Cellulase biocatalysis: key influencing factors and mode of action

Cellulose

Volumn 22, Issue 4, 2015, Pages 2157-2182

  Hamid, Sharifah Bee Abd ^a   Islam, Mohammed Moinul ^b   Das, Rasel ^a  

^a UNIVERSITY OF MALAYA   (Malaysia)

^b UNIVERSITY OF CHITTAGONG   (Bangladesh)

Author keywords

Cellulases; Cellulose; Endoglucanase; Exoglucanase; Factors controlling cellulase cellulose interactions; Structures

Indexed keywords

CATALYST ACTIVITY; ENZYMES; STRUCTURE (COMPOSITION);

CELLULASE ENGINEERINGS; CELLULASES; ENDOGLUCANASES; EXOGLUCANASE; KEY INFLUENCING FACTORS; SCIENCE AND TECHNOLOGY; SUBSTRATE INTERACTION; TECHNOLOGICAL CHALLENGES;

CELLULOSE;

EID: 84937967461     PISSN: 09690239     EISSN: 1572882X     Source Type: Journal    
DOI: 10.1007/s10570-015-0672-5     Document Type: Review

References (201)

1. Alekozai EM, GhattyVenkataKrishna PK, Uberbacher EC, Crowley MF, Smith JC, Cheng X (2013) Simulation analysis of the cellulase Cel7A carbohydrate binding module on the surface of the cellulose Iβ. Cellulose 21(2):951–971. doi:10.1007/s10570-013-0026-0
2. Asensio JL, Arda A, Canada FJ, Jimenez-Barbero J (2013) Carbohydrate–aromatic interactions. Acc Chem Res 46(4):946–954. doi:10.1021/ar300024d
3. Atalla R (1999) The individual structures of native celluloses. In: Proceedings of the 10th International Symposium on Wood and Pulping Chemistry, Main Symposium, pp 608–614
4. Atalla R (2011) The diversity of native celluloses. Vimeo, New York
5. Atalla R, VanderHart DL (1999) The role of solid state 13C NMR spectroscopy in studies of the nature of native celluloses. Solid State Nucl Magn Reson 15(1):1–19
6. Barnett CB, Wilkinson KA, Naidoo KJ (2011) Molecular details from computational reaction dynamics for the cellobiohydrolase I glycosylation reaction. J Am Chem Soc 133(48):19474–19482. doi:10.1021/ja206842j
7. Barr BK, Hsieh YL, Ganem B, Wilson DB (1996) Identification of two functionally different classes of exocellulases. Biochemistry 35(2):586–592. doi:10.1021/Bi9520388
8. Beckham GT, Matthews JF, Bomble YJ, Bu LT, Adney WS, Himmel ME, Nimlos MR, Crowley MF (2010) Identification of amino acids responsible for processivity in a family 1 carbohydrate-binding module from a fungal cellulase. J Phys Chem B 114(3):1447–1453. doi:10.1021/Jp908810a
9. Beguin P (1990) Molecular biology of cellulose degradation. Annu Rev Microbiol 44:219–248. doi:10.1146/annurev.mi.44.100190.001251
10. Beldman G, Voragen AG, Rombouts FM, Searle-van Leeuwen MF, Pilnik W (1987) Adsorption and kinetic behavior of purified endoglucanases and exoglucanases from Trichoderma viride. Biotechnol Bioeng 30(2):251–257. doi:10.1002/bit.260300215
11. Beltrame PL, Carniti P, Focher B, Marzetti A, Cattaneo M (1982) Cotton cellulose: enzyme adsorption and enzymatic hydrolysis. J Appl Polym Sci 27(9):3493–3502. doi:10.1002/app.1982.070270925
12. Berghem LE, Pettersson LG (1973) The mechanism of enzymatic cellulose degradation. Purification of a cellulolytic enzyme from Trichoderma viride active on highly ordered cellulose. Eur J Biochem 37(1):21–30
13. Bhat MK, Bhat S (1997) Cellulose degrading enzymes and their potential industrial applications. Biotechnol Adv 15(3–4):583–620. doi:10.1016/S0734-9750(97)00006-2
14. Boisset C, Chanzy H, Henrissat B, Lamed R, Shoham Y, Bayer EA (1999) Digestion of crystalline cellulose substrates by the clostridium thermocellum cellulosome: structural and morphological aspects. Biochem J 340(Pt 3):829–835
15. Boisset C, Fraschini C, Schulein M, Henrissat B, 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(4):1444–1452. doi:10.1128/aem.66.4.1444-1452.2000
16. Bommarius AS, Katona A, Cheben SE, Patel AS, Ragauskas AJ, Knudson K, Pu Y (2008) Cellulase kinetics as a function of cellulose pretreatment. Metab Eng 10(6):370–381. doi:10.1016/j.ymben.2008.06.008
17. Boraston AB, Bolam DN, Gilbert HJ, Davies GJ (2004) Carbohydrate-binding modules: fine-tuning polysaccharide recognition. Biochem J 382(Pt 3):769–781. doi:10.1042/bj20040892
18. Breyer WA, Matthews BW (2001) A structural basis for processivity. Protein Sci 10(9):1699–1711. doi:10.1110/ps.10301
19. Bu L, Nimlos MR, Shirts MR, Stahlberg J, Himmel ME, Crowley MF, Beckham GT (2012) Product binding varies dramatically between processive and nonprocessive cellulase enzymes. J Biol Chem 287(29):24807–24813. doi:10.1074/jbc.M112.365510
20. Carrard G, Linder M (1999) Widely different off rates of two closely related cellulose-binding domains from Trichoderma reesei. Eur J Biochem 262(3):637–643
21. Chang M, Chou TC, Tsao G (1981) Structure, pretreatment and hydrolysis of cellulose. In: Fiechter A (ed) Bioenergy, vol 20. advances in biochemical engineering. Springer, Berlin Heidelberg, pp 15–42. doi:10.1007/3-540-11018-6_2
22. Chanzy H, Henrissat B, Vuong R (1984) Colloidal gold labelling of l,4-β-D-glucan cellobiohydrolase adsorbed on cellulose substrates. FEBS Lett 172(2):193–197. doi:10.1016/0014-5793(84)81124-2
