Structural, biochemical, and computational characterization of the glycoside hydrolase family 7 cellobiohydrolase of the tree-killing fungus heterobasidion irregulare

Journal of Biological Chemistry

Volumn 288, Issue 8, 2013, Pages 5861-5872

  Momeni, Majid Haddad ^a   Payne, Christina M ^b,d   Hansson, Henrik ^a   Mikkelsen, Nils Egil ^a   Svedberg, Jesper ^a   Engström, Ake ^e   Sandgren, Mats ^a   Beckham, Gregg T ^c,f   Stahlberg, Jerry ^a  

^a SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^b Chemical and Biosciences Center   (United States)

^c NATIONAL RENEWABLE ENERGY LABORATORY   (United States)

^d UNIVERSITY OF KENTUCKY   (United States)

^e UPPSALA UNIVERSITY   (Sweden)

^f Department of Geology and Geological Engineering   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELLOBIOHYDROLASES; CELLULOSE DEGRADATION; DISSOCIATION RATES; GLYCOSIDE HYDROLASES; HETEROBASIDION; HYPOCREA; PHANEROCHAETE CHRYSOSPORIUM; PROCESSIVITY;

CARBOHYDRATES; DISSOCIATION;

CELLULOSE;

CELLULOSE; CELLULOSE 1,4 BETA CELLOBIOSIDASE; GLUCAN SYNTHASE; GLYCOSIDASE; TYROSINE;

ARTICLE; BINDING SITE; BIOCHEMISTRY; BIOMASS; CRYSTAL STRUCTURE; DISSOCIATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME BINDING; ENZYME STRUCTURE; ENZYME SUBSTRATE; FUNGAL GENOME; FUNGUS CULTURE; FUNGUS GROWTH; HETEROBASIDIOMYCETES; HETEROBASIDION IRREGULARE; HYPOCREA JECORINA; LIGAND BINDING; MOLECULAR DYNAMICS; MOLECULAR MODEL; NONHUMAN; PHANEROCHAETE; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN INTERACTION; SOLVATION; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; BINDING SITES; BIOFUELS; CELLULASE; CELLULOSE; CELLULOSE 1,4-BETA-CELLOBIOSIDASE; COMPUTER SIMULATION; CRYSTALLOGRAPHY, X-RAY; GLYCOSIDE HYDROLASES; HYDROGEN-ION CONCENTRATION; HYDROLYSIS; HYPOCREA; LIGANDS; MOLECULAR CONFORMATION; MOLECULAR SEQUENCE DATA; PHANEROCHAETE; SEQUENCE HOMOLOGY, AMINO ACID; TREES; TRICHODERMA;

EID: 84874318103     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.440891     Document Type: Article

References (63)

