Role of residual water hydrogen bonding in sugar/water/biomolecule systems: a possibleexplanation for trehalose peculiarity

Abstract

We report on the set of experimental and simulative evidences which enabled us to suggesthow biological structures embedded in a non-liquid water–saccharide solvent are anchoredto the surrounding matrix via a hydrogen bond network. Such a network, whose rigidityincreases by decreasing the sample water content, couples the degrees of freedom of thebiostructure to those of the matrix and gives place to protein–saccharide–water structures(protein–solvent conformational substates). In particular, the whole set of data evidencesthat, while the protein–sugar interaction is well described in terms of a waterentrapment hypothesis, the water replacement hypothesis better describes thesugar–membrane interaction; furthermore, it gives a hint towards the understanding ofthe origin of the trehalose peculiarity since the biomolecule–matrix coupling,specific to each particular sugar, always results in being the tightest for trehalose.In line with the heterogeneous dynamics in supercooled fluids and in carbohydrate glassesof different residual water contents, recent results confirm, at the single molecule level, theexistence of protein–solvent conformational substates, spatially heterogeneousand interconverting, whose rigidity increases by lowering the sample hydration.