23. Chawla PR, Bajaj IB, Survase SA, Singhal RS (2009) Microbial cellulose: fermentative production and applications. Food Technol Biotechnol 47(2):107–124
24. Chipman DM, Sharon N (1969) Mechanism of lysozyme action. Science 165:454–465
25. Ciolacu D, Kovac J, Kokol V (2010) The effect of the cellulose-binding domain from Clostridium cellulovorans on the supramolecular structure of cellulose fibers. Carbohydr Res 345(5):621–630. doi:10.1016/j.carres.2009.12.023
26. Converse A (1993) Substrate factors limiting enzymatic hydrolysis. In: Saddler JN (ed) Bioconversion of forest and agricultural plant residues. CAB International, Walligford, pp 93–106
27. Dadi AP, Schall CA, Varanasi S (2007) Mitigation of cellulose recalcitrance to enzymatic hydrolysis by ionic liquid pretreatment. Appl biochem biotecnol 137–140(1–12):407–421. http://link.springer.com/article/10.1007%2Fs12010-007-9068-9
28. Dagel DJ, Liu YS, Zhong L, Luo Y, Himmel ME, Xu Q, Zeng Y, Ding SY, Smith S (2011) In situ imaging of single carbohydrate-binding modules on cellulose microfibrils. J Phys Chem B 115(4):635–641. doi:10.1021/jp109798p
29. Dale BE, Leong CK, Pham TK, Esquivel VM, Rios I, Latimer VM (1996) Hydrolysis of lignocellulosics at low enzyme levels: application of the AFEX process. Bioresour Technol 56(1):111–116. doi:10.1016/0960-8524(95)00183-2
30. Davies G, Henrissat B (1995) Structures and mechanisms of glycosyl hydrolases. Structure 3(9):853–859. doi:10.1016/S0969-2126(01)00220-9
31. Davies GJ, Wilson KS, Henrissat B (1997) Nomenclature for sugar-binding subsites in glycosyl hydrolases. Biochem J 321(Pt 2):557–559
32. Ding H, Xu F (2004) Productive Cellulase Adsorption on Cellulose. In: Saha BC, Hayashi K (eds) Lignocellulose Biodegradation, vol 889. ACS Symposium Series, vol 889. American Chemical Society, pp 154–169. doi:10.1021/bk-2004-0889.ch009
33. Divne C, Stahlberg J, Reinikainen T, Ruohonen L, Pettersson G, Knowles J, Teeri TT, Jones TA (1994) The three-dimensional crystal structure of the catalytic core of cellobiohydrolase I from Trichoderma reesei. Science 265(5171):524–528
34. Divne C, Stahlberg J, Teeri TT, Jones TA (1998) 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 275(2):309–325. doi:10.1006/jmbi.1997.1437
35. Endler A, Persson S (2011) Cellulose synthases and synthesis in Arabidopsis. Mol Plant 4(2):199–211. doi:10.1093/mp/ssq079
36. Fägerstam LG, Pettersson LG (1980) The 1.4-β-glucan cellobiohydrolases of Trichoderma reesei QM 9414: a new type of cellulolytic synergism. FEBS Lett 119(1):97–100
37. Fan LT, Lee Y-H, Beardmore DH (1980) Mechanism of the enzymatic hydrolysis of cellulose: effects of major structural features of cellulose on enzymatic hydrolysis. Biotechnol Bioeng 22(1):177–199. doi:10.1002/bit.260220113
38. Fan LT, Lee YH, Beardmore DR (1981) The influence of major structural features of cellulose on rate of enzymatic hydrolysis. Biotechnol Bioeng 23(2):419–424. doi:10.1002/bit.260230215
39. Fengel DW, Wegener G (1984) Wood: chemistry, ultrastructure, reactions. Walter de Gruyter, Berlin
40. Fernandes AN, Thomas LH, Altaner CM, Callow P, Forsyth VT, Apperley DC, Kennedy CJ, Jarvis MC (2011) Nanostructure of cellulose microfibrils in spruce wood. Proc Natl Acad Sci USA 108(47):E1195–E1203. doi:10.1073/pnas.1108942108
41. Fierobe HP, Bayer EA, Tardif C, Czjzek M, Mechaly A, Belaich A, Lamed R, Shoham Y, Belaich JP (2002) Degradation of cellulose substrates by cellulosome chimeras. Substrate targeting versus proximity of enzyme components. J Biol Chem 277(51):49621–49630. doi:10.1074/jbc.M207672200
42. Fleming K, Gray DG, Matthews S (2001) Cellulose crystallites. Chemistry 7(9):1831–1835
43. Ganner T, Bubner P, Eibinger M, Mayrhofer C, Plank H, Nidetzky B (2012) Dissecting and reconstructing synergism: in situ visualization of cooperativity among cellulases. J Biol Chem 287(52):43215–43222. doi:10.1074/jbc.M112.419952
44. Gao D, Chundawat SP, Krishnan C, Balan V, Dale BE (2010) Mixture optimization of six core glycosyl hydrolases for maximizing saccharification of ammonia fiber expansion (AFEX) pretreated corn stover. Bioresour Technol 101(8):2770–2781. doi:10.1016/j.biortech.2009.10.056
45. Gao SH, You C, Renneckar S, Bao J, Zhang YHP (2014) New insights into enzymatic hydrolysis of heterogeneous cellulose by using carbohydrate-binding module 3 containing GFP and carbohydrate-binding module 17 containing CFP. Biotechnol Biofuels. doi:10.1186/1754-6834-7-24
46. Gardiner ES, Sarko A (1985) Packing analysis of carbohydrates and polysaccharides. 16. The crystal structures of celluloses IVI and IVII. Can J Chem 63(1):173–180
47. Gatenholm P, Davalos R (2008) Invention controls weavers of nanoscale biomaterials. http://www.vtnews.vt.edu/articles/2008/11/2008-693.html
