Competitive sorption kinetics of inhibited endo- and exoglucanases on a model cellulose substrate

Langmuir

Volumn 28, Issue 41, 2012, Pages 14598-14608

  Maurer, Samuel A ^a   Bedbrook, Claire N ^a   Radke, Clayton J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BULK CONCENTRATION; CELLOBIOHYDROLASE I; CELLOBIOHYDROLASES; CELLULOSE HYDROLYSIS; CELLULOSE SUBSTRATES; CELLULOSE SURFACES; COMPETITIVE ADSORPTION; COMPETITIVE SORPTION; COOPERATIVE ACTIVITY; DESORPTION RATE CONSTANTS; ENDOGLUCANASE I; ENDOGLUCANASES; ENZYME CONCENTRATIONS; EXOGLUCANASE; FIRST-ORDER; IRREVERSIBLE BINDING; LANGMUIR KINETICS; MULTICOMPONENTS; QUARTZ CRYSTAL MICROGRAVIMETRY; SURFACE SITES; TIME-SCALES;

ADSORPTION; DESORPTION; ENZYMES; QUARTZ CRYSTAL MICROBALANCES; RATE CONSTANTS;

CELLULOSE;

CELLULASE; CELLULOSE; CELLULOSE 1,4 BETA CELLOBIOSIDASE;

ADSORPTION; ARTICLE; CHEMICAL MODEL; CHEMISTRY; DRUG ANTAGONISM; ENZYME SPECIFICITY; ENZYMOLOGY; HYDROLYSIS; KINETICS; METABOLISM; SURFACE PROPERTY; TRICHODERMA;

ADSORPTION; CELLULASES; CELLULOSE; CELLULOSE 1,4-BETA-CELLOBIOSIDASE; HYDROLYSIS; KINETICS; MODELS, CHEMICAL; SUBSTRATE SPECIFICITY; SURFACE PROPERTIES; TRICHODERMA;

EID: 84867519662     PISSN: 07437463     EISSN: 15205827     Source Type: Journal    
DOI: 10.1021/la3024524     Document Type: Article

References (53)

