Stepwise photosensitized thymine dimerization mediated by an exciton intermediate

Monatshefte für Chemie - Chemical Monthly, Dec 2017

Clemens Rauer, Juan J. Nogueira, Philipp Marquetand, Leticia González

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Stepwise photosensitized thymine dimerization mediated by an exciton intermediate

Stepwise photosensitized thymine dimerization mediated by an exciton intermediate Clemens Rauer 0 1 Juan J. Nogueira 0 1 Philipp Marquetand 0 1 Leticia Gonza´ lez 0 1 0 Institute of Theoretical Chemistry, Faculty of Chemistry, University of Vienna , Vienna , Austria 1 & Clemens Rauer Cyclobutane thymine dimerization is the most prominent DNA photoinduced damage. While the ultrafast mechanism that proceeds in the singlet manifold is nowadays well established, the triplet-state pathway is not completely understood. Here we report the underlying mechanism of the photosensitized dimerization process in the triplet state. Quantum chemical calculations, combined with wavefunction analysis, and nonadiabatic molecular dynamics simulations demonstrate that this is a stepwise reaction, traversing a long-lived triplet biradical intermediate, which is characterized as a Frenkel exciton with very small charge-transfer character. The low yield of the reaction is regulated by two factors: (i) a relatively large energy barrier that needs to be overcome to form the exciton intermediate, and (ii) a bifurcation of the groundstate potential-energy surface that mostly leads back to the Franck-Condon region because dimerization requires a very restricted combination of coordinates and velocities at the event of non-radiative decay to the ground state. Graphical abstract; DNA; Thymine dimerization; Quantum chemical calculations; Non-adiabatic dynamics; Wavefunction analysis; Charge transfer Introduction The formation of cyclobutane thymine ThiT dimers between two adjacent thymine bases is the most frequent DNA damage under UV radiation [ 1 ]. This photolesion, which can take place in both the singlet and triplet manifolds, has been extensively investigated spectroscopically [ 2–7 ] and computationally [ 8–15 ]. The triplet pathway is a much slower process [ 7 ] and exhibits a smaller yield [ 6, 16 ] than the singlet mechanism due to inefficient intersystem crossing. As a consequence, this pathway yields very weak spectroscopic signals that preclude unambiguous statements regarding the mechanism [ 5–7 ]. In order to enhance the triplet signals, photosensitization is commonly used, increasing the ThiT dimerization yield [ 5, 17–19 ]. This enhancement can also play a role with photosensitizers acting as phototoxic drugs [ 20 ]. Photosensitization involves intersystem crossing of a photosensitizer after excitation, transferring its electronic energy to a Fig. 1 Chemical formula and electronic arrangement of two thymines for a the local triplet state (3L) and b biradical triplet states (3BR). Schematic representation of c a local state, d a Frenkel exciton state, and e a charge-resonance state. The black rectangles represent the thymine monomers. The black arrow connects the hole (red circle) and the electron (blue circle) generated after excitation. Delocalization length (DL) and charge-transfer (CT) contribution are also indicated (color figure online) neighboring thymine, which is then promoted to the lowest triplet state. Using the photosensitizer 20-methoxyacetophenone and the dinucleotide TpT, stationary and time-resolved experiments provided two time constants, 22.5 and 62 ns, for the decay of the TpT in the triplet manifold [ 5 ]. These constants have been related to a local triplet state (3L, see Fig. 1a, c), which is populated after triplet–triplet energy transfer (TTET) from the photosensitizer, and a biradical triplet state (3BR, see Fig. 1b, d, e), which can be formed from 3L. Quantum chemical calculations [ 14 ] suggested that the ThiT dimerization is triggered by the formation of the biradical intermediate, but the barrierless pathway calculated for the transition from 3L to 3BR is in conflict with the experimental lifetime of 22.5 ns assigned to the 3L species. This conflict is likely caused by the use in the theoretical study of a perfectly stacked geometrical configuration with Cs symmetry, which is hardly achieved in a DNA strand or in a TpT dimer due to the geometrical constraints of the sugar-phosphate backbone. Recent quantum mechanics/molecular mechanics (QM/MM) calculations have found a small barrier of 0.15 eV separating the 3L and 3BR minima, in better agreement with the experimental lifetime of 22.5 ns assigned to the 3L species [ 15 ]. An intriguing question in the dimerization process is the character of the 3BR state. Calculations showed that the excited electronic density of 3BR is distributed over the two thymine units [ 14 ] and spectroscopic measurements suggested that dimerization involves the participation of delocalized triplet states [ 18 ]. However, electronic delocalization over the two monomers can correspond to two different electronic states: (i) a Frenkel exciton, in which two local excitations are coupled (Fig. 1d), or a chargeresonance state, in which two charge-transfer states with charge flow in opposite directions are combined (Fig. 1e) [ 21 ]. It has (...truncated)


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Clemens Rauer, Juan J. Nogueira, Philipp Marquetand, Leticia González. Stepwise photosensitized thymine dimerization mediated by an exciton intermediate, Monatshefte für Chemie - Chemical Monthly, 2017, pp. 1-9, DOI: 10.1007/s00706-017-2108-4