Crystal structures of glycoside hydrolase family 3 β-glucosidase 1 from Aspergillus aculeatus

Biochemical Journal

Volumn 452, Issue 2, 2013, Pages 211-221

  Suzuki, Kentaro ^a   Sumitani, Jun Ichi ^b   Nam, Young Woo ^a   Nishimaki, Toru ^b   Tani, Shuji ^b   Wakagi, Takayoshi ^a   Kawaguchi, Takashi ^b   Fushinobu, Shinya ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b Osaka Prefecture University   (Japan)

Author keywords

glucosidase; Biorefinery; Cellulase; Glycoside hydrolase family 3; N glycan; Protein glycosylation

Indexed keywords

BETA GLUCOSIDASE; DIMER; FIBRONECTIN; GLYCOSIDASE; OLIGOSACCHARIDE;

ARTICLE; ASPERGILLUS ACULEATUS; BIOMASS; CRYSTAL STRUCTURE; ENZYME ACTIVITY; ENZYME BINDING; GENE INSERTION; GLYCOSYLATION; HYDROPHOBICITY; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN DOMAIN; STRUCTURE ANALYSIS;

ASPERGILLUS; BETA-GLUCOSIDASE; CARBOHYDRATE CONFORMATION; CARBOHYDRATE SEQUENCE; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; FUNGAL PROTEINS; GLYCOSYLATION; LIGANDS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; POLYSACCHARIDES; PROTEIN CONFORMATION;

EID: 84877757413     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20130054     Document Type: Article

References (63)