48. Ghose TK, Bisaria VS (1979) Studies on the mechanism of enzymatic hydrolysis of cellulosic substances. Biotechnol Bioeng 21(1):131–146. doi:10.1002/bit.260210110
49. Gilkes NR, Jervis E, Henrissat B, Tekant B, Miller RC Jr, Warren RA, Kilburn DG (1992) The adsorption of a bacterial cellulase and its two isolated domains to crystalline cellulose. J Biol Chem 267(10):6743–6749
50. Grethlein HE (1985) The effect of pore size distribution on the rate of enzymatic hydrolysis of cellulosic substrates. Nat Biotechnol 3(2):155–160
51. Guo JC, Catchmark JM (2013) Binding specificity and thermodynamics of cellulose-binding modules from Trichoderma reesei Cel7A and Cel6A. Biomacromolecules 14(5):1268–1277. doi:10.1021/bm300810t
52. Habibi Y, Lucia LA, Rojas OJ (2010) Cellulose nanocrystals: chemistry, self-assembly, and applications. Chem Rev 110(6):3479–3500
53. Hall M, Bansal P, Lee JH, Realff MJ, Bommarius AS (2010) Cellulose crystallinity–a key predictor of the enzymatic hydrolysis rate. FEBS J 277(6):1571–1582. doi:10.1111/j.1742-4658.2010.07585.x
54. Hall M, Bansal P, Lee JH, Realff MJ, Bommarius AS (2011) Biological pretreatment of cellulose: enhancing enzymatic hydrolysis rate using cellulose-binding domains from cellulases. Bioresour Technol 102(3):2910–2915. doi:10.1016/j.biortech.2010.11.010
55. Han SJ, Yoo YJ, Kang HS (1995) Characterization of a bifunctional cellulase and its structural gene—the cel gene of Bacillus Sp D04 Has exoglucanase and endoglucanase activity. J Biol Chem 270(43):26012–26019
56. Harjunpää V, Teleman A, Koivula A, Ruohonen L, Teeri TT, Teleman O, Drakenberg T (1996) Cello-Oligosaccharide hydrolysis by cellobiohydrolase II from Trichoderma reesei. Eur J Biochem 240(3):584–591
57. Hayashi N, Sugiyama J, Okano T, Ishihara Mitsuro (1998) Selective degradation of the cellulose I s component in Cladophora cellulose with Trichoderma viride cellulase. Carbohydr Res 305:109–116
58. Henriksson G, Nutt A, Henriksson H, Pettersson B, Stahlberg J, Johansson G, Pettersson G (1999) Endoglucanase 28 (Cel12A), a new Phanerochaete chrysosporium cellulase. Eur J Biochem 259(1–2):88–95
59. Henrissat B (1994) Cellulases and their interaction with cellulose. Cellulose 1(3):169–196. doi:10.1007/BF00813506
60. Henrissat B, Driguez H, Viet C, Schülein M (1985) Synergism of cellulases from Trichoderma reesei in the degradation of cellulose. Nat Biotechnol 3(8):722–726
61. 13C CP-MAS NMR. Carbohydr Polym 40(2):115–124. doi:10.1016/s0144-8617(99)00051-x
62. Himmel ME, Ding S-Y, Johnson DK, Adney WS, Nimlos MR, Brady JW, Foust TD (2007) Biomass recalcitrance: engineering plants and enzymes for biofuels production. Science 315(5813):804–807. doi:10.1126/science.1137016
63. Hoshino E, Sasaki Y, Okazaki M, Nisizawa K, Kanda T (1993) Mode of action of exo-type and endo-Type cellulases from Irpex-Lacteus in the hydrolysis of cellulose with different crystallinities. J Biochem 114(2):230–235
64. Hoshino E, Shiroishi M, Amano Y, Nomura M, Kanda T (1997) Synergistic actions of exo-type cellulases in the hydrolysis of cellulose with different crystallinities. J Ferment Bioeng 84(4):300–306. doi:10.1016/S0922-338X(97)89248-3
65. Huang AA (1975) Kinetic studies on insoluble cellulose–cellulase system. Biotechnol Bioeng 17(10):1421–1433. doi:10.1002/bit.260171003
66. Igarashi K, Koivula A, Wada M, Kimura S, Penttila M, Samejima M (2009) High speed atomic force microscopy visualizes processive movement of Trichoderma reesei cellobiohydrolase I on crystalline cellulose. J Biol Chem 284(52):36186–36190. doi:10.1074/jbc.M109.034611
67. Igarashi K, Uchihashi T, Koivula A, Wada M, Kimura S, Okamoto T, Penttilä M, Ando T, Samejima M (2011) Traffic jams reduce hydrolytic efficiency of cellulase on cellulose surface. Science 333(6047):1279–1282
68. Irwin DC, Spezio M, Walker LP, Wilson DB (1993) Activity studies of eight purified cellulases: specificity, synergism, and binding domain effects. Biotechnol Bioeng 42(8):1002–1013
69. Irwin D, Shin DH, Zhang S, Barr BK, Sakon J, Karplus PA, Wilson DB (1998) Roles of the catalytic domain and two cellulose binding domains of Thermomonospora fusca E4 in cellulose hydrolysis. J Bacteriol 180(7):1709–1714
70. Jalak J, Kurašin M, Teugjas H, Väljamäe P (2012) Endo-exo synergism in cellulose hydrolysis revisited. J Biol Chem 287(34):28802–28815
71. Jarvis M (2003) Chemistry: cellulose stacks up. Nature 426(6967):611–612. doi:10.1038/426611a
72. Jauris S, Rucknagel KP, Schwarz WH, Kratzsch P, Bronnenmeier K, Staudenbauer WL (1990) Sequence analysis of the Clostridium stercorarium celZ gene encoding a thermoactive cellulase (Avicelase I): identification of catalytic and cellulose-binding domains. Mol Gen Genet 223(2):258–267
73. Jeoh T, Wilson DB, Walker LP (2002) Cooperative and competitive binding in synergistic mixtures of Thermobifida fusca cellulases Cel5A, Cel6B, and Cel9A. Biotechnol Prog 18(4):760–769. doi:10.1021/bp0200402
