Photoinduced Thymine Dimerization Studied by Semiclassical

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Photoinduced Thymine Dimerization Studied by Semiclassical Dynamics Simulation† Wenying Zhang,‡,§ Shuai Yuan,‡ Anyang Li,‡ Yusheng Dou,*,‡,| Jianshe Zhao,§ and Weihai Fang⊥ Institute of Computational Chemistry, Chongqing UniVersity of Posts and Telecommunications, Chongqing, 400065 P. R. China, Key Laboratory of Synthetic and Natural Functional Molecule Chemistry of Ministry of Education, Shaanxi, Key Laboratory of PhysicosInorganic Chemistry, Department of Chemistry, Northwest UniVersity, Xi’an, 710069 China, Department of Physical Sciences, Nicholls State UniVersity, PO Box 2022, Thibodaux, Louisiana 70310, Department of Chemistry, Beijing Normal UniVersity, Beijing, 100875 PR China ReceiVed: July 30, 2009; ReVised Manuscript ReceiVed: September 4, 2009

Response to ultrashort laser pulses of two stacked thymine molecules has been studied by semiclassical dynamics simulation with laser radiation explicitly incorporated. The laser pulses used to excite the thymine molecule have a 25 (fwhm) fs Gaussian shape with a photon energy of 4.0 eV. Simulation follows two different reaction paths produced by the laser pulses with two different fluences. In one reaction, the stacked thymine molecules form a cyclobutane pyrimidine dimer, which is the main course of photoinduced DNA damage, and the formation of two chemical bonds linking two thymines occurs nonsynchronously after the excimer decays to electronic ground state. In the other reaction, only one bond is formed between the two thymine molecules. In the second reaction, the bond breaks about 50 fs after formation, and then the two molecules move away from each other. This reaction leads to the DNA damage repair. The simulation finds that the deformation of the pyrimidine ring plays an important role in cleaving this bond. I. Introduction Exposure of DNA to UV radiation in the 200-300 nm range causes DNA damage mainly because of the formation of cyclobutane pyrimidine dimers (CPD) between two adjacent pyrimidine bases within the same DNA strand. The formation of CPDs has been linked with a range of human health problems, including cell lethality, mutagenesis, and the development of skin cancers. Since the first isolation of CPDs a half century ago,1 there have been intensive experimental2-5 and theoretical6-13 investigations in understanding how and to what extent the initially photon-excited thymine molecules lead to the formation of CPDs. It has been reported that the yield of damage is only about 2-3%.14 The very low yield is ascribed to that either rare conformers absorb UV light15-17 or the thymine bases may be favorably aligned so as to undergo dimerization for only a short period of time. The last explanation is based on the fact that the dimerization quantum yield is about unit when the thymine molecules are aligned perfectly, as found in the solid state experiment.18-21 Thymine dimerization in DNA is an ultrafast photoreaction.22 It was found by femtosecond time-resolved IR spectroscopy measurement that if flashed by 272 nm UV light, CPD was completely formed in an 18-mer, all-thymine single strand of DNA within 1 ps of irradiation,23 which is shorter than the time scale for the larger conformational changes of a DNA strand. The formation of CPDs is a [2 + 2] photocycloaddition reaction, in which the reaction of the C5-C6 double bonds of

adjacent thymines leads to the formation of a cyclobutane ring, linking the two bases covalently. The formation of CPDs is on a subpicosecond time scale, suggesting that the reaction follows a barrierless nonadiabatic mechanism. There is a long-standing debate regarding whether the formation of CPDs proceeds via singlet or triplet excited states. Principally, the formation of CPDs in DNA can proceed via either excited triplet or singlet states. The electronically excited singlet state has a very short lifetime and may be a predominant pathway for CPD formation because the thymine bases in a DNA strand are located in close proximity to each other. High-level ab initio calculations favor the proposal that the CPD formation follows a singlet state,5 which either bypasses or competes with the lowest-lying triplet excited state. The singlet mechanism has been verified by femtosecond time-resolved IR spectroscopy experiment23 and time-resolved experiments.24 The longer-lived triplet state has also been proposed to play a potential role in the formation of CPDs.25,26 A hybrid density functional calculation26 finds that in addition to the singlet excited state, the CPD formation also exhibits a favorable energy barrier along the triplet excited potential energy surface. A very recent study using a combined femtosecond time-resolved fluorescence and transient absorption spectroscopies showed27 that both monomer thymine and singlestranded thymine oligonucleotide found rapid branching of the excited state population between a predominant decay channel and a minor pathway. The former leads to the ground state and

