Abstract
Molecular dynamics (MD) simulations were performed to study the dynamics of cello-oligosaccharides on the cellulose crystal surface in the presence of water. In particular, single chains of cello-oligomers containing 2–10 repeat units, i.e. cellobiose, cellotetraose, cellohexaose, cellooctaose as well as cellodecaose—were simulated separately on the (1,0,0) cellulose crystal surface. The dynamics of cello-oligosaccharides were characterized as a function of the distance from the cellulose crystal surface. When the initial location of the cello-oligosaccharides was in the vicinity of the cellulose crystal (separation distance ~4–5Å), they exhibited very small changes in their location and conformation. The cello-oligosaccharides with initial positions far from the surface moved either towards or away from the surface, as would be expected for diffusive behavior. However, once these molecules came in contact with the cellulose crystal surface, they became effectively immobile and got adsorbed on the surface. The dynamics of cellodecaose were studied in detail. From several MD trajectories, three stable conformations for the alignment of cellodecaose on the crystal surface were identified. These are: chain axis of cellodecaose is aligned parallel to the axes of the chains on the crystal surface, chain axis is approximately at right angles to the axes of the chains on the surface, and an obtuse angle conformation in which part of the chain is parallel and the other part is at an angle to the axes of the chains on the surface. The mechanism of adsorption of the cellodecaose on the surface was also identified.
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Beckham GT, Matthews JF, Peters B, Bomble YJ, Himmel ME, Crowley MF (2011) Molecular-level origins of biomass recalcitrance: decrystallization free energies for four common cellulose polymorphs. J Phys Chem B 115(14):4118–4127. doi:10.1021/jp1106394
Berendsen HJC, Postma JPM, Vangunsteren WF, Dinola A, Haak JR (1984) Molecular-dynamics with coupling to an external bath. J Chem Phys 81(8):3684–3690
Bergenstråhle M, Thormann E, Nordgren N, Berglund LA (2009) Force pulling of single cellulose chains at the crystalline cellulose—liquid interface: a molecular dynamics study. Langmuir 25(8):4635–4642. doi:10.1021/la803915c
Bergenstråhle M, Wohlert J, Himmel ME, Brady JW (2010) Simulation studies of the insolubility of cellulose. Carbohydr Res 345(14):2060–2066. doi:10.1016/j.carres.2010.06.017
Case DA, Darden TA, Cheatham ITE, Wang J, Duke RE, Luo R, Crowley M, Walker RC, Zhang W, Merz KM, Wang B, Hayik S, Roitberg A, Seabra G, Kolossváry I, Wong KF, Paesani F, Vanicek J, Wu X, Brozell SR, Steinbrecher H, Gohlke T, Yang L, Tan C, Mongan J, Hornak V, Cui G, Mathews DH, Seetin MG, Sagui C, Babin V, Kollman PA (2008) AMBER 10.