74. Jeon SD, Yu KO, Kim SW, Han SO (2012) The processive endoglucanase EngZ is active in crystalline cellulose degradation as a cellulosomal subunit of Clostridium cellulovorans. New Biotechnol 29(3):365–371. doi:10.1016/j.nbt.2011.06.008
75. John MJ, Thomas S (2008) Biofibres and biocomposites. Carbohydr Polym 71(3):343–364. doi:10.1016/j.carbpol.2007.05.040
76. Jonas R, Farah LF (1998) Production and application of microbial cellulose. Polym Degrad Stab 59(1):101–106
77. Jongkees SA, Withers SG (2013) Unusual enzymatic glycoside cleavage mechanisms. Acc Chem Res 47(1):226–235
78. Jung H, Wilson DB, Walker LP (2002) Binding mechanisms for Thermobifida fusca Cel5A, Cel6B, and Cel48A cellulose-binding modules on bacterial microcrystalline cellulose. Biotechnol Bioeng 80(4):380–392. doi:10.1002/bit.10375
79. Kennedy CJ, Cameron GJ, Šturcová A, Apperley DC, Altaner C, Wess TJ, Jarvis MC (2007) Microfibril diameter in celery collenchyma cellulose: X-ray scattering and NMR evidence. Cellulose 14(3):235–246
80. Kim YJ, Kim D-O, Chun OK, Shin D-H, Jung H, Lee CY, Wilson DB (2005) Phenolic extraction from apple peel by cellulases from Thermobifida fusca. J Agric Food Chem 53(24):9560–9565. doi:10.1021/jf052052j
81. Kipper K, Valjamae P, Johansson G (2005) Processive action of cellobiohydrolase Cel7A from Trichoderma reesei is revealed as ‘burst’ kinetics on fluorescent polymeric model substrates. Biochem J 385(Pt 2):527–535
82. Klein GL SW (1993) Cellulose. In: Macrae R RR, Saddler MJ (ed) Encyclopedia of food science, food technology and nutrition. Academic Press, USA, pp 758–767
83. Kleman-Leyer K, Agosin E, Conner AH, Kirk TK (1992) Changes in molecular size distribution of cellulose during attack by white rot and brown rot fungi. Appl Environ Microbiol 58(4):1266–1270
84. Kleman-Leyer KM, Gilkes NR, Miller RC Jr, Kirk TK (1994) Changes in the molecular-size distribution of insoluble celluloses by the action of recombinant Cellulomonas fimi cellulases. Biochem J 302(Pt 2):463–469
85. Kleman-Leyer KM, Siika-Aho M, Teeri TT, Kirk TK (1996) The cellulases endoglucanase I and cellobiohydrolase II of Trichoderma reesei act synergistically to solubilize native cotton cellulose but not to decrease its molecular size. Appl Environ Microbiol 62(8):2883–2887
86. Kleywegt GJ, Zou JY, Divne C, Davies GJ, Sinning I, Stahlberg J, Reinikainen T, Srisodsuk M, Teeri TT, Jones TA (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(3):383–397. doi:10.1006/jmbi.1997.1243
87. Klyosov AA (1990) Trends in biochemistry and enzymology of cellulose degradation. Biochemistry 29(47):10577–10585
88. Knott BC, Haddad Momeni M, Crowley MF, Mackenzie LF, Gotz AW, Sandgren M, Withers SG, Stahlberg J, Beckham GT (2014) The mechanism of cellulose hydrolysis by a two-step, retaining cellobiohydrolase elucidated by structural and transition path sampling studies. J Am Chem Soc 136(1):321–329. doi:10.1021/ja410291u
89. Knowles J, Lehtovaara P, Teeri T (1987) Cellulase families and their genes. Trends Biotechnol 5(9):255–261. doi:10.1016/0167-7799(87)90102-8
90. Koivula A, Reinikainen T, Ruohonen L, Valkeajarvr A, Claeyssens M, Teleman O, Kleyweg GJ, Szardenings M, Rouvinen J, Jones TA, Teeri TT (1996) The active site of Trichoderma reesei cellobiohydrolase II: the role of tyrosine 169. Protein Eng 9(8):691–699
91. Koshland DE (1953) Stereochemistry and the mechanism of enzymatic reactions. Biol Rev 28(4):416–436
92. Kraulis J, Clore GM, Nilges M, Jones TA, Pettersson G, Knowles J, Gronenborn AM (1989) Determination of the three-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 28(18):7241–7257
93. Kruus K, Wang WK, Ching J, Wu JH (1995) Exoglucanase activities of the recombinant Clostridium thermocellum CelS, a major cellulosome component. J Bacteriol 177(6):1641–1644
94. Kuhad RC, Gupta R, Singh A (2011) Microbial cellulases and their industrial applications. Enzyme Res 2011:280696. doi:10.4061/2011/280696
95. Kurasin M, Valjamae P (2011) Processivity of cellobiohydrolases is limited by the substrate. J Biol Chem 286(1):169–177. doi:10.1074/jbc.M110.161059
96. Kyriacou A, Neufeld RJ, Mackenzie CR (1989) Reversibility and competition in the adsorption of Trichoderma reesei cellulase components. Biotechnol Bioeng 33(5):631–637. doi:10.1002/bit.260330517
97. Landín M, Martínez-Pacheco R, Gómez-Amoza JL, Souto C, Concheiro A, Rowe RC (1993) Effect of country of origin on the properties of microcrystalline cellulose. Int J Pharm 91(2–3):123–131. doi:10.1016/0378-5173(93)90331-9
98. Lee YH, Fan LT (1982) Kinetic studies of enzymatic hydrolysis of insoluble cellulose: analysis of the initial rates. Biotechnol Bioeng 24(11):2383–2406. doi:10.1002/bit.260241107
99. Lee SB, Shin HS, Ryu DD, Mandels M (1982) Adsorption of cellulase on cellulose: effect of physicochemical properties of cellulose on adsorption and rate of hydrolysis. Biotechnol Bioeng 24(10):2137–2153. doi:10.1002/bit.260241003
