Dynamics and mechanism of ultrafast water–protein interactions

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 113; no. 30; pp. 8424 - 8429
• Main Authors: Qin, Yangzhong, Wang, Lijuan, Zhong, Dongping
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences 26-07-2016
• Series: From the Cover
• Subjects: Algorithms; Biological Sciences; Kinetics; Models, Chemical; Molecular Dynamics Simulation; Molecules; Motion; Physical Sciences; Protein Binding; Protein Conformation; Proteins; Proteins - chemistry; Proteins - metabolism; Spectrometry, Fluorescence - methods; Spectrum analysis; Surface Properties; Temperature; Thermodynamics; Time Factors; Tryptophan; Water; Water - chemistry; Water - metabolism; protein side-chain motion; water-driven relaxation; tryptophan scan; coupled fluctuation; hydration shell dynamics
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.1602916113

Protein hydration is essential to its structure, dynamics, and function, but water–protein interactions have not been directly observed in real time at physiological temperature to our awareness. By using a tryptophan scan with femtosecond spectroscopy, we simultaneously measured the hydration water dynamics and protein side-chain motions with temperature dependence. We observed the heterogeneous hydration dynamics around the global protein surface with two types of coupled motions, collective water/side-chain reorientation in a few picoseconds and cooperative water/side-chain restructuring in tens of picoseconds. The ultrafast dynamics in hundreds of femtoseconds is from the outer-layer, bulk-type mobile water molecules in the hydration shell. We also found that the hydration water dynamics are always faster than protein side-chain relaxations but with the same energy barriers, indicating hydration shell fluctuations driving protein side-chain motions on the picosecond time scales and thus elucidating their ultimate relationship.