Abstract
A homogeneous cellulose-binding module (CBM) of cellobiohydrolase I (CBHI) from Trichoderma pseudokoningii S-38 was obtained by the limited proteolysis with papain and a series of chromatographs filtration. Analysis of FT-IR spectra demonstrated that the structural changes result from a weakening and splitting of the hydrogen bond network in cellulose by the action of CBMCBHI at 40°C for 24 h. The results of molecular dynamic simulations are consistent with the experimental conclusions, and provide a nanoscopic view of the mechanism that strong and medium H-bonds decreased dramatically when CBM was bound to the cellulose surface. The function of CBMCBHI is not only limited to locating intact CBHI in close proximity with cellulose fibrils, but also is involved in the structural disruption at the fibre surface. The present studies provided considerable evidence for the model of the intramolecular synergy between the catalytic domain and their CBMs.
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References
Zhang Y H, Lynd L R. Toward an aggregated understanding of enzymatic hydrolysis of cellulose: Noncomplexed cellulase systems. Biotechnol Bioeng, 2004, 88(7): 797–824, 15538721, 10.1002/bit.20282, 1:CAS:528:DC%2BD2cXhtVOitrjE
Klyosov A A. Trends in biochemistry and enzymology of cellulose degradation. Biochemistry, 1990, 29: 10577–10585, 2271668, 10.1021/bi00499a001, 1:CAS:528:DyaK3cXmt1Kktrg%3D
Shoseyov O, Shani Z, Levy I. Carbohydrate binding modules: Biochemical properties and novel applications. Microbiol Mol Biol Rev, 2006, 70(2): 283–295, 16760304, 10.1128/MMBR.00028-05, 1:CAS:528:DC%2BD28XmvFGrtLk%3D
Bourne Y, Henrissat B. Glycoside hydrolases and glycosyltransferases: Families and functional modules. Curr Opin Struct Biol, 2001, 11(5): 593–600, 11785761, 10.1016/S0959-440X(00)00253-0, 1:CAS:528:DC%2BD3MXntlyisL0%3D
Beguin P, Aubert J P. The biological degradation of cellulose. FEMS Microbiol Rev, 1994, 13: 25–58, 8117466, 10.1111/j.1574-6976.1994.tb00033.x, 1:CAS:528:DyaK2cXhsFyhsbk%3D
Tomme P, Warren R A, Gilkes N R. Cellulose hydrolysis by bacteria and fungi. Adv Microb Physiol, 1995, 37: 1–81, 8540419, 10.1016/S0065-2911(08)60143-5, 1:STN:280:DyaK287is1Wgsw%3D%3D
Linder M, Teeri T T. The roles and function of cellulose-binding domains. J Biotechnol, 1997, 57: 15–28, 10.1016/S0168-1656(97)00087-4, 1:CAS:528:DyaK2sXmvVarsL4%3D
Din N, Gilkes N R, Tekant B, et al. Non-hydrolytic disruption of cellulose fibres by the binding domain of a bacterial cellulase. Bio/Technology, 1991, 9: 1096–1099, 10.1038/nbt1191-1096, 1:CAS:528:DyaK38Xhslansrg%3D
Din N, Damude H G, Gilkes M N R, et al. C1-Cx revisited: intramolecular synergism in a cellulase. Proc Natl Acad Sci USA, 1994, 91: 11383–11387., 7972069, 10.1073/pnas.91.24.11383, 1:CAS:528:DyaK2MXitlyrsrY%3D
Yan B X, Sun Y Q. Domain structure and confurmation of a cellobiohydrolase I from Trichodrma Pseudokoningii S-38. J Protein Chem, 1997, 16: 59–66, 9055208, 10.1023/A:1026394912245, 1:STN:280:DyaK2s3gsl2ksA%3D%3D