1. Woodward, S. (1998) Heterobasidion annosum: Biology, Ecology, Impact and Control (S. Woodward, J. S., R. Karjalainen and A. Hüttermann, eds) pp. 589, CAB International, Wallingford, UK
2. Olson, A., Aerts, A., Asiegbu, F., Belbahri, L., Bouzid, O., Broberg, A., Canbäck, B., Coutinho, P. M., Cullen, D., Dalman, K., Deflorio, G., van Diepen, L. T., Dunand, C., Duplessis, S., Durling, M., Gonthier, P., Grimwood, J., Fossdal, C. G., Hansson, D., Henrissat, B., Hietala, A., Himmelstrand, K., Hoffmeister, D., Högberg, N., James, T. Y., Karlsson, M., Kohler, A., Kües, U., Lee, Y. H., Lin, Y. C., Lind, M., Lindquist, E., Lombard, V., Lucas, S., Lundén, K., Morin, E., Murat, C., Park, J., Raffaello, T., Rouzé, P., Salamov, A., Schmutz, J., Solheim, H., Ståhlberg, J., Vélëz, H., de Vries, R. P., Wiebenga, A., Woodward, S., Yakovlev, I., Garbelotto, M., and Martin, F. (2012) Insight into trade-off between wood decay and parasitism from the genome of a fungal forest pathogen. New Phytol. 194, 1001-1013
3. 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, D233-238
4. Lynd, L. R., Weimer, P. J., van Zyl, W. H., and Pretorius, I. S. (2002) Microbial cellulose utilization. Fundamentals and biotechnology. Microbiol. Mol. Biol. Rev. 66, 506-577
5. Medie, F. M., Davies, G. J., Drancourt, M., and Henrissat, B. (2012) Genome analyses highlight the different biological roles of cellulases. Nat. Rev. Microbiol. 10, 227-234
6. Horn, S. J., Vaaje-Kolstad, G., Westereng, B., and Eijsink, V. G. (2012) Novel enzymes for the degradation of cellulose. Biotechnol. Biofuels 5, 45
7. Yakovlev, I., Vaaje-Kolstad, G., Hietala, A. M., Stefanczyk, E., Solheim, H., and Fossdal, C. G. (2012) Substrate-specific transcription of the enigmatic GH61 family of the pathogenic white-rot fungus Heterobasidion irregulare during growth on lignocellulose. Appl. Microbiol. Biotechnol. 95, 979-990
8. Ilmén, M., Saloheimo, A., Onnela, M. L., and Penttilä, M. E. (1997) Regulation of cellulase gene expression in the filamentous fungus Trichoderma reesei. Appl. Environ. Microbiol. 63, 1298-1306
9. Uzcategui, E., Ruiz, A., Montesino, R., Johansson, G., and Pettersson, G. (1991) The 1,4-β-D-glucan cellobiohydrolases from Phanerochaete chrysosporium. I. A system of synergistically acting enzymes homologous to Trichoderma reesei. J. Biotechnol. 19, 271-285
10. King, A. J., Cragg, S. M., Li, Y., Dymond, J., Guille, M. J., Bowles, D. J., Bruce, N. C., Graham, I. A., and McQueen-Mason, S. J. (2010) Molecular insight into lignocellulose digestion by a marine isopod in the absence of gut microbes. Proc. Natl. Acad. Sci. U.S.A. 107, 5345-5350
11. 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
12. Stals, I., Sandra, K., Geysens, S., Contreras, R., Van Beeumen, J., and Claeyssens, M. (2004) Factors influencing glycosylation of Trichoderma reesei cellulases. I. Postsecretorial changes of theO-andN-glycosylation pattern of Cel7A. Glycobiology 14, 713-724
13. Harrison, M. J., Nouwens, A. S., Jardine, D. R., Zachara, N. E., Gooley, A. A., Nevalainen, H., and Packer, N. H. (1998) Modified glycosylation of cellobiohydrolase I from a high cellulase-producing mutant strain of Trichoderma reesei. Eur. J. Biochem. 256, 119-127
14. Sammond, D. W., Payne, C. M., Brunecky, R., Himmel, M. E., Crowley, M. F., and Beckham, G. T. (2012) Cellulase linkers are optimized based on domain type and function. Insights from sequence analysis, biophysical measurements, and molecular simulation. PLoS One 7, e48615
15. Beckham, G. T., Bomble, Y. J., Matthews, J. F., Taylor, C. B., Resch, M. G., Yarbrough, J. M., Decker, S. R., Bu, L., Zhao, X., McCabe, C., Wohlert, J., Bergenstråhle, M., Brady, J. W., Adney, W. S., Himmel, M. E., and Crowley, M. F. (2010) The O-glycosylated linker from the Trichoderma reesei family 7 cellulase is a flexible, disordered protein. Biophys. J. 99, 3773-3781