†

Part of the “Barbara J. Garrison Festschrift”. * Corresponding author. Phone: 1 985 448 4880. Fax: 985 448 4927. E-mail: [email protected]. ‡ Chongqing University of Posts and Telecommunications. § Northwest University. | Nicholls State University. ⊥ Beijing Normal University.

Figure 1. Structure and atomic labeling for the thymine molecule.

10.1021/jp907290f  2010 American Chemical Society Published on Web 10/19/2009

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Figure 2. The diagrams of the (a) HOMO/HOMO (b) HOMO/LUMO, and (c) LUMO/LUMO of two stacked thymine molecules at the equilibrated geometry.

Figure 3. Snapshots taken from the simulation of two stacked thymine molecules at (a) 0, (b) 533, (c) 604, (d) 626, (e) 743, and (f) 926 fs. The molecule at the bottom is subjected to the irradiation of a 25 fs (fwhm) laser pulse with a fluence of 36.74 J/m2 and a photon energy of 4.0 eV.

brings the molecules to their native states. The latter leads to a triplet state, which is identified as a major precursor for CPD formation. Despite the importance of this process regarding DNA photostability and photodamage and the intense work in the field, the molecular dynamics for the entire process is still poorly understood. In this paper, we present semiclassical dynamics simulation investigation on this process. The simulation results provide detailed dynamics features for this process from photon excitation to the formation of product. II. Methodology We carried out the dynamics simulations using a so-called semiclassical electron-radiation-ion dynamics method. In this approach, the valence electrons are calculated by the timedependent Schro¨dinger equation, and both the radiation field and the motion of the nuclei are treated by the classical approximation. A detailed description of this technique has been published elsewhere,28,29 and only a brief review is given here. The one-electron states are updated by solving the timedependent Schro¨dinger equation at each time step (typically 0.05 fs in duration) on a nonorthogonal basis,

ip

∂Ψj ) S-1 · H · Ψj ∂t

(1)

where S is the overlap matrix for the atomic orbitals. The laser pulse is characterized by the vector potential A, which is coupled to the Hamiltonian via the time-dependent Peierls substitution30

( pciq A · (X - X′))

Hab(X - X′) ) Hab0(X - X′) exp

(2) Here, Hab(X - X′) is the Hamiltonian matrix element for basis functions a and b on atoms at X and X′ respectively, and q ) -e is the charge of the electron. The Hamiltonia matrix elements, overlap matrix elements, and repulsive energy are calculated with the density-functionalbased tight bonding (DFTB) method, which is described in detail elsewhere.31,32 The DFTB method does have essentially the same strengths and limitations as TDDFT. In particular, the bonding is well-described, but the excited-state energies are typically too low. For this reason, we matched the effective central photon energy of the laser pulse to the relevant density functional (rather than experimental) excitation energy, and this should not have

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Figure 4. The variations with time of the lengths between the C5 and C6 atoms and the C5′ and C6′ atoms in two stacked thymine molecules. Only one thymine molecule is subjected to the irradiation of a 25 fs (fwhm) laser pulse with a fluence of 36.74 J/m2 and photon energy of 4.0 eV.

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Figure 6. The variations with time of the HOMO - 1, HOMO, LUMO, and LUMO + 1 energies of two stacked thymine molecules, one of which is subjected to the irradiation of a 25 fs (fwhm) laser pulse with a fluence of 36.74 J/m2 and a photon energy of 4.0 eV.

