We report experimental and theoretical studies on water and protein
dynamics following photoexcitation of apomyoglobin. Using
site-directed mutation and with femtosecond resolution, we
experimentally observed relaxation dynamics with a biphasic
distribution of time scales, 5 and 87 ps, around the site Trp7.
Theoretical studies using both linear response and direct
nonequilibrium molecular dynamics (MD) calculations reproduced the
biphasic behavior. Further constrained MD simulations with either
frozen protein or frozen water revealed the molecular mechanism of
slow hydration processes and elucidated the role of protein
fluctuations. Observation of slow water dynamics in MD simulations
requires protein flexibility, regardless of whether the slow Stokes
shift component results from the water or protein contribution. The
initial dynamics in a few picoseconds represents fast local motions
such as reorientations and translations of hydrating water
molecules, followed by slow relaxation involving strongly coupled
water-protein motions. We observed a transition from one isomeric
protein configuration to another after 10 ns during our 30 ns
ground-state simulation. For one isomer, the surface hydration
energy dominates the slow component of the total relaxation energy.
For the other isomer, the slow component is dominated by protein
interactions with the chromophore. In both cases, coupled
water-protein motion is shown to be necessary for observation of the
slow dynamics. Such biologically important water-protein motions
occur on tens of picoseconds. One significant discrepancy exists
between theory and experiment, the large inertial relaxation
predicted by simulations but clearly absent in experiment. Further
improvements required in the theoretical model are discussed.
Linear response theory has been reported to give good approximations
with the nonequilibrium relaxation of Stokes shift in the studies of
solvation dynamics. It breaks down for Trp-140 (W140) in
Staphylococcus nuclease. Two isomers are found in the electronic
ground state of Trp on the time scale of 35 nanosecond simulation.
Isomerization of local structure around W151 is crucial to explain
the mechanism how linear response theory deviates from the
nonequilibrium process.