Altenbuchner J. 2008. Optimization of an E. coli L-rhamnose-inducible expression vector: Test of various genetic module combinations. BMC Biotechnol. 8: 1-12.
45. Wind RD, Liebl W, Buitelaar RM, Penninga D, Spreinat A, Dijkhuizen L, Bahl H. 1995. Cyclodextrin formation by the thermostable alpha-amylase of Thermoanaerobacterium Thermosulfurigenes Em1 and reclassification of the enzyme as a cyclodextrin glycosyltransferase. Appl Environ Microb. 61: 1257-1265.
46. Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, Miller W, Lipman DJ. 1997. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res. 25: 3389-3402.
47. Atanasova N, Kitayska T, Bojadjieva I, Yankov D, Tonkova A. 2011. A novel cyclodextrin glucanotransferase from alkaliphilic Bacillus pseudalcaliphilus 20RF: Purification and properties. Process Biochem. 46: 116-122.
48. Cao XZ, Jin ZY, Wang X, Chen F. 2005. A novel cyclodextrin glycosyltransferase from an alkalophilic Bacillus species: Purification and characterization. Food Res Int. 38: 309-314.
49. Chotipanang K, Bhunthumnavin W, Prousoontorn MH. 2011. Synthesis of alkyl glycosides from cyclodextrin using cyclodextrin glycosyltransferase from Paenibacillus sp RB01. J Incl Phenom Macro. 70: 359-368.
50. Elias Meezan BAL, Dennis J, Pillion BAL. 1997. Absorption enhancers for drug administration. US: US 4868289 (Sep, 1989) Magnusson et al. 36/4.1; US 5182258 (Jan, 1993) Chiou 514/3; US 5369095 (Nov, 1994) Kee et al. 514/24. Patent US4868289.
51. Felsenstein J. 1985. Confidence-limits on phylogenies - An approach using the bootstrap. Evolution. 39: 783-791.
52. Geer LY, Domrachev M, Lipman DJ, Bryant SH. 2002. CDART: Protein homology by domain architecture. Genome Res. 12: 1619-1623.
53. Hashimoto Y, Yamamoto T, Fujiwara S, Takagi M, Imanaka T. 2001. Extracellular synthesis, specific recognition, and intracellular degradation of cyclomaltodextrins by the hyperthermophilic archaeon Thermococcus sp strain B1001. J Bacteriol. 183: 5050-5057.
54. Ibrahim ASS, Al-Salamah AA, Bahl H. 2011. An alkaliphilic cyclodextrin glycosyltransferase from a new Bacillus agaradhaerens WN-I strain isolated from an Egyptian soda lake: Purification and properties. Afr J Biotechnol. 10: 6107-6119.
55. Ibrahim ASS, Al-Salamah AA, El-Tayeb MA, El-Badawi YB, Antranikian G. 2012. A novel cyclodextrin glycosyltransferase from alkaliphilic Amphibacillus sp NPST-10: Purification and properties. Int J Mol Sci. 13: 10505-10522.
56. Janecek Š, Svensson B, MacGregor EA. 2003. Relation between domain evolution, specificity, and taxonomy of the α-amylase family members containing a C-terminal starch-binding domain. Eur J Biochem. 270: 635-645.
57. Kelly RM, Dijkhuizen L, Leemhuis H. 2009. The evolution of cyclodextrin glucanotransferase product specificity. Appl Microbiol Biot. 84: 119-133.
58. Kim YH, Bae KH, Kim TJ, Park KH, Lee HS, Byun SM. 1997. Effect on product specificity of cyclodextrin glycosyltransferase by site-directed mutagenesis. Biochem Mol Biol Int. 41: 227-234.
59. Kitayska T, Petrova P, Ivanova V, Tonkova AI. 2011. Purification and properties of a new thermostable cyclodextrin glucanotransferase from Bacillus pseudalcaliphilus 8SB. Appl Biochem Biotech. 165: 1285-1295.
60. Krieger E, Koraimann G, Vriend G. 2002. Increasing the precision of comparative models with YASARA NOVA - A self-parameterizing force field. Proteins Struct Funct Bioinf. 47: 393-402.
61. Labes A, Karlsson EN, Fridjonsson OH, Turner P, Hreggvidson GO, Kristjansson JK, Holst O, Schonheit P. 2008. Novel members of glycoside hydrolase family 13 derived from environmental DNA. Appl Environ Microb. 74: 1914-1921.
62. Laemmli UK 1970. Cleavage of structural proteins during assembly of head of bacteriophage-T4. Nature. 227: 680.
63. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, et al. 2007. Clustal W and clustal X version 2.0. Bioinformatics. 23: 2947-2948.
64. le Maire M, Champeil P, Moller JV. 2000. Interaction of membrane proteins and lipids with solubilizing detergents. Biochim Biophys Acta. 1508: 86-111.
65. Leemhuis H, Kelly RM, Dijkhuizen L. 2009. Directed evolution of enzymes: Library screening strategies. IUBMB Life. 61: 222-228.
66. MacGregor EA, Janecek S, Svensson B. 2001. Relationship of sequence and structure to specificity in the alpha-amylase family of enzymes. Biochim Biophys Acta. 1546: 1-20.
67. Martins RF, Hatti-Kaul R. 2002. A new cyclodextrin glycosyltransferase from an alkaliphilic Bacillus agaradhaerens isolate: Purification and characterisation. Enzyme Microb Technol. 30: 116-124.
