Abstract
Dynamics of hydration water is essential for the function of biomacromolecules. Previous studies have demonstrated that water molecules exhibit subdiffusion on the surface of biomacromolecules; yet the microscopic mechanism remains vague. Here, by performing neutron scattering, molecular dynamics simulations, and analytic modeling on hydrated perdeuterated protein powders, we found water molecules jump randomly between trapping sites on protein surfaces, whose waiting times obey a broad distribution, resulting in subdiffusion. Moreover, the subdiffusive exponent gradually increases with observation time towards normal diffusion due to a many-body volume-exclusion effect.
| Original language | English |
|---|---|
| Article number | 248101 |
| Journal | Physical Review Letters |
| Volume | 120 |
| Issue number | 24 |
| DOIs | |
| State | Published - Jun 11 2018 |
| Externally published | Yes |
Funding
We have developed a comprehensive and compelling physical picture for the diffusion of hydration water on protein surfaces. We have demonstrated the existence of trapping basins for hydration water and have shown that the subdiffusive motion arises from the broad distribution of trapping times. The deep trapping sites are, however, mostly occupied, and thus water molecules preferentially jump to shallow sites. This many-body volume-exclusion interaction leads to biased sampling of trapping times, and results in a continuous increase of the effective diffusion exponent β with the observation time, i.e., a gradual crossover from subdiffusion to normal diffusion. All these features are accurately captured by our mean field lattice toy model (many-body continuous time random walk) with remarkable precision. It has been widely demonstrated that dynamics of water is strongly coupled to that of the enclosed protein molecule, e.g., through hydrogen bonds [44,49] . The mobility of water can thus be passed on to the protein through such coupling, influencing or even controlling the dynamical behaviors of functional importance, such as the fluctuation rate of the protein among different enzymatic states and the migration rate of ligands in and out of the catalytic pocket of the protein molecule, etc. [50] . The present work shows that the many-body volume-exclusion effect makes water molecules jump preferentially among shallow sites, and thus effectively diffuse faster. The resulting greater mobility in water can be eventually delivered to the enclosed protein molecule to gain sufficient flexibility required for its function. This might provide a mechanism to explain why certain hydration (about 20% in weight) is required for enzymes to present appreciable anharmonic dynamics and bioactivity [1] as such many-body effect will be insufficient when the hydration is too low. The authors acknowledge NSF China 11674217, 11504231, 31400704, 31770772, 11771289, and 31630002 and Shanghai Municipal Education Commission and Shanghai Education Development Foundation via “Shu Guang” Project for financial support, and the Center for High Performance Computing at Shanghai Jiao Tong University for computing resources. The authors also thank for Miss Keyi Wu for discussion about the CTRW model and Mr. Zhuo Liu for assistance on the neutron scattering experiment at Oak Ridge National Laboratory (ORNL). The neutron scattering experiment on BASIS (SNS, ORNL) was supported by the Scientific User Facilities Division, Office of Basic Energy Sciences, U.S. Department of Energy. Oak Ridge National Laboratory is managed by UT-Battelle, LLC, for the U.S. DOE under Contract No. DE-AC05-00OR22725. [1] 1 J. A. Rupley and G. Careri , Adv. Protein Chem. 41 , 37 ( 1991 ). APCHA2 0065-3233 10.1016/S0065-3233(08)60197-7 [2] 2 M. C. Bellissent-Funel , A. Hassanali , M. Havenith , R. 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| Funders | Funder number |
|---|---|
| Center for High Performance Computing | |
| NSF China 11674217 | 11771289, 31400704, 11674217, 31630002, 31770772, 11504231 |
| Office of Basic Energy Sciences | |
| Scientific User Facilities Division | |
| U.S. DOE | |
| UT-Battelle | |
| U.S. Department of Energy | |
| Oak Ridge National Laboratory | |
| Shanghai Municipal Education Commission | |
| Shanghai Jiao Tong University | ORNL |