1. Himmel, M.; Ding, S. Y.; Johnson, D. K.; Adney, W. S.; Nimlos, M. R.; Brady, J. W.; Foust, T. D. Biomass Recalcitrance: Engineering Plants and Enzymes for Biofuels Production Science 2007, 315, 804-807
2. Beguin, P.; Aubert, J. P. The Biological Degradation of Cellulose FEMS Microbiol. Rev. 1994, 13, 25-58
3. Wyman, C. E. Ethanol from Lignocellulosic Biomass: Technology, Economics, and Opportunities Bioresour. Technol. 1994, 50, 3-16
4. Houghton, J.; Weatherwax, S.; Ferrell, J. Breaking the Biological Barriers to Cellulosic Ethanol: A Joint Research Agenda. DOE/SC-0095: U.S. DOE: Washington, DC, 2005.
5. Macmillan, J. D. Bioethanol Production: Status and Prospects Renewable Energy 1997, 2-3, 295-302
6. Pauly, M.; Keegstra, K. Cell-Wall Carbohydrates and Their Modification as a Resource for Biofuels Plant J. 2008, 54, 559-568
7. Kumar, R.; Singh, S.; Singh, O. V. Bioconversion of Lignocellulosic Biomass: Biochemical and Molecular Perspectives J Ind. Microbiol. Biotechnol. 2008, 35, 377-391
8. Bai, F. W.; Anderson, W. A.; Moo-Young, M. Ethanol Fermentation Technologies from Sugar to Starch Feedstocks Biotechnol. Adv. 2008, 26, 89-105
9. Kontturi, E.; Tammelin, T.; Österberg, M. Cellulose-Model Films and the Fundamental Approach Chem Soc Rev 2006, 35, 1287-1313
10. Lee, S. B.; Shin, H. S.; Ryu, D. D. Y.; Mandels, M. Adsorption of Cellulase on Cellulose: Effect of Physicochemical Properties of Cellulose on Adsorption and Rate of Hydrolysis Biotechnol. Bioeng. 1982, 24, 2137-2153
11. Abdmziem, K.; Passas, R.; Belgacem, M. N. Inverse Gas Chromatography as a Tool to Characterize the Specific Surface Area of Cellulose Fibers Cell Chem. Technol. 2006, 40, 199-204
12. Maurer, S. A.; Bedbrook, C. N.; Radke, C. J. Cellulase Adsorption and Reactivity on a Cellulose Surface from Flow Ellipsometry Ind. Eng. Chem. Res. 2012, 51, 11389-11400
13. Gunnars, S.; Wågberg, L.; Stuart, M. A. C. Model Films of Cellulose: I. Method Development and Initial Results Cellulose 2002, 9, 239-249
14. Falt, S.; Wågberg, L.; Vesterlind, E. L.; Larsson, P. T. Model Films of Cellulose II-Improved Preparation Method and Characterization of the Cellulose Film Cellulose 2004, 11, 151-162
15. Eriksson, J.; Malmsten, M.; Tiberg, F.; Callisen, T. H.; Damhus, T.; Johansen, K. S. Enzymatic Degradation of Model Cellulose Films J. Colloid Interface Sci. 2005, 284, 99-106
16. Turon, X.; Rojas, O. J.; Deinhammer, R. S. Enzymatic Kinetics of Cellulose Hydrolysis: A QCM-D Study Langmuir 2008, 24, 3880-3887
17. Josefsson, P.; Henriksson, G.; Wågberg, L. The Physical Action of Cellulases Revealed by a Quartz Crystal Microbalance Study Using Ultrathin Cellulose Films and Pure Cellulases Biomacromolecules 2008, 9, 249-254
18. Ahola, S.; Turon, X.; Österberg, M.; Laine, J.; Rojas, O J. Enzymatic Hydrolysis of Native Cellulose Nanofibrils and Other Cellulose Model Films: Effect of Surface Structure Langmuir 2008, 24, 11592-11599
19. Hu, G.; Heitmann, J. A.; Rojas, O. J. In Situ Monitoring of Cellulase Activity by Microgravimetry with a Quartz Crystal Microbalance J. Phys. Chem. B 2009, 113, 14761-14768
20. Hu, G.; Heitmann, J. A.; Rojas, O. J. Quantification of Cellulase Activity Using the Quartz Crystal Microbalance Technique Anal. Chem. 2009, 81, 1872-1880
21. Suchy, M.; Linder, M. B.; Tammelin, T.; Campbell, J. M.; Vuorinen, T.; Kontturi, E. Quantitative Assessment of the Enzymatic Degradation of Amorphous Cellulose by Using a Quartz Crystal Microbalance with Dissipation Monitoring Langmuir 2011, 27, 8819-8828
