The building blocks of cellulose: the intrinsic conformational structures of cellobiose, its epimer, lactose, and their singly hydrated complexes.

A combination of vibrational spectroscopy conducted under molecular beam conditions and quantum chemical calculation has established the intrinsic three-dimensional structures of the cellulose disaccharide and, focusing on the critical beta1,4-linkage at the nonreducing end of the growing cellulose polymer, its C-4' epimer. Left to their own devices they both adopt a cis (anti-phi/syn-psi) glycosidic configuration, supported in the epimer by strong, cooperative inter-ring hydrogen bonding. In the cellulose disaccharide, however, where the OH-4'(Glc) group is equatorial, the cooperativity is reduced and the corresponding inter-ring hydrogen bonding is relatively weak. The cis conformational preference is still retained in their singly hydrated complexes. In the cellulose disaccharide insertion of the water molecule at the favored binding site between OH-4' and the neighboring hydroxyl group OH-6' promotes a structural reorganization to create a configuration that parallels that of its unhydrated epimer and greatly strengthens the inter-ring hydrogen bonding. In the C-4' epimer, the axial orientation of OH-4' blocks this binding site and the bound water molecule simply adds on at the end of the (OH-O)(n) chain, which has a negligible effect on the (already strong) inter-ring bonding. The implications of these results are discussed with respect to the structure and insolubility of native cellulose polymers.

[1]  J. Simons,et al.  Peptide secondary structures in the gas phase: consensus motif of N-linked glycoproteins. , 2009, Journal of the American Chemical Society.

[2]  J. Simons,et al.  Conformational choice and selectivity in singly and multiply hydrated monosaccharides in the gas phase. , 2008, Chemistry.

[3]  J. Simons,et al.  Solvent interactions and conformational choice in a core N-glycan segment: gas phase conformation of the central, branching trimannose unit and its singly hydrated complex. , 2008, Journal of the American Chemical Society.

[4]  G. P. Johnson,et al.  Roles of starting geometries in quantum mechanics studies of cellobiose , 2008 .

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

[6]  R. Stenutz,et al.  Conformational analysis of beta-glycosidic linkages in 13C-labeled glucobiosides using inter-residue scalar coupling constants. , 2008, The journal of physical chemistry. B.

[7]  R. Campen,et al.  Influence of glycosidic linkage neighbors on disaccharide conformation in vacuum. , 2007, The journal of physical chemistry. B.

[8]  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 .

[9]  Wayne B. Bosma,et al.  Stepwise hydration of cellobiose by DFT methods: 1. Conformational and structural changes brought about by the addition of one to four water molecules , 2006 .

[10]  J. Simons,et al.  Hydrogen bonding and cooperativity in isolated and hydrated sugars: mannose, galactose, glucose, and lactose. , 2005, Journal of the American Chemical Society.

[11]  N. Macleod,et al.  Sugars in the gas phase. Spectroscopy, conformation, hydration, co-operativity and selectivity , 2005 .

[12]  R. Brown,et al.  Cellulose biosynthesis: current views and evolving concepts. , 2005, Annals of botany.

[13]  M. Martín-Pastor,et al.  Limited flexibility of lactose detected from residual dipolar couplings using molecular dynamics simulations and steric alignment methods. , 2005, Journal of the American Chemical Society.

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

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

[16]  J. Simons,et al.  Probing the glycosidic linkage: UV and IR ion-dip spectroscopy of a lactoside. , 2004, Journal of the American Chemical Society.

[17]  A. French.  Comments on the paper ‘The behavior of cellulose molecules in aqueous environments’ by Tanaka and Fukui , 2004 .

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

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

[20]  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.

[21]  P. Zugenmaier.  Conformation and packing of various crystalline cellulose fibers , 2001 .

[22]  J. L. Asensio,et al.  The use of the AMBER force field in conformational analysis of carbohydrate molecules: Determination of the solution conformation of methyl α‐lactoside by NMR spectroscopy, assisted by molecular mechanics and dynamics calculations , 1995, Biopolymers.

[23]  G. Chang,et al.  Macromodel—an integrated software system for modeling organic and bioorganic molecules using molecular mechanics , 1990 .

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

[25]  C. Hudson,et al.  The Alkaline Degradation of Phenyl-β-lactoside, Phenyl-β-cellobioside and Phenyl-D-gluco-β-D-gulo-heptoside , 1943 .