Local site selectivity and conformational structures in the glycosidic bond scission of cellobiose.

Car-Parrinello molecular dynamics combined with metadynamics simulations were used to study the acid-catalyzed hydrolysis of cellobiose (CB) in aqueous solution. The hydrolysis was studied in two steps. Step 1 involves the proton transfer from solvent to CB and dissociation of the glycosidic bond to β-glucose and oxacarbenium ion species. Step 2 involves the formation of α-glucose from oxacarbenium and regeneration of the acid proton species. Step 1 is endothermic, while Step 2 is exothermic. The overall activation free energy of CB hydrolysis is 32.5 kcal mol(-1), and the overall reaction free energy is -5.9 kcal mol(-l), consistent with available experimental data. We observe that a stepwise mechanism generally described in the literature for Step 1 is not significantly favored relative to a concerted β-1,4' linkage dissociation process.

[1]  Dominik Marx,et al.  Aspects of glycosidic bond formation in aqueous solution: chemical bonding and the role of water. , 2005, Chemistry.

[2]  I. J. Barker,et al.  Mechanism of xylobiose hydrolysis by GH43 β-xylosidase. , 2010, The journal of physical chemistry. B.

[3]  Alessandro Laio,et al.  A Hamiltonian electrostatic coupling scheme for hybrid Car-Parrinello molecular dynamics simulations , 2002 .

[4]  Nicolas Abatzoglou,et al.  Phenomenological kinetics of complex systems: mechanistic considerations in the solubilization of hemicelluloses following aqueous/steam treatments , 1991 .

[5]  J. Sugiyama,et al.  Electron diffraction study on the two crystalline phases occurring in native cellulose from an algal cell wall , 1991 .

[6]  J. R. Pliego,et al.  Gibbs energy of solvation of organic ions in aqueous and dimethyl sulfoxide solutions , 2002 .

[7]  R N Goldberg,et al.  Thermodynamics of hydrolysis of disaccharides. Cellobiose, gentiobiose, isomaltose, and maltose. , 1989, The Journal of biological chemistry.

[8]  M. Cascella,et al.  Formamide Hydrolysis Investigated by Multiple-Steering ab Initio Molecular Dynamics , 2004 .

[9]  Serge Kaliaguine,et al.  A Monte Carlo analysis of acid hydrolysis of glycosidic bonds in polysaccharides , 1991 .

[10]  G. A. Jeffrey,et al.  The refinement of the crystal structures of -D-glucose and cellobiose , 1968 .

[11]  Wayne B. Bosma,et al.  Stepwise hydration of cellobiose by DFT methods: 2. Energy contributions to relative stabilities of cellobiose·(H2O)1–4 complexes , 2006 .

[12]  David K. Johnson,et al.  Free energy landscape for glucose condensation reactions. , 2010, The journal of physical chemistry. A.

[13]  Dominik Marx,et al.  Influence of extreme thermodynamic conditions and pyrite surfaces on peptide synthesis in aqueous media. , 2008, Journal of the American Chemical Society.

[14]  W. Jencks.  Ingold Lecture. How does a reaction choose its mechanism , 1981 .

[15]  Bernhardt L Trout,et al.  A molecular mechanism of hydrolysis of peptide bonds at neutral pH using a model compound. , 2011, The journal of physical chemistry. B.

[16]  C. Rovira,et al.  Mechanism of cellulose hydrolysis by inverting GH8 endoglucanases: a QM/MM metadynamics study. , 2009, The journal of physical chemistry. B.

[17]  D. Zahn.  Theoretical Study of the Mechanisms of Acid-Catalyzed Amide Hydrolysis in Aqueous Solution , 2003 .

[18]  R. Atalla,et al.  The role of solid state 13C NMR spectroscopy in studies of the nature of native celluloses. , 1999, Solid state nuclear magnetic resonance.

[19]  G. Csonka.  Proper basis set for quantum mechanical studies of potential energy surfaces of carbohydrates , 2002 .

[20]  C. Passingham,et al.  Fourier transform Raman studies of materials and compounds of biological importance—II. The effect of moisture on the molecular structure of the alpha and beta anomers of d-glucose , 1991 .

[21]  Donald G. Truhlar,et al.  Factors controlling relative stability of anomers and hydroxymethyl conformers of glucopyranose , 1998, J. Comput. Chem..

[22]  Manuel Calderón Sánchez,et al.  Theoretical study of the relative stability of rotational conformers of alpha and beta-D-glucopyranose in gas phase and aqueous solution. , 2004, Journal of the American Chemical Society.

[23]  Paramita Dasgupta,et al.  NMR and modelling studies of disaccharide conformation. , 2003, Carbohydrate research.

[24]  Car,et al.  Unified approach for molecular dynamics and density-functional theory. , 1985, Physical review letters.

[25]  Donald G. Truhlar,et al.  Relative stability of alternative chair forms and hydroxymethyl conformations of β-d-glucopyranose , 1995 .

[26]  Xianghong Qian,et al.  The effects of water on beta-D-xylose condensation reactions. , 2009, The journal of physical chemistry. A.