100. Lee SB, Kim IH, Ryu DD, Taguchi H (1983) Structural properties of cellulose and cellulase reaction mechanism. Biotechnol Bioeng 25(1):33–51. doi:10.1002/bit.260250105
101. Lee NE, Lima M, Woodward J (1988) Hydrolysis of cellulose by a mixture of Trichoderma reesei cellobiohydrolase and Aspergillus niger endoglucanase. Biochim Biophys Acta 967(3):437–440
102. Lehtio J, Sugiyama J, Gustavsson M, Fransson L, Linder M, Teeri TT (2003) The binding specificity and affinity determinants of family 1 and family 3 cellulose binding modules. Proc Natl Acad Sci USA 100(2):484–489. doi:10.1073/pnas.212651999
103. Lehtiö J, Sugiyama J, Gustavsson M, Fransson L, Linder M, Teeri TT (2003) The binding specificity and affinity determinants of family 1 and family 3 cellulose binding modules. Proc Natl Acad Sci 100(2):484–489. doi:10.1073/pnas.212651999
104. Lenz J, Esterbauer H, Sattler W, Schurz J, Wrentschur E (1990) Changes of structure and morphology of regenerated cellulose caused by acid and enzymatic hydrolysis. J Appl Polym Sci 41(5–6):1315–1326. doi:10.1002/app.1990.070410538
105. Li Y, Irwin DC, Wilson DB (2007) Processivity, substrate binding, and mechanism of cellulose hydrolysis by Thermobifida fusca Cel9A. Appl Environ Microbiol 73(10):3165–3172. doi:10.1128/aem.02960-06
106. Li L, Mu Q, Zhang B, Yan B (2010) Analytical strategies for detecting nanoparticle-protein interactions. Analyst 135(7):1519–1530. doi:10.1039/c0an00075b
107. Linder M, Teeri TT (1996) 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 USA 93(22):12251–12255
108. Linder M, Teeri TT (1997) The roles and function of cellulose-binding domains. J Biotechnol 57(1–3):15–28. doi:10.1016/S0168-1656(97)00087-4
109. Linder M, Lindeberg G, Reinikainen T, Teeri TT, Pettersson G (1995a) The difference in affinity between two fungal cellulose-binding domains is dominated by a single amino acid substitution. FEBS Lett 372(1):96–98. doi:10.1016/0014-5793(95)00961-8
110. Linder M, Mattinen ML, Kontteli M, Lindeberg G, Stahlberg J, Drakenberg T, Reinikainen T, Pettersson G, Annila A (1995b) Identification of functionally important amino-acids in the cellulose-binding domain of Trichoderma-Reesei cellobiohydrolase-I. Protein Sci 4(6):1056–1064
111. Liu YS, Baker JO, Zeng Y, Himmel ME, Haas T, Ding SY (2011) Cellobiohydrolase hydrolyzes crystalline cellulose on hydrophobic faces. J Biol Chem 286(13):11195–11201. doi:10.1074/jbc.M110.216556
112. Lotfi G (2014) Cellulolytic microorganism. Int J Curr Res Chem Pharm Sci 1(2):52–58
113. Lu Q, Dong X, Li L-J, Hu X (2010) Direct electrochemistry-based hydrogen peroxide biosensor formed from single-layer graphene nanoplatelet–enzyme composite film. Talanta 82(4):1344–1348
114. Lynd LR, Weimer PJ, van Zyl WH, Pretorius IS (2002) Microbial cellulose utilization: fundamentals and biotechnology. Microbiol Mol Biol Rev 66(3):506–577. doi:10.1128/mmbr.66.3.506-577.2002
115. Mangan D, McCleary B, Liadova A, Ivory R, McCormack N (2014) Quantitative fluorometric assay for the measurement of endo-1, 4-β-glucanase. Carbohydr Res 395:47–51
116. Mansfield SD, Mooney C, Saddler JN (1999) Substrate and enzyme characteristics that limit cellulose hydrolysis. Biotechnol Prog 15(5):804–816. doi:10.1021/Bp9900864
117. Maurer SA, Bedbrook CN, Radke CJ (2012) Cellulase adsorption and reactivity on a cellulose surface from flow ellipsometry. Ind Eng Chem Res 51(35):11389–11400. doi:10.1021/ie3008538
118. Mazeau K, Heux L (2003) Molecular dynamics simulations of bulk native crystalline and amorphous structures of cellulose. J Phys Chem B 107(10):2394–2403. doi:10.1021/Jp0219395
119. McCrae SI, Wood TM (1986) The cellulase of Penicillium pinophilum. Synergism between enzyme components in solubilizing cellulose with special reference to the involvement of two immunologically distinct cellobiohydrolases. Biochem J 234(1):93–99
120. Medve J, Stahlberg J, Tjerneld F (1994) Adsorption and synergism of cellobiohydrolase I and II of Trichoderma reesei during hydrolysis of microcrystalline cellulose. Biotechnol Bioeng 44(9):1064–1073. doi:10.1002/bit.260440907
121. Mertz B, Hill AD, Mulakala C, Reilly PJ (2007) Automated docking to explore subsite binding by glycoside hydrolase family 6 cellobiohydrolases and endoglucanases. Biopolymers 87(4):249–260. doi:10.1002/bip.20831
122. Mishra C, Rao M (1988) Mode of action and synergism of cellulases from Penicillium funiculosum. Appl Biochem Biotechnol 19(2):139–150
123. Moloney A, Coughlan MP (1983) Sorption of Talaromyces emersonii cellulase on cellulosic substrates. Biotechnol Bioeng 25(1):271–280. doi:10.1002/bit.260250120
124. Nidetzky B, Steiner W, Hayn M, Claeyssens M (1994) Cellulose hydrolysis by the cellulases from Trichoderma reesei: a new model for synergistic interaction. Biochem J 298(Pt 3):705–710
