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 Å) 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 Re ^I (His)(CO) ₃ (dmp) ⁺ -W ₁ (-W ₂ ) exhibited crossings between sensitizer-localized (*Re) and charge-separated [Re ^I (His)(CO) ₃ (dmp ^•- )/(W ₁ ^•+ or W ₂ ^•+ )] (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 ^•- )/W ₁ ^•+ electron/hole interaction and enhanced W ₁ ^•+ solvation. The second hop, W ₁ ^•+ ←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 W ₁ ^•+ Insufficient solvation and reorganization around W ₂ make W ₁ ^•+ ←W ₂ ET endergonic, shifting the equilibrium toward W ₁ ^•+ 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.
Competing Interests: The authors declare no competing interest.