The DNA nucleobase thymine in motion – Intersystem crossing simulated with surface hopping

Highlights

• Intersystem crossing in gas phase thymine is found to be an efficient process.

• The mechanism involves a crossing of the ${}^{1}n{\pi }^{\ast }$ and ${}^3\pi {\pi }^{\ast }$ electronic states.

• The change in electronic state might be observable via specific vibrational modes.

Abstract

We report ab initio excited-state dynamics simulations on isolated thymine to investigate the mechanism of intersystem crossing, based on CASSCF potential energy surfaces and the Sharc surface hopping method. We show that even though $S_2\to S_1$ internal conversion is not described accurately with CASSCF, intersystem crossing can be correctly simulated. Intersystem crossing in thymine occurs from the $S_1$ (${}^{1}n{\pi }^{\ast }$) minimum, via a nearby crossing with $T_2$ (${}^3\pi {\pi }^{\ast }$). The system further relaxes via ultrafast internal conversion in the triplet manifold to the $T_1$ (${}^3\pi {\pi }^{\ast }$) state. The simulations reveal that, once the system is trapped in the ${}^{1}n{\pi }^{\ast }$ minimum, intersystem crossing might proceed with a time constant of 1 ps. Furthermore, the change of the system’s electronic state is accompanied respectively by elongation/shortening of specific bonds, which could thus be used as indicators to identify which state is populated in the dynamics.

Introduction

DNA and RNA are among the primary absorbers of UV light in all known organisms, stemming from the large absorption cross-section of the nucleobases which are part of DNA and RNA strands. Absorption of UV light by the nucleobases leads to the formation of excited electronic states, which for this class of compounds mostly deactivate to the electronic ground state within a few ps [1], [2], [3], [4], [5]. A very small fraction of excitations of nucleobases in DNA leads to the formation of photochemical products called photolesions, which constitute damage to DNA/RNA and interferes with normal cellular processes. Among the photolesions, the dimerization of thymine to generate cyclobutane pyrimidine dimers is the most common one [6], [7], [8], [9]. Because of this relevance, the photophysical and photochemical properties of thymine were studied intensively in the last decades.

Among the most controversial aspects of thymine’s excited-state dynamics is the importance of intersystem crossing (ISC). ISC is the radiationless transition between states of different multiplicities, in particular from the initially populated singlet states to triplet states. Due to the high reactivity and long lifetime of triplet states, once formed, those states could be involved in the formation of photolesions like cyclobutane pyrimidine dimers and pyrimidine 6–4 pyrimidone adducts, as was suggested in the literature [10]. However, other authors have argued that these photolesions are formed without the involvement of triplet states [11], [12], or at least that triplet states only marginally contribute to these reactions [13], [14]. For these reasons, it is interesting to study the photophysics of thymine. Besides studies in biological environments, also photophysical investigations in solution and in the gas phase are important here, since they allow separating the intrinsic dynamics of thymine from the effect of the surrounding.

Measurements in aqueous solutions find that ISC yields are 0.004 [15] to 0.006 [16], while in chloroform the yield is 0.08 [17]. In acetonitrile the reported values range from 0.06 [16] to 0.18 [18], suggesting that ISC in thymine is solvent dependent and that less polar solvents enhance ISC. More recently, much effort has been devoted to use time-resolved experimental methods to probe the ultrafast dynamics of thymine. Gas phase pump–probe experiments are reported by several groups [19], [20], [21], [22], [23], [24], [25], [26]; mostly a sub-ps and a few-ps (5–7 ps) time constant were found, some groups also reported a ns time constant [19], [22], [23], [24], [25]. In aqueous solution, Hare et al. have shown that thymine decays biexponentially with two time constants of 2.8 and 30 ps [27].

Nevertheless, an assignment of the experimental time constants to either internal conversion or ISC is difficult solely based on the experimental data and hence the last years have seen a large number of theoretical calculations on thymine. A number of authors have optimized excited-state minima and crossing points, as well as calculated various paths between these geometries [28], [29], [30], [31], [32], [33], [34], [35], [36], [37]. Some authors have also investigated possible stationary pathways for intersystem crossing [34], [38], showing that ISC is feasible through several singlet–triplet crossing points along its relaxation pathway. Furthermore, a number of non-adiabatic dynamics studies were performed [30], [32], [35], [39], [40], [41], [42], but none included the possibility of ISC.

Thus, a logical next step in the investigation of intersystem crossing in thymine is to perform non-adiabatic dynamics simulations including singlet and triplet states with the possibility of ISC. The Sharc (Surface Hopping including ARbitrary Couplings) excited-state dynamics methodology [43], [44], [45] is especially well suited for this application, and has already been used successfully for describing ISC in other pyrimidine nucleobases [46], [47], [48].