125. Nishiyama Y (2009) Structure and properties of the cellulose microfibril. J Wood Sci 55(4):241–249
126. Nishiyama Y, Langan P, Chanzy H (2002) Crystal structure and hydrogen-bonding system in cellulose Iβ from synchrotron X-ray and neutron fiber diffraction. J Am Chem Soc 124(31):9074–9082
127. Nishiyama Y, Sugiyama J, Chanzy H, Langan P (2003) Crystal structure and hydrogen bonding system in cellulose Iα from synchrotron X-ray and neutron fiber diffraction. J Am Chem Soc 125(47):14300–14306. doi:10.1021/ja037055w
128. Ooshima H, Sakata M, Harano Y (1983) Adsorption of cellulase from Trichoderma viride on cellulose. Biotechnol Bioeng 25(12):3103–3114. doi:10.1002/bit.260251223
129. Ooshima H, Kurakake M, Kato J, Harano Y (1991) Enzymatic activity of cellulase adsorbed on cellulose and its change during hydrolysis. Appl Biochem Biotechnol 31(3):253–266. doi:10.1007/BF02921752
130. O’Sullivan A (1997) Cellulose: the structure slowly unravels. Cellulose 4(3):173–207. doi:10.1023/A:1018431705579
131. Palonen H, Tenkanen M, Linder M (1999) Dynamic interaction of Trichoderma reesei cellobiohydrolases Cel6A and Cel7A and cellulose at equilibrium and during hydrolysis. Appl Environ Microbiol 65(12):5229–5233
132. Park S, Baker JO, Himmel ME, Parilla PA, Johnson DK (2010) Cellulose crystallinity index: measurement techniques and their impact on interpreting cellulase performance. Biotechnol Biofuels 3:10. doi:10.1186/1754-6834-3-10
133. Payne CM, Knott BC, Mayes HB, Hansson H, Himmel ME, Sandgren M, Ståhlberg J, Beckham GT (2015) Fungal Cellulases. Chem Rev 115(3):1308–1448. doi:10.1021/cr500351c
134. Phillips DC (1967) The hen egg-white lysozyme molecule. Proc Natl Acad Sci USA 57(3):483–495
135. Pilz I, Schwarz E, Kilburn DG, Miller RC Jr, Warren RA, Gilkes NR (1990) The tertiary structure of a bacterial cellulase determined by small-angle X-ray-scattering analysis. Biochem J 271(1):277–280
136. Pinto R, Moreira S, Mota M, Gama M (2004) Studies on the cellulose-binding domains adsorption to cellulose. Langmuir 20(4):1409–1413
137. Poidevin L, Feliu J, Doan A, Berrin JG, Bey M, Coutinho PM, Henrissat B, Record E, Heiss-Blanquet S (2013) Insights into exo- and endoglucanase activities of family 6 glycoside hydrolases from Podospora anserina. Appl Environ Microbiol 79(14):4220–4229. doi:10.1128/AEM.00327-13
138. Reinikainen T, Ruohonen L, Nevanen T, Laaksonen L, Kraulis P, Jones TA, Knowles JKC, Teeri TT (1992) Investigation of the function of mutated cellulose-binding domains of Trichoderma reesei cellobiohydrolase I. Proteins Struct Funct Bioinf 14(4):475–482. doi:10.1002/prot.340140408
139. Reinikainen T, Teleman O, Teeri TT (1995) Effects of pH and high ionic strength on the adsorption and activity of native and mutated cellobiohydrolase I from Trichoderma reesei. Proteins 22(4):392–403. doi:10.1002/prot.340220409
140. Reverbel-Leroy C, Pages S, Belaich A, Belaich JP, Tardif C (1997) The processive endocellulase CelF, a major component of the Clostridium cellulolyticum cellulosome: purification and characterization of the recombinant form. J Bacteriol 179(1):46–52
141. Robson LM, Chambliss GH (1989) Cellulases of bacterial origin. Enzyme Microb Technol 11(10):626–644. doi:10.1016/0141-0229(89)90001-X
142. Rouvinen J, Bergfors T, Teeri T, Knowles JK, Jones TA (1990) Three-dimensional structure of cellobiohydrolase II from Trichoderma reesei. Science 249(4967):380–386
143. Rowe RC, McKillop AG, Bray D (1994) The effect of batch and source variation on the crystallinity of microcrystalline cellulose. Int J Pharm 101(1–2):169–172. doi:10.1016/0378-5173(94)90087-6
144. Ryu DD, Mandels M (1980) Cellulases: biosynthesis and applications. Enzyme Microb Technol 2(2):91–102
145. Ryu DD, Kim C, Mandels M (1984a) Competitive adsorption of cellulase components and its significance in a synergistic mechanism. Biotechnol Bioeng 26(5):488–496. doi:10.1002/bit.260260513
146. Ryu DD, Kim C, Mandels M (1984b) Competitive adsorption of cellulase components and its significance in a synergistic mechanism. Biotechnol Bioeng 26(5):488–496
147. Saharay M, Guo H, Smith JC (2010) Catalytic mechanism of cellulose degradation by a cellobiohydrolase, CelS. PloS One 5(10):e12947. doi:10.1371/journal.pone.0012947
148. Sandgren M, Shaw A, Ropp TH, Wu S, Bott R, Cameron AD, Stahlberg J, Mitchinson C, Jones TA (2001) The X-ray crystal structure of the Trichoderma reesei family 12 endoglucanase 3, Cel12A, at 1.9 A resolution. J Mol Biol 308(2):295–310. doi:10.1006/jmbi.2001.4583
149. Sattler W, Esterbauer H, Glatter O, Steiner W (1989) The effect of enzyme concentration on the rate of the hydrolysis of cellulose. Biotechnol Bioeng 33(10):1221–1234. doi:10.1002/bit.260331002
150. Shang BZ, Chu J-W (2014) Kinetic modeling at single-molecule resolution elucidates the mechanisms of cellulase synergy. ACS Catal. doi:10.1021/cs500126q
