Excited-State Tautomerization of Gas-Phase Cytosine - The Journal of

Article pubs.acs.org/JPCA

Excited-State Tautomerization of Gas-Phase Cytosine Catherine G. Triandafillou and Spiridoula Matsika* Department of Chemistry, Temple University, Philadelphia, Pennsylvania 19122, United States S Supporting Information *

ABSTRACT: In order to investigate experimentally observed phototautomerization of gas-phase cytosine, several excited-state tautomerization mechanisms were characterized at the EOM-CCSD and TDDFT levels. All pathways that took place exclusively on the S1 surface were found to have significant barriers that were much higher than the barriers involved in radiationless decay of cytosine tautomers through conical intersections back to the ground state; tautomerization in this fashion cannot compete with radiationless relaxation. However, an alternative possibility is that the conical intersections that facilitate radiationless decay could also facilitate tautomerization. Barrierless pathways indicate that it is energetically possible that bifurcation at the conical intersections can lead to a subset of the population reaching different tautomers. This could be an explanation for the observed tautomerization of keto cytosine after exposure to low-energy UV light.

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have been challenged by some theoretical studies20,23 but have been supported by others when used to distinguish between tautomers.24 More recently Lobsiger et al.14 have measured the S0/S1 vibronic spectra of keto cytosine at 31 927 cm−1. They were able to measure vibronic bands very close to the origin of the ππ* excited state and found that below 500 cm−1 the lifetime is 45 ps and decreases rapidly above that threshold, indicating that a barrier to the conical intersection is present with energy around 500 cm−1. It still remains unclear which tautomers are present and in what ratio they exist in the vapor phase. In a recent matrixisolation study of gas-phase cytosine, Bazsó et al.20 found that the mole ratio was 0.22:0.26:0.44:0.08, keto/enol(1)/enol(2)/ keto-imino(1) at 450 K. However, they consider these results to be semiquantitative (but reliable) due to the difficulty in comparing the computational and experimental portions of the study and slight differences between the conditions at which the experimental IR and UV spectroscopic measurements were taken. Other gas-phase experiments have found only two tautomers present, most likely because the observed properties did not allow distinguishing between the keto and keto-imino tautomers.12 A comprehensive theoretical treatment of the tautomers by Wolken et al.16 indicated that the ratio of keto/ enol(1)/enol(2)/keto-imino(1) at 473 K was 0.31:0.20:0.43:0.05 at the highest level of theory employed. The stability order of the tautomers in aqueous solution differs from that of the gas phase. The relatively large dipole moment of the keto tautomer causes it to be the most stable when

INTRODUCTION The short excited state lifetimes of the five natural nucleobases of DNA and RNA are generally attributed to the presence of energetically accessible conical intersections (CIs) between the excited electronic states and the ground state;1−5 these surface crossings allow for the efficient dispersion of energy acquired from UV radiation and preclude photoreactions which can change the nature of the base and damage the genetic code. This behavior is indicated by the low fluorescence yields of all five nucleobases, observable both in the gas phase and in solution.1 Although the most accurate picture of the photodecay of DNA may only be obtained by studying the double helix in vivo, valuable information about its photostability vs photoreactivity may be obtained through theoretical and experimental studies of the quantum effects of UV irradiation on its components. The excited state lifetimes of gaseous cytosine have been experimentally characterized by several studies,6−14 where fast relaxation to the ground state has been proposed. Although the overall decay lifetime is on the order of picoseconds, several studies have noted a long-lived component as well.10,11 An important problem, however, with measuring the excited-state decay is that cytosine exists in several forms; this complicates the interpretation of the results of such experiments. Cytosine is known to exist in multiple tautomeric forms15−22 (see Figure 1). The presence of multiple tautomers may explain the relatively complex UV and near-UV absorption spectrum of cytosine. In a resonance-enhanced multiphoton ionization (REMPI) study of gas-phase cytosine, 1-methylcytosine, and 5-methylcytosine, Nir et al.12 observed two distinct areas of the REMPI spectrum: one at 31 000−32 500 cm−1, which was attributed to the keto tautomer, and another at 36 000−37 500 cm−1, which was attributed to the enol tautomer (no distinction between the two enol rotamers was made). These attributions © 2013 American Chemical Society

