Letter pubs.acs.org/JPCL
Femtosecond Intersystem Crossing in the DNA Nucleobase Cytosine Martin Richter,† Philipp Marquetand,‡ Jesús González-Vázquez,¶ Ignacio Sola,¶ and Leticia González*,‡ †
Institute of Physical Chemistry, Friedrich Schiller University Jena, Helmholtzweg 4, 07743 Jena, Germany Institute of Theoretical Chemistry, University of Vienna, Währinger Strasse 17, 1090 Vienna, Austria ¶ Departamento de Química Física I, Universidad Complutense, 28040 Madrid, Spain ‡
S Supporting Information *
ABSTRACT: Ab initio molecular dynamics including nonadiabatic and spin−orbit couplings on equal footing is used to unravel the deactivation of cytosine after UV light absorption. Intersystem crossing (ISC) is found to compete directly with internal conversion in tens of femtoseconds, thus making cytosine the organic compound with the fastest triplet population calculated so far. It is found that close degeneracy between singlet and triplet states can more than compensate for very small spin−orbit couplings, leading to efficient ISC. The femtosecond nature of the ISC process highlights its importance in photochemistry and challenges the conventional view that large singlet−triplet couplings are required for an efficient population flow into triplet states. These findings are important to understand DNA photostability and the photochemistry and dynamics of organic molecules in general. SECTION: Spectroscopy, Photochemistry, and Excited States
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ISC, respectively) on equal footing. The applicability of SHARC to include spin−orbit as well as dipole couplings is documented in refs 37−39. Here, SHARC is employed to investigate the role of the triplet states in the deactivation of cytosine within the framework of nonadiabatic molecular dynamics based on ab initio multiconfigurational methods. Such study is necessary to provide a mechanistic insight that goes beyond what can be learned from quantum chemical calculations alone. Cytosine presents three tautomers, enol-, keto-, and ketoimine-cytosine. Keto-cytosine is the biologically relevant tautomer found in the DNA’s nucleotides linked to the deoxyribose sugar moiety and the only one for which a crystalline structure exists.40 Therefore, here, we focus on ketocytosine. Several stationary points3,41,42 of keto-cytosine, including two-43−48 and three-state49−51 conical intersections involved in the process of IC, have been calculated with ab initio methods. Time-dependent calculations have indicated that the dynamical behavior of cytosine after photoexcitation is one of the most complicated among nucleobases, involving delocalization of the excited wave packet and relaxation through multiple competing pathways in the singlet excited-state manifold.6,52−54 The possible triplet-state formation via ISC along the IC pathway of excited singlet keto-cytosine has been discussed by Merchán et al.55,56 in light of quantum chemical calculations.
he interaction of DNA and RNA with radiation, from mobile phone emissions1 to UV wavelengths,2 has enthralled the scientific community for years due to its implications in photodamage.3 Of particular interest is to understand photostability, that is, the relaxation mechanisms that bring DNA4−6 to the ground state before any other photoreaction can occur. This means that, instead of fluorescence or phosphorescence, the electronic energy provided upon photoexcitation in DNA is transferred to the nuclear degrees of freedom of the molecular system in different ways. It is precisely the atomistic description of these different relaxation pathways that is still heavily discussed in the literature. In the last years, it has been clearly established that excited states of isolated DNA nucleobases undergo ultrafast internal conversion (IC), allowing for an efficient radiationless decay toward lower-lying electronic states.7−15 The role of intersystem crossing (ISC) in the process of photostability is, however, much less discussed,15−19 probably because it is thought to be a much slower process in comparison to IC20 and also because the quantum yields of triplet-state populations in DNA and RNA nucleobases are generally very small and thus difficult to access from the experimental point of view.10,15,21 We note, however, that ultrafast time scales for ISC in other organic molecules have been experimentally reported or predicted before.22−36 In this work, we present the first excited-state dynamical study of a DNA nucleobase including singlet and triplet states. Such simulations are done using the newly developed surfacehopping method SHARC.37 SHARC stands for surface hopping including arbitrary couplings. With SHARC, one can treat nonadiabatic and spin−orbit couplings (which mediate IC and © XXXX American Chemical Society
Received: August 31, 2012 Accepted: October 5, 2012
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Our ab initio molecular dynamic simulations are performed on seven states simultaneously, four singlets and three triplets. Energies, energy gradients, and nonadiabatic and spin−orbit couplings are computed on-the-fly using the state-average complete active space self-consistent field (CASSCF) method.57,58 Further details are given in the Supporting Information (SI). The first singlet excited state, S1, has ππ* character at the equilibrium geometry, and it is bright, while the states higher in energy, S2 and S3, correspond to dark nπ* excitations, that is, they have negligible oscillator strengths when vertically excited. The order of states at equilibrium geometry is not altered when going to higher levels of theory that include dynamical correlation (see Table S2 of the SI). Since the on-the-fly approach used in this work