Figure 7. The time-dependent populations of the HOMO and LUMO of two stacked thymine molecules, one of which is subjected to the irradiation of a 25 fs (fwhm) laser pulse with a fluence of 36.74 J/m2 and photon energy of 4.0 eV. Figure 5. The variations with time of the lengths between the C5 and C′ atoms and the C6 and C6′ atoms in two stacked thymines. One of two stacked molecules is subjected to the irradiation of a 25 fs (fwhm) laser pulse with a fluence of 36.74 J/m2 and photon energy of 4.0 eV. Note that the two bond lengths are almost equal to each other at 606 fs.

an obvious effect on the interpretation of the results. This model has been used to study several photochemical reactions and was found to yield good descriptions of molecular response to ultrashort laser pulses. The examples include that the calculation of the formation of the tetramethylene33 intermediate diradical is consistent with time-of-flight mass spectrometry measurements, the nonthermal fragmentation of C6034 is in good agreement with experimental observations, and the characterization of the geometry changes at some critical points35 is compatible with molecular mechanics valence bond calculations. We also studied the photoisomerization mechanism of azobenzene by nπ* excited36 and isomerization quantum yield37 in both nπ* and ππ* excited. The results are compatible with experimental observations.

In this technique, forces acting on the nucleus or ions are computed by the Ehrenfest equation:

Ml

d2XlR 2

dt

)-

1 2

∑ Ψj+ · j

(

)

∂H 1 ∂S ∂ - ip · · Ψj ∂XlR 2 ∂XlR ∂t ∂Urep /∂XlR (3)

where Urep is the effective nuclear-nuclear repulsive potential, and XlR )〈XˆlR〉 is the expectation value of the time-dependent Heisenberg operator for the R coordinate of the nucleus labeled by l (with R ) x, y, z). Equation 3 is obtained by neglecting the second- and higher-order terms of the quantum fluctuations Xˆ - 〈XˆlR〉 in the exact Ehrenfest theorem. The time-dependent Schro¨dinger eq 1 is solved by using a unitary algorithm obtained from the equation for the time evolution operator38 to eq 3 numerically integrated with the velocity Verlet algorithm. A time step of 0.05 fs is used for this study, and energy conservation was then found to hold better than 1 part in 106 in a 1 ps simulation at 298 K. The present “Ehrenfest” principle is complementary to other methods based on different approximations; for instance, the full multiple spawning model developed by the Martinez

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J. Phys. Chem. C, Vol. 114, No. 12, 2010 5597 gap between the HOMO and LUMO calculated by the present model. A fluency of 0.01-0.03 kJ/m2 was chosen for this study. This fluency results in an effective electronic excitation, but the forces produced do not break any bonds. The simulation was run at the selected laser pulse for 20 trajectories, and only a typical trajectory is reported in this paper. III. Results and Discussion

Figure 8. The molecular geometry taken from the simulation of case 1 at 606 fs.

group.39 The limitation of this method is that the simulation trajectory moves along a path dominated by averaging over all the terms in the Born-Oppenheimer expansion,40-44

Ψtotal(Xn, xe, t) )

∑ Ψin(Xn, t)Ψie(xe, Xn)

(4)

i

rather than following the time evolution of a single potential energy surface, which is approximately decoupled from all the others.42-46 (Here Xn and xe represent the sets of nuclear and electronic coordinates, respectively, and the Ψei are eigen states of the electronic Hamiltonian at fixed Xn.) The strengths of the present approach include that it retains all of the 3N nuclear degrees of freedom, and it incorporates both the excitation due to a laser pulse and the subsequent de-excitation at an avoided crossing near a conical intersection. To obtain a ground state equilibrium configuration of thymine, the simulation was run at room temperature for 2000 fs before any laser pulse was coupled. For the generation of the initial geometry of the thymine molecule for dynamics simulation, the equilibrated geometry was simulated for another 2000 fs. For each path, 20 geometries taken at equal time intervals were used as starting geometries for any laser intensity. The equilibrated geometry of the thymine molecule with atomic labeling is shown in Figure 1. The second thymine molecule of the same geometry was placed in such way that C5-C5′ ) 3.33 Å, C6-C6′ ) 3.55 Å, and C7-C5-C5′-C7′ ) 36.4°. This configuration was reported to form CPD effectively.6 A 25 fs fwhm laser pulse with a Gaussian profile and frequency of 4.0 eV was applied to one thymine molecule. The energy selected matches the energy

