How biomolecules influence water structure and dynamics

Abstract

Interactions between solutes and water impact both water structure and structural dynamics as well as solute properties (e.g. conformational fluctuations of proteins). To understand these interactions we investigate water near disaccharides using classical atomistic molecular dynamics simulations. Disaccharides show topological and chemical complexity characteristic of larger biomolecules but are sufficiently small to permit detailed study. We observe that increases in hydrophobicity precisely map slow down in water translation and rotation of local water populations. In line with recent studies of proteins, we find that chemically similar functional groups may interact differently with water depending on neighboring functional groups. To explain these observations we examine the mechanism of hydrogen bond exchange for waters hydrogen bonded to other waters but within the sugar first solvation shell, as well as waters hydrogen bonded to the sugar. Recent work showed that water in bulk rotates through large angular jumps that pass through bifurcated hydrogen bond intermediates and that rotation rates can be rationalized through transition state theory. Previous reports found that the rotational slow down of water near small solutes can be predicted from changes in the accessible transition state volume or the enthalpy of the hydrogen bonds. For our larger solutes we find that accounting for the transition state volume alone overestimates water rotational slow down. Differences in hydrogen bond enthalpy are also insufficient to predict rotational slowdown. Water slowdown can only be understood by additionally accounting for subtle changes in the free energy landscape associated with water rotation - reduction in the number of available reactant states and broadening of the transition state barriers. The presence of solutes of even moderate size thus affects water dynamics in ways difficult to predict using simple scaling considerations from bulk, making water response system dependent.