Structural micro-heterogeneities of crystalline Iβ-cellulose

The crystal structure of the native I beta-allomorph of cellulose [Nishiyama et al. 2002. J. Am. Chem. Soc. 124: 9074-9082] reveals subtle but significant conformational differences between the two different chains and also a multiplicity of positions of the hydrogen atoms of the HO2 and HO6 hydroxyl groups. Two structures differing in the hydrogen bonding networks were then proposed, however, the static or dynamic origin of the observed disorder remains to be specified. Molecular modelling was used to address this question: 18 minicrystal and 2 macrocrystal models of cellulose were generated differing by the initial orientations of the HO2 and HO6 hydroxyl groups; among which the two proposed structures (called N1 and N16) together with a random structure which respect the experimental percentage of hydroxyl hydrogen orientations. Results showed that only 10 of the studied combinations were stable, the major structure (N1) defined by crystallographers was estimated viable whereas not the minor one (N16). All the calculated data from the retained crystals, which describe the solid dimensions, the individual chain conformations and the supermolecular organisation, 1/ remained stable at their equilibrium value during the dynamics and 2/ were sensitive to the initial positions of the hydrogen atoms. Analysis of the hydrogen bonds revealed that sheet stacking might be stabilised by unexpected hydrogen bonds in addition to hydrophobic interactions. Our results thus favoured local disorders which involve a limited number of chains; they revealed the structural microheterogeneity of the I beta-phase of cellulose and a complex disorder of its corresponding hydrogen bonding networks.