Cintrón MS, Johnson GP, French AD (2011) Young’s modulus calculations for cellulose I(beta) by MM3 and quantum mechanics. Cellulose 18(3):505–516. doi:10.1007/s10570-011-9507-1
Darden T, York D, Pedersen L (1993) Particle mesh ewald—an N.LOG(N) method for ewald sums in large systems. J Chem Phys 98(12):10089–10092. doi:10.1063/1.464397
Duan Y, Wu C, Chowdhury S, Lee MC, Xiong GM, Zhang W, Yang R, Cieplak P, Luo R, Lee T, Caldwell J, Wang JM, Kollman P (2003) A point-charge force field for molecular mechanics simulations of proteins based on condensed-phase quantum mechanical calculations. J Comput Chem 24(16):1999–2012. doi:10.1002/jcc.10349
Finkenstadt VL, Millane RP (1998) Crystal structure of Valonia cellulose I beta. Macromolecules 31(22):7776–7783. doi:10.1021/ma9804895
French AD, Johnson GP (2004) What crystals of small analogs are trying to tell us about cellulose structure. Cellulose 11(1):5–22. doi:10.1023/B:CELL.0000014765.94239.fe
French AD, Johnson GP (2009) Cellulose and the twofold screw axis: modeling and experimental arguments. Cellulose 16(6):959–973. doi:10.1007/s10570-009-9347-4
French AD, Miller DP, Aabloo A (1993) Miniature crystal models of cellulose polymorphs and other carbohydrates. Int J Biol Macromol 15(1):30–36
French AD, Johnson GP, Cramer CJ, Csonka GI (2012) Conformational analysis of cellobiose by electronic structure theories. Carbohydr Res 350:68–76. doi:10.1016/j.carres.2011.12.023
Guvench O, Hatcher E, Venable RM, Pastor RW, MacKerell AD (2009) CHARMM additive all-atom force field for glycosidic linkages between hexopyranoses. J Chem Theory Comput 5(9):2353–2370. doi:10.1021/ct900242e
Hardy BJ, Sarko A (1993) Conformational analysis and molecular dynamics simulation of cellobiose and larger cellooligomers. J Comput Chem 14(7):831–847. doi:10.1002/jcc.540140709
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
IUPAC-IUB Joint Commission on Biochemical Nomenclature (JCBN) (1983) Symbols for specifying the conformation of polysaccharide chains: recommendations 1981. Eur J Biochem 131:5–7
Johnson GP, Petersen L, French AD, Reilly PJ (2009) Twisting of glycosidic bonds by hydrolases. Carbohydr Res 344(16):2157–2166. doi:10.1016/j.carres.2009.08.011
Jorgensen H, Kristensen JB, Felby C (2007) Enzymatic conversion of lignocellulose into fermentable sugars: challenges and opportunities. Biofuels, Bioprod Biorefin 1(2):119–134. doi:10.1002/bbb.4
Kirschner KN, Yongye AB, Tschampel SM, Gonzalez-Outeirino J, Daniels CR, Foley BL, Woods RJ (2008) GLYCAM06: a generalizable biomolecular force field. Carbohydrates. J Comput Chem 29(4):622–655. doi:10.1002/jcc.20820
Klemanleyer 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
Klemanleyer KM, Gilkes NR, Miller RC, Kirk TK (1994) Changes in the molecular size distribution of insoluble celluloses by the action of recombinant cellulomonas fimi cellulases. Biochem J 302:463–469
Leeflang BR, van Kuik JA, Kroon-Bratenburg LMJ (2006) Oligosaccharides and cellulose crystal surfaces: computer simulations. In: NMR spectroscopy and computer modeling of carbohydrates: recent advances, vol 930. Acs Symposium Series, pp 133–155
Li Y, Lin ML, Davenport JW (2011) Ab initio studies of cellulose I: crystal structure, intermolecular forces, and interactions with water. J Phys Chem C 115(23):11533–11539. doi:10.1021/jp2006759
Mark P, Nilsson L (2001) Structure and dynamics of the TIP3P, SPC, and SPC/E water models at 298 K. J Phys Chem A 105(43):9954–9960. doi:10.1021/jp003020w
Matthews JF, Skopec CE, Mason PE, Zuccato P, Torget RW, Sugiyama J, Himmel ME, Brady JW (2006a) Computer simulation studies of microcrystalline cellulose I beta. Carbohydr Res 341(1):138–152. doi:10.1016/j.carres.2005.09.028
Matthews JF, Skopec CE, Mason PE, Zuccato P, Torget RW, Sugiyama J, Himmel ME, Brady JW (2006b) Computer simulation studies of microcrystalline cellulose I beta. Carbohydr Res 341(1):138–152. doi:10.1016/j.carres.2005.09.028
