Genome mining and motif modifications of glycoside hydrolase family 1 members encoded by Geobacillus kaustophilus HTA426 provide thermostable 6-phospho-β-glycosidase and β-fucosidase

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• 作者：Hirokazu Suzuki (1)
  Fumiyoshi Okazaki (1)
  Akihiko Kondo (2)
  Ken-ichi Yoshida (3)
  
• 关键词：β ; Fucosidase ; 6 ; Phospho ; β ; glycosidase ; Thermostable ; Glycoside hydrolase family 1 ; Geobacillus
• 刊名：Applied Microbiology and Biotechnology
• 出版年：2013
• 出版时间：April 2013
• 年：2013
• 卷：97
• 期：7
• 页码：2929-2938
• 全文大小：392KB
• 参考文献：1. Bailey RW, Bourne EJ (1960) Colour reactions given by sugars and diphenylamine-aniline spray reagents on paper chromatograms. J Chromatogr 4(3):206-13. doi:10.1016/S0021-9673(01)98394-3
  2. Barabote RD, Saier MH Jr (2005) Comparative genomic analyses of the bacterial phosphotransferase system. Microbiol Mol Biol Rev 69(4):608-34. doi:10.1128/MMBR.69.4.608-634 CrossRef
  3. Bauer MW, Bylina EJ, Swanson RV, Kelly RM (1996) Comparison of a β-glucosidase and a β-mannosidase from the hyperthermophilic archaeon / Pyrococcus furiosus. J Biol Chem 271(39):23749-3755. doi:10.1074/jbc.271.39.23749 CrossRef
  4. Bene?ová E, Lipovová P, Dvo?áková H, Králová B (2010) β-d -Galactosidase from / Paenibacillus thiaminolyticus catalyzing transfucosylation reactions. Glycobiology 20(4):442-51. doi:10.1093/glycob/cwp196 CrossRef
  5. Cairns JRK, Champattanachai V, Srisomsap C, Wittman-Liebold B, Thiede B, Svasti J (2000) Sequence and expression of Thai Rosewood β-glucosidase/β-fucosidase, a family 1 glycosyl hydrolase glycoprotein. J Biochem 128:999-008 CrossRef
  6. Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B (2009) The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res 37:D233–D238. doi:10.1093/nar/gkn663 CrossRef
  7. Corbett K, Fordham-Skelton AP, Gatehouse JA, Davis BG (2001) Tailoring the substrate specificity of the β-glycosidase from the thermophilic archaeon / Sulfolobus solfataricus. FEBS Lett 509:355-60. doi:10.1016/S0014-5793(01)03154-4 CrossRef
  8. Eijsink VGH, Bj?rk A, G?seidnes S, Sirev?g R, Synstad B, van den Burg B, Vriend G (2004) Rational engineering of enzyme stability. J Biotechnol 113:105-20. doi:10.1016/j.jbiotec.2004.03.026 CrossRef
  9. Giordani R, Noat G (1988) Isolation, molecular properties and kinetics studies of a strict β-fucosidase from / Lactuca sativa latex. Eur J Biochem 175:619-25. doi:10.1111/j.1432-1033.1988.tb14237.x CrossRef
  10. González-Blasco G, Sanz-Aparicio J, González B, Hermoso JA, Polaina J (2000) Directed evolution of β-glucosidase A from / Paenibacillus polymyxa to thermal resistance. J Biol Chem 275(18):13708-3712. doi:10.1074/jbc.275.18.13708 CrossRef
  11. Hancock SM, Corbett K, Fordham-Skelton AP, Gatehouse JA, Davis BG (2005) Developing promiscuous glycosidases for glycoside synthesis: residues W433 and E432 in / Sulfolobus solfataricus β-glycosidase are important glucoside- and galactoside-specificity determinants. Chembiochem 6:866-75. doi:10.1002/cbic.200400341 CrossRef
  12. Harada KM, Tanaka K, Fukuda Y, Hashimoto W, Murata K (2005) Degradation of rice bran hemicellulose by / Paenibacillus sp strain HC1: gene cloning, characterization and function of β-d -glucosidase as an enzyme involved in degradation. Arch Microbiol 184:215-24. doi:10.1007/s00203-005-0038-8 CrossRef
  13. Hengsenberg W, Morse ML (1969) An improved method of synthesis of / o-nitrophenyl β-d -galactopyranoside 6-phosphate. Carbohyd Res 10:463-65. doi:10.1016/S0008-6215(00)80909-X CrossRef
  14. Isorna P, Polaina J, Latorre-García L, Ca?ada FJ, González B, Sanz-Aparicio J (2007) Crystal structures of / Paenibacillus polymyxa β-glucosidase B complexes reveal the molecular basis of substrate specificity and give new insights into the catalytic machinery of family 1 glycosidases. J Mol Biol 371:1204-218. doi:10.1016/j.jmb.2007.05.082 CrossRef
  15. Kaper T, Lebbink JHG, Pouwels J, Kopp J, Schulz GE, van der Oost J, de Vos WM (2000) Comparative structural analysis and substrate specificity engineering of the hyperthermostable β-glucosidase CelB from / Pyrococcus furiosus. Biochemistry 39(17):4963-970. doi:10.1021/bi992463r CrossRef
  16. Kempton JB, Withers SG (1992) Mechanisms of / Agrobacterium β-glucosidase: kinetic studies. Biochemistry 31:9961-969. doi:10.1021/bi00156a015 CrossRef
