Photoinduced hole hopping through tryptophans in proteins

Hole hopping through tryptophan/tyrosine chains enables rapid unidirectional charge transport over long distances. We have elucidated structural and dynamical factors controlling hopping speed and efficiency in two modified azurin constructs that include a rhenium(I) sensitizer, Re(His)(CO)(3)(dmp)(+), and one or two tryptophans (W-1, W-2). Experimental kinetics investigations showed that the two closely spaced (3 to 4 angstrom) intervening tryptophans dramatically accelerated long-range electron transfer (ET) from Cu-I to the photoexcited sensitizer. In our theoretical work, we found that time-dependent density-functional theory (TDDFT) quantum mechanics/molecular mechanics/molecular dynamics (QM/MM/MD) trajectories of low-lying triplet excited states of ReI(His)(CO)(3)(dmp)+-W-1(-W-2) exhibited crossings between sensitizer-localized (*Re) and charge-separated [ReI(His)(CO)(3)(dmp(center dot-))/(W1(center dot+) or W2(center dot+))] (CS1 or CS2) states. Our analysis revealed that the distances, angles, and mutual orientations of ET-active cofactors fluctuate in a relatively narrow range in which the cofactors are strongly coupled, enabling adiabatic ET. Water-dominated electrostatic field fluctuations bring *Re and CS1 states to a crossing where *Re(CO)(3)(dmp)(+)<- W-1 ET occurs, and CS1 becomes the lowest triplet state. ET is promoted by solvation dynamics around *Re(CO)(3)(dmp)+(W-1); and CS1 is stabilized by Re(dmp(center dot-))/W-1(center dot+) electron/hole interaction and enhanced W-1(center dot+) solvation. The second hop, W-1(center dot+)<- W-2, is facilitated by water fluctuations near the W-1/W-2 unit, taking place when the electrostatic potential at W-2 drops well below that at W1(center dot+). Insufficient solvation and reorganization around W2 make W-1(center dot+)<- W-2 ET endergonic, shifting the equilibrium toward W-1(center dot+) and decreasing the charge-separation yield. We suggest that multiscale TDDFT/MM/MD is a suitable technique to model the simultaneous evolution of photogenerated excited-state manifolds.