1. Ragauskas, A. J., Williams, C. K., Davison, B. H., Britovsek, G., Cairney, J., Eckert, C. A., Frederick, Jr, W. J., Hallett, J. P., Leak, D. J., Liotta, C. L. et al. (2006) The path forward for biofuels and biomaterials. Science 311, 484-489
2. Kamm, B. and Kamm, M. (2007) Biorefineries: multi product processes. Adv. Biochem. Eng. Biotechnol. 105, 175-204
3. Himmel, M. E., Ding, S. Y., Johnson, D. K., Adney, W. S., Nimlos, M. R., Brady, J. W. and Foust, T. D. (2007) Biomass recalcitrance: engineering plants and enzymes for biofuels production. Science 315, 804-807
4. Nakari-Setala, T., Paloheimo, M., Kallio, J., Vehmaanpera, J., Penttila, M. and Saloheimo, M. (2009) Genetic modification of carbon catabolite repression in Trichoderma reesei for improved protein production. Appl. Environ. Microbiol. 75, 4853-4860
5. van den Brink, J. and de Vries, R. P. (2011) Fungal enzyme sets for plant polysaccharide degradation. Appl. Microbiol. Biotechnol. 91, 1477-1492
6. Kubicek, C. P. (1981) Release of carboxymethylcellulose and β-glucosidase from cell walls of Trichoderma reesei. Eur. J. Appl. Miciobiol. Biotechnol. 13, 226-231
7. Xin, Z., Yinbo, Q. and Peiji, G. (1993) Acceleration of ethanol production from paper mill waste fiber by supplementation with beta-glucosidase. Enzyme Microb. Technol. 15, 62-65
8. Berlin, A., Maximenko, V., Gilkes, N. and Saddler, J. (2007) Optimization of enzyme complexes for lignocellulose hydrolysis. Biotechnol. Bioeng. 97, 287-296
9. Chen, M., Zhao, J. and Xia, L. (2008) Enzymatic hydrolysis of maize straw polysaccharides for the production of reducing sugars. Carbohydr. Polym. 71, 411-415
10. Barnett, C. C., Berka, R. M. and Fowler, T. (1991) Cloning and amplification of the gene encoding an extracellular beta-glucosidase from Trichoderma reesei: evidence for improved rates of saccharification of cellulosic substrates. Biotechnology 9, 562-567
11. Rahman, Z., Shida, Y., Furukawa, T., Suzuki, Y., Okada, H., Ogasawara, W. and Morikawa, Y. (2009) Application of Trichoderma reesei cellulase and xylanase promoters through homologous recombination for enhanced production of extracellular β-glucosidase I. Biosci. Biotechnol. Biochem. 73, 1083-1089
12. Nakazawa, H., Kawai, T., Ida, N., Shida, Y., Kobayashi, Y., Okada, H., Tani, S., Sumitani, J., Kawaguchi, T., Morikawa, Y. and Ogasawara, W. (2012) Construction of a recombinant Trichoderma reesei strain expressing Aspergillus aculeatus β-glucosidase 1 for efficient biomass conversion. Biotechnol. Bioeng. 109, 92-99
13. Sternberg, D., Vijayakumar, P. and Reese, E. T. (1977) β-Glucosidase: microbial production and effect on enzymatic hydrolysis of cellulose. Can. J. Microbiol. 23, 139-147
14. Chauve, M., Mathis, H., Huc, D., Casanave, D., Monot, F. and Lopes Ferreira, N. (2010) Comparative kinetic analysis of two fungal β-glucosidases. Biotechnol. Biofuels. 3, 3
15. Sakamoto, R., Kanamoto, J., Arai, M. and Murao, S. (1985) Purification and physicochemical properties of three β-glucosidases from Aspergillus aculeatus No. F-50. Agric. Biol. Chem. 49, 1275-1281
16. Sakamoto, R., Arai, M. and Murao, S. (1985) Enzymic properties of three β-glucosidases from Aspergillus aculatus No. F-50. Agric. Biol. Chem. 49, 1283-1290
17. Murao, S., Sakamoto, R. and Arai, M. (1988) Cellulases of Aspergillus aculeatus. Methods Enzymol. 160C, 274-299
18. Kawai, T., Nakazawa, H., Ida, N., Okada, H., Tani, S., Sumitani, J., Kawaguchi, T., Ogasawara, W., Morikawa, Y. and Kobayashi, Y. (2012) Analysis of the saccharification capability of high-functional cellulase JN11 for various pretreated biomasses through a comparison with commercially available counterparts. J. Ind. Microbiol. Biotechnol. 39, 1741-1749
19. Murai, T., Ueda, M., Kawaguchi, T., Arai, M. and Tanaka, A. (1998) Assimilation of cellooligosaccharides by a cell surface-engineered yeast expressing β-glucosidase and carboxymethylcellulase from Aspergillus aculeatus. Appl. Environ. Microbiol. 64, 4857-4861
20. Fujita, Y., Takahashi, S., Ueda, M., Tanaka, A., Okada, H., Morikawa, Y., Kawaguchi, T., Arai, M., Fukuda, H. and Kondo, A. (2002) Direct and efficient production of ethanol from cellulosic material with a yeast strain displaying cellulolytic enzymes. Appl. Environ. Microbiol. 68, 5136-5141
21. Fujita, Y., Ito, J., Ueda, M., Fukuda, H. and Kondo, A. (2004) Synergistic saccharification, and direct fermentation to ethanol, of amorphous cellulose by use of an engineered yeast strain codisplaying three types of cellulolytic enzyme. Appl. Environ. Microbiol. 70, 1207-1212
22. Tokuhiro, K., Ishida, N., Kondo, A. and Takahashi, H. (2008) Lactic fermentation of cellobiose by a yeast strain displaying β-glucosidase on the cell surface. Appl. Microbiol. Biotechnol. 79, 481-488
23. Ito, J., Kosugi, A., Tanaka, T., Kuroda, K., Shibasaki, S., Ogino, C., Ueda, M., Fukuda, H., Doi, R. H. and Kondo, A. (2009) Regulation of the display ratio of enzymes on the Saccharomyces cerevisiae cell surface by the immunoglobulin G and cellulosomal enzyme binding domains. Appl. Environ. Microbiol. 75, 4149-4154
24. Yanase, S., Yamada, R., Kaneko, S., Noda, H., Hasunuma, T., Tanaka, T., Ogino, C., Fukuda, H. and Kondo, A. (2010) Ethanol production from cellulosic materials using cellulase-expressing yeast. Biotechnol. J. 5, 449-455
25. Yanase, S., Hasunuma, T., Yamada, R., Tanaka, T., Ogino, C., Fukuda, H. and Kondo, A. (2010) Direct ethanol production from cellulosic materials at high temperature using the thermotolerant yeast Kluyveromyces marxianus displaying cellulolytic enzymes. Appl. Microbiol. Biotechnol. 88, 381-388
26. Sakamoto, T., Hasunuma, T., Hori, Y., Yamada, R. and Kondo, A. (2012) Direct ethanol production from hemicellulosic materials of rice straw by use of an engineered yeast strain codisplaying three types of hemicellulolytic enzymes on the surface of xylose-utilizing Saccharomyces cerevisiae cells. J. Biotechnol. 158, 203-210
27. Okano, K., Zhang, Q., Yoshida, S., Tanaka, T., Ogino, C., Fukuda, H. and Kondo, A. (2010) D-Lactic acid production from cellooligosaccharides and beta-glucan using L-LDH gene-deficient and endoglucanase-secreting Lactobacillus plantarum. Appl. Microbiol. Biotechnol. 85, 643-650
28. Tsuchidate, T., Tateno, T., Okai, N., Tanaka, T., Ogino, C. and Kondo, A. (2011) Glutamate production from β-glucan using endoglucanase-secreting Corynebacterium glutamicum. Appl. Microbiol. Biotechnol. 90, 895-901
29. Kim, H. W. and Ishikawa, K. (2010) Complete saccharification of cellulose at high temperature using endocellulase and β-glucosidase from Pyrococcus sp. J. Microbiol. Biotechnol. 20, 889-892
30. Cantarel, B. L., Coutinho, P. M., Rancurel, C., Bernard, T., Lombard, V. and Henrissat, B. (2009) The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res. 37, D233-D238
31. Kawaguchi, T., Enoki, T., Tsurumaki, S., Sumitani, J., Ueda, M., Ooi, T. and Arai, M. (1996) Cloning and sequencing of the cDNA encoding β-glucosidase 1 from Aspergillus aculeatus. Gene 173, 287-288
32. Litzinger, S., Fischer, S., Polzer, P., Diederichs, K., Welte, W. and Mayer, C. (2010) Structural and kinetic analysis of Bacillus subtilis N-acetylglucosaminidase reveals a unique Asp-His dyad mechanism. J. Biol. Chem. 285, 35675-35684
33. Varghese, J. N., Hrmova, M. and Fincher, G. B. (1999) Three-dimensional structure of a barley β-D-glucan exohydrolase, a family 3 glycosyl hydrolase. Structure 7, 179-190
34. Pozzo, T., Pasten, J. L., Karlsson, E. N. and Logan, D. T. (2010) Structural and functional analyses of β-glucosidase 3B from Thermotoga neapolitana : a thermostable three-domain representative of glycoside hydrolase 3. J. Mol. Biol. 397, 724-739
35. Yoshida, E., Hidaka, M., Fushinobu, S., Koyanagi, T., Minami, H., Tamaki, H., Kitaoka, M., Katayama, T. and Kumagai, H. (2010) Role of a PA14 domain in determining substrate specificity of a glycoside hydrolase family 3 β-glucosidase from Kluyveromyces marxianus. Biochem. J. 431, 39-49
36. Nakatani, Y., Cutfield, S. M., Cowieson, N. P. and Cutfield, J. F. (2012) Structure and activity of exo-1,3/1,4-β-glucanase from marine bacterium Pseudoalteromonas sp. BB1 showing a novel C-terminal domain. FEBS J. 279, 464-478
37. Harvey, A. J., Hrmova, M., De Gori, R., Varghese, J. N. and Fincher, G. B. (2000) Comparative modeling of the three-dimensional structures of family 3 glycoside hydrolases. Proteins 41, 257-269
38. Cournoyer, B. and Faure, D. (2003) Radiation and functional specialization of the family-3 glycoside hydrolases. J. Mol. Microbiol. Biotechnol. 5, 190-198
39. Minetoki, T., Tsuboi, H., Koda, A. and Ozeki, K. (2003) Development of high expression system with the improved promoter using the cis-acting element in Aspergillus species. J. Biol. Macromol. 3, 89-96
40. Kanamasa, S., Takada, G., Kawaguchi, T., Sumitani, J. and Arai, M. (2001) Overexpression and purification of Aspergillus aculeatus β-mannosidase and analysis of the integrated gene in Aspergillus oryzae. J. Biosci. Bioeng. 92, 131-137
41. Rashid, M. H., Javed, M. R., Kawaguchi, T., Sumitani, J. and Arai, M. (2008) Improvement of Aspergillus oryzae for hyperproduction of endoglucanase: expression cloning of cmc-1 gene of Aspergillus aculeatus. Biotechnol. Lett. 30, 2165-2172
42. Otwinowski, Z. and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326
43. Vagin, A. and Teplyakov, A. (1997) MOLREP: an automated program for molecular replacement. J. Appl. Cryst. 30, 1022-1025
44. Perrakis, A., Morris, R. and Lamzin, V. S. (1999) Automated protein model building combined with iterative structure refinement. Nat. Struct. Biol. 6, 458-463
45. Emsley, P., Lohkamp, B., Scott, W. G. and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr., Sect. D: Biol. Crystallogr. 66, 486-501
46. Murshudov, G. N., Vagin, A. A. and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr., Sect. D: Biol. Crystallogr. 53, 240-255
47. Krissinel, E. and Henrick, K. (2007) Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 372, 774-797
48. Holm, L. and Sander, C. (1995) Dali: a network tool for protein structure comparison. Trends Biochem. Sci. 20, 478-480
49. Chiba, Y., Yamagata, Y., Nakajima, T. and Ichishima, E. (1992) A new high-mannose type N-linked oligosaccharide from Aspergillus carboxypeptidase. Biosci. Biotechnol. Biochem. 56, 1371-1372
50. Archer, D. B. and Peberdy, J. F. (1997) The molecular biology of secreted enzyme production by fungi. Crit. Rev. Biotechnol. 17, 273-306
51. Kainz, E., Gallmetzer, A., Hatzl, C., Nett, J. H., Li, H., Schinko, T., Pachlinger, R., Berger, H., Reyes-Dominguez, Y., Bernreiter, A. et al. (2008) N-glycan modification in Aspergillus species. Appl. Environ. Microbiol. 74, 1076-1086
52. Aleshin, A. E., Hoffman, C., Firsov, L. M. and Honzatko, R. B. (1994) Refined crystal structures of glucoamylase from Aspergillus awamori var. X100. J. Mol. Biol. 238, 575-591
53. Petersen, T. N., Kauppinen, S. and Larsen, S. (1997) The crystal structure of rhamnogalacturonase A from Aspergillus aculeatus: a right-handed parallel β-helix. Structure 5, 533-544
54. Davies, G. and Henrissat, B. (1995) Structures and mechanisms of glycosyl hydrolases. Structure 3, 853-859
55. Dan, S., Marton, I., Dekel, M., Bravdo, B. A., He, S., Withers, S. G. and Shoseyov, O. (2000) Cloning, expression, characterization, and nucleophile identification of family 3, Aspergillus niger β-glucosidase. J. Biol. Chem. 275, 4973-4980
56. Thongpoo, P., McKee, L. S., Araujo, A. C., Kongsaeree, P. T. and Brumer, H. (2012) Identification of the acid/base catalyst of a glycoside hydrolase family 3 (GH3) β-glucosidase from Aspergillus niger ASKU28. Biochim. Biophys. Acta 1830, 2739-2749
57. 262 is a key residue for the hydrolytic and transglucosidic reactivity of the Aspergillus niger family 3 beta-glucosidase: substitution results in enzymes with mainly transglucosidic activity. Arch. Biochem. Biophys. 444, 66-75
58. Seidle, H. F., Marten, I., Shoseyov, O. and Huber, R. E. (2004) Physical and kinetic properties of the family 3 beta-glucosidase from Aspergillus niger which is important for cellulose breakdown. Protein J. 23, 11-23
59. Seidle, H. F. and Huber, R. E. (2005) Transglucosidic reactions of the Aspergillus niger family 3 β-glucosidase: qualitative and quantitative analyses and evidence that the transglucosidic rate is independent of pH. Arch. Biochem. Biophys. 436, 254-264
60. Langston, J., Sheehy, N. and Xu, F. (2006) Substrate specificity of Aspergillus oryzae family 3 β-glucosidase. Biochim. Biophys. Acta 1764, 972-978
61. Hrmova, M., De Gori, R., Smith, B. J., Fairweather, J. K., Driguez, H., Varghese, J. N. and Fincher, G. B. (2002) Structural basis for broad substrate specificity in higher plant β-D-glucan glucohydrolases. Plant Cell 14, 1033-1052
62. Hrmova, M., Varghese, J. N., De Gori, R., Smith, B. J., Driguez, H. and Fincher, G. B. (2001) Catalytic mechanisms and reaction intermediates along the hydrolytic pathway of a plant β-D-glucan glucohydrolase. Structure 9, 1005-1016
63. Stubbs, K. A., Balcewich, M., Mark, B. L. and Vocadlo, D. J. (2007) Small molecule inhibitors of a glycoside hydrolase attenuate inducible AmpC-mediated β-lactam resistance. J. Biol. Chem. 282, 21382-21391