  17. Kuo LC, Lee KT (2008) Cloning, expression, and characterization of two β-glucosidases from isoflavone glycoside-hydrolyzing / Bacillus subtilis natto. J Agric Food Chem 56(1):119-25. doi:10.1021/jf072287q CrossRef
  18. Marana SR, Jacobs-Lorena M, Terra WR, Ferreira C (2001) Amino acid residues involved in substrate binding and catalysis in an insect digestive β-glycosidase. Biochim Biophys Acta 1545:41-2. doi:10.1016/S0167-4838(00)00260-0 CrossRef
  19. Marques AR, Coutinho PM, Videira P, Fialho AM, Sá-Correia I (2003) / Sphingomonas paucimobilis β-glucosidase Bgl1: a member of a new bacterial subfamily in glycoside hydrolase family 1. Biochem J 370:793-04. doi:10.1042/BJ20021249 CrossRef
  20. Nunoura N, Ohdan K, Tanaka K, Tamaki H, Yano T, Inui M, Yukawa H, Yamamoto K, Kumagai H (1996) Cloning and nucleotide sequence of the β-d -glucosidase gene from / Bifidobacterium breve clb, and expression of β-d -glucosidase activity in / Escherichia coli. Biosci Biotech Biochem 60(12):2011-018 CrossRef
  21. Sanz-Aparicio J, Hermoso JA, Martínez-Ripoll M, Lequerica JL, Polaina J (1998) Crystal structure of β-glucosidase A from / Bacillus polymyxa: insights into the catalytic activity in family 1 glycosyl hydrolases. J Mol Biol 275:491-02. doi:10.1006/jmbi.1997.1467 CrossRef
  22. Scharf ME, Kovaleva ES, Jadhao S, Campbell JH, Buchman GW, Boucias DG (2010) Functional and translational analyses of a beta-glucosidase gene (glycosyl hydrolase family 1) isolated from the gut of the lower termite / Reticulitermes flavipes. Insect Biochem Mol Biol 40:611-20. doi:10.1016/j.ibmb.2010.06.002 CrossRef
  23. Schulte D, Hengstenberg W (2000) Engineering the active center of the 6-phospho-β-galactosidase from / Lactococcus lactis. Protein Eng 13(7):515-18. doi:10.1093/protein/13.7.515 CrossRef
  24. Setlow B, Cabrera-Hernandez A, Cabrera-Martinez RM, Setlow P (2004) Identification of aryl-phospho-β-d -glucosidases in / Bacillus subtilis. Arch Microbiol 181:60-7. doi:10.1007/s00203-003-0628-2 CrossRef
  25. Takami H, Nishi S, Lu J, Shinamura S, Takaki Y (2004a) Genomic characterization of thermophilic / Geobacillus species isolated from the deepest sea mud of the Mariana Trench. Extremophiles 8(5):351-56. doi:10.1007/s00792-004-0394-3 CrossRef
  26. Takami H, Takaki Y, Chee GJ, Nishi S, Shimamura S, Suzuki H, Matsui S, Uchiyama I (2004b) Thermoadaptation trait revealed by the genome sequence of thermophilic / Geobacillus kaustophilus. Nucleic Acids Res 32(21):6292-303. doi:10.1093/nar/gkh970 CrossRef
  27. Trincone A, Nicolaus B, Lama L, Morzillo P, De Rosa M, Gambacorta A (1991) Enzyme-catalyzed synthesis of alkyl β-d -glycosides with crude homogenate of / Sulfolobus solfataricus. Biotechnol Lett 13(4):235-40. doi:10.1007/BF01041476 CrossRef
  28. Wiegel J, Ljungdahl LG (1986) The importance of thermophilic bacteria in biotechnology. Crit Rev Biotechnol 3(1):39-08 CrossRef
  29. Wiesmann C, Hengstenberg W, Schulz GE (1997) Crystal structures and mechanism of 6-phospho-β-galactosidase from / Lactococcus lactis. J Mol Biol 269:851-60. doi:10.1006/jmbi.1997.1084 CrossRef
  30. Wilson G, Fox CF (1974) The β-glucoside system in / Escherichia coli. J Biol Chem 249(17):5586-598. doi:10.1016/0168-6445(89)90018-1
  31. Witt E, Frank R, Hengstenberg W (1993) 6-Phospho-β-galactosidases of Gram-positive and 6-phospho-β-glucosidase B of Gram-negative bacteria: comparison of structure and function by kinetic and immunological methods and mutagenesis of the / lacG gene of / Staphylococcus aureus. Protein Eng 6(8):913-20. doi:10.1093/protein/6.8.913 CrossRef
  32. Yip VLY, Withers SG (2006) Mechanistic analysis of the unusual redox-elimination sequence employed by / Thermotoga maritima BgIT: a 6-phospho-β-glucosidase from glycoside hydrolase family 4. Biochemistry 45:571-80. doi:10.1021/bi052054x CrossRef
  33. Yoshida S, Park DS, Bae B, Mackie R, Cann IKO, Nair SK (2011) Structural and functional analyses of a glycoside hydrolase family 5 enzyme with an unexpected β-fucosidase activity. Biochemistry 50:3369-375. doi:10.1021/bi200222u CrossRef
  34. Zechel DL, Withers SG (2000) Glycosidase mechanisms: anatomy of a finely tuned catalyst. Acc Chem Res 33:11-8. doi:10.1021/ar970172 CrossRef
  