68. Matsumura S, Imai K, Yoshikawa S, Kawada K, Uchibor T. 1990. Surface activities, biodegradability and antimicrobial properties of N-alkyl glucosides, mannosides and galactosides. J Am Oil Chem Soc. 67: 996-1001.
69. Miller GL 1959. Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem. 31: 426-428.
70. More SS, Niraja R, Evelyn C, Byadgi AM, Shwetha V, Das Mangaraj S. 2012. Isolation, purification and biochemical characterization of CGTase from Bacillus halodurans. Croatian J Food Technol Biotech Nutr. 7: 90-97.
71. Moriwaki C, Ferreira LR, Rodella JRT, Matioli G. 2009. A novel cyclodextrin glycosyltransferase from Bacillus sphaericus strain 41: Production, characterization and catalytic properties. Biochem Eng J. 48: 124-131.
72. Nakagawa Y, Saburi W, Yamamoto T, Takada M, Ogawa K, Yamamoto M, Hatada Y, Nakamura N, Horikoshi K. 2010. Characterization of two γ-cyclodextrin-specific enzymes from Bacillus clarkii 7364. J Appl Glycosci. 57: 121-129.
73. Nakano H, Kiso T, Okamoto K, Tomita T, Manan MBA, Kitahata S. 2003. Synthesis of glycosyl glycerol by cyclodextrin glucanotransferases. J Biosci Bioeng. 95: 583-588.
74. Penninga D, Strokopytov B, Rozeboom HJ, Lawson CL, Dijkstra BW, Bergsma J, Dijkhuizen L. 1995. Site-directed mutations in tyrosine-195 of cyclodextrin glycosyltransferase from Bacillus-circulans strain-251 affect activity and product specificity. Biochemistry. 34: 3368-3376.
75. Penninga D, van der Veen BA, Knegtel RMA, van Hijum SAFT, Rozeboom HJ, Kalk KH, Dijkstra BW, Dijkhuizen L. 1996. The raw starch binding domain of cyclodextrin glycosyltransferase from Bacillus circulans strain 251. J Biol Chem. 271: 32777-32784.
76. Petersen TN, Brunak S, von Heijne G, Nielsen H. 2011. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Meth. 8(10): 785-786.
77. Rose TM, Henikoff JG, Henikoff S. 2003. CODEHOP (consensus-degenerate hybrid oligonucleotide primer) PCR primer design. Nucleic Acids Res. 31: 3763-3766.
78. Saitou N, Nei M. 1987. The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol Biol EVol. 4: 406-425.
79. Saw JH, Mountain BW, Feng L, Omelchenko MV, Hou S, Saito JA, Stott MB, Li D, Zhao G, Wu J, et al. 2008. Encapsulated in silica: Genome, proteome and physiology of the thermophilic bacterium Anoxybacillus flavithermus WK1. Genome Biol. 9: R161.
80. Slobodkina GB, Panteleeva AN, Sokolova TG, Bonch-Osmolovskaya EA, Slobodkin AI. 2012. Carboxydocella manganica sp nov., a thermophilic, dissimilatory Mn(IV)- and Fe(III)-reducing bacterium from a Kamchatka hot spring. Int J Syst Evol Micr. 62: 890-894.
81. Sokolova TG, Kostrikina NA, Chernyh NA, Tourova TP, Kolganova TV, Bonch-Osmolovskaya EA. 2002. Carboxydocella thermautotrophica vgen. nov., sp. nov., a novel anaerobic, CO-utilizing thermophile from a Kamchatkan hot spring. Int J Syst Evol Micr. 52: 1961-1967.
82. Svensson D, Ulvenlund S, Adlercreutz P. 2009a. Efficient synthesis of a long carbohydrate chain alkyl glycoside catalyzed by cyclodextrin glycosyltransferase (CGTase). Biotechnol Bioeng. 104: 854-861.
83. Svensson D, Ulvenlund S, Adlercreutz P. 2009b. Enzymatic route to alkyl glycosides having oligomeric head groups. Green Chemistry. 11: 1222-1226.
84. Szejtli J. 1982. Cyclodextrins in food, cosmetics and toiletries. Starch (Weinheim, Fed. Repub. Ger.). 34: 379-385.
85. Tamura K, Nei M, Kumar S. 2004. Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci USA. 101: 11030-11035.
86. van der Veen BA, Uitdehaag JCM, Penninga D, van Alebeek GJWM, Smith LM, Dijkstra BW, Dijkhuizen L. 2000. Rational design of cyclodextrin glycosyltransferase from Bacillus circulans strain 251 to increase alpha-cyclodextrin production. J Mol Biol. 296: 1027-1038.
87. Vikmon M. 1982. Rapid and simple spectrophotometric method for determination of microamounts of cyclodextrins. Proc First Int Symp Cyclodextrins. J. Szejtli, Springer Netherlands. 1: 69-74.
88. von Rybinski W, Hill K. 1998. Alkyl polyglycosides - Properties and applications of a new class of surfactants. Angew Chem Int Ed Engl. 37: 1328-1345.
89. Wegerer A, Sun TQ, Altenbuchner J. 2008. Optimization of an E. coli L-rhamnose-inducible expression vector: Test of various genetic module combinations. BMC Biotechnol. 8: 1-12.
90. Wind RD, Liebl W, Buitelaar RM, Penninga D, Spreinat A, Dijkhuizen L, Bahl H. 1995. Cyclodextrin formation by the thermostable alpha-amylase of Thermoanaerobacterium Thermosulfurigenes Em1 and reclassification of the enzyme as a cyclodextrin glycosyltransferase. Appl Environ Microb. 61: 1257-1265.