The hydration layer surrounding a protein plays an essential role in its biochemical function and consists of a heterogeneous ensemble of water molecules with different local environments and different dynamics. What determines the degree of dynamical heterogeneity within the hydration shell and how this changes with temperature remains unclear. Here, we combine molecular dynamics simulations and analytic modeling to study the hydration shell structure and dynamics of a typical globular protein, ubiquitin, and of the spruce budworm hyperactive antifreeze protein over the 230–300 K temperature range. Our results show that the average perturbation induced by both proteins on the reorientation dynamics of water remains moderate and changes weakly with temperature. The dynamical heterogeneity arises mostly from the distribution of protein surface topographies and is little affected by temperature. The ice-binding face of the antifreeze protein induces a short-ranged enhancement of water structure and a greater slowdown of water reorientation dynamics than the non-ice-binding faces whose effect is similar to that of ubiquitin. However, the hydration shell of the ice-binding face remains less tetrahedral than the bulk and is not “ice-like”. We finally show that the hydrogen bonds between water and the ice-binding threonine residues are particularly strong due to a steric confinement effect, thereby contributing to the strong binding of the antifreeze protein on ice crystals.

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