22. Andersen, M.; Johansson, L. S.; Tanem, B. S.; Stenius, P. Properties and Characterization of Hydrophobized Microfibrillated Cellulose Cellulose 2006, 13, 665-677
23. Mohan, T.; Kargl, R.; Doliska, A.; Vesel, A.; Kostler, S.; Ribitsch, V.; Stana-Kleinschek, K. Wettability and Surface Composition of Partly and Fully Regenerated Cellulose Thin Films from Trimethylsilyl Cellulose J. Colloid Interface Sci. 2011, 358, 604-610
24. Habibi, Y.; Foulon, L.; Aguie-Beghin, V.; Molinari, M.; Douillard, R. Langmuir-Blodgett Films of Cellulose Nanocrystals: Preparation and Characterization J. Colloid Interface Sci. 2007, 316, 388-397
25. Cheng, G.; Liu, Z.; Murton, J. K.; Jablin, M.; Dubey, M.; Majewski, K.; Halbert, C.; Browning, J.; Ankner, J.; Akgun, B.; Wang, C.; Esker, A. R.; Sale, K. L.; Simmons, B. A.; Kent, M. S. Neutron Reflectometry and QCM-D Study of the Interaction of Cellulases With Films of Amorphous Cellulose Biomacromolecules 2011, 12, 2216-24
26. O'Sullivan, A. C. Cellulose: The Structure Slowly Unravels Cellulose 1997, 4, 173-207
27. Gross, A.; Chu, J.-W. On the Molecular Origins of Biomass Recalcitrance: The Interaction Network and Solvation Structures of Cellulose Microfibrils J. Phys. Chem. B 2010, 114, 13333
28. Cho, H. M.; Gross, A.; Chu, J.-W. Dissecting Force Interactions in Cellulose Deconstruction Reveals the Required Solvent Versatility for Overcoming Biomass Recalcitrance J. Am. Chem. Soc. 2011, 133, 14033-14041
29. Zhang, Y. H. P.; Himmel, M. E.; Mielenz, J. Outlook for Cellulase Improvement: Screening and Selection Strategies Biotechnol. Adv. 2005, 24, 452-481
30. Zhang, Y. H. P.; Lynd, L. R. A Functionally Based Model for Hydrolysis of Cellulose by Fungal Cellulase Biotechnol. Bioeng. 2006, 94, 889-898
31. Fox, J. M.; Levine, S. E.; Blanch, H. W.; Clark, D. S. Initial- and Processive-Cut Products Reveal Cellobiohydrolase Rate Limitations and the Role of Companion Enzymes Biochemistry. 2012, 51, 442-452
32. Xu, F.; Ding, H. A New Kinetic Model for Heterogeneous (Or Spatially Confined) Enzymatic Catalysis: Contributions from the Fractal and Jamming (Overcrowding) Effects Appl. Catal., A 2007, 317, 70-81
33. Linder, M.; Mattinen, M. L.; Kontteli, M.; Lindeberg, G.; Stahlberg, J.; Drakenberg, T.; Reinikainen, T.; Pettersson, G.; Annila, A. Identification of Functionally Important Amino-Acids in the Cellulose-Binding Domain of Trichoderma-reesei Cellobiohydrolase I Protein Sci. 1995, 4, 1056-1064
34. Tavagnacco, L.; Mason, P. E.; Schnupf, U.; Pitici, F.; Zhong, L. H.; Himmel, M. E.; Crowley, M.; Cesaro, A.; Brady, J. W. Sugar-Binding Sites on the Surface of the Carbohydrate-Binding Module of Cel7A from T. reesei Carbohydr. Res. 2011, 346, 839-846
35. Linder, M.; Teeri, T. T. The Cellulose-Binding Domain of the Major Cellobiohydrolase of Trichoderma Reesei Exhibits True Reversibility and a High Exchange Rate on Crystalline Cellulose Proc. Natl. Acad. Sci. U.S.A. 1996, 93, 12251-12255
36. Jung, H.; Wilson, D. B.; Walker, L. P. Binding and Reversibility of Thermobifida fusca Cel5A, Cel6B, and Cel48A and Their Respective Catalytic Domains to Bacterial Microcrystalline Cellulose Biotechnol. Bioeng. 2003, 84, 151-159
37. Cascão Pereira, L. G.; Hickel, A.; Radke, C. J.; Blanch, H. W. A Kinetic Model for Enzyme Interfacial Activity and Stability: pa-Hydroxynitrile Lyase at the Diisopropyl Ether/Water Interface Biotechnol. Bioeng. 2002, 78, 595-605