16. Divne, C., Ståhlberg, J., Reinikainen, T., Ruohonen, L., Pettersson, G., Knowles, J. K., Teeri, T. T., and Jones, T. A. (1994) The three-dimensional crystal structure of the catalytic core of cellobiohydrolase I from Trichoderma reesei. Science 265, 524-528
17. Divne, C., Ståhlberg, J., Teeri, T. T., and Jones, T. A. (1998) High-resolution crystal structures reveal how a cellulose chain is bound in the 50 angstrom long tunnel of cellobiohydrolase I from Trichoderma reesei. J. Mol. Biol. 275, 309-325
18. Munoz, I. G., Ubhayasekera, W., Henriksson, H., Szabó, I., Pettersson, G., Johansson, G., Mowbray, S. L., and Ståhlberg, J. (2001) Family 7 cellobiohydrolases from Phanerochaete chrysosporium. Crystal structure of the catalytic module of Cel7D (CBH58) at 1.32 Å resolution and homology models of the isozymes. J. Mol. Biol. 314, 1097-1111
19. Parkkinen, T., Koivula, A., Vehmaanperä, J., and Rouvinen, J. (2008) Crystal structures of Melanocarpus albomyces cellobiohydrolase Cel7B in complex with cello-oligomers show high flexibility in the substrate binding. Protein Sci. 17, 1383-1394
20. Grassick, A., Murray, P. G., Thompson, R., Collins, C. M., Byrnes, L., Birrane, G., Higgins, T. M., and Tuohy, M. G. (2004) Three-dimensional structure of a thermostable native cellobiohydrolase, CBH IB, and molecular characterization of the cel7 gene from the filamentous fungus, Talaromyces emersonii. Eur. J. Biochem. 271, 4495-4506
21. Textor, L. C., Colussi, F., Silveira, R. L., Serpa, V., de Mello, B. L., Muniz, J. R., Squina, F. M., Pereira, N., Jr., Skaf, M. S., and Polikarpov, I. (2013) Joint x-ray crystallographic and molecular dynamics study of cellobiohydrolase I from Trichoderma harzianum. Deciphering the structural features of cellobiohydrolase catalytic activity. FEBS J. 280, 56-69
22. Kleywegt, G. J., Zou, J. Y., Divne, C., Davies, G. J., Sinning, I., Ståhlberg, J., Reinikainen, T., Srisodsuk, M., Teeri, T. T., and Jones, T. A. (1997) The crystal structure of the catalytic core domain of endoglucanase I from Trichoderma reesei at 3.6 Å resolution, and a comparison with related enzymes. J. Mol. Biol. 272, 383-397
23. MacKenzie, L. F., Sulzenbacher, G., Divne, C., Jones, T. A., Wöldike, H. F., Schülein, M., Withers, S. G., and Davies, G. J. (1998) Crystal structure of the family 7 endoglucanase I (Cel7B) from Humicola insolens at 2.2 angstrom resolution and identification of the catalytic nucleophile by trapping of the covalent glycosyl-enzyme intermediate. Biochem. J. 335, 409-416
24. Sulzenbacher, G., Driguez, H., Henrissat, B., Schülein, M., and Davies, G. J. (1996) Structure of the Fusarium oxysporum endoglucanase I with a nonhydrolyzable substrate analogue. Substrate distortion gives rise to the preferred axial orientation for the leaving group. Biochemistry 35, 15280-15287
25. Beckham, G. T., Matthews, J. F., Peters, B., Bomble, Y. J., Himmel, M. E., and Crowley, M. F. (2011) Molecular-level origins of biomass recalcitrance. Decrystallization free energies for four common cellulose polymorphs. J. Phys. Chem. B 115, 4118-4127
26. Chundawat, S. P., Beckham, G. T., Himmel, M. E., and Dale, B. E. (2011) Deconstruction of lignocellulosic biomass to fuels and chemicals. Annu. Rev. Chem. Biomol. Eng. 2, 121-145
27. Igarashi, K., Koivula, A., Wada, M., Kimura, S., Penttilä, M., and Samejima, M. (2009) High speed atomic force microscopy visualizes processive movement of Trichoderma reesei cellobiohydrolase I on crystalline cellulose. J. Biol. Chem. 284, 36186-36190
28. Kurasin, M., and Väljamäe, P. (2011) Processivity of cellobiohydrolases is limited by the substrate. J. Biol. Chem. 286, 169-177
29. Igarashi, K., Uchihashi, T., Koivula, A., Wada, M., Kimura, S., Okamoto, T., Penttilä, M., Ando, T., and Samejima, M. (2011) Traffic jams reduce hydrolytic efficiency of cellulase on cellulose surface. Science 333, 1279-1282