151. Shoseyov O, Shani Z, Levy I (2006) Carbohydrate binding modules: biochemical properties and novel applications. Microbiol Mol Biol Rev 70(2):283–295. doi:10.1128/mmbr.00028-05
152. Sinitsyn AP, Gusakov AV, Vlasenko EY (1991) Effect of structural and physico-chemical features of cellulosic substrates on the efficiency of enzymatic hydrolysis. Appl Biochem Biotechnol 30(1):43–59. doi:10.1007/BF02922023
153. Srisodsuk M, Kleman-Leyer K, Keranen S, Kirk TK, Teeri TT (1998) Modes of action on cotton and bacterial cellulose of a homologous endoglucanase–exoglucanase pair from Trichoderma reesei. Eur J Biochem 251(3):885–892
154. Ståhlberg J, Johansson G, Pettersson G (1991) A new model for enzymatic hydrolysis of cellulose based on the two-domain structure of cellobiohydrolase I. Nat Biotechnol 9:286–290
155. Ståhlberg J, Johansson G, 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 (BBA) General Subjects 1157(1):107–113
156. Steiner W, Sattler W, Esterbauer H (1988) Adsorption of Trichoderma reesei cellulase on cellulose: experimental data and their analysis by different equations. Biotechnol Bioeng 32(7):853–865. doi:10.1002/bit.260320703
157. Streamer M, Eriksson KE, Pettersson B (1975) Extracellular enzyme system utilized by the fungus Sporotrichum pulverulentum (Chrysosporium lignorum) for the breakdown of cullulose. Functional characterization of five endo-1,4-beta-glucanases and one exo-1,4-beta-glucanase. Eur J Biochem 59(2):607–613
158. Sugiyama J, Okano T, Yamamoto H, Horii F (1990) Transformation of Valonia cellulose crystals by an alkaline hydrothermal treatment. Macromolecules 23(12):3196–3198
159. Sugiyama J, Persson J, Chanzy H (1991a) Combined infrared and electron diffraction study of the polymorphism of native celluloses. Macromolecules 24(9):2461–2466. doi:10.1021/ma00009a050
160. Sugiyama J, Vuong R, Chanzy H (1991b) Electron diffraction study on the two crystalline phases occurring in native cellulose from an algal cell wall. Macromolecules 24(14):4168–4175
161. Sulzenbacher G, Driguez H, Henrissat B, Schulein M, Davies GJ (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(48):15280–15287. doi:10.1021/bi961946h
162. Sulzenbacher G, Schulein M, Davies GJ (1997) Structure of the endoglucanase I from Fusarium oxysporum: native, cellobiose, and 3,4-epoxybutyl beta-D-cellobioside-inhibited forms, at 2.3 A resolution. Biochemistry 36(19):5902–5911. doi:10.1021/bi962963+
163. Taylor CB, Payne CM, Himmel ME, Crowley MF, McCabe C, Beckham GT (2013) Binding site dynamics and aromatic-carbohydrate interactions in processive and non-processive family 7 glycoside hydrolases. J Phys Chem B 117(17):4924–4933. doi:10.1021/jp401410h
164. Teeri TT (1997) Crystalline cellulose degradation: new insight into the function of cellobiohydrolases. Trends Biotechnol 15(5):160–167. doi:10.1016/S0167-7799(97)01032-9
165. Tingaut P, Eyholzer C, Zimmermann T (2011) Functional polymer nanocomposite materials from microfibrillated cellulose. INTECH Open Access Publisher, Croatia
166. Tomme P, Van Tilbeurgh H, Pettersson G, Van Damme J, Vandekerckhove J, Knowles J, Teeri T, Claeyssens M (1988) Studies of the cellulolytic system of Trichoderma reesei QM 9414. Eur J Biochem 170(3):575–581. doi:10.1111/j.1432-1033.1988.tb13736.x
167. Tomme P, Warren RA, Gilkes NR (1995) Cellulose hydrolysis by bacteria and fungi. Adv Microb Physiol 37:1–81
168. Tomme P, Kwan E, Gilkes NR, Kilburn DG, Warren RA (1996) Characterization of CenC, an enzyme from Cellulomonas fimi with both endo- and exoglucanase activities. J Bacteriol 178(14):4216–4223
169. Tormo J, Lamed R, Chirino AJ, Morag E, Bayer EA, Shoham Y, Steitz TA (1996) Crystal structure of a bacterial family-III cellulose-binding domain: a general mechanism for attachment to cellulose. EMBO J 15(21):5739–5751
170. Väljamäe P, Sild V, Nutt A, Pettersson G, Johansson G (1999) Acid hydrolysis of bacterial cellulose reveals different modes of synergistic action between cellobiohydrolase I and endoglucanase I. Eur J Biochem 266(2):327–334
171. Várnai A, Siika-aho M, Viikari L (2013) Carbohydrate-binding modules (CBMs) revisited: reduced amount of water counterbalances the need for CBMs. Biotechnology for Biofuels 2013, 6:30
172. Várnai A, Mäkelä MR, Djajadi DT, Rahikainen J, Hatakka A, Viikari L (2014) Chapter four—carbohydrate-binding modules of fungal cellulases: occurrence in nature, function, and relevance in industrial biomass conversion. In: Sima S, Geoffrey Michael G (eds) Advances in applied microbiology. Academic Press, Waltham, pp 103–165. doi: 10.1016/B978-0-12-800260-5.00004-8
173. Velleste R, Teugjas H, Väljamäe P (2010) Reducing end-specific fluorescence labeled celluloses for cellulase mode of action. Cellulose 17(1):125–138. doi:10.1007/s10570-009-9356-3