Special Issue: Curt Wittig Festschrift Received: August 2, 2013 Revised: September 23, 2013 Published: October 4, 2013 12165

dx.doi.org/10.1021/jp407758w | J. Phys. Chem. A 2013, 117, 12165−12174

The Journal of Physical Chemistry A

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increasingly clear that there is no one decay mechanism, which predominates; many of the proposed pathways may be involved.9,29 Investigations of the other tautomers are limited. The first study of all three tautomers was by Tomić et al.24 at the DFT/ MRCI level, which examined the radiationless decay of each. In that work S1/S0 conical intersections for the keto and ketoimino isomers were found, but no equivalent CI was found for the enol tautomer, leading the authors to the conclusion that the excited state lifetime for this tautomer is long. Very recently, two detailed studies have appeared examining the excited-state deactivation of the enol and keto-imino tautomers. Nakayama et al.47 used high level MS-CASPT2 calculations to explore the potential energy surfaces (PESs) and nonadiabatic dynamics to study the dynamics. In their results the keto-imino tautomer has the fastest deactivation, while the keto lifetime is somewhat longer and the enol tautomer has the longest lifetime. All three, however, have CIs to the ground state and the main difference is the energetic barrier which must be surmounted to reach these CIs. Mai et al.48 have compared the enol and keto cytosine excited-state dynamics including the triplet states. They also conclude that the excited-state decay for the enol tautomer is slower than the decay of the keto tautomer and that both forms have CIs connecting to the ground state. The experiments of Lapinski et al.15 are notable in that they give proof of the existence of five tautomers of cytosine in the gas phase (isolated in an argon matrix) and that they demonstrate interconversion between the tautomers induced by UV radiation near the band origin of keto cytosine. This is evidence that there is a barrierless mechanism for tautomerization in the keto tautomer, which can be activated upon irradiation with λ = 313−311 nm. There are several potential ways in which the keto form of cytosine may be converted to the other tautomers upon irradiation with UV light. Given the evidence that the tautomers have different excited-state lifetimes and decay pathways and that many tautomers are present in the gas phase, it seems that understanding the excited-state tautomerization process is key to understanding the overall photochemical behavior of cytosine. Our motivation in this study was to theoretically investigate the potential for excited-state tautomerization of the cytosine nucleobase. Tautomerization can change the essential nature of DNA and lead to mispairing and incorrect replication. Tautomerization may also be one way in which the nucleobase relaxes back to the ground state without engaging in any photoreactions that significantly change the character of the base itself or surrounding bases. Initially, an excited-state intramolecular proton transfer (ESIPT) mechanism was considered. Although we found that the barriers to tautomerization via ESIPT are lower than ground state tautomerization, these barriers are still too high to effectively compete with ultrafast, nonradiative decay through conical intersections. Decay through a conical intersection between the ground state and a low-lying repulsive πσ* state was also considered as a potential decay pathway that could lead to phototautomerism. This process is also energetically demanding and thus unlikely to efficiently induce tautomerization. A final tautomerization mechanism, involving S1/S0 CIs of the keto tautomer was considered. The mechanism is similar to the one proposed by Li et al.49 in order to explain the phototautomerization of 1methylcytosine but also explores pathways to the enol tautomer of cytosine for which no equivalent structure exists in the analogue. A barrierless pathway from the ππ* keto CI was

Figure 1. Ground-state optimized geometries of the five lowest-energy cytosine tautomers obtained at the MP2/cc-pVDZ level. Bond lengths given in angstroms (Å). Numbering of the ring atoms is also shown.