Mazeau K (2011) On the external morphology of native cellulose microfibrils. Carbohydr Polym 84(1):524–532. doi:10.1016/j.carbpol.2010.12.016
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
Mazeau K, Rivet A (2008) Wetting the (110) and (100) surfaces of I beta cellulose studied by molecular dynamics. Biomacromolecules 9(4):1352–1354. doi:10.1021/bm7013872
Nishiyama Y, Langan P, Chanzy H (2002) Crystal structure and hydrogen-bonding system in cellulose 1 beta from synchrotron X-ray and neutron fiber diffraction. J Am Chem Soc 124(31):9074–9082. doi:10.1021/ja0257319
Patel HA, Nauman EB, Garde S (2003) Molecular structure and hydrophobic solvation thermodynamics at an octane-water interface. J Chem Phys 119(17):9199–9206. doi:10.1063/1.1605942
Queyroy S, Muller-Plathe F, Brown D (2004) Molecular dynamics simulations of cellulose oligomers: conformational analysis. Macromol Theory Simul 13(5):427–440. doi:10.1002/mats.200300054
Rubin EM (2008) Genomics of cellulosic biofuels. Nature 454(7206):841–845. doi:10.1038/nature07190
Ryckaert J-P, Ciccotti G, Berendsen HJC (1977) Numerical integration of the cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes. J Comput Phys 23(3):327–341
Sanchez OJ, Cardona CA (2008) Trends in biotechnological production of fuel ethanol from different feedstocks. Bioresour Technol 99(13):5270–5295. doi:10.1016/j.biortech.2007.11.013
Shen T, Gnanakaran S (2009) The stability of cellulose: a statistical perspective from a coarse-grained model of hydrogen-bond networks. Biophys J 96(8):3032–3040. doi:10.1016/j.bpj.2008.12.3953
Shen T, Langan P, French AD, Johnson GP, Gnanakaran S (2009) Conformational flexibility of soluble cellulose oligomers: chain length and temperature dependence. J Am Chem Soc 131(41):14786–14794. doi:10.1021/ja9034158
Stalbrand H, Mansfield SD, Saddler JN, Kilburn DG, Warren RAJ, Gilkes NR (1998) Analysis of molecular size distributions of cellulose molecules during hydrolysis of cellulose by recombinant Cellulomonas fimi beta-1,4-glucanases. Appl Environ Microbiol 64(7):2374–2379
Stephanopoulos G (2007) Challenges in engineering microbes for biofuels production. Science 315(5813):801–804. doi:10.1126/science.1139612
Stortz CA, French AD (2008) Disaccharide conformational maps: adiabaticity in analogues with variable ring shapes. Mol Simul 34(4):373–389. doi:10.1080/08927020701663339
Umemura M, Yuguchi Y, Hirotsu T (2004) Interaction between cellooligosaccharides in aqueous solution from molecular dynamics simulation: comparison of cellotetraose, cellopentaose, and cellohexaose. J Phys Chem A 108(34):7063–7070. doi:10.1021/jp049044a
Umemura M, Yuguchi Y, Hirotsu T (2005) Hydration at glycosidic linkages of malto- and cello-oligosaccharides in aqueous solution from molecular dynamics simulation: effect of conformational flexibility. J Mol Struct: Theochem 730(1–3):1–8. doi:10.1016/j.theochem.2005.05.034
Wang JM, Wolf RM, Caldwell JW, Kollman PA, Case DA (2004) Development and testing of a general amber force field. J Comput Chem 25(9):1157–1174. doi:10.1002/jcc.20035
Zhang YHP, 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
Acknowledgments
We thank an anonymous reviewer for detailed and insightful comments that have resulted in a better presentation and interpretation of our results. The authors gratefully acknowledge financial support of this work by the National Science Foundation (Grant number: NSF CBET 0854463). Part of the simulations were done on a computational cluster supported by CRIF MU instrumentation grant (Grant number: NSF CHE-0840493) from National Science Foundation.
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Peri, S., Muthukumar, L., Nazmul Karim, M. et al. Dynamics of cello-oligosaccharides on a cellulose crystal surface. Cellulose 19, 1791–1806 (2012). https://doi.org/10.1007/s10570-012-9771-8
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DOI: https://doi.org/10.1007/s10570-012-9771-8