Effects of sulfate groups on the adsorption and activity of cellulases on cellulose substrates

Langmuir

Volumn 29, Issue 10, 2013, Pages 3280-3291

  Jiang, Feng ^a   Kittle, Joshua D ^a   Tan, Xinyi ^a   Esker, Alan R ^a   Roman, Maren ^a  

^a VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMICAL CONVERSION; CELLULASE ADSORPTION; CELLULOSE BINDING DOMAINS; CELLULOSE NANO-CRYSTALS; CELLULOSE SUBSTRATES; LIGNOCELLULOSIC BIOMASS; QUARTZ CRYSTAL MICROBALANCE WITH DISSIPATION MONITORING; RATE OF HYDROLYSIS;

ADSORPTION; ATOMIC FORCE MICROSCOPY; CELLULOSE; ENZYMATIC HYDROLYSIS; SULFUR COMPOUNDS; SURFACE ROUGHNESS;

SUBSTRATES;

CELLULASE; CELLULOSE; SULFATE;

ADSORPTION; ARTICLE; CHEMISTRY; ENZYME SPECIFICITY; METABOLISM; THEORETICAL MODEL;

ADSORPTION; CELLULASES; CELLULOSE; MODELS, THEORETICAL; SUBSTRATE SPECIFICITY; SULFATES;

EID: 84874880794     PISSN: 07437463     EISSN: 15205827     Source Type: Journal    
DOI: 10.1021/la3040193     Document Type: Article

References (63)