solvated.24 The enol tautomer has the lowest dipole moment of the three and is less stable in aqueous solution, although some evidence from quantum calculations points to its presence as a minor subset of the population.17 Despite this experimental and theoretical evidence that suggests that more than one tautomer of cytosine is present at high temperatures in the gas phase,15−22 many theoretical studies of the excited-state behavior of cytosine focus on the canonical keto form of the base exclusively;4,25−38 this is the form that appears in DNA and is the most stable in solution. The lowest-lying singlet excited state of the canonical keto form of cytosine is of ππ* character; this finding has been confirmed at many levels of theory including DFT,24 TDDFT,39−41 CASSCF/CASPT2,25,39,42 MRCI,28 CC2,43,44 CCSD,42 and CCSD(T).45,46 However, further theoretical characterization of both the vertical excitation spectrum and excited-state decay pathways varies widely with method and basis set used. Although it is commonly accepted that there is more than one conical intersection connecting the ground state with the lowlying excited states, energetic accessibility as well as the precise deactivation mechanism vary depending on the theoretical method employed. In addition to radiationless decay through several S1/S0 CIs, other decay pathways that have been proposed include three-state conical intersections30,32,33 and involvement of dark triplet states.36,37 Dynamics studies of the relaxation of keto cytosine in the gas phase have made it 12166



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Table 1. Mole Percentages of the Five Lowest-Energy Tautomers of Cytosine Theoretically and Experimentally Determined keto (canonical) enol 1 enol 2 keto-Imino 1 keto-Imino 2 a

MP2/cc-pVDZa

CCSD(T)/aug-cc-pVTZ16,b

CCSD(T)/cc-pVQZ20,c

IR Ar matrix20,d

MW jet-cooled54,e

4.3 31.6 61.7 2.0 0.4

31 20 43 5

29 17 37 17

22 26 44 8

44 44 11

This work. MP2/cc-pVDZ + ZPE corrections. Percents were calculated at 450 K. bOn the basis of ΔG at 473 K. cOn the basis of ΔG at 450 K. ∼450 K. e568 K.

d

Table 2. Vertical Excitation Energies, Oscillator Strengths, and State Characters of the Lowest-Lying Singlet States of Five Tautomers of Cytosine EOM-CCSD/6-311+G*a state

energy (eV)

Keto ππ* 4.8733 nπ* 5.3329 πσ* 5.7252 ππ* 5.9238 ππ* 5.9578 Enol (1) ππ* 5.0395 nNπ* 5.3216 πσ* 5.8924 nNπ* 6.0441 ππ* 6.1705 Enol (2) ππ* 5.0875 nNπ* 5.4213 πσ* 5.9431 nNπ* 6.0559 ππ* 6.1487 Keto-Imino (1) ππ* 5.3756 πσ* 5.6842 nNπ* 5.9352 ππ* 6.3227 Keto-Imino (2) ππ* 5.5163 πσ* 5.7030 nNπ* 6.0701 πσ* 6.1743 ππ* 6.5572

CC3-LR/aug-pVDZ20,45b

DFT/MRCI/TZVP24c

MS-CASPT2/DZP47d state

f

energy (eV)

f

state

energy (eV)

0.07501 0.00551 0.00410 0.05888 0.08293

4.71 5.18 5.46 5.55 5.97

0.065

ππ* nOπ* nNπ* ππ* nπ*

4.83 5.02 5.50 5.67 5.91

ππ* nNπ* nNπ* ππ* πσ*

5.14 5.27 5.99 6.13 6.35

0.138

0.10726 0.00587 0.01644 0.00602 0.11226 0.09874 0.00664 0.03258 0.00708 0.10046

4.88

0.113

5.84

0.174

5.07

0.209

5.89

0.003

nNπ* ππ* ππ* nπ*

5.19 5.26 5.96 6.18

EOM-CCSD(T) /aug-pVTZ45e

energy (eV)

state

energy (eV)

ππ* nπ* nπ*

4.48 4.74 5.26

ππ* nNπ* πσ* ππ* nOπ*

4.69 5.18 5.59 5.60 5.82

ππ* nπ* ππ*

4.81 4.88 5.48

ππ* nN8π* ππ*

4.67 5.59 5.75

0.26600 0.00098 0.00659 0.00179 0.17107

a

MP2/cc-pVDZ optimized geometry. bCCSD/cc-pVDZ geometry optimized under planarity constraints. cBHLYP geometry optimized under planarity constraints. dMP2/DZP geometry. eCCSD/cc-pVDZ optimized geometry.