38. Levine, S. E.; Fox, J. M.; Blanch, H. W.; Clark, D. S. A Mechanistic Model of the Enzymatic Hydrolysis of Cellulose Biotechnol. Bioeng. 2010, 107, 37-51
39. Bharadwaj, R.; Wong, A.; Knierim, B.; Singh, S.; Holmes, B. M.; Auer, M.; Simmons, B. A.; Adams, P. D.; Singh, A. K. High-Throughput Enzymatic Hydrolysis of Lignocellulosic Biomass via in-Situ Regeneration Bioresour. Technol. 2011, 102, 1329-1337
40. Holtzapple, M.; Cognata, M.; Shu, Y.; Hendrickson, C. Inhibition of Trichoderma-Reesei Cellulase by Sugars and Solvents Biotechnol. Bioeng. 1990, 36, 275-287
41. Rodahl, M.; Höök, F.; Krozer, A.; Brzezinski, P.; Kasemo, B. Quartz-Crystal Microbalance Setup for Frequency and Q-Factor Measurements in Gaseous and Liquid Environments Rev. Sci. Instrum. 1995, 66, 3924-3930
42. Kwon, H. J.; Bradfield, C. K.; Dodge, B. T.; Agoki, G. S. Study of Simultaneous Fluid and Mass Adsorption Model in the QCM-D Sensor for Characterization of Biomolecular Interactions. Proceedings of the COMSOL Conference; Boston, 2009.
43. Srisodsuk, M.; Lehtiö, J.; Linder, M.; Margolles-Clark, E.; Reinikainen, T.; Teeri, T. T. Trichoderma reesei Cellobiohydrolase I with an Endoglucanase Cellulose-Binding Domain: Action on Bacterial Microcrystalline Cellulose J. Biotechnol. 1997, 57, 49-57
44. Bray, M. R.; Johnson, P. E.; Gilkes, N. R.; McIntosh, L. P.; Kilburn, D. G.; Warren, R. A. J. Probing the Role of Tryptophan Residues in a Cellulose-Binding Domain by Chemical Modification Protein Sci. 1996, 5, 2311-2318
45. Soderquist, M. E.; Walton, A. G. Structural Changes in Proteins Adsorbed on Polymer Surfaces J. Colloid Interface Sci. 1979, 75, 386-397
46. Castells, V.; Yang, S. X.; Van Tassel, P. R. Surface-Induced Conformational Changes in Lattice Model Proteins by Monte Carlo Simulation Phys. Rev. E 2002, 65, 031912
47. Larsson, A. M.; Bergfors, T.; Dultz, E.; Irwin, D. C.; Roos, A.; Driguez, H.; Wilson, D. B.; Jones, T. A. Crystal Structure of Thermobifida busca Endoglucanase Cel6A in Complex with Substrate and Inhibitor: The Role of Tyrosine Y73 in Substrate Ring Distortion Biochemistry 2005, 44, 12915-12922
48. Taylor, C. B.; Talib, M. F.; McCabe, C.; Bu, L. T.; Adney, W. S.; Himmel, M. E.; Crowley, M. F.; Becham, G. T. Computational Investigation of Glycosylation Effects on a Family 1 Carbohydrate-Binding Module J. Biol. Chem. 2012, 287, 3147-3155
49. Teeri, T. T.; Reinikainen, T.; Ruohonen, L; Alwyn Jones, T.; Knowles, J. K. C. Domain Function in Trichoderma reesei Cellobiohydrolases J. Biotechnol. 1992, 24, 169-176
50. Henrissat, B. Cellulases and Their Interaction with Cellulose Cellulose 1994, 1, 169-196
51. Lin, Y.; Silvestre-Ryan, J.; Himmel, M.; Crowley, M.; Beckham, G. T.; Chu, J.-W. Protein Allostery at the Solid-Liquid Interface: Endoglucanase Attachment to Cellulose Affects Glucan Clenching in the Binding Cleft J. Am. Chem. Soc. 2011, 133, 16617-16624
52. Hoshino, E.; Kanda, T.; Sasaki, Y.; Nisizawa, K. Adsorption Mode of Exo- and Endo-Cellulases from Irpex lacteus (Polyporus tulipiferae) on Cellulose with Difference Crystallinities J. Biochem. 1992, 111, 600-605
53. Ma, A.; Hu, Q.; Qu, Y.; Bai, Z.; Liu, W.; Zhuang, G. The Enzymatic Hydrolysis Rate of Cellulose Decreases with Irreversible Adsorption of Cellobiohydrolase I Enzyme Microb. Technol. 2008, 42, 543-547