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) (dmp) ,...
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| Vydané v: | Proceedings of the National Academy of Sciences - PNAS Ročník 118; číslo 11 |
|---|---|
| Hlavní autori: | , , , , , |
| Médium: | Journal Article |
| Jazyk: | English |
| Vydavateľské údaje: |
United States
16.03.2021
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| ISSN: | 1091-6490, 1091-6490 |
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| Abstract | 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)
(dmp)
, and one or two tryptophans (W
, W
). Experimental kinetics investigations showed that the two closely spaced (3 to 4 Å) intervening tryptophans dramatically accelerated long-range electron transfer (ET) from Cu
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
(His)(CO)
(dmp)
-W
(-W
) exhibited crossings between sensitizer-localized (*Re) and charge-separated [Re
(His)(CO)
(dmp
)/(W
or W
)] (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)
(dmp)
←W
ET occurs, and CS1 becomes the lowest triplet state. ET is promoted by solvation dynamics around *Re(CO)
(dmp)
(W
); and CS1 is stabilized by Re(dmp
)/W
electron/hole interaction and enhanced W
solvation. The second hop, W
←W
, is facilitated by water fluctuations near the W
/W
unit, taking place when the electrostatic potential at W
drops well below that at W
Insufficient solvation and reorganization around W
make W
←W
ET endergonic, shifting the equilibrium toward W
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. |
|---|---|
| AbstractList | 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 (W1, W2). Experimental kinetics investigations showed that the two closely spaced (3 to 4 Å) intervening tryptophans dramatically accelerated long-range electron transfer (ET) from CuI 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)+-W1(-W2) exhibited crossings between sensitizer-localized (*Re) and charge-separated [ReI(His)(CO)3(dmp•-)/(W1•+ or W2•+)] (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)+←W1 ET occurs, and CS1 becomes the lowest triplet state. ET is promoted by solvation dynamics around *Re(CO)3(dmp)+(W1); and CS1 is stabilized by Re(dmp•-)/W1•+ electron/hole interaction and enhanced W1•+ solvation. The second hop, W1•+←W2, is facilitated by water fluctuations near the W1/W2 unit, taking place when the electrostatic potential at W2 drops well below that at W1•+ Insufficient solvation and reorganization around W2 make W1•+←W2 ET endergonic, shifting the equilibrium toward W1•+ 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.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 (W1, W2). Experimental kinetics investigations showed that the two closely spaced (3 to 4 Å) intervening tryptophans dramatically accelerated long-range electron transfer (ET) from CuI 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)+-W1(-W2) exhibited crossings between sensitizer-localized (*Re) and charge-separated [ReI(His)(CO)3(dmp•-)/(W1•+ or W2•+)] (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)+←W1 ET occurs, and CS1 becomes the lowest triplet state. ET is promoted by solvation dynamics around *Re(CO)3(dmp)+(W1); and CS1 is stabilized by Re(dmp•-)/W1•+ electron/hole interaction and enhanced W1•+ solvation. The second hop, W1•+←W2, is facilitated by water fluctuations near the W1/W2 unit, taking place when the electrostatic potential at W2 drops well below that at W1•+ Insufficient solvation and reorganization around W2 make W1•+←W2 ET endergonic, shifting the equilibrium toward W1•+ 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. 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) (dmp) , and one or two tryptophans (W , W ). Experimental kinetics investigations showed that the two closely spaced (3 to 4 Å) intervening tryptophans dramatically accelerated long-range electron transfer (ET) from Cu 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 (His)(CO) (dmp) -W (-W ) exhibited crossings between sensitizer-localized (*Re) and charge-separated [Re (His)(CO) (dmp )/(W or W )] (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) (dmp) ←W ET occurs, and CS1 becomes the lowest triplet state. ET is promoted by solvation dynamics around *Re(CO) (dmp) (W ); and CS1 is stabilized by Re(dmp )/W electron/hole interaction and enhanced W solvation. The second hop, W ←W , is facilitated by water fluctuations near the W /W unit, taking place when the electrostatic potential at W drops well below that at W Insufficient solvation and reorganization around W make W ←W ET endergonic, shifting the equilibrium toward W 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. |
| Author | Záliš, Stanislav Šebesta, Filip Heyda, Jan Winkler, Jay R Gray, Harry B Vlček, Antonín |
| Author_xml | – sequence: 1 givenname: Stanislav orcidid: 0000-0003-4345-3205 surname: Záliš fullname: Záliš, Stanislav email: hbgray@caltech.edu, zalis@jh-inst.cas.cz, a.vlcek@qmul.ac.uk organization: J. Heyrovský Institute of Physical Chemistry, Academy of Sciences of the Czech Republic, CZ-182 23 Prague, Czech Republic; hbgray@caltech.edu zalis@jh-inst.cas.cz a.vlcek@qmul.ac.uk – sequence: 2 givenname: Jan orcidid: 0000-0002-9428-9508 surname: Heyda fullname: Heyda, Jan organization: Department of Physical Chemistry, University of Chemistry and Technology, Prague, CZ-166 28 Prague, Czech Republic – sequence: 3 givenname: Filip orcidid: 0000-0001-6707-8118 surname: Šebesta fullname: Šebesta, Filip organization: School of Biological and Chemical Sciences, Queen Mary University of London, London E1 4NS, United Kingdom – sequence: 4 givenname: Jay R orcidid: 0000-0002-4453-9716 surname: Winkler fullname: Winkler, Jay R organization: Beckman Institute, California Institute of Technology, Pasadena, CA 91125 – sequence: 5 givenname: Harry B orcidid: 0000-0002-7937-7876 surname: Gray fullname: Gray, Harry B email: hbgray@caltech.edu, zalis@jh-inst.cas.cz, a.vlcek@qmul.ac.uk organization: Beckman Institute, California Institute of Technology, Pasadena, CA 91125 hbgray@caltech.edu zalis@jh-inst.cas.cz a.vlcek@qmul.ac.uk – sequence: 6 givenname: Antonín orcidid: 0000-0002-6413-8311 surname: Vlček fullname: Vlček, Antonín email: hbgray@caltech.edu, zalis@jh-inst.cas.cz, a.vlcek@qmul.ac.uk organization: School of Biological and Chemical Sciences, Queen Mary University of London, London E1 4NS, United Kingdom |
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| Keywords | electron transfer molecular dynamics hole hopping tryptophan azurin |
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