High-Precision Megahertz-to-Terahertz Dielectric Spectroscopy of Protein Collective Motions and Hydration Dynamics

TL;DR

This study uses advanced dielectric spectroscopy from megahertz to terahertz frequencies to uncover detailed protein-water interactions and collective motions, providing new insights into hydration dynamics and their role in protein function.

Contribution

The paper introduces high-precision dielectric measurements combined with simulations to analyze protein hydration layers and collective vibrational modes at unprecedented frequency ranges.

Findings

Identification of multiple polarization mechanisms with distinct time constants.

Determination of hydration water molecules extending beyond the first solvation layer.

Water molecules near the protein surface exhibit significant dynamical slowdown.

Abstract

The low-frequency collective vibrational modes in proteins as well as the protein-water interface have been suggested as dominant factors controlling the efficiency of biochemical reactions and biological energy transport. It is thus crucial to uncover the mystery of hydration structure and dynamics as well as their coupling to collective motions of proteins in aqueous solutions. Here we report dielectric properties of aqueous bovine serum albumin protein solutions as a model system using an extremely sensitive dielectric spectrometer with frequencies spanning from megahertz to terahertz. The dielectric relaxation spectra reveal several polarization mechanisms at the molecular level with different time constants and dielectric strengths, reflecting the complexity of protein-water interactions. Combining the effective-medium approximation and molecular dynamics simulations, we have determined collective vibrational modes at terahertz frequencies and the number of water molecules in the tightly-bound and loosely-bound hydration layers. High-precision measurements of the number of hydration water molecules indicate that the dynamical influence of proteins extends beyond the first solvation layer, to around 7 {\AA} distance from the protein surface, with the largest slowdown arising from water molecules directly hydrogen-bonded to the protein. Our results reveal critical information of protein dynamics and protein-water interfaces, which determine biochemical functions and reactivity of proteins.