30. Boisset, C., Fraschini, C., Schülein, M., Henrissat, B., and Chanzy, H. (2000) Imaging the enzymatic digestion of bacterial cellulose ribbons reveals the endo character of the cellobiohydrolase Cel6A from Humicola insolens and its mode of synergy with cellobiohydrolase Cel7A. Appl. Environ. Microbiol. 66, 1444-1452
31. Ståhlberg, J., Divne, C., Koivula, A., Piens, K., Claeyssens, M., Teeri, T. T., and Jones, T. A. (1996) Activity studies and crystal structures of catalytically deficient mutants of cellobiohydrolase I from Trichoderma reesei. J. Mol. Biol. 264, 337-349
32. von Ossowski, I., Ståhlberg, J., Koivula, A., Piens, K., Becker, D., Boer, H., Harle, R., Harris, M., Divne, C., Mahdi, S., Zhao, Y., Driguez, H., Claeyssens, M., Sinnott, M. L., and Teeri, T. T. (2003) Engineering the exo-loop of Trichoderma reesei cellobiohydrolase, Cel7A.Acomparison with Phanerochaete chrysosporium Cel7D. J. Mol. Biol. 333, 817-829
33. Beckham, G. T., Bomble, Y. J., Bayer, E. A., Himmel, M. E., and Crowley, M. F. (2011) Applications of computational science for understanding enzymatic deconstruction of cellulose. Curr. Opin. Biotechnol. 22, 231-238
34. Beckham, G. T., Matthews, J. F., Bomble, Y. J., Bu, L., Adney, W. S., Himmel, M. E., Nimlos, M. R., and Crowley, M. F. (2010) Identification of amino acids responsible for processivity in a family 1 carbohydrate-binding module from a fungal cellulase. J. Phys. Chem. B 114, 1447-1453
35. Bu, L., Beckham, G. T., Crowley, M. F., Chang, C. H., Matthews, J. F., Bomble, Y. J., Adney, W. S., Himmel, M. E., and Nimlos, M. R. (2009) The energy landscape for the interaction of the family 1 carbohydrate-binding module and the cellulose surface is altered by hydrolyzed glycosidic bonds. J. Phys. Chem. B 113, 10994-11002
36. Taylor, C. B., Talib, M. F., McCabe, C., Bu, L., Adney, W. S., Himmel, M. E., Crowley, M. F., and Beckham, G. T. (2012) Computational investigation of glycosylation effects on a family 1 carbohydrate-binding module. J. Biol. Chem. 287, 3147-3155
37. Nimlos, M. R., Beckham, G. T., Matthews, J. F., Bu, L., Himmel, M. E., and Crowley, M. F. (2012) Binding preferences, surface attachment, diffusivity, and orientation of a family 1 carbohydrate-binding module on cellulose. J. Biol. Chem. 287, 20603-20612
38. Bu, L., Nimlos, M. R., Shirts, M. R., Ståhlberg, J., Himmel, M. E., Crowley, M. F., and Beckham, G. T. (2012) Product binding varies dramatically between processive and nonprocessive cellulase enzymes. J. Biol. Chem. 287, 24807-24813
39. Bu, L., Beckham, G. T., Shirts, M. R., Nimlos, M. R., Adney, W. S., Himmel, M. E., and Crowley, M. F. (2011) Probing carbohydrate product expulsion from a processive cellulase with multiple absolute binding free energy methods. J. Biol. Chem. 286, 18161-18169
40. Stenlid, J. (1985) Population-structure of Heterobasidion annosum as determined by somatic incompatibility, sexual incompatibility, and isoenzyme patterns. Can. J. Bot. 63, 2268-2273
41. Kremer, S. M., Wood, P. M. (1992) Evidence that cellobiose oxidase from Phanerochaete chrysosporium is primarily an Fe(III) reductase. Kinetic comparison with neutrophil NADPH oxidase and yeast flavocytochrome b2. Eur. J. Biochem. 205, 133-138
42. Shevchenko, A., Wilm, M., Vorm, O., and Mann, M. (1996) Mass spectrometric sequencing of proteins from silver stained polyacrylamide gels. Anal. Chem. 68, 850-858
43. Grigoriev, I. V., Nordberg, H., Shabalov, I., Aerts, A., Cantor, M., Goodstein, D., Kuo, A., Minovitsky, S., Nikitin, R., Ohm, R. A., Otillar, R., Poliakov, A., Ratnere, I., Riley, R., Smirnova, T., Rokhsar, D., and Dubchak, I. (2011) The genome portal of the Department Of Energy Joint Genome Institute. Nucleic Acids Res., 1-7
44. McPherson, A. (1982) Preparation and Analysis of Protein Crystals, John Wiley & Sons, New York
45. Bailey, S. (1994) The CCP4 suite. Programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50, 760-763
46. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007) Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674
47. Murshudov, G. N., Skubák, P., Lebedev, A. A., Pannu, N. S., Steiner, R. A., Nicholls, R. A., Winn, M. D., Long, F., and Vagin, A. A. (2011) REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr. D Biol. Crystallogr. 67, 355-367
48. Guex, N., and Peitsch, M. C. (1997) SWISS-MODEL and the Swiss-PDBViewer. An environment for comparative protein modeling. Electrophoresis 18, 2714-2723
49. Emsley, P., and Cowtan, K. (2004) COOT. Model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr 60, 2126-2132
50. Ubhayasekera, W., Munoz, I. G., Vasella, A., Ståhlberg, J., and Mowbray, S. L. (2005) Structures of Phanerochaete chrysosporium Cel7D in complex with product and inhibitors. FEBS J. 272, 1952-1964
51. Payne, C. M., Baban, J., Horn, S. J., Backe, P. H., Arvai, A. S., Dalhus, B., Bjørås, M., Eijsink, V. G., Sørlie, M., Beckham, G. T., and Vaaje-Kolstad, G. (2012) Hallmarks of processivity in glycoside hydrolases from crystallographic and computational studies of the Serratia marcescens chitinases. J. Biol. Chem. 287, 36322-36330
52. Cruys-Bagger, N., Elmerdahl, J., Praestgaard, E., Tatsumi, H., Spodsberg, N., Borch, K., and Westh, P. (2012) Pre-steady-state kinetics for hydrolysis of insoluble cellulose by cellobiohydrolase Cel7A. J. Biol. Chem. 287, 18451-18458
53. Jalak, J., and Väljamäe, P. (2010) Mechanism of initial rapid rate retardation in cellobiohydrolase catalyzed cellulose hydrolysis. Biotechnol. Bioeng. 106, 871-883
54. Ståhlberg, J., Johansson, G., and Pettersson, G. (1993) Trichoderma reesei has no true exo-cellulase. All intact and truncated cellulases produce new reducing end groups on cellulose. Biochim. Biophys. Acta 1157, 107-113
55. Fox, J. M., Levine, S. E., Clark, D. S., and Blanch, H. W. (2012) Initial-and processive-cut products reveal cellobiohydrolase rate limitations and the role of companion enzymes. Biochemistry 51, 442-452
56. Gruno, M., Väljamäe, P., Pettersson, G., and Johansson, G. (2004) Inhibition of the Trichoderma reesei cellulases by cellobiose is strongly dependent on the nature of the substrate. Biotechnol. Bioeng. 86, 503-511
57. Horn, S. J., Sikorski, P., Cederkvist, J. B., Vaaje-Kolstad, G., Sørlie, M., Synstad, B., Vriend, G., Vårum, K. M., and Eijsink, V. G. (2006) Costs and benefits of processivity in enzymatic degradation of recalcitrant polysaccharides. Proc. Natl. Acad. Sci. U.S.A. 103, 18089-18094
58. Horn, S. J., Sørbotten, A., Synstad, B., Sikorski, P., Sørlie, M., Vårum, K. M., and Eijsink, V. G. (2006) Endo/exo mechanism and processivity of family 18 chitinases produced by Serratia marcescens. FEBS J. 273, 491-503
59. Payne, C. M., Bomble, Y. J., Taylor, C. B., McCabe, C., Himmel, M. E., Crowley, M. F., and Beckham, G. T. (2011) Multiple functions of aromaticcarbohydrate interactions in a processive cellulase examined with molecular simulation. J. Biol. Chem. 286, 41028-41035
60. van Aalten, D. M., Synstad, B., Brurberg, M. B., Hough, E., Riise, B. W., Eijsink, V. G., and Wierenga, R. K. (2000) Structure of a two-domain chitotriosidase from Serratia marcescens at 1.9 Å resolution. Proc. Natl. Acad. Sci. U.S.A. 97, 5842-5847
61. Koivula, A., Kinnari, T., Harjunpaa, V., Ruohonen, L., Teleman, A., Drakenberg, T., Rouvinen, J., Jones, T. A., and Teeri, T. T. (1998) Tryptophan 272. An essential determinant of crystalline cellulose degradation by Trichoderma reesei cellobiohydrolase Cel6A. FEBS Lett. 429, 341-346
62. Jalak, J., Kurasin, M., Teugjas, H., and Väljamäe, P. (2012) Endo-exo synergism in cellulose hydrolysis revisited. J. Biol. Chem. 287, 28802-28815
63. Lin, Y., Silvestre-Ryan, J., Himmel, M. E., Crowley, M. F., Beckham, G. T., and Chu, J.-W. (2011) Protein allostery at the solid-liquid interface. Endoglucanase attachment to cellulose affects glucan clenching in the binding cleft. J. Am. Chem. Soc. 133, 16617-16624