[27]  Norman L. Allinger,et al.  Theoretical Studies of the Potential Energy Surfaces and Compositions of the d-Aldo- and d-Ketohexoses , 1998 .

[28]  A. Catellani,et al.  Ab initio molecular dynamics study of the keto-enol tautomerism of acetone in solution. , 2006, Chemphyschem : a European journal of chemical physics and physical chemistry.

[29]  G. Widmalm,et al.  Determination of the Conformational Flexibility of Methyl α-Cellobioside in Solution by NMR Spectroscopy and Molecular Simulations , 2004 .

[30]  Nobuaki Miura,et al.  A theoretical study of α- and β-d-glucopyranose conformations by the density functional theory , 2006 .

[31]  Teter,et al.  Separable dual-space Gaussian pseudopotentials. , 1996, Physical review. B, Condensed matter.

[32]  K. Houk,et al.  Molecular dynamics prediction of the mechanism of ester hydrolysis in water. , 2008, Journal of the American Chemical Society.

[33]  Alessandro Laio,et al.  Dissociation mechanism of acetic acid in water. , 2006, Journal of the American Chemical Society.

[34]  Bernd Ensing,et al.  Formamide hydrolysis in alkaline aqueous solution: insight from Ab initio metadynamics calculations. , 2006, Angewandte Chemie.

[35]  S. Kaliaguine,et al.  Acid hydrolysis of cellulose. part i. experimental kinetic analysis , 1993 .

[36]  D. Vlachos,et al.  Converting fructose to 5-hydroxymethylfurfural: a quantum mechanics/molecular mechanics study of the mechanism and energetics. , 2011, Carbohydrate research.

[37]  C. Brown.  The crystalline structure of the sugars. Part VI. A three-dimensional analysis of β-celloboise , 1966 .

[38]  Alessandro Laio,et al.  Efficient exploration of reactive potential energy surfaces using Car-Parrinello molecular dynamics. , 2003, Physical review letters.

[39]  David K. Johnson,et al.  Glucose reversion reaction kinetics. , 2010, Journal of agricultural and food chemistry.

[40]  J. L. Willett,et al.  Ab initio computational study of β-cellobiose conformers using B3lYP/6-311++G** , 2002 .

[41]  J. Simons,et al.  The building blocks of cellulose: the intrinsic conformational structures of cellobiose, its epimer, lactose, and their singly hydrated complexes. , 2009, Journal of the American Chemical Society.

[42]  S. Nosé.  A unified formulation of the constant temperature molecular dynamics methods , 1984 .

[43]  Preston Moore,et al.  Metadynamics as a tool for exploring free energy landscapes of chemical reactions. , 2006, Accounts of chemical research.

[44]  A. Becke,et al.  Density-functional exchange-energy approximation with correct asymptotic behavior. , 1988, Physical review. A, General physics.

[45]  Parr,et al.  Development of the Colle-Salvetti correlation-energy formula into a functional of the electron density. , 1988, Physical review. B, Condensed matter.

[46]  Donald G. Truhlar,et al.  AM1-SM2 and PM3-SM3 parameterized SCF solvation models for free energies in aqueous solution , 1992, J. Comput. Aided Mol. Des..

[47]  Frank A. Momany,et al.  B3LYP/6-311++G** study of α- and β-d-glucopyranose and 1,5-anhydro-d-glucitol: 4C1 and 1C4 chairs, 3,OB and B3,O boats, and skew-boat conformations , 2004 .

[48]  R. Goldberg,et al.  Thermodynamics of the hydrolysis reactions of 1,4-β-d-xylobiose, 1,4-β-d-xylotriose, d-cellobiose, and d-maltose☆ , 2008 .

[49]  Wilfred F van Gunsteren,et al.  Conformational and dynamical properties of disaccharides in water: a molecular dynamics study. , 2006, Biophysical journal.

[50]  G. Zaikov,et al.  The mechanism of the acid-catalysed hydrolysis of glucosides , 1976 .

[51]  G. Thatcher.  Anomeric and Associated Stereoelectronic Effects: Scope and Controversy , 1993 .

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

[53]  M. Sinnott,et al.  Catalytic mechanism of enzymic glycosyl transfer , 1990 .

[54]  D. Whitfield.  Computational studies of the role of glycopyranosyl oxacarbenium ions in glycobiology and glycochemistry. , 2009, Advances in carbohydrate chemistry and biochemistry.

[55]  A. Cieplak.  Stereochemistry of Nucleophilic Addition to Cyclohexanone. The Importance of Two-Electron Stabilizing Interactions , 1981 .

[56]  C. Cramer,et al.  Universal solvation model based on solute electron density and on a continuum model of the solvent defined by the bulk dielectric constant and atomic surface tensions. , 2009, The journal of physical chemistry. B.

[57]  K. Bhat,et al.  Structure of 4-[4-(Dimethylamino)-Phenylazo] Benzeneboronic Acid and Its Cyclic Esters with D-Glucose: A Computational Study , 2004 .

[58]  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.