Lehtio J, Sugiyama J, Gustavsson, M, et al. The binding specificity and affinity determinants of family 1 and family 3 cellulose binding modules. Proc Natl Acad Sci USA, 2003, 100(2): 484–489, 12522267, 10.1073/pnas.212651999, 1:CAS:528:DC%2BD3sXnvVKgsA%3D%3D
Tormo J, Lamed R, Chirino A J, et al. Crystal structure of a bacterial family-III cellulose-binding domain: A general mechanism for attachment to cellulose. EMBO J, 1996, 15(21): 5739–5751, 8918451, 1:CAS:528:DyaK28XntVakurc%3D
Mattinen M L, Linder M, Teleman A, et al. Interaction between cellohexaose and cellulose binding domains from Trichoderma reesei cellulases. FEBS Lett, 1997, 407(3): 291–296, 9175871, 10.1016/S0014-5793(97)00356-6, 1:CAS:528:DyaK2sXivFyrsro%3D
Reinikainen T, Ruohonen L, Nevanen T, et al. Investigation of the function of mutated cellulose-binding domains of Trichoderma reesei cellobiohydrolase. Proteins, 1989, 14: 475–482, 10.1002/prot.340140408
Linder M, Mattinen M L, Kontteli M, et al. Identification of functionally important amino acids in the cellulose-binding domain of Trichoderma reesei cellobiohydrolase I. Protein Sci, 1995, 4(6): 1056–1064, 7549870, 1:CAS:528:DyaK2MXmsFyrs7w%3D
Hoffren A M, Teeri T T, Teleman O. Molecular dynamics simulation of fungal cellulose-binding domains: differences in molecular rigidity but a preserved cellulose binding surface. Protein Eng, 1995, 8(5): 443–450, 8532665, 10.1093/protein/8.5.443, 1:CAS:528:DyaK2MXnsV2isLs%3D
Carrard G, Koivula A, Soderlund H, et al. Cellulose-binding domains promote hydrolysis of different sites on crystalline cellulose. Proc Natl Acad Sci USA, 2000, 97(19): 10342–10347, 10962023, 10.1073/pnas.160216697, 1:CAS:528:DC%2BD3cXms1Crs7s%3D
Linder M, Teeri T T. The cellulose-binding domain of the major cellubiohydrolase I of Trichoderma reesei exhibits true reversibility and a high exchange rate on crystalline cellulose. Proc Natl Acad Sci USA, 1996, 93: 12251–12255, 8901566, 10.1073/pnas.93.22.12251, 1:CAS:528:DyaK28Xms1Gjsbw%3D
Bray M R, Johnson P E, Gilkes N R, et al. Probing the role of tryptophan residues in a cellulose-binding domain by chemical modification. Protein Sci, 1996, 5(11): 2311–2318, 8931149, 1:CAS:528:DyaK28XntVKqtbs%3D, 10.1002/pro.5560051117
Creagh A L, Ong E, Jervis E, et al. Binding of the cellulose-binding domain of exoglucanase Cex from Cellulomonas fimi to insoluble microcrystalline cellulose is entropically driven. Proc Natl Acad Sci USA, 1996, 93(22): 12229–12234, 8901562, 10.1073/pnas.93.22.12229, 1:CAS:528:DyaK28Xms1GjsLg%3D
Pala H, Mota M, Gama F M. Enzymatic versus chemical deinking of non-impact ink printed paper. J Biotechnol, 2004, 108(1): 79–89, 14741771, 10.1016/j.jbiotec.2003.10.016, 1:CAS:528:DC%2BD2cXmvF2jsg%3D%3D
Gao P J, Chen G J, Wang T H, et al. Non-hydrolytic disruption of crystalline structure of cellulose by cellulose-binding domain and linker sequence of cellobiohydrolase I from Penicillium Janthinellum. Acta Biochim Biophys Sin, 2001, 33: 13–18, 12053182, 1:CAS:528:DC%2BD3MXhvFWjsrg%3D