1. Lynd, L. R.; Cushman, J. H.; Nichols, R. J.; Wyman, C. E. Fuel Ethanol from Cellulosic Biomass Science 1991, 251, 1318-1323
2. Wyman, C. E. Biomass Ethanol: Technical Progress, Opportunities, and Commercial Challenges Ann. Rev. Energy Environ. 1999, 24, 189-226
3. Lynd, L. R.; Weimer, P. J.; van Zyl, W. H.; Pretorius, I. S. Microbial Cellulose Utilization: Fundamentals and Biotechnology Microbiol. Mol. Biol. Rev. 2002, 66, 506-577
4. Kraulis, P. J.; Clore, G. M.; Nilges, M.; Jones, T. A.; Pettersson, G.; Knowles, J.; Gronenborn, A. M. Determination of the 3-Dimensional Solution Structure of the C-Terminal Domain of Cellobiohydrolase I from Trichoderma Reesei. A Study Using Nuclear Magnetic-Resonance and Hybrid Distance Geometry-Dynamical Simulated Annealing Biochemistry 1989, 28, 7241-7257
5. Linder, M.; Lindeberg, G.; Reinikainen, T.; Teeri, T. T.; Pettersson, G. The Difference in Affinity between 2 Fungal Cellulose-Binding Domains Is Dominated by a Single Amino-Acid Substitution FEBS Lett. 1995, 372, 96-98
6. Linder, M.; Teeri, T. T. The Roles and Function of Cellulose-Binding Domains J. Biotechnol. 1997, 57, 15-28
7. Himmel, M. E.; 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
8. Mosier, N.; Wyman, C.; Dale, B.; Elander, R.; Lee, Y. Y.; Holtzapple, M.; Ladisch, M. Features of Promising Technologies for Pretreatment of Lignocellulosic Biomass Bioresour. Technol. 2005, 96, 673-686
9. Wyman, C. E.; Dale, B. E.; Elander, R. T.; Holtzapple, M.; Ladisch, M. R.; Lee, Y. Y. Coordinated Development of Leading Biomass Pretreatment Technologies Bioresour. Technol. 2005, 96, 1959-1966
10. Gohdes, M.; Mischnick, P. Determination of the Substitution Pattern in the Polymer Chain of Cellulose Sulfates Carbohydr. Res. 1998, 309, 109-115
11. Rojas, O. J.; Jeong, C.; Turon, X.; Argyropoulos, D. S. Measurement of Cellulase Activity with Piezoelectric Resonators. In Materials, Chemicals, and Energy from Forest Biomass; Argyropoulos, D. S., Ed.; ACS Symposium Series 954; American Chemical Society: Washington, DC, 2007; pp 478-494.
12. Turon, X.; Rojas, O. J.; Deinhammer, R. S. Enzymatic Kinetics of Cellulose Hydrolysis: A QCM-D Study Langmuir 2008, 24, 3880-3887
13. 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
14. 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
15. Hu, G.; Heitmann, J. A.; Rojas, O. J. Quantification of Cellulase Activity Using the Quartz Crystal Microbalance Technique Anal. Chem. 2009, 81, 1872-1880
16. Josefsson, P.; Henriksson, G.; WaÌŠgberg, 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
17. 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
18. Cheng, G.; Datta, S.; Liu, Z. L.; Wang, C.; Murton, J. K.; Brown, P. A.; Jablin, M. S.; Dubey, M.; Majewski, J.; Halbert, C. E.; Browning, J. F.; Esker, A. R.; Watson, B. J.; Zhang, H. T.; Hutcheson, S. W.; Huber, D. L.; Sale, K. L.; Simmons, B. A.; Kent, M. S. Interactions of Endoglucanases with Amorphous Cellulose Films Resolved by Neutron Reflectometry and Quartz Crystal Microbalance with Dissipation Monitoring Langmuir 2012, 28, 8348-8358
19. Cheng, G.; Liu, Z. L.; Murton, J. K.; Jablin, M.; Dubey, M.; Majewski, J.; 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, 2216-2224
20. RaÌŠnby, B. G. Aqueous Colloidal Solutions of Cellulose Micelles Acta Chem. Scand. 1949, 3, 649-650
21. RaÌŠnby, B. G. Fibrous Macromolecular Systems. Cellulose and Muscle. The Colloidal Properties of Cellulose Micelles Discuss. Faraday Soc. 1951, 11, 158-164
22. Marchessault, R. H.; Morehead, F. F.; Koch, M. J. Hydrodynamic Properties of Neutral Suspensions of Cellulose Crystallites as Related to Size and Shape J. Colloid Sci. 1961, 16, 327-344