Figure 2 presents the diagrams for the HOMO/HOMO, HOMO/LUMO, and LUMO/LUMO of two close thymine molecules at the equilibrated structure computed by the DFTB approximation. On the basis of Woodward-Hoffmann rules, the formation of cyclobutane pyrimidine dimer is a symmetryforbidden reaction when both molecules are at the electronic ground states or have one electron promoted from the HOMO to the LUMO. However, the reaction is symmetry-allowed when one molecule is at the electronic ground state and another one has one electron excited from the HOMO to the LUMO. These features are well replicated by the molecular orbital diagram. Case 1. Formation of Cyclobutane Pyrimidine Dimer. In this section, we present and discuss the simulation results for the formation of cyclobutane pyrimidine dimer, which is a major pathway of DNA photodamage. Six snapshots taken from the simulation at different times are shown in Figure 3. Starting from the equilibrium geometries of two thymine molecules at the designed locations in the electronic ground state at 0 fs (Figure 3a), one of the thymine molecules is electronically excited by the laser pulse. The excited molecule is distorted and moving toward the unexcited molecule (Figure 3b). The unexcited molecule is deformed by the approach of the excited molecule (Figure 3c). At 626 fs, a C6-C6′ bond has been formed (Figure 3d). Soon after then, the C5-C5′ atoms are formed (Figure 3e), indicating the formation of cyclobutane pyrimidine dimer. The structure of cyclobutane pyrimidine dimer remains stable by the end of the simulation (Figure 3f). The variations with time of the lengths of the C5-C6 and C5′-C6′ bonds are presented in Figure 4. Both C5-C6 and C5′-C6′ bonds are double bonds in the thymine molecules but become single bonds in the thymine dimer. Starting at about 1.38 Å, which is the length of a typical C-C double bond, the C5-C6 bond increases in length after the laser pulse is applied. The excited thymine molecule approaches the unexcited thymine molecule and influences its structure, as shown by the increase

Figure 9. Snapshots taken from the simulation of two stacked thymine molecules at (a) 0, (b) 550, (c) 602, (d) 634, (e) 690, and (f) 770 fs. The bottom molecule is subjected to the irradiation of a 25 fs (fwhm) laser pulse with a fluence of 42.17 J/m2 and a photon energy of 4.0 eV.

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Figure 10. The variations with time of the C5-C6 and C5′-C6′ bond lengths of two stacked thymine molecules. The bottom molecule is subjected to the irradiation of a 25 fs (fwhm) laser pulse with a fluence of 42.17 J/m2 and a photon energy of 4.0 eV.

Figure 11. The variations with time of the lengths of the C5 and C5′ and C6 and C6′ atoms of two stacked thymine molecules, one of which is subjected to the irradiation of a 25 fs (fwhm) laser pulse with a fluence of 42.17 J/m2 and photon energy of 4.0 eV.

in the C5′-C6′ bond length after 200 fs. Both bond lengths increase to about 1.5 Å after 600 fs because of the formation of the cyclobutane pyrimidine dimer, and they remain at this length until the end of the simulation. The variations with time of the C5-C5′ and C6-C6′ distances are shown in Figure 5. Both distances remain at roughly their initial values by 400 fs and start to decrease after then. The C6-C6′ distance decreases to below 1.5 Å at about 650 fs. The C5-C5′ distance drops to about 2.1 Å at about 600 fs and farther drops to about 1.5 Å at about 750 fs. This is the time for the formation of the cyclobutane pyrimidine dimer. This time is compatible with experimental observations and theoretical predications.5,23,24 The variations with time of the HOMO - 1, HOMO, LUMO, and LUMO + 1 energies are presented in Figure 6, and the time-dependent population of the HOMO and LUMO is shown in Figure 7. (Note that the HOMO and HOMO - 1 are initially two identical HOMOs of the thymine monomer molecules and

Zhang et al.