prohibits the use of higher-level methods such as CASPT2, we employ CASSCF. The Franck− Condon region, from which excitations take place, is comprised of not only the equilibrium geometry but also slightly distorted geometries. These distortions are due to the different vibrations included within the zero-point energy of the system. Because in cytosine rather small deviations of the equilibrium geometry lead to a different ordering of the state character, the S2 and S3 states can also be bright states and contribute to the absorption spectrum (see refs 6 and 53 and Figure S1 of the SI). The character of the lowest three excited triplet states at equilibrium is ππ* for T1 and T2 and nπ* for T3. A comprehensive report of vertical excitation energies at different levels of theory can be found in the SI. In order to obtain a global picture of the relaxation mechanisms of keto-cytosine, we first used initial conditions spanning the whole first absorption band of the UV spectrum, that is, covering excitation energies from ∼4 to 7 eV. As explained above, this requires launching trajectories from the first three excited states, S1, S2, and S3. Most time-resolved spectroscopic experiments in cytosine9,12,48,59,60 use a pumping wavelength of 267 nm (4.64 eV), just below the center of the first absorption band located at 260 nm (4.77 eV). In order to narrow the initial conditions to the energy range corresponding to the experimental one, we have also analyzed the results (Figure S2 of the SI) limited to the bandwidth at 4.75 ± 0.25 eV, just below our theoretically predicted first absorption band maximum. Also in this energy range, states S1−S3 are excited. The results from both energy ranges qualitatively agree with each other; therefore, we will limit the discussion to the more general broad range. Figure 1 displays the time evolution of all of the state populations, and Figure 2 summarizes the most important deactivation paths found in keto-cytosine with SHARC, including decay times and branching efficiencies. One should note that because the calculations are done at levels of theory that do not include sufficient dynamic correlation, the potential energy surface for the dynamics is not accurate enough to derive quantitative conclusions. Because the energy gaps between the states are highly dependent on the level of theory, the branching efficiencies and the decay times should be considered as an informative basis rather than quantitative numbers. We indicate the total branching efficiencies over the whole simulation time so that in some cases, numbers can be higher than the initial population. Percentages not adding to 100% are due to minor pathways not indicated. The decay times are obtained by fitting the net amount of hops between two particular states (see Figure S3 and Table S1 of the SI) to an exponential function. The branching efficiencies given in % are also graphically indicated by arrows of different thicknesses
Figure 1. Time evolution of the singlet (solid) and triplet (dotted) states during the first picosecond. The inset zooms the first 100 fs. The S0 ground-state population is in black, S1/T1 state populations are in red, S2/T2 are in blue, and S3/T3 are in green.
Figure 2. Deactivation pathways of keto-cytosine including IC (in black) and ISC (in gray). The propensity of each path is sketched by the thickness of the arrows. The dotted line indicates the deactivation pathway of T1.
according to their importance. After photoexcitation, which corresponds to time zero in our simulations, the population of the ππ* is distributed as 13% in S3, 47% in S2, and 40% in S1, as dictated by the weight of the oscillator strength of each state. Because the character of a state can adiabatically change during the simulation, hereafter, we shall refer to the states by their energetic order rather than by their character. Analyzing the 13% population of S3, 10% relaxes nonadiabatically to the S2 and from there to the S1 within 25 fs. After ∼155 fs, the system populates the electronic ground state S0. The remaining 3% of the population of S3 deactivates directly to S1 via a three-fold degeneracy S3/S2/S1, as proposed in ref 51. Our calculations show that this process is slower than the previous one, with a time constant of 110 fs. Most of the population in S2 transfers preferably to the lower-lying electronic states within less than 100 fs. Also in this case, the process of IC is possible via a cascade of subsequent S2/S1 and S1/S0 conical intersections or directly via three-state conical intersections S2/S1/S0, as proposed in refs 49 and 51. Both pathways to the ground state are relevant, in agreement with the time-dependent simulations of ref 53. As deduced from the time constants, the three-state conical intersection pathway is faster (25 fs) than the two-step pathway (25 fs/155 fs). As noticeable from Figure 1, the first encounter with a conical intersection takes place within only 10 fs; however, complete 3091
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spin−orbit coupling of 20−30 cm−1 is found along this path.55 In their calculations, the S1/T1 crossing corresponds to a transition between the 1ππ* and the 3ππ* states, in agreement with the El-Sayed selection rules for ISC.64,65 In contrast, we find out that the ISC takes place fundamentally between the 1 nπ* (S1) and the 3nπ* (T2) states, while the 3ππ* state is the T1. Accordingly, and in agreement with the El-Sayed rules, the spin−orbit coupling between S1 and T1 is larger (∼15−20 cm−1 on average; maximum of 40 cm−1) than that between the S1 and T2 state (∼5 cm−1 on average). However, the S1 → T2 transition is predominant because the T2 state is separated from the S1 by a very small energy gap (