174. Vocadlo DJ, Davies GJ (2008) Mechanistic insights into glycosidase chemistry. Curr Opin Chem Biol 12(5):539–555
175. Vocadlo DJ, Davies GJ, Laine R, Withers SG (2001) Catalysis by hen egg-white lysozyme proceeds via a covalent intermediate. Nature 412(6849):835–838
176. Vuong TV, Wilson DB (2009) Processivity, synergism, and substrate specificity of Thermobifida fusca Cel6B. Appl Environ Microbiol 75(21):6655–6661. doi:10.1128/AEM.01260-09
177. Wada M, Chanzy H, Nishiyama Y, Langan P (2004a) Cellulose IIII crystal structure and hydrogen bonding by synchrotron X-ray and neutron fiber diffraction. Macromolecules 37(23):8548–8555. doi:10.1021/ma0485585
178. Wada M, Heux L, Sugiyama J (2004b) Polymorphism of cellulose I family: reinvestigation of cellulose IVI. Biomacromolecules 5(4):1385–1391. doi:10.1021/bm0345357
179. Wada M, Nishiyama Y, Langan P (2006) X-ray structure of ammonia–cellulose I: new insights into the conversion of cellulose I to cellulose IIII. Macromolecules 39(8):2947–2952. doi:10.1021/ma060228s
180. Wald S, Wilke CR, Blanch HW (1984) Kinetics of the enzymatic hydrolysis of cellulose. Biotechnol Bioeng 26(3):221–230. doi:10.1002/bit.260260305
181. Wang J, Quirk A, Lipkowski J, Dutcher JR, Hill C, Mark A, Clarke AJ (2012) Real-time observation of the swelling and hydrolysis of a single crystalline cellulose fiber catalyzed by cellulase 7B from Trichoderma reesei. Langmuir 28(25):9664–9672
182. Weimer PJ, Hackney JM, French AD (1995) Effects of chemical treatments and heating on the crystallinity of celluloses and their implications for evaluating the effect of crystallinity on cellulose biodegradation. Biotechnol Bioeng 48(2):169–178. doi:10.1002/bit.260480211
183. White AR, Brown RM (1981) Enzymatic hydrolysis of cellulose: visual characterization of the process. Proc Natl Acad Sci 78(2):1047–1051
184. Wolfenden R, Snider MJ (2001) The depth of chemical time and the power of enzymes as catalysts. Acc Chem Res 34(12):938–945
185. Wood TM (1975) Properties and mode of action of cellulases. Biotechnol Bioeng Symp 5:111–133
186. Wood TM (1985) Properties of cellulolytic enzyme systems. Biochem Soc Trans 13(2):407–410
187. Wood TM (1988a) Preparation of crystalline, amorphous, and dyed cellulase substrates. Methods Enzymol 160:19–25
188. Wood TM (1988b) Preparation of crystalline, amorphous, and dyed cellulase substrates. Methods Enzymol 160C:19–25
189. Wood TM, Bhat KM (1988) Methods for measuring cellulase activities. Methods Enzymol 160:87–112
190. Wood T, McCrae SI (1972) The purification and properties of the C 1 component of Trichoderma koningii cellulase. Biochem J 128:1183–1192
191. Wood TM, McCrae SI, Bhat KM (1989) The mechanism of fungal cellulase action. Synergism between enzyme components of Penicillium pinophilum cellulase in solubilizing hydrogen bond-ordered cellulose. Biochem J 260(1):37–43
192. Xu F, Ding H (2007) A new kinetic model for heterogeneous (or spatially confined) enzymatic catalysis: contributions from the fractal and jamming (overcrowding) effects. Appl Catal A 317(1):70–81. doi:10.1016/j.apcata.2006.10.014
193. Yan S, Li T, Yao L (2011) Mutational effects on the catalytic mechanism of cellobiohydrolase I from Trichoderma reesei. J Phys Chem B 115(17):4982–4989. doi:10.1021/jp200384m
194. Yang B, Willies DM, Wyman CE (2006) Changes in the enzymatic hydrolysis rate of Avicel cellulose with conversion. Biotechnol Bioeng 94(6):1122–1128. doi:10.1002/bit.20942
195. Zhang YH, Lynd LR (2004) Toward an aggregated understanding of enzymatic hydrolysis of cellulose: noncomplexed cellulase systems. Biotechnol Bioeng 88(7):797–824. doi:10.1002/bit.20282
196. Zhang J, Rong J, Li W, Lin Z, Zhang X (2011) Preparation and characterization of bacterial cellulose/polyacrylamide hydrogel. Acta Polym Sin 6:602–607
197. Zhang Y, Lu X-B, Gao C, Lv W-J, Yao J-M (2012) Preparation and characterization of nano crystalline cellulose from bamboo fibers by controlled cellulase hydrolysis. J Fiber Bioeng Inform 5(3):263–271. doi:10.3993/jfbi09201204
198. Zhang Y, Yan S, Yao L (2013) A mechanistic study of Trichoderma reesei Cel7B catalyzed glycosidic bond cleavage. J Phys Chem B 117(29):8714–8722. doi:10.1021/jp403999s
199. Zheng F, Ding SJ (2013) Processivity and enzymatic mode of a glycoside hydrolase family 5 endoglucanase from Volvariella volvacea. Appl Environ Microbiol 79(3):989–996. doi:10.1128/Aem.02725-12
200. Zhou WL, Irwin DC, Escovar-Kousen J, Wilson DB (2004) Kinetic studies of Thermobifida fusca Cel9A active site mutant enzymes. Biochemistry 43(30):9655–9663. doi:10.1021/Bi049394n
201. Zou J-Y, Kleywegt GJ, Ståhlberg J, Driguez H, Nerinckx W, Claeyssens M, Koivula A, Teeri TT, Jones TA (1999) Crystallographic evidence for substrate ring distortion and protein conformational changes during catalysis in cellobiohydrolase Ce16A from Trichoderma reesei. Structure 7(9):1035–1045. doi:10.1016/S0969-2126(99)80171-3