Esteghlalian A R, Srivastava V, Gilkes N R, et al. Do cellulose binding domains increase substrate accessibility? Appl Biochem Biotechnol, 2001, 91–93: 575–592, 11963886, 10.1385/ABAB:91-93:1-9:575
Jervis E J, Haynes C A, Kilburn D G. Surface diffusion of cellulases and their isolated binding domains on cellulose. J Biol Chem, 1997, 272(38): 24016–24023, 9295354, 10.1074/jbc.272.38.24016, 1:CAS:528:DyaK2sXmtlOmurs%3D
Mansfield S D, Mooney C, Saddler J N. Substrate and enzyme characteristics that limit cellulose hydrolysis. Biotechnol Prog, 1999, 15(5): 804–816, 10514250, 10.1021/bp9900864, 1:CAS:528:DyaK1MXlvVeqsrs%3D
Ma D B, Gao P J, Wang Z N. Preliminary Studies on the mechanism of cellulose formation by Trichoderma pserdokoningii S-38. Enzyme Microb Technol, 1990, 12: 631–635, 10.1016/0141-0229(90)90139-H, 1:CAS:528:DyaK3cXkvFCmurs%3D
Yan B X, Gao P J. Purification of two cellobiohydrolase from Trichoderma pseudokoningii S-38. Chin Biochem J (in Chinese), 1997, 13: 362–364, 1:CAS:528:DyaK2sXkslWitb8%3D
Wang T H, Wang C H, Gao P J, et al. Subcloning and expression of coding region for cellulose binding domain of CBHI from P. janthinelium in E. coli. Acta Microbiol Sin (in Chinese), 1998, 38: 269–275, 1:CAS:528:DyaK1cXmtV2qtLo%3D
Gao PJ, Zhang Y S. Studies of the fucntion of cellulose binding domain of cellobiohydrolase. Abstr Sci J China, 1994, 4: 974–976
Medve J, Stahlberg J, Tjerneld F. Isotherms for adsorption of cellobiohydrolase I and II from Trichoderma reesei on microcrystalline cellulose. Appl Biochem Biotechnol, 1997, 66(1): 39–56, 9204518, 10.1007/BF02788806, 1:CAS:528:DyaK2sXktVCqsrs%3D
Tripp VW. Measurement of crystallinity. In: Bikales N M, Segel L. eds. Cellulose and Cellulose Derivatives. New York: Wiley Inter Science, 1971. 319–320
Kraulis J, Clore G M, Nilges M, et al. 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, 1989, 28(18): 7241–7257, 2554967, 10.1021/bi00444a016, 1:CAS:528:DyaL1MXlt12ksrk%3D
Nishiyama Y, Langan P, Chanzy H. Crystal structure and hydrogen-bonding system in cellulose Ibeta from synchrotron X-ray and neutron fiber diffraction. J Am Chem Soc, 2002, 124(31): 9074–9082, 12149011, 10.1021/ja0257319, 1:CAS:528:DC%2BD38Xlt1eqsLk%3D
Heiner A P, Sugiyama J, Teleman O. Crystalline cellulose I and I studied by molecular dynamics simulation. Carbohydr Res, 1995, 273(2): 207–223, 10.1016/0008-6215(95)00103-Z, 1:CAS:528:DyaK2MXotFOkt7w%3D
Sugiyama J, Vuong R, Chanzy H. Electron diffraction study on the two crystalline phases occurring in native cellulose from an algal cell wall. Macromolecules, 1991, 24(14): 4168–4175, 10.1021/ma00014a033, 1:CAS:528:DyaK3MXktlWgtLg%3D
Nimlos M R, Matthews J F, Crowley M F, et al. Molecular modeling suggests induced fit of Family I carbohydrate-binding modules with a broken-chain cellulose surface. Protein Eng Des Sel, 2007, 20(4): 179–187, 17430975, 10.1093/protein/gzm010, 1:CAS:528:DC%2BD2sXmt1Oju7Y%3D
