Effects of Nonthermal Excitation Mediated by Sub-Terahertz Radiation on Hydrogen Exchange in Ubiquitin.

Abstract

Water dynamics in the hydration layers of biomolecules play crucial roles in a wide range of biological functions. A hydrated protein contains multiple components of diffusional and vibrational dynamics of water and protein, which may be coupled at approximately 0.1-terahertz frequency (10-picosecond timescale) at room temperature. However, the microscopic description of biomolecular functions based on various modes of protein-water-coupled motions remains elusive. A novel approach for perturbing the hydration dynamics in the sub-terahertz frequency range and probing them at the atomic level is therefore warranted. In this study, we investigated the effect of klystron-based, intense 0.1-terahertz excitation on the slow dynamics of ubiquitin using NMR-based measurements of hydrogen-deuterium exchange. We demonstrated that the sub-terahertz irradiation accelerated the hydrogen-deuterium exchange of the amides located in the interior of the protein and hydrophobic surfaces, while decelerating this exchange in the amides located in the surface loop and short 310 helix regions. This sub-terahertz-radiation-induced effect was qualitatively contradictory to the increased temperature-induced effect. Our results suggest that the heterogeneous water dynamics occurring at the protein-water interface include components that are nonthermally excited by the sub-terahertz radiation. Such sub-terahertz-excited components may be linked to the slow function-related dynamics of the protein.