Figure 12. The variations with time of the HOMO - 1, HOMO, LUMO, and LUMO + 1 energies of two stacked thymine molecules. The bottom molecule is subjected to the irradiation of a 25 fs (fwhm) laser pulse with a fluence of 42.17 J/m2 and photon energy of 4.0 eV.

Figure 13. The time-dependent population of the HOMO and LUMO of two stacked thymine molecules. The bottom molecule is subjected to the irradiation of to a 25 fs (fwhm) laser pulse with a fluence of 42.17 J/m2 and photon energy of 4.0 eV.

the LUMO and LUMO + 1 are initially two identical LUMOs of the two molecules before laser excitation.) Figure 6 shows that there is an abrupt change in the LUMO energy soon after application of the laser pulse. The HOMO and LUMO levels find one close approach, with avoided crossings, with the energy gaps being 0.04 eV at 606 fs. Figure 7 shows that by the end of the laser pulse radiation (which is 50 fs), about 1.5 electrons are excited from the HOMO to the LUMO, which promotes one thymine molecule to an electronically excited state. The coupling between the HOMO and LUMO, as observed in Figure 6, leads to remarkable electronic transitions from the LUMO to the HOMO. This de-excitation eventually brings the molecule to the electronic ground state. It can be seen from Figure 6 that shortly after the coupling, both the LUMO and HOMO levels move toward their initial values. After 800 fs, when the formation of the cyclobutane pyrimidine dimer is completed, these two energy levels show fluctuations only about constants values that are essentially the same as their initial values. On

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Figure 14. The molecular geometry taken at 605 fs from the simulation of case 2.

the other hand, the LUMO + 1 and HOMO - 1 levels show only slight variations during the reaction, since they are the LUMO and HOMO of the unexcited molecule, respectively. The molecular geometry taken at 606 fs, the time when the excited molecule decays to the ground state, is shown in Figure 8 with a few critical geometry parameters indicated. The distances between the C5 and C5′ atoms and the C6 and C6′ atoms are 2.12 and 2.13 Å, respectively, as compared with 2.27 and 2.17 Å found in CASSCF and CASPT2 calculation at the conical intersection between the lowest excited singlet state and the ground state.6 A good agreement between two sets of parameters indicates that the avoided crossing found at 606 fs indeed is in close proximity to the conical intersection. Photoinduced [2 + 2] cycloadditions proceed via a cyclic transition state and are concerted reactions in which bond breaking and bond formation take place simultaneously and no intermediate state is involved. For the photoinduced dimerization of thymines, cycloaddition results in the conversion of C5-C6 and C5′-C6′ π-bonds, one on each pyrimidine ring, into two σ-bonds of the cyclobutane ring (C5-C5′ and C6-C6′ bonds). The CASSCF calculation suggests that in the photochemical [2 + 2] cycloaddition, two stacked thymines decay to the electronic ground state via the conical intersection before the formation of the C5-C5′ and C6-C6′ bonds and that at the conical intersection, the distance C5-C5′ is longer than C6-C6′. It is therefore inferred that the C5-C5′ and C6-C6′ bonds are formed nonsynchronously. This inference is consistent with our simulation results. Case 2. Formation of Only One σ-Bond between Two Thymine Molecules Only for a Short Time. The simulation results presented in this section show that under laser irradiation, two molecules form a σ-bond between the C5 and C5′ atom sites, which may cause DNA damage. However, this σ-bond has a lifetime of only several tens of femtoseconds and breaks shortly after it is formed. Six snapshots taken from the simulation at different times are shown in Figure 9. One finds that at 634 fs, two molecules have already formed a chemical bond between the C5 and C5′ atoms (Figure 9d), but shortly after then, the bond breaks and the two molecules move away from each other (Figure 9e and f). The variations with time of the C5-C6 and C5′-C6′ bond lengths are plotted in Figure 10. The C5-C6 bond stretches in length soon after the laser pulse is applied due to the excitation of electrons from the HOMO to LUMO and shrinks to its original length shortly after 600 fs when the bond linking the two thymine molecules is broken. The C5′-C6′ bond also shows an increase in length from 200 to about 600 fs as a result of the influence of the excited thymine molecule. A sharp jump up