Sun H, Mumby S J, Maple J R, et al. An ab initio cff93 all-atom force field for polycarbonates. J Am Chem Soc, 1994, 116: 2978–2987, 10.1021/ja00086a030, 1:CAS:528:DyaK2cXitFyqt7w%3D
Berendsen H J C, Postma J P M, Gunsteren W F, et al. Molecular dynamics with coupling to an external bath. J Chem Phys, 1984, 81: 3684–3690, 10.1063/1.448118, 1:CAS:528:DyaL2cXmtlGksbY%3D
Xiao Z H, Gao P J, Qu Y B, et al. Cellulose-binding domain of endoglucanase III from Trichoderma reesei disrupting the structure of cellulose. Biotechnol Lett, 2001, 23: 711–715, 10.1023/A:1010325122851, 1:CAS:528:DC%2BD3MXjvVSjur0%3D
Wang L S, Liu J, Zhang Y Z, et al. Comparison of domains function between cellobiohydrolase I and endoglucanase I from Trichoderma pseudokoningii S-38 by limited proteolysis. J Mol Cata B: Enzymatic, 2003, 24–25: 27–38, 10.1016/S1381-1177(03)00070-5, 1:CAS:528:DC%2BD3sXmvVyhu78%3D
Nidetzky B, Steiner W, Claecyssens M. Cellulose hydrolysis by The cellulose from Trichoderma reesei: adsorption of two cellobiohydrlases, two endoglucannases and their core proteins on filter paper and their relation to hydrolysis. Biochem J, 1994, 303: 817–823, 7980450, 1:CAS:528:DyaK2cXmvFGrtr0%3D
Kyriacon A, Neufeld R J, MacKenzi C R. Reversibility and competition in the adsorption of Trichoderma reesei cellulose components. Biotechnol Bioeng, 1989, 33: 631–637, 10.1002/bit.260330517
Stahlberg J, Johansson G, Pettersson G. Trichoderma reesei has no true exo-cellulase: all intact and truncated cellulase produce new reducing end groups on cellulose. Biochim Biophys Acta, 1993, 1157: 107–113, 8499476, 1:CAS:528:DyaK3sXkt1ens74%3D
Michell A J. Second-derivative F.T-I.R spectra of cellulose I and II and related mono-and oligo-saccharides. Carbohydr Res, 1988, 193: 185–195, 10.1016/S0008-6215(00)90814-0
Michell A J. Second-derivative F.T-I.R spectra of native cellulose. Carbohydr Res, 1990, 197: 53–60, 10.1016/0008-6215(90)84129-I, 1:CAS:528:DyaK3cXhs1SrsrY%3D
Linder M, Lindeberg G, Reinikainen T, et al. The difference in affinity between two fungal cellulose-binding domains is dominated by a single amino acid substution. FEBS Lett, 1995, 372: 96–98, 7556652, 10.1016/0014-5793(95)00961-8, 1:CAS:528:DyaK2MXosVOit70%3D
Nishio M, Hirota M, Umezwa Y. The CH/p Interaction: Evidence, Nature, and Consequences. New York: Wiley, 1998
Marechal Y, Chanzy H. The hydrogen bond network in I cellulose as observed by infrared spectrometry. J Mol Struct, 2000, 523: 183–196, 10.1016/S0022-2860(99)00389-0, 1:CAS:528:DC%2BD3cXitlKrsb8%3D
Leach AR. Molecular Modelling. 2nd ed. London: Pearson Education, 2001
Jeffrey GA. An Introduction to Hydrogen Bonding. Oxford: Oxford University Press, 1997
Nishiyama Y, Sugiyama J, Chanzy H, et al. Crystal structure and hydrogen bonding system in cellulose I(alpha) from synchrotron X-ray and neutron fiber diffraction. J Am Chem Soc, 2003, 125(47): 14300–14306, 14624578, 10.1021/ja037055w, 1:CAS:528:DC%2BD3sXoslWhsr4%3D