23. Kittle, J. D.; Du, X. S.; Jiang, F.; Qian, C.; Heinze, T.; Roman, M.; Esker, A. R. Equilibrium Water Contents of Cellulose Films Determined via Solvent Exchange and Quartz Crystal Microbalance with Dissipation Monitoring Biomacromolecules 2011, 12, 2881-2887
24. 4-Hydrolyzed Cellulose Nanocrystals Langmuir 2010, 26, 17919-17925
25. Araki, J.; Wada, M.; Kuga, S.; Okano, T. Flow Properties of Microcrystalline Cellulose Suspension Prepared by Acid Treatment of Native Cellulose Colloids Surf., A 1998, 142, 75-82
26. Sauerbrey, G. Verwendung Von Schwingquarzen zur Wägung Dünner Schichten und zur Mikrowägung Z. Phys. 1959, 155, 206-222
27. Lide, D. R. CRC Handbook of Chemistry and Physics, 91 st ed.; CRC Press: Boca Raton, FL, 2011.
28. Kanazawa, K. K.; Gordon, J. G. Frequency of a Quartz Microbalance in Contact with Liquid Anal. Chem. 1985, 57, 1770-1771
29. Kotiranta, P.; Karlsson, J.; Siika-Aho, M.; Medve, J.; Viikari, L.; Tjerneld, F.; Tenkanen, M. Adsorption and Activity of Trichoderma Reesei Cellobiohydrolase I, Endoglucanase II, and the Corresponding Core Proteins on Steam Pretreated Willow Appl. Biochem. Biotechnol. 1999, 81, 81-90
30. Eriksson, T.; Karlsson, J.; Tjerneld, F. A Model Explaining Declining Rate in Hydrolysis of Lignocellulose Substrates with Cellobiohydrolase I (Cel7a) and Endoglucanase I (Cel7b) of Trichoderma Reesei Appl. Biochem. Biotechnol. 2002, 101, 41-60
31. Rabinovich, M. L.; Melnik, M. S.; Boloboba, A. V. Microbial Cellulases (Review) Appl. Biochem. Microbiol. 2002, 38, 305-321
32. Bezerra, R. M. F.; Dias, A. A. Enzymatic Kinetic of Cellulose Hydrolysis-Inhibition by Ethanol and Cellobiose Appl. Biochem. Biotechnol. 2005, 126, 49-59
33. Yang, B.; Wyman, C. E. BSA Treatment to Enhance Enzymatic Hydrolysis of Cellulose in Lignin Containing Substrates Biotechnol. Bioeng. 2006, 94, 611-617
34. Borjesson, J.; Peterson, R.; Tjerneld, F. Enhanced Enzymatic Conversion of Softwood Lignocellulose by Poly(ethylene glycol) Addition Enzyme Microb. Technol. 2007, 40, 754-762
35. Medve, J.; Karlsson, J.; Lee, D.; Tjerneld, F. Hydrolysis of Microcrystalline Cellulose by Cellobiohydrolase I and Endoglucanase II from Trichoderma Reesei: Adsorption, Sugar Production Pattern, and Synergism of the Enzymes Biotechnol. Bioeng. 1998, 59, 621-634
36. Ghose, T. K. Measurement of Cellulase Activities Pure Appl. Chem. 1987, 59, 257-268
37. 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
38. Johansson, G.; Stahlberg, J.; Lindeberg, G.; Engstrom, A.; Pettersson, G. Isolated Fungal Cellulase Terminal Domains and a Synthetic Minimum Analog Bind to Cellulose FEBS Lett. 1989, 243, 389-393
39. Lemos, M. A.; Teixeira, J. A.; Mota, M.; Gama, F. M. A Simple Method to Separate Cellulose-Binding Domains of Fungal Cellulases after Digestion by a Protease Biotechnol. Lett. 2000, 22, 703-707
40. Tomme, P.; Vantilbeurgh, H.; Pettersson, G.; Vandamme, J.; Vandekerckhove, J.; Knowles, J.; Teeri, T.; Claeyssens, M. Studies of the Cellulolytic System of Trichoderma Reesei QM 9414. Analysis of Domain Function in 2 Cellobiohydrolases by Limited Proteolysis Eur. J. Biochem. 1988, 170, 575-581
41. Vantilbeurgh, H.; Tomme, P.; Claeyssens, M.; Bhikhabhai, R.; Pettersson, G. Limited Proteolysis of the Cellobiohydrolase I from Trichoderma Reesei-Separation of Functional Domains FEBS Lett. 1986, 204, 223-227
42. 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
43. Rodahl, M.; Kasemo, B. On the Measurement of Thin Liquid Overlayers with the Quartz-Crystal Microbalance Sens. Actuators, A 1996, 54, 448-456