Figure15. ComparisonbetweentheN3-C2-N1-C6andC2-N1-C6-C5 dihedral angles and the energy gap between the HOMO and LUMO of two stacked thymine molecules: (a) case 1 and (b) case 2.

and down in the C5′-C6′ bond length at about 610 fs indicates the formation and breakage of the bond between the two thymine molecules. The variations with time of the C5-C5′ and C6-C6′ distances are plotted in Figure 11 for this process. Both distances do not exhibit significant changes until 400 fs but show a decrease afterward due to the interaction between two close molecules. The C6-C6′ distance becomes ∼1.5 Å at ∼610 fs, indicating the formation of a C-C σ-bond. Immediately after that, the distances between the C5 and C5′ atoms and the C6 and C6′ atoms increase quickly because the two molecules separated from each other. The variations of the HOMO - 1, HOMO, LUMO, and LUMO + 1 energies as a function of time are shown in Figure 12, and the time-dependent populations of the HOMO and LUMO are shown in Figure 13. An avoided crossing between the HOMO and LUMO levels is found with the energy gaps being 0.05 eV at 605 fs. This avoided crossing leads to a remarkable electronic transition from the LUMO to HUMO, which eventually directs the excimer to the electronic ground state. The molecular geometry found at the avoided crossing is demonstrated in Figure 14. Again, the distances between the C5 and C5′ atoms, and the C6 and C6′ atoms are consistent with ones found at the conical intersection by CASSCF calculation,6 indicating the decay occurs in close proximity to the conical intersection. It is seen from Figures 5-7 and 11-13 that the formation of the C5-C5′ and C6-C6′ bands has a crucial impact on the

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Zhang et al. the formation of the C6-C6′ bond, the C2-N1-C6-C5 dihedral angle shows a variation similar to that in case 1. However, it drops sharply from about 40° to -40°. This change makes the C6-C6′ bond unstable. We therefore conclude that the forces produced by the deformation of the pyrimidine ring at the C6 site break the C6-C6′ bond and prohibit the formation of the cyclobutane pyrimidine dimer. IV. Conclusions

Figure 16. Comparison between the distances of the C5 and C5′ and C6 and C6′ atoms and the N3-C2-N1-C6 and C2-N1-C6-C5 dihedral angles for two stacked thymine molecules: (a) case 1 and (b) case 2.

nonadiabatic transition of the excimer to the electronic ground state. In addition, the deformation of the pyrimidine ring, especially the deformtion of the pyrimidine ring at C5 and C6 atoms sites, also has a notable influence on the nonadiabatic transition of the excimer to ground state. To understand this, a comparison between the N3-C2-N1-C6 and C2-N1-C6-C5 dihedral angles and the energy gap between the HOMO and LUMO for each case is plotted in Figure 15. The deformation of the pyrimidine ring at the C5 and C6 atom sites is represented by these two dihedral angles. It is seen that for each case, the minimum of the energy gap is in line with a sharp peak in the variation of the C2-N1-C6-C5 dihedral angle and a sharp dip in the variation of the N3-C2-N1-C6 dihedral angle, suggesting that in both cases, the deformation of the pyridine ring plays an important role in the nonadiabatic transition of the excimer to ground state. In case 2, the C6-C6′ bond between two thymines is removed 56 fs after its formation. To understand how the structural deformation of the pyrimidine ring impacts the cleavage of the C6-C6′ bond, it is worthwhile to compare the distances between the C5 and C5′ atoms and the C6 and C6′ atoms and the N3-C2-N1-C6 and C2-N1-C6-C5 dihedral angles, as shown in Figure 16 for both cases studied. For the formation of the cyclobutane pyrimidine dimer, the dihedral angle of C2-N1-C6-C5 increases quickly soon before the formation of the C5-C5′ and C6 -C6′ bonds and then fluctuates about this value. However, the dihedral angle of N3-C2-N1-C6 does not have a significant deviation from its original value. For case 2, in which the C6-C6′ bond exists for only a short time, before

