Decrystallization of Oligosaccharides from the Cellulose Iβ Surface with Molecular Simulation

Bundles of cellulose polymers in plant cell walls exhibit a robust network of hydrogen bonds and hydrophobic interactions that must be overcome to decrystallize and hydrolyze the individual polymers to sugars. To investigate the molecular interactions that impart recalcitrance and insolubility to cellulose, we use simulation to determine the decrystallization work, a fundamental, yet experimentally inaccessible measurement, of cello-oligomers from the middle and edge of the hydrophobic face of cellulose Iβ. We demonstrate that cellobiose and cellotetraose decrystallization work does not depend on the position of the oligomer on the crystal surface but that larger oligomers are more difficult to decrystallize depending on the number of intralayer neighbors due to a larger number of stabilizing intralayer hydrogen bonds. The presented results are relevant to mesoscale, morphology-based models of cellulose deconstruction, understanding the molecular details of cellulose decrystallization and insolubility, an...

[1]  David A. Case,et al.  Dynamics of ligand escape from the heme pocket of myoglobin , 1988 .

[2]  Rajesh Khare,et al.  Potential of mean force for separation of the repeating units in cellulose and hemicellulose. , 2011, Carbohydrate research.

[3]  H. Blanch,et al.  A mechanistic model of the enzymatic hydrolysis of cellulose , 2010, Biotechnology and bioengineering.

[4]  Paul Langan,et al.  Crystal structure and hydrogen-bonding system in cellulose Ibeta from synchrotron X-ray and neutron fiber diffraction. , 2002, Journal of the American Chemical Society.

[5]  Edward A Bayer,et al.  Applications of computational science for understanding enzymatic deconstruction of cellulose. , 2011, Current opinion in biotechnology.

[6]  Lars Berglund,et al.  A Coarse-Grained Model for Molecular Dynamics Simulations of Native Cellulose , 2011 .

[7]  Alfred D. French,et al.  Quantum mechanics studies of cellobiose conformations , 2006 .

[8]  G. P. Johnson,et al.  Conformational flexibility of soluble cellulose oligomers: chain length and temperature dependence. , 2009, Journal of the American Chemical Society.

[9]  Jianpeng Ma,et al.  CHARMM: The biomolecular simulation program , 2009, J. Comput. Chem..

[10]  M. Himmel,et al.  Simulation studies of the insolubility of cellulose. , 2010, Carbohydrate research.

[11]  L. Lynd,et al.  A functionally based model for hydrolysis of cellulose by fungal cellulase , 2006, Biotechnology and bioengineering.

[12]  Ilpo Vattulainen,et al.  Analysis of twisting of cellulose nanofibrils in atomistic molecular dynamics simulations. , 2011, The journal of physical chemistry. B.

[13]  A. C. O'sullivan.  Cellulose: the structure slowly unravels , 1997, Cellulose.

[14]  C. Felby,et al.  Yield-determining factors in high-solids enzymatic hydrolysis of lignocellulose , 2009, Biotechnology for biofuels.

[15]  David K. Johnson,et al.  Biomass Recalcitrance: Engineering Plants and Enzymes for Biofuels Production , 2007, Science.

[16]  Bruce E Dale,et al.  Deconstruction of lignocellulosic biomass to fuels and chemicals. , 2011, Annual review of chemical and biomolecular engineering.

[17]  M. Ladisch,et al.  Preparation of cellodextrins: An engineering approach , 1978 .

[18]  P. Väljamäe,et al.  Mechanism of initial rapid rate retardation in cellobiohydrolase catalyzed cellulose hydrolysis , 2010, Biotechnology and bioengineering.

[19]  M. McCarthy,et al.  The effects of water interactions in cellulose suspensions on mass transfer and saccharification efficiency at high solids loadings , 2011 .

[20]  H. Schüttler,et al.  Cellulose hydrolysis in evolving substrate morphologies I: A general modeling formalism , 2009, Biotechnology and bioengineering.

[21]  Alfred D. French,et al.  Disaccharide conformational maps: adiabaticity in analogues with variable ring shapes , 2008 .

[22]  Esben Thormann,et al.  Force pulling of single cellulose chains at the crystalline cellulose-liquid interface: a molecular dynamics study. , 2009, Langmuir : the ACS journal of surfaces and colloids.

[23]  T. Yui,et al.  Swelling behavior of the cellulose Ibeta crystal models by molecular dynamics. , 2006, Carbohydrate research.

[24]  M. Crowley,et al.  Examination of the α-chitin structure and decrystallization thermodynamics at the nanoscale. , 2011, The journal of physical chemistry. B.

[25]  G. P. Johnson,et al.  Cellulose and the twofold screw axis: modeling and experimental arguments , 2009 .

[26]  G. Torrie,et al.  Nonphysical sampling distributions in Monte Carlo free-energy estimation: Umbrella sampling , 1977 .

[27]  Baron Peters,et al.  Molecular-level origins of biomass recalcitrance: decrystallization free energies for four common cellulose polymorphs. , 2011, The journal of physical chemistry. B.

[28]  K Schulten,et al.  VMD: visual molecular dynamics. , 1996, Journal of molecular graphics.

[29]  Christopher H. Chang,et al.  The energy landscape for the interaction of the family 1 carbohydrate-binding module and the cellulose surface is altered by hydrolyzed glycosidic bonds. , 2009, The journal of physical chemistry. B.

[30]  Alexander D. MacKerell,et al.  CHARMM Additive All-Atom Force Field for Glycosidic Linkages between Hexopyranoses. , 2009, Journal of chemical theory and computation.

[31]  R. Swendsen,et al.  THE weighted histogram analysis method for free‐energy calculations on biomolecules. I. The method , 1992 .

[32]  M. Himmel,et al.  Computer simulation studies of microcrystalline cellulose Iβ , 2006 .

[33]  Bernard R. Brooks,et al.  Solvent-Induced Forces between Two Hydrophilic Groups , 1994 .

[34]  Alexander D. MacKerell,et al.  Additive empirical force field for hexopyranose monosaccharides , 2008, J. Comput. Chem..

[35]  G. P. Johnson,et al.  Advanced conformational energy surfaces for cellobiose** , 2004 .

[36]  Jay H. Lee,et al.  Modeling cellulase kinetics on lignocellulosic substrates. , 2009, Biotechnology advances.

[37]  C L Brooks,et al.  Calculations on folding of segment B1 of streptococcal protein G. , 1998, Journal of molecular biology.

[38]  W. L. Jorgensen,et al.  Comparison of simple potential functions for simulating liquid water , 1983 .

[39]  H. Schüttler,et al.  Cellulose hydrolysis in evolving substrate morphologies II: Numerical results and analysis , 2009, Biotechnology and bioengineering.

[40]  J. Chu,et al.  On the molecular origins of biomass recalcitrance: the interaction network and solvation structures of cellulose microfibrils. , 2010, The journal of physical chemistry. B.

[41]  C. Wyman,et al.  Sugar monomer and oligomer solubility , 2003, Applied biochemistry and biotechnology.