Observation of fragile-to-strong dynamic crossover in protein hydration water

Abstract

At low temperatures, proteins exist in a glassy state, a state that has no conformational flexibility and shows no biological functions. In a hydrated protein, at temperatures greater-- similar 220 K, this flexibility is restored, and the protein is able to sample more conformational substates, thus becoming biologically functional. This "dynamical" transition of protein is believed to be triggered by its strong coupling with the hydration water, which also shows a similar dynamic transition. Here we demonstrate experimentally that this sudden switch in dynamic behavior of the hydration water on lysozyme occurs precisely at 220 K and can be described as a fragile-to-strong dynamic crossover. At the fragile-to-strong dynamic crossover, the structure of hydration water makes a transition from predominantly high-density (more fluid state) to low-density (less fluid state) forms derived from the existence of the second critical point at an elevated pressure.

Fig. 1.

Measured neutron spectra. Shown are normalized QENS spectra at Q = 0.87 Å⁻¹, displaying the height of the peak (A) and the wing of the peak (B) at a series of temperatures. (A Inset) A plot of the peak heights vs. temperature. Arrows in B highlight the wing of the spectra at the crossover temperature.

Fig. 2.

Neutron spectra and their RCM analyses. Measured QENS spectra (filled symbols) and their RCM analysis results (solid lines) at Q = 0.87 Å⁻¹ and at a series of temperatures are shown. (Inset) One particular spectrum at T = 230 K is singled out and contrasted with the resolution function of the instrument for this Q value (dashed line).

Fig. 3.

Evidence for the dynamic transition. (A) The temperature dependence of the mean-squared atomic displacement of the hydrogen atom at 2-ns time scale measured by an elastic scan with resolution of 0.8 μeV. (B) Temperature dependence of the average translational relaxation times plotted in log(〈τ_T〉) vs. T₀/T, where T₀ is the ideal glass transition temperature. Here, there is a clear and abrupt transition from a Vogel–Fulcher–Tammann law at high temperatures to an Arrhenius law at low temperatures, with the fitted crossover temperature T_L = 220 K and the activation energy E_A = 3.13 kcal/mol extracted from the Arrhenius part indicated in the figure.

Fig. 4.

Temperature dependence of the exponents β (Inset) and βγ giving, respectively, the power laws of t and Q-dependence of the ISF.