44. Voinova, M. V.; Rodahl, M.; Jonson, M.; Kasemo, B. Viscoelastic Acoustic Response of Layered Polymer Films at Fluid-Solid Interfaces: Continuum Mechanics Approach Phys. Scr. 1999, 59, 391-396
45. Hook, F.; Kasemo, B.; Nylander, T.; Fant, C.; Sott, K.; Elwing, H. Variations in Coupled Water, Viscoelastic Properties, and Film Thickness of a Mefp-1 Protein Film During Adsorption and Cross-Linking: A Quartz Crystal Microbalance with Dissipation Monitoring, Ellipsometry, and Surface Plasmon Resonance Study Anal. Chem. 2001, 73, 5796-5804
46. Dutta, A. K.; Nayak, A.; Belfort, G. Viscoelastic Properties of Adsorbed and Cross-Linked Polypeptide and Protein Layers at a Solid-Liquid Interface J. Colloid Interface Sci. 2008, 324, 55-60
47. 2 Anal. Chem. 2003, 75, 5080-5087
48. Holst, M.; Baker, N.; Wang, F. Adaptive Multilevel Finite Element Solution of the Poisson-Boltzmann Equation I. Algorithms and Examples J. Comput. Chem. 2000, 21, 1319-1342
49. Baker, N. A.; Sept, D.; Joseph, S.; Holst, M. J.; McCammon, J. A. Electrostatics of Nanosystems: Application to Microtubules and the Ribosome Proc. Natl. Acad. Sci. U.S.A. 2001, 98, 10037-10041
50. Humphrey, W.; Dalke, A.; Schulten, K. VMD: Visual Molecular Dynamics J. Mol. Graphics Modell. 1996, 14, 33-38
51. Kontturi, E.; Johansson, L. S.; Kontturi, K. S.; Ahonen, P.; Thüne, P. C.; Laine, J. Cellulose Nanocrystal Submonolayers by Spin Coating Langmuir 2007, 23, 9674-9680
52. Langmuir, I. The Adsorption of Gases on Plane Surfaces of Glass, Mica and Platinum J. Am. Chem. Soc. 1918, 40, 42
53. Freundlich, H. Über die Adsorption in Lösungen Z. Phyz. Chem. 1907, 57, 385-470
54. 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
55. Sugimoto, N.; Igarashi, K.; Wada, M.; Samejima, M. Adsorption Characteristics of Fungal Family 1 Cellulose-Binding Domain from Trichoderma Reesei Cellobiohydrolase I on Crystalline Cellulose: Negative Cooperative Adsorption via a Steric Exclusion Effect Langmuir 2012, 28, 14323-14329
56. Goyal, A.; Ghosh, B.; Eveleigh, D. Characteristics of Fungal Cellulases Bioresour. Technol. 1991, 36, 37-50
57. Zhang, Y. H. P.; Lynd, L. R. Toward an Aggregated Understanding of Enzymatic Hydrolysis of Cellulose: Noncomplexed Cellulase Systems Biotechnol. Bioeng. 2004, 88, 797-824
58. Divne, C.; Stahlberg, J.; Reinikainen, T.; Ruohonen, L.; Pettersson, G.; Knowles, J. K. C.; Teeri, T. T.; Jones, T. A. The 3-Dimensional Crystal-Structure of the Catalytic Core of Cellobiohydrolase-I from Trichoderma Reesei Science 1994, 265, 524-528
59. Divne, C.; Stahlberg, J.; Teeri, T. T.; Jones, T. A. High-Resolution Crystal Structures Reveal How a Cellulose Chain Is Bound in the 50 Å Long Tunnel of Cellobiohydrolase I from Trichoderma Reesei J. Mol. Biol. 1998, 275, 309-325
60. Stahlberg, J.; Divne, C.; Koivula, A.; Piens, K.; Claeyssens, M.; Teeri, T. T.; Jones, T. A. Activity Studies and Crystal Structures of Catalytically Deficient Mutants of Cellobiohydrolase I from Trichoderma Reesei J. Mol. Biol. 1996, 264, 337-349
61. Kleywegt, G. J.; Zou, J. Y.; Divne, C.; Davies, G. J.; Sinning, I.; Stahlberg, J.; Reinikainen, T.; Srisodsuk, M.; Teeri, T. T.; Jones, T. A. 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. 1997, 272, 383-397
62. Bhikhabhai, R.; Johansson, G.; Pettersson, G. Isolation of Cellulolytic Enzymes from Trichoderma Reesei QM 9414 J. Appl. Biochem. 1984, 6, 336-345
63. Shoemaker, S.; Watt, K.; Tsitovsky, G.; Cox, R. Characterization and Properties of Cellulases Purified from Trichoderma Reesei Strain L27 Nat. Biotechnol. 1983, 1, 687-690