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

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 the 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 Å 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.

How Does Solvation Layer Mobility Affect Protein Structural Dynamics?

“…The model can be readily tested by comparing solvation shell dynamics at different locations, which can be achieved through a variety of spectroscopic techniques (e.g., ultrafast fluorescence, IR, NMR spectroscopies). Using simulations to predict changes in solvation shell dynamics is also viable, as calculated solvent dynamics have reasonably reproduced experimental measurements in recent studies (King et al, 2012 ; Dielmann-Gessner et al, 2014 ; Abel et al, 2016 ; George et al, 2016 ; Charkhesht et al, 2018 ).…”

Insights into Hydration Dynamics and Cooperative Interactions in Glycerol–Water Mixtures by Terahertz Dielectric Spectroscopy

“…These changes are expected to occur as a water molecular and a glycerol molecule have different molecular weight and polarity, which affect the orientational relaxation of the associated dipoles. 17,20,[25][26] Figure 2: Dielectric response of the 19.69 mol % glycerol-water mixture in the frequency range from 50 MHz to 0.5 THz reflecting the complexity of glycerol-water interactions. The imaginary and the real (in the inset) components of the dielectric spectra have been decomposed in to four relaxational processes with different relaxation time constants.…”

Investigation of the hydration shell of a membrane in an open system molecular dynamics simulation

“…Results similar to ours are also found in direct determination of the hydration layer around biomolecules using spectroscopic and molecular dynamics data. For example, in a recent paper by Charkhest and coworkers [19], it was shown that a protein (bovine serum albumin) influences the dynamics of water well beyond the first solvation layer, to around 0.7 nm from the protein surface. In conclusion, while we certainly cannot claim that our criteria of analysis represents a universal definition of hydration shell, our technique can certainly be employed in a complementary way to identify relevant degrees of freedom involved in the hydration process and be used in relation to findings of other groups that employ other tools of analysis for a proper interpretation of hydration mechanisms.…”