• 作者单位：Hirokazu Suzuki (1)
  Fumiyoshi Okazaki (1)
  Akihiko Kondo (2)
  Ken-ichi Yoshida (3)
  
  1. Organization of Advanced Science and Technology, Kobe University, 1-1 Rokkodaicho, Nada-ku, Kobe, Hyogo, 657-8501, Japan
  2. Department of Chemical Science and Engineering, Graduate School of Engineering, Kobe University, 1-1 Rokkodaicho, Nada-ku, Kobe, Hyogo, 657-8501, Japan
  3. Department of Agrobioscience, Graduate School of Agricultural Science, Kobe University, 1-1 Rokkodaicho, Nada-ku, Kobe, Hyogo, 657-8501, Japan
  
• ISSN：1432-0614

文摘

Members of glycoside hydrolase family 1 (GH1) hydrolyze various glycosides and are widely distributed in organisms. With the aim of producing thermostable GH1 catalysts with potential applications in biotechnology, three GH1 members encoded by the thermophile Geobacillus kaustophilus HTA426 (GK1856, GK2337, and GK3214) were characterized using 24 p-nitrophenyl glycosides as substrates. GK1856 and GK3214 exhibited 6-phospho-β-glycosidase activity, while GK2337 did not. GK3214 was extremely thermostable and retained most of its activity during 7?days of incubation at 60?°C. GK3214 was found to have transglycosylation activity, a dimeric structure, and a possible motif that governed its substrate specificity. Substitution of the GK3214 motif with that of a β-glucosidase resulted in the unexpected generation of a thermostable, highly specific β-fucosidase, concomitant with large increases in β-glucosidase, β-cellobiosidase, α-arabinofuranosidase, β-mannosidase, β-glucuronidase, β-xylopyranosidase, and β-fucosidase activities and a dramatic decline in 6-phospho-β-glycosidase activity. This is the first report to identify a gene encoding thermostable 6-phospho-β-glycosidase and to generate a thermostable β-fucosidase. These results provided thermostable enzyme catalysts and also suggested a promising approach to develop novel GH1 biocatalysts.