Hinterstoisser B, Salmen L. Application of dynamic 2D FTIR to cellulose. Vib Spectrosc, 2000, 22: 111–118, 10.1016/S0924-2031(99)00063-6, 1:CAS:528:DC%2BD3cXhtFensrk%3D
Benziman M, Haigler C H, Brown R M J, et al. Cellulose biogenesis: Polymerization and crystallization are coupled processes in Acetobacter xylium. Proc Natl Acad Sci USA, 1980, 77: 6678–6682, 16592918, 10.1073/pnas.77.11.6678, 1:CAS:528:DyaL3MXislSqug%3D%3D
Henriksson H, Stahlberg I R, Pettersson G. The active sites of cellulases are involved in chiral recognition: A comparison of cellobiohydrolase I and endoglucanase I. FEBS Lett, 1996, 390: 339–344, 8706890, 10.1016/0014-5793(96)00685-0, 1:CAS:528:DyaK28XksF2gurc%3D
Teeri T T, Koivula A, Linder M, et al. Trichoderma reesei cellobiohydrolase: Why so efficient on crystalline cellulose? Biochem Soc Trans, 1998, 26: 173–178, 9649743, 1:CAS:528:DyaK1cXjvVaktbs%3D
Varrot A, Frandsen T P, Ossowski I, et al. Structural basis for ligand binding and processivity in cellobiohydrolase Cel6A from Humicola insolens. Structure (Camb), 2003, 11(7): 855–864, 10.1016/S0969-2126(03)00124-2, 1:CAS:528:DC%2BD3sXltF2mtr0%3D
Davies G J, Henrissat B. Structures and mechanisms of glycosyl hydrolases. Structure, 1995, 3: 853–859, 8535779, 10.1016/S0969-2126(01)00220-9, 1:CAS:528:DyaK2MXotlWktrY%3D
Rouvinen J, Bergfors T, Teeri T, et al. Three-dimensional structure of cellobiohydrolase II from Trichoderma reesei. Science, 1990, 249(4967): 380–386, 2377893, 10.1126/science.2377893, 1:CAS:528:DyaK3cXmtVOgurw%3D
Sinnott M L. The cellobiohydrolase of Trichoderma reesei: A review of indirect and direct evidence that their function is not just glycoside bond hydrolysis. Biochem Soc Trans, 1998, 26: 160–164, 9649740, 1:CAS:528:DyaK1cXjvVaktbw%3D
Armand S, Drouillard S, Schulein M, et al. Bifunctionalized fluorogenic tetrasaccharide as a substrate to study cellulases. J Biol Chem, 1997, 272(5): 2709–2713, 9006908, 10.1074/jbc.272.5.2709, 1:CAS:528:DyaK2sXpslelsA%3D%3D
Reese E T, Siu R G H, Leyinson H S. Biological degradation of soluble cellulose derivatives. J Bact, 1950, 59: 485–497, 15436422, 1:CAS:528:DyaG3cXjsVGrug%3D%3D
McQueen-Mason S, Cosgrove J. Disruption of hydrogen binding between plant cell wall polymers by proteins that induce wall extension. Proc Natl Acad Sci USA, 1994, 91: 6574–6578, 11607483, 10.1073/pnas.91.14.6574, 1:CAS:528:DyaK2cXkslyms7c%3D
Saloheimo M, Paloheimo M, Hakola S, et al. Swollenin, a Trichoderma reesei protein with sequence similarity to the plant expansins, exhibits disruption activity on cellulosic materials. Eur J Biochem, 2002, 269(17): 4202–4211, 12199698, 10.1046/j.1432-1033.2002.03095.x, 1:CAS:528:DC%2BD38Xnt1eitbc%3D
Shpigel E, Roiz L, Goren R, et al. Bacterial cellulose-binding domain modulates in Yitro elongation of different plant cells. Plant Physiol, 1998, 117: 1185–1194, 9701575, 10.1104/pp.117.4.1185, 1:CAS:528:DyaK1cXlsFaqtr8%3D