In this paper, we report a semiclassical dynamics simulation study of response to ultrashort laser pulses of stacked thymine molecules. The simulation follows two different reaction paths produced by two laser pulses. Two different reaction paths lead to the formation of two different products. The first leads to the formation of cyclobutane pyrimidine dimer, and the second eventually returns back to reactants after deactivation. The simulation results are summarized as follows: 1. In the first reaction, the formations of two chemical bonds linking two thymines occur after the excimer decays to the electronic ground state and the formation of these bonds is nonsynchronous. The difference between the times of forming two bonds found by the simulation is 110 fs. 2. In the second reaction, only one bond is formed between two thymine molecules. However, this bond exists for only 54 fs. After the removal of the bond, the two molecules move away from each other. The deformation of the pyrimidine ring plays an important role in the breaking of this bond. 3. In both reactions, the distances between the C5 and C5′ atoms and the C6 and C6′ atoms have a great impact on the formation of the avoided crossings, which leads to the deactivation of the photon-excited molecule. 4. The distances between the C5 and C5′ atoms and the C6 and C6′ atoms found by the simulation at the time when the excimer decays to electronic ground state are consistent with those of quantum chemical calculation at the CASSCF level. The simulation results provide detailed information on the dynamics of these reactions from photon excitation to deactivation and are expected to help in understanding these processes. Acknowledgment. This work is supported by the National Natural Science Foundation of China (No. 20773168) and Research Fund of Chongqing University of Posts and Telecommunications (A2006-81). Acknowledgment is also made to the donors of The American Chemical Society Petroleum Research Fund for support of this research at Nicholls State University. The Supercomputer Facility at Texas A&M University provided computational assistance. References and Notes (1) Beukers, R.; Berends, W. Biochim. Biophys. Acta 1960, 41, 550– 551. (2) Beukers, R.; Eker, A. P. M.; Lohman, P. H. M. DNA Repair 2008, 7, 530–543. (3) Sihna, R. P.; Ha¨der, D.-P. Photochem. Photobiol. Sci. 2002, 1, 225– 236. (4) Mouret, S.; Baudouin, C.; Charveron, M.; Favier, A.; Cadet, J.; Douki, T. Proc. Natl. Acad. Sci. 2006, 103, 13765–13770. (5) Schreier, W. J.; Kubon, J.; Regner, N.; Haiser, K.; Schrader, T. E.; Zinth, W.; Clivio, P.; Gilch, P. J. Am. Chem. Soc. 2009, 131, 5038–5039. (6) Boggio-Pasqua, M.; Groenhof, G.; Scha¨fer, L. V.; Grubmu¨ller, H.; Robb, M. A. J. Am. Chem. Soc. 2007, 129, 10996–10997. (7) Blancafort, L.; Celani, P.; Bearpark, M. J.; Robb, M. A. Theor. Chem. Acc. 2003, 110, 92–99. (8) Blancafort, L.; Migani, A. J. Am. Chem. Soc. 2007, 129, 14540– 14541. (9) Crespo-Herna´ndez, C. E.; Kohler, B. J. Phys. Chem. B 2004, 108, 11182–11188.

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