Photoinduced hole hopping through tryptophans in proteins
| Autor: | Harry B. Gray, Jan Heyda, Stanislav Záliš, Filip Šebesta, Jay R. Winkler, Antonín Vlček |
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| Jazyk: | angličtina |
| Rok vydání: | 2021 |
| Předmět: |
Physics
Multidisciplinary Photochemistry Static Electricity Solvation Tryptophan Water Electrons Electron Time-dependent density functional theory Molecular Dynamics Simulation Biological Sciences Electron Transport Molecular dynamics Electron transfer Rhenium Chemical physics Azurin Excited state Pseudomonas aeruginosa Quantum Theory Triplet state Oxidation-Reduction |
| Zdroj: | Proc Natl Acad Sci U S A |
| Popis: | 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. |
| Databáze: | OpenAIRE |
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