Banka R R, Mishra S. Adsorption properties of the fibril forming protein from Trichoderma reesei. Enzyme Microb Technol, 2002, 31: 784–793, 10.1016/S0141-0229(02)00176-X, 1:CAS:528:DC%2BD38Xns1aksLo%3D
Srisodsuk M, Lehtio J, Linder M, et al. Trichoderma reesei cellobio-hydrolase I with an endoglucanase cellulose-binding domain: action on bacterial microcrystalline cellulose. J Biotechnol, 1997, 57(1–3): 49–57, 9335165, 10.1016/S0168-1656(97)00088-6, 1:CAS:528:DyaK2sXmvVarsL0%3D
Nigmatullin R, Lovitt R, Wright C, et al. Atomic force microscopy study of cellulose surface interaction controlled by cellulose binding domains. Colloids Surf B Biointerfaces, 2004, 35(2): 125–135, 15261045, 10.1016/j.colsurfb.2004.02.013, 1:CAS:528:DC%2BD2cXjvVKjtbo%3D
Post C B. Reexamination of induced fit as a determinant of substrate specificity in enzymatic reactions. Biochemistry, 1995, 34: 15881–15885, 8519743, 10.1021/bi00049a001, 1:CAS:528:DyaK2MXpsVGitro%3D
Lee I, Evans B R, Woodward J. The mechanism of cellulase action on cotton fibers: Evidence from atomic force microscopy. Ultramicroscopy, 2000, 82(1–4): 213–221, 10741672, 10.1016/S0304-3991(99)00158-8, 1:CAS:528:DC%2BD3cXosleisQ%3D%3D
Henrissat B, Vigny B, Buleon A, et al. Possible adsorption sites of cellulases on crystalline cellulose. FEBS Lett, 1988, 231: 177–182, 10.1016/0014-5793(88)80726-9, 1:CAS:528:DyaL1cXktF2gtr0%3D
Sild V, Stahlberg J, Pettersson G, et al. Effect of potential binding site overlap to binding of cellulase to cellulose: A two-dimensional simulation. FEBS Lett, 1996, 378(1): 51–56, 8549801, 10.1016/0014-5793(95)01420-9, 1:CAS:528:DyaK28Xns1yktQ%3D%3D
Bolam D N, Ciruela A, McQueen-Mason S, et al. Pseudomonas cellulose-binding domains mediate their effects by increasing enzyme substrate proximity. Biochem J, 1998, 331( Pt 3): 775–781, 9560304, 1:CAS:528:DyaK1cXjt12hsr8%3D
Receveur V, Czjzek M, Schulein M, et al. Dimension, shape, and conformational flexibility of a two domain fungal cellulase in solution probed by small angle X-ray scattering. J Biol Chem, 2002, 277(43): 40887–40892, 12186865, 10.1074/jbc.M205404200, 1:CAS:528:DC%2BD38XnvFynu7w%3D
Wang C C, Tsou C L. Protein disulfide isomerase is both an enzyme and a chaperone. FASEB J, 1993, 7(15): 1515–1517, 7903263, 1:CAS:528:DyaK2cXnt1SisA%3D%3D
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Supported by the National Natural Science Foundation of China (Grants No. 30500007), Major State Basic Research Development Research Program of China (Grant No. 2004CB719702), and Scientific Research Reward Fund for Excellent Young and Middle-Aged Scientists in Shandong Province (Grants No. 2005BS06004)
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Wang, L., Zhang, Y. & Gao, P. A novel function for the cellulose binding module of cellobiohydrolase I. SCI CHINA SER C 51, 620–629 (2008). https://doi.org/10.1007/s11427-008-0088-3
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DOI: https://doi.org/10.1007/s11427-008-0088-3