for such calculations.17,21,43 Ground-state transition states were also located at the MP2 level. All minima and transition states optimized at this and every other level of theory employed in this study were confirmed by frequency analysis. Zero-point energy (ZPE) vibrational corrections to the ground state energies were obtained from the MP2 optimizations. Singlet excited state optimizations and transition state searches were performed using the time-dependent density functional theory (TDDFT) method with the B3LYP functional and the 6-31+G* basis set. ZPE corrections to the excited state energies were obtained from the TDDFT optimizations. The energies of the singlet excited states at optimized geometries were refined using equation-of-motion coupled-

found, which would allow for tautomerization as part of radiationless decay, circumventing the high energetic barriers required for ESIPT and repulsive πσ* tautomerization. This final mechanism is the most likely explanation for the observed phototautomerization of cytosine.15

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METHODS The ground state minimum energy geometries of the five tautomers studied were obtained using the Møller−Plesset 2nd order perturbation theory (MP2) method with the cc-pVDZ basis set of Dunning and co-workers. These MP2 ground-state minimum energy geometries were used for later energetic and vertical excitation calculations; it has been noted that MP2 generated geometries may be considered good starting points 12167



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tautomers. The electronic transitions between the two enol rotamers are similar, with an average difference of 0.05 eV, while the differences between the keto-imino rotamers are larger, with an average difference of 0.1 eV. The average difference of the oscillator strengths of the enol rotamers is 0.008. Because of technical issues, we were unable to obtain the oscillator strengths of the keto-imino (1) tautomer, but on the basis of the enol results, we expect the keto-imino (1) oscillator strengths to be very similar to those of the keto-imino (2) tautomer. The keto tautomer is the most extensively studied, and for this form, the excitation energies have been reported previously at the EOM-CCSD(T)/aug-cc-pVDZ level.45 These energies are also shown in Table 2. A comparison between these results and ours shows that the effect of triple excitations (and the different basis set) on the excitation energies is to lower their values by 0.13 to 0.3 eV. Although the EOM-CCSD energies are not in exact agreement with those generated by Szalay and co-workers,45 it will be shown later that the magnitude of the barriers to excited-state tautomerization calculated using these energies is significant enough that the discrepancy between the CCSD and CCSD(T) values is considered irrelevant to the conclusions drawn about the possibility of excited-state tautomerization. Bazsó et al.20 used CC3 and the aug-cc-pVDZ basis set to study the three tautomers but only calculated the A′ symmetry states; the aim was to reproduce the absorption spectrum, and A″ states do not contribute to it. Szalay et al. do include CC3 calculated A″ states of the keto tautomer in their study; they are combined into a single column in Table 2. The CC3 energies are very close to the CCSD(T) ones for the keto tautomer. Furthermore, modeling the absorption spectrum using the CC3 energies gives a spectrum very close to the experimental UV spectrum.20 Comparison of the CC3 energies of the A′ states to our results shows a difference of 0.2−0.4 eV, with the higher deviations corresponding to the higher states. Table 2 also shows results obtained by Tomić et al.24 using the DFT/MRCI method with the BHLYP functional.59,60 In general, the DFT/MRCI energies are lower; however, the energy of the states involving σ* orbitals is significantly higher due to the lack of diffuse functions in the basis set employed in the study. Another important difference between our results and the DFT/MRCI ones is that they predict the lowest state in the keto-imino (1) tautomer to be nπ*, while our results indicate that this state is 0.5 eV higher than the S1 state. This difference can have significant effects on the deactivation pathways of this tautomer. Although the DFT/MRCI results were the most comprehensive for comparing the tautomers for several years, higher level MS-CASPT2 energies have recently been published by Nakayama et al.47 for the three tautomers. These results show lower excitation energies compared to all other methods. The first singlet excited state of the keto-imino tautomer is of ππ* character, in agreement with our results as opposed to the DFT/MRCI results. Figure 2 shows the vertical excitation energies of the tautomers relative to the ground state energy of the keto tautomer. What is obvious in this figure is that the different tautomeric forms of cytosine absorb maximally at different wavelengths. It may therefore be possible to selectively excite the keto tautomer, as it absorbs at lower energies than the other tautomers. However, if excitation of the keto tautomer can trigger phototautomeric reactions, then the interpretation of the resultant spectra and excited-state relaxation behavior

cluster singles and doubles (EOM-CCSD) single-point calculations; the 6-311+G* basis set was employed in these calculations. Excitation energies, oscillator strengths of the electronic transitions, and state characters were obtained. Several linear-least-motion (LLM) paths were used in order to investigate excited-state tautomerization pathways. The LLM geometries were generated with the MacMolPlt program;50 internal coordinates were used in order to reduce the likelihood of artificial barriers as the result of translational motion. Single points on each LLM geometry were performed at the same level as the S1 optimizations (TDDFT/6-31+G*). All EOM-CCSD and TDDFT calculations were done using QChem51 or NWChem.52 MP2 optimizations and transition state searches were done with the GAMESS computational package.53 MacMolPlt50 was used to view all geometries and orbitals.

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RESULTS AND DISCUSSION Tautomers: Geometries and Vertical Excitations. The geometries of the five tautomers studied in this work optimized at the MP2/cc-pVDZ level are shown in Figure 1. Although there are three basic forms the molecule can take depending on the location of the hydrogens, for both the enol and keto-imino tautomers there are two rotamers depending on the OH/NH orientation resulting in a total of five tautomers. Other higherenergy tautomers exist, but the five shown here were chosen for study as they are the lowest in energy and have been experimentally observed in gaseous samples of cytosine.15 The geometries we find compare well with previously published ones.16,21 Although the presence of many tautomers in gas phase cytosine has been demonstrated, the exact molar fraction of each tautomer is difficult to quantify. The very small energy differences make theoretical calculation of these fractions challenging, while experimental determination is also not trivial. Table 1 summarizes the mole percentages of the five lowest energy tautomers according to the most accurate recent calculations as well as experimental determinations. The temperatures chosen correspond roughly to the range of evaporation temperatures used to prepare gaseous samples of cytosine. Upon evaporation, these distributions are expected to be present. Table S1 in Supporting Information gives the relative energies of the tautomers for various levels of theory. The results obtained at the MP2/cc-pVDZ level of theory here are also shown, although one should not expect them to produce very accurate results. Since the main goal of this work is not to establish the relative ratios, we believe the MP2 and CCSD methods employed here are sufficient for our purposes. Evidence of the presence of more than one tautomer of cytosine in the gas phase has also been observed experimentally.10,12,15,20,55,56 Table 1 shows two representative experimental results. In the work of Bazsó et al.20 the ratios are estimated using IR spectroscopy of cytosine in Ar matrix, while Brown et al.54 used microwave spectroscopy of jet-cooled cytosine. These results confirm the presence of all three keto, enol, and keto-imino tautomers. The presence of multiple tautomers has also been demonstrated for structural variants of cytosine such as 1-methylcytosine10,57 and isocytosine.44,58 The vertical excitation energies and oscillator strengths are compiled in Table 2. To the best of our knowledge, this is the first study that reports the excitation energies of all five tautomers. Previous studies are also shown in Table 2, which show only one of the two rotamers for the enol and keto-imino 12168



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Figure 2. Vertical excitation energies of the five lowest-energy tautomers of cytosine at the EOM-CCSD/6-311+G* level. Energies are in eV and are given relative to the ground state energy of the keto tautomer.

becomes much more complex, as the results will include contributions from other tautomers. The discovery of an accessible tautomerization mechanism may change the interpretation of past studies, which claimed to exclusively excite the keto tautomer and discounted contributions from other forms of cytosine. Ground-State Tautomerization. Before focusing on excited-state tautomerization, we show our results on the ground-state tautomerization process. Although our main concern is excited-state tautomerization, we include this information about the ground state process in order to provide a reference point for the later excited-state data. Transition states along the tautomerization coordinate were located at the MP2/cc-pVDZ level, and the energies at these geometries were calculated at the CCSD/6-311+G* level and compared to the energies of the optimized geometries of each tautomer. The barriers to ground-state tautomerization at the CCSD/6311+G* level including ZPE corrections at the MP2/ccpVDZ level are presented in Figure 3. For the keto to enol tautomerization the barrier was found to be 1.81 eV (175.1 kJ/ mol); for keto to keto-imino the value was higher at 2.03 eV (195.6 kJ/mol). The value of the imaginary frequencies for the keto to enol (KE) and keto to keto-imino (KKI) transition states are 1827 and 1841 cm−1, respectively, indicating that the barriers are rather steep. The transition state geometries are shown in Figure 3b,c and can be compared with the minima shown in Figure 1. The transition states are planar, except for a small pyramidalization of the NH2 group in the KE transition state. The ground-state tautomerization barriers have been found in previous studies as well. In a B3LYP/6-311+G(2df,2p) theoretical study of the S0 tautomerization process, Mazzuca and co-workers estimated the ground-state keto to enol and keto to keto-imino tautomerization barriers to be 1.62 and 1.88 eV, respectively.61 Although these values are lower than those found in this work by about 0.2 eV, the relative height of the barriers is consistent. Yang et al. also calculated the ground state tautomerization barriers at the MP2(full)/6-311+G(2d,2p)//MP2(full)/6-31+G* level and found the barrier for

Figure 3. (a) Energetic barriers to ground-state tautomerization calculated at the CCSD/6-311+G* level including ZPE corrections. Energies are given relevant to the ground state energy of the keto tautomer. (b) Keto to enol (2) transition state on the S0 surface. (c) Keto to keto-imino (1) transition state on the S0 surface. Geometries and ZPE corrections calculated at the MP2/cc-pVDZ level; bond lengths in Å. Barriers shown (EA) are for the keto to relevant tautomer transition.

keto to enol tautomerization to be 1.47 eV; the barrier for keto to keto-imino tautomerization was found to be 1.75 eV.62 Even though there is some disagreement about the exact value of the barriers, it is clear that regardless of the level of theory the ground-state tautomerization barriers are too high to be overcome by thermal evaporation; it appears that the presence of multiple tautomers in gas phase experiments is not due to ground-state proton transfer processes in the absence of water. However, these results do not explain experimentally observed15,55,57 UV-induced tautomerization; our aim in the rest of this article is to explain this phenomenon. Excited-State Tautomerization. S1 Minima. The three tautomers involved in excited-state tautomerization reactions were optimized on the first excited state PES and are shown in Figure 4. Many of the ring bond lengths are different than in the ground state, particularly the C5−C6 bond; this difference

Figure 4. S1 optimized geometries of the three tautomers relevant to the tautomerization reactions of cytosine. Geometries were obtained at the TDDFT/6-31+G* level. Bond lengths in Å. 12169



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is due to changes in aromaticity resulting from photon-induced electronic rearrangement. Calculating the S1 minima has more complications compared to the vertical excited states, so we spend some time here explaining the problems. The S1 minimum of the keto tautomer has mixing between the nπ* and ππ* states since they are very close in energy at this geometry and significant coupling between them occurs. The mixing between the states is evident in the geometry, which has both the C5−C6 and the carbonyl bonds elongated. Whether the nπ* or the ππ* state is lower in energy at this geometry is very sensitive to the method used. Table S2, Supporting Information, shows adiabatic energies at various levels of theory. The CCSD results have the ππ* state as the S1 state in agreement with high level MRCI and CASPT2 calculations.25,28,47 TDDFT, however, has the nπ* as being the S1 state at this geometry.39 This problem appears in CASSCF and CC2 calculations, too. Despite the fact that CCSD gives the correct character at this geometry, the adiabatic energy is higher than what MRCI and MS-CASPT2 predict and higher than the experimentally observed origin that is believed to originate from the keto tautomer. Experimentally the adiabatic energy has been determined by resonant two-photon ionization spectra to be 3.947 eV.13,14 CCSD overestimates this energy by 0.66 eV. Bazsó et al. used CCSD and linear vibronic coupling to model the spectrum, and suggested that the origin should actually be higher than the experimentally proposed value, and the problem is with the experimental interpretations rather than CCSD.20,23 The enol minimum found in this work is an nπ* state at both the TDDFT and CCSD levels. Tomić et al.24 located both ππ* and nπ* minimum with similar energies. Nakayama and coworkers47 were able to locate only a ππ* minimum at the MSCASPT2 level and only an nπ* minimum at the CASSCF level, underlining the importance of dynamic electron correlation. The origin of the enol tautomer is at 4.46 eV according to Nir et al.12,13 CCSD again overestimates this number by 0.37 eV. Furthermore, CCSD predicts both keto and enol origins 0.5− 0.6 eV higher than MS-CASPT2, while at vertical excitation the two methods differed by 0.3−0.4 eV for these tautomers. Finally, the S1 minimum found here for the keto-imino tautomer has ππ* character. Tomić et al.24 found both nπ* and ππ* minima, while Nakayama et al.47 did not locate any minima since they found a downhill path to the conical intersections. Clearly, describing the S1 minima is more complicated than describing the vertical excitation energies. The close proximity of states where crossings can occur along the way to the minimum complicates the issue. Nondynamical and dynamical correlation are both required to accurately describe the surfaces and thus the minima. Although we acknowledge these problems here, we still do not believe they affect the purpose of the present study. As will be seen in the next section, the barriers found are quite high, and the discrepancies between the S1 minima should not affect our conclusions. Excited-State Intramolecular Proton Transfer. Figure 5 shows the tautomerization barriers and the transition states involved in ESIPT. The ZPE corrected barriers to ESIPT, where a hydrogen shift causes tautomerization from the S1 minimum geometry of one tautomer to the S1 minimum of another, were found to be 1.53 eV for keto to enol tautomerization and 1.04 eV for keto to keto-imino tautomerization. The barriers are similar at the TDDFT level, 1.49 and 0.93 eV, respectively. The KE transition state has an imaginary frequency of 2093.39 cm−1, while the KKI transition

Figure 5. (a) Adiabatic energy barriers to first excited state (S1) tautomerization calculated at the EOM-CCSD/6-311+G* level. Energies are given relevant to the ground state energy of the keto tautomer. (b) Keto to enol (2) transition state on the S1 surface. (c) Keto to keto-imino (1) transition state on the S1 surface. Geometries and ZPE corrections calculated at the TDDFT/B3LYP/6-31+G* level; bond lengths in Å. Barriers shown (EA) are for the keto to relevant tautomer transition.

state has 636.63 cm−1. The values of the frequencies indicate that the two transition states are quite different, the first one being much steeper than the second one. The value of the barrier is also 0.5 eV lower for the keto to keto-imino transition. We will see later that the differences between the transition states are reflected in their geometries, and ultimately in the character of the excited states. The barriers shown in Figure 5 are quite high, and the associated processes will not compete effectively with radiationless decay to which there is little or no barrier as has been recently shown for every tautomer;47 the ESIPT mechanism is thus not energetically competitive for any form of cytosine. As mentioned earlier the barriers are both ≥1 eV, high enough that the errors expected in CCSD do not alter the main conclusion that this mechanism is not energetically feasible. In the KE S1 transition state, the distance between the hydrogen atom and the oxygen and carbon atoms are similar to the respective distances in the ground state transition state, although the hydrogen is closer to the oxygen than to the carbon in the excited state. In the KKI S1 transition state, however, the hydrogen is significantly further away from the nitrogens than in the corresponding S0 transition state. Analysis of the orbitals involved in excitation revealed promotion from a molecular π orbital to an S-like σ* orbital of the transitioning hydrogen as the first singlet excited state at the transition state. Figure 6 reveals another important property at this geometry. In this figure, the energies of the ground and first two excited states are shown for the minima and transition state geometries of S1. What is unique about the KKI transition state is that the 12170



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Figure 6. Energies of the singlet excited states at the S1 minima and transition states involved in the ESIPT mechanism at the EOMCCSD/6-311+G* level. Energies are given relative to the ground state energy of the ground state minimum of the keto tautomer (not shown). Black, S0; red, S1; green, S2. KE TS: Keto to enol transition state. KKI TS: Keto to keto-imino transition state. See geometries in Figure 5b,c.

Figure 7. LLM path between the keto (left) and keto-imino (right) S1 minima passing through the S1 transition state. Excited-state energies at the TDDFT/6-31+G* level given relative to the ground state energy of the keto S0 minimum at the same level of theory. Average N−H distance refers to distance between transferred hydrogen and the substituent nitrogen, averaged with the distance between the same hydrogen and the N3 ring nitrogen. Keto to TS path (left half of the figure): Smaller substituent-to-hydrogen distance. TS to keto-imino path (right half of the figure): Smaller ring nitrogen-to-hydrogen distance. Purple bar: energy of the keto-like transition state. Orange bar: energy of the keto-imino-like transition state.

ground state has been destabilized considerably, and the gap between S0 and S1 is only 0.7 eV. The proximity of the energies of these states led us to investigate an alternate mechanism to ESIPT for tautomerization, which will be discussed in the following section. Role of Repulsive πσ* States. Figure 6 shows the energies and character of states at the geometries of the S1 minima and transition states connecting the different tautomers. The two transition states on the S1 surface have very distinct properties. For the keto to enol reaction, at the transition state geometry the gap between the electronic ground state and the S1 state is large. At the keto to keto-imino transition state the first excited state and the ground state approach each other energetically, suggesting the possibility of a nearby conical intersection in that region of the coordinate space. Furthermore, although the character of both the keto and the keto-imino (1) S1 minima is ππ* at the CCSD level, the character of the S1 state at the KKI transition state is πσ*. The energy of the ground state at the KKI transition state is close to the energy of the S1 state of the keto-imino S1 minimum, suggesting a keto-imino to keto tautomerization process, which may be feasible if there is crossing between the ππ* state of the keto-imino tautomer with the ground state leading directly to the ground state. To further investigate the potential for tautomerization in this manner, geometries between the KKI transition state and the S1 minima of both keto and keto-imino tautomers were linearly interpolated to generate an LLM path. TDDFT/631+G* single-point calculations were performed on each geometry in order to approximate the potential energy surfaces of the lowest-lying states along the reaction coordinate. The results are shown in Figure 7. TDDFT is not a method suitable for describing conical intersections; however, the path constructed here is only used to provide a qualitative picture of the energetics of this mechanism. In neither the keto nor the keto-imino (1) tautomer is the lowest-lying singlet excited state of πσ* character. Note that as previously mentioned, the keto S1 minimum is of nπ* character at the TDDFT level. At a minimum distance of 2.09 Å from the amino moiety or 1.43 Å from the ring nitrogen along the LLM path, the πσ* state becomes the lowest-lying singlet state. The crossings are

obvious in the LLM path. Note that the x axis of the plot uses the average distance between H and each of the two nitrogens. The PES of the πσ* state is flat and somewhat downhill as a function of average NH distance. However, the energy of the ground state continues to increase, so the two states approach each other until, at the transition state, they are very close in energy. Close to the crossings between the initial ππ* state and the πσ* state the LLM shows maxima on the S1 surface, but these are not true transition states since the LLM path does not represent the true minimum energy path (MEP) of a reaction. Saddle point searches were performed starting from the geometries associated with these maxima leading to two more transition states: one between the keto tautomer and the transition state (keto-like), and the other between the ketoimino (1) tautomer and the transition state (keto-imino-like). Their structures are shown in Figure S1, Supporting Information. The barrier to the keto-like transition state is 1.60 eV (from the keto tautomer). The barrier to the ketoimino-like transition state is 0.62 eV (from the keto-imino tautomer). Neither of the additional transition states was higher in energy than the midpoint (fully dissociated hydrogen) transition state, suggesting that the overall energetic barrier to tautomerization may be represented by the difference between the energies of the tautomer and midpoint transition state geometries. For comparison the LLM path for the keto to enol transition is shown in the Supporting Information (Figure S3), where it is obvious that the behavior is much different. In that case there are no additional transition states, and the stationary point found connects the two minima directly. The above mechanism has been discussed by Chmura and co-workers in pyridinone systems.63 In this mechanism, the S1 minimum of the product tautomer is not reached. Once the system crosses to the πσ* state, it will travel downhill to another crossing, this one between the πσ* state and the ground state. When the system crosses to the S0 surface, it may 12171



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relax to the starting geometry or to the other tautomeric form of the molecule. This is known as a photoinduced dissociation association (PIDA) mechanism.63 Exploratory calculations, given in the Supporting Information, showed that the πσ*/ ground state crