Dissecting structure-function-stability relationships of a thermostable GH5-CBM3 cellulase from Bacillus subtilis 168

Biochemical Journal

Volumn 441, Issue 1, 2012, Pages 95-104

  Santos, Camila R ^a   Paiva, Joice H ^a   Sforça, Maurício L ^a   Neves, Jorge L ^a   Navarro, Rodrigo Z ^a   Cota, Júnio ^b   Akao, Patrícia K ^a   Hoffmam, Zaira B ^b   Meza, Andréia N ^a   Smetana, Juliana H ^a   Nogueira, Maria L ^a   Polikarpov, Igor ^c   Xavier Neto, José ^a   Squina, Fábio M ^b   Ward, Richard J ^c   Ruller, Roberto ^b   Zeri, Ana C ^a   Murakami, Mário T ^a  

^a BRAZILIAN CENTER FOR RESEARCH IN ENERGY AND MATERIALS CNPEM   (Brazil)

^b BRAZILIAN CENTER FOR RESEARCH IN ENERGY AND MATERIALS CNPEM   (Brazil)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Accessory domain; Carbohydrate binding module; Cellulase 5A; Kinetics; Structure; Thermal stability

Indexed keywords

CARBOHYDRATE BINDING PROTEIN; CELLULASE; GLYCOSIDASE; GLYCOSIDE HYDROLASE 5; UNCLASSIFIED DRUG;

ARTICLE; BACILLUS SUBTILIS; CATALYSIS; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME STABILITY; ENZYME STRUCTURE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN MOTIF; THERMOSTABILITY; X RAY CRYSTALLOGRAPHY;

BACILLUS SUBTILIS; BACTERIAL PROTEINS; CALCIUM; CELLULASES; CLONING, MOLECULAR; GENE EXPRESSION REGULATION, BACTERIAL; HOT TEMPERATURE; KINETICS; MANGANESE; MODELS, MOLECULAR; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; SUBSTRATE SPECIFICITY;

EID: 84055185201     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20110869     Document Type: Article

References (66)

1. Farrell, A. E., Plevin, R. J., Turner, B. T., Jones, A. D., O'Hare, M. and Kammen, D. M. (2006) Ethanol can contribute to energy and environmental goals. Science 311, 506-508 (Pubitemid 43157725)
2. Lynd, L. R., Laser, M. S., Bransby, D., Dale, B. E., Davison, B., Hamilton, R., Himmel, M., Keller, M., McMillan, J. D., Sheehan, J. and Wyman, C. E. (2008) How biotech can transform biofuels. Nat. Biotechnol. 26, 169-172 (Pubitemid 351225943)
3. Binder, J. B. and Raines, R. T. (2010) Fermentable sugars by chemical hydrolysis of biomass. Proc. Natl. Acad. Sci. U.S.A. 107, 4516-4521
4. Shaw, A. J., Podkaminer, K. K., Desai, S. G., Bardsley, J. S., Rogers, S. R., Thorne, P. G., Hogsett, D. A. and Lynd, L. R. (2008) Metabolic engineering of a thermophilic bacterium to produce ethanol at high yield. Proc. Natl. Acad. Sci. U.S.A. 105, 13769-13774
5. Margeot, A., Hahn-Hagerdal, B., Edlund, M., Slade, R. and Monot, F. (2009) New improvements for lignocellulosic ethanol. Curr. Opin. Biotechnol. 20, 372-380
6. Wen, F., Nair, N. U. and Zhao, H. (2009) Protein engineering in designing tailored enzymes and microorganisms for biofuels production. Curr. Opin. Biotechnol. 20, 412-419
7. Heinzelman, P., Snow, C. D., Wu, I., Nguyen, C., Villalobos, A., Govindarajan, S., Minshull, J. and Arnold, F. H. (2009) A family of thermostable fungal cellulases created by structure-guided recombination. Proc. Natl. Acad. Sci. U.S.A. 106, 5610-5615
8. Moraïs, S., Heyman, A., Barak, Y., Caspi, J., Wilson, D. B., Lamed, R., Shoseyov, O. and Bayer, E. A. (2010) Enhanced cellulose degradation by nano-complexed enzymes: synergism between a scaffold-linked exoglucanase and a free endoglucanase. J. Biotechnol. 147, 205-211
9. van der Veen, B. A., Skov, L. K., Potocki-Véronèse, G., Gajhede, M., Monsan, P. and Remaud-Simeon, M. (2006) Increased amylosucrase activity and specificity, and identification of regions important for activity, specificity and stability through molecular evolution. FEBS J. 273, 673-681
10. Liu, M., Wang, J., Liu, J., Yao, J. and Yu, Z. (2006) Expression of Bacillus subtilis JA18 endo-β-1,4-glucanase gene in Escherichia coli and characterization of the recombinant enzyme. Ann. Microbiol. 56, 41-45
11. Li, W., Zhang, W. W., Yang, M. M. and Chen, Y. L. (2008) Cloning of the thermostable cellulase gene from newly isolated Bacillus subtilis and its expression in Escherichia coli. Mol. Biotechnol. 40, 195-201
12. Li, W., Huan, X., Zhou, Y., Ma, Q. and Chen, Y. (2009) Simultaneous cloning and expression of two cellulase genes from Bacillus subtilis newly isolated from Golden Takin (Budorcas taxicolor Bedfordi). Biochem. Biophys. Res. Commun. 383, 397-400
13. Wang, Y., Yuan, H., Wang, J. and Yu, Z. (2009) Truncation of the cellulose binding domain improved thermal stability of endo-β-1,4-glucanase from Bacillus subtilis JA18. Bioresour. Technol. 100, 345-349
14. Yang, D., Weng, H., Wang, M., Xu, W., Li, Y. and Yang, H. (2010) Cloning and expression of a novel thermostable cellulase from newly isolated Bacillus subtilis strain I15. Mol. Biol. Rep. 37, 1923-1929
15. Deka, D., Bhargavi, P., Sharma, A., Goyal, D., Jawed, M. and Goyal, A. (2011) Enhancement of cellulase activity from a new strain of Bacillus subtilis by medium optimization and analysis with various cellulosic substrates. Enzyme Res. 2011, 151656
16. Liao, H., Zhang, X. Z., Rollin, J. A. and Zhang, Y. H. (2011) A minimal set of bacterial cellulases for consolidated bioprocessing of lignocellulose. Biotechnol. J., doi:10.1002/biot.201100157
17. Zhang, X. Z. and Zhang, Y. H. (2011) Simple, fast and high-efficiency transformation system for directed evolution of cellulase in Bacillus subtilis. Microb. Biotechnol. 4, 98-105
18. Wolf, M., Geczi, A., Simon, O. and Borriss, R. (1995) Genes encoding xylan and β-glucan hydrolysing enzymes in Bacillus subtilis: characterization, mapping and construction of strains deficient in lichenase, cellulase and xylanase. Microbiology 141, 281-290
19. Boraston, A. B., Bolam, D. N., Gilbert, H. J. and Davies, G. J. (2004) Carbohydrate-binding modules: fine-tuning polysaccharide recognition. Biochem. J. 382, 769-781 (Pubitemid 39312891)
20. Shoseyov, O., Shani, Z. and Levy, I. (2006) Carbohydrate binding modules: biochemical properties and novel applications. Microbiol. Mol. Biol. Rev. 70, 283-295 (Pubitemid 43895029)
21. Hashimoto, H. (2006) Recent structural studies of carbohydrate-binding modules. Cell. Mol. Life Sci. 63, 2954-2967
22. Fontes, C. M., Hazlewood, G. P., Morag, E., Hall, J., Hirst, B. H. and Gilbert, H. J. (1995) Evidence for a general role for non-catalytic thermostabilizing domains in xylanases from thermophilic bacteria. Biochem J. 307, 151-158
23. Winterhalter, C., Heinrich, P., Candussio, A., Wich, G. and Liebl, W. (1995) Identification of a novel cellulose-binding domain within the multidomain 120 kDa xylanase XynA of the hyperthermophilic bacterium Thermotoga maritima . Mol. Microbiol. 15, 431-444
24. Irwin, D., Shin, D. H., Zhang, S., Barr, B. K., Sakon, J., Karplus, P.A and Wilson, D. B. (1998) Roles of the catalytic domain and two cellulose binding domains of Thermomonospora fusca E4 in cellulose hydrolysis. J. Bacteriol. 180, 1709-1714 (Pubitemid 28173048)
25. Kataeva, I. A., Blum, D. L., Li, X. L. and Ljungdahl, L. G. (2001) Do domain interactions of glycosyl hydrolases from Clostridium thermocellum contribute to protein thermostability? Protein Eng. 14, 167-172 (Pubitemid 32487970)
26. Xie, H., Gilbert, H. J., Charnock, S. J., Davies, G. J., Williamson, M. P., Simpson, P. J., Raghothama, S., Fontes, C. M., Dias, F. M., Ferreira, L. M. and Bolam, D. N. (2001) Clostridium thermocellum Xyn10B carbohydrate-binding module 22-2: the role of conserved amino acids in ligand binding. Biochemistry 40, 9167-9176 (Pubitemid 32730038)
27. Shin, E. S., Yang, M. J., Jung, K. H., Kwon, E. J., Jung, J. S., Park, S. K., Kim, J., Yun, H. D. and Kim, H. (2002) Influence of the transposition of the thermostabilizing domain of Clostridium thermocellum xylanase (XynX) on xylan binding and thermostabilization. Appl. Environ. Microbiol. 68, 3496-3501 (Pubitemid 34734050)
28. Zhao, G., Ali, E., Araki, R., Sakka, M., Kimura, T. and Sakka, K. (2005) Function of the family-9 and family-22 carbohydrate-binding modules in a modular β-1,3-1,4-glucanase/xylanase derived from Clostridium stercorarium Xyn10B. Biosci. Biotechnol. Biochem. 69, 1562-1567 (Pubitemid 41207347)
29. Zhang, S., Yin, Q. Y., Li, Y. H., Ding, M., Xu, G. J. and Zhao, F. K. (2007) Molecular and biochemical characterization of Ba-EGA, a cellulase secreted by Bacillus sp. AC-1 from Ampullaria crosseans. Appl. Microbiol. Biotechnol. 75, 1327-1334 (Pubitemid 46976676)
30. Sunna, A. (2010) Modular organisation and functional analysis of dissected modular β-mannanase CsMan26 from Caldicellulosiruptor Rt8B.4. Appl. Microbiol. Biotechnol. 86, 189-200
31. Kittur, F. S., Mangala, S. L., Rus'd, A. A., Kitaoka, M., Tsujibo, H. and Hayashi, K. (2003) Fusion of family 2b carbohydrate-binding module increases the catalytic activity of a xylanase from Thermotoga maritima to soluble xylan. FEBS Lett. 549, 147-151 (Pubitemid 36959860)
32. Mahadevan, S. A., Wi, S. G., Lee, D. S. and Bae, H. J. (2008) Site-directed mutagenesis and CBM engineering of Cel5A (Thermotoga maritima) . FEMS Microbiol. Lett. 287, 205-211
33. Mamo, G., Hatti-Kaul, R. and Mattiasson, B. (2007) Fusion of carbohydrate binding modules from Thermotoga neapolitana with a family 10 xylanase from Bacillus halodurans S7. Extremophiles 11, 169-177 (Pubitemid 46089640)
34. Zhang, Y., Chen, S., Xu, M., Cavaco-Paulo, A., Wu, J. and Chen, J. (2010) Characterization of Thermobifida fusca cutinase-carbohydrate-binding module fusion proteins and their potential application in bioscouring. Appl. Environ. Microbiol. 76, 6870-6876
35. Sonan, G. K., Receveur-Brechot, V., Duez, C., Aghajari, N., Czjzek, M., Haser, R. and Gerday, C. (2007) The linker region plays a key role in the adaptation to cold of the cellulase from an Antarctic bacterium. Biochem. J. 407, 293-302 (Pubitemid 47556994)
36. Morris, D. D., Gibbs, M. D., Chin, C. W., Koh, M. H., Wong, K.K, Allison, R.W, Nelson, P. J. and Bergquist, P. L. (1998) Cloning of the xynB gene from Dictyoglomus thermophilum Rt46B.1 and action of the gene product on kraft pulp. Appl. Environ. Microbiol. 64, 1759-1765 (Pubitemid 28234781)
37. Blanco, A., Díaz, P., Zueco, J., Parascandola, P. and Javier Pastor, F. I. (1999) A multidomain xylanase from aBacillus sp. with a region homologous to thermostabilizing domains of thermophilic enzymes. Microbiology 145, 2163-2170 (Pubitemid 29396947)
38. Li, M. X., Corson, D. C. and Sykes, B. D. (2002) Structure determination by NMR isotope labeling. Methods Mol. Biol. 173, 255-265
39. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685
40. Miller, G. L. (1959) Use of dinitrosalicyIic acid reagent for determination of reducing sugar. Anal. Chem. 31, 426-42
41. Myers, R. H. and Montgomery, D. C. (2002) Response Surface Methodology: Process and Product Optimization Using Designed Experiments (2nd edn), John Wiley & Sons, New York
42. Hammersley, A. P., Brown, K., Burmeister, W., Claustre, L., Gonzalez, A., McSweeney, S., Mitchell, E., Moy, J. P., Svensson, S. O. and Thompson, A. W. (1997) Calibration and application of an X-ray image intensifier/charge-coupled device detector for monochromatic macromolecular crystallography. J. Synchrotron Radiat. 4, 67-77
43. Svergun, D. I. (1992) Determination of the regularization parameter in indirect-transform methods using perceptual criteria. J. Appl. Crystallogr. 25, 495-503
44. Svergun, D. I. (1999) Restoring low resolution structure of biological macromolecules from solution scattering using simulated annealing. Biophys. J. 76, 2879-2886
45. Volkov, V. V. and Svergun, D. I. (2003) Uniqueness of ab initio shape determination in small-angle scattering. J. Appl. Crystallogr. 36, 860-864
46. Kozin, M. B. and Svergun, D. I. (2000) Automated matching of high- and low-resolution structural models. J. Appl. Crystallogr. 34, 33-41 (Pubitemid 32151714)
47. Petoukhov, M. V. and Svergun, D. I. (2005) Global rigid body modelling of macromolecular complexes against small-angle scattering data. Biophys. J. 89, 1237-1250 (Pubitemid 41099005)
48. Svergun, D. I., Barberato, C. and Koch, M. H.J. (1995) CRYSOL-a program to evaluate X-ray solution scattering of biological macromolecules from atomic coordinates. J. Appl. Crystallogr. 28, 768-773 (Pubitemid 3014671)
49. Piotto, M., Saudek, V. and Sklenar, V. (1992) Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solutions. J. Biomol. NMR 2, 661-665
50. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J. and Bax, A. (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6, 277-293
51. Johnson, B. A. and Blevins, R. A. (1994) NMRView: a computer program for the visualization and analysis of NMR data. J. Biomol. NMR 4, 603-614
52. Sattler, M., Schleucher, J. and Griesinger, C. (1999) Heteronuclear multidimensional NMR experiments for the structure determination of proteins in solution employing pulsed field gradients. Prog. Nucl. Magn. Reson. Spectrosc. 34, 93-158 (Pubitemid 129595216)
53. Guntert, P., Mumenthaler, C. and Wuthrich, K. (1997) Torsion angle dynamics for NMR structure calculation with the new program DYANA. J. Mol. Biol. 273, 283-298 (Pubitemid 27460230)
54. Brunger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J.-S., Kuszewski, J., Nilges, M., Panuu, N. S. et al. (1998) Crystallography and NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54, 905-921
55. Laskowski, R. A., Rullmannn, J. A., MacArthur, M. W., Kaptein, R. and Thornton, J. M. (1996) AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J. Biomol. NMR 8, 477-486 (Pubitemid 126706801)
56. Otwinowski, Z. and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326 (Pubitemid 27085611)
57. Vagin, A. and Teplyakov, A. (2010) Molecular replacement with MOLREP. Acta Crystallogr. D Biol. Crystallogr. 66, 22-25
58. Murshudov, G. N., Vagin, A. A. and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240-255 (Pubitemid 27235885)
59. Emsley, P. and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (Pubitemid 41742764)
60. Vogt, G., Woell, S. and Argos, P. (1997) Protein thermal stability, hydrogen bonds, and ion pairs. J. Mol. Biol. 269, 631-643 (Pubitemid 27267875)
61. Bayer, E. A., Chanzy, H., Lamed, R. and Shoham, Y. (1998) Cellulose, cellulases and cellulosomes. Curr. Opin. Struct. Biol. 8, 548-557 (Pubitemid 28486379)
62. Jindou, S., Xu, Q., Kenig, R., Shulman, M., Shoham, Y., Bayer, E. A. and Lamed, R. (2006) Novel architecture of family-9 glycoside hydrolases identified in cellulosomal enzymes of Acetivibrio cellulolyticus and Clostridium thermocellum. FEMS Microbiol. Lett. 254, 308-316
63. Tormo, J., Lamed, R., Chirino, A. J., Morag, E., Bayer, E. A., Shoham, Y. and Steitz, T. A. (1996) Crystal structure of a bacterial family-III cellulose-binding domain: a general mechanism for attachment to cellulose. EMBO J. 15, 5739-5751 (Pubitemid 26375495)
64. Shaw, A., Bott, R., Vonrhein, C., Bricogne, G., Power, S. and Day, A. G. (2002) A novel combination of two classic catalytic schemes. J. Mol. Biol. 320, 303-309 (Pubitemid 34722220)
65. Pereira, J. H., Chen, Z., McAndrew, R. P., Sapra, R., Chhabra, S. R., Sale, K. L., Simmons, B. A. and Adams, P. D. (2010) Biochemical characterization and crystal structure of endoglucanase Cel5A from the hyperthermophilic Thermotoga maritima. J. Struct. Biol. 172, 372-329
66. Varrot, A., Frandsen, T. P., Driguez, H. and Davies, G. J. (2002) Structure of the Humicola insolens cellobiohydrolase Cel6A D416A mutant in complex with a non-hydrolysable substrate analogue, methyl cellobiosyl-4-thio- β-cellobioside, at 1.9 Å. Acta Crystallogr. D Biol. Crystallogr. 58, 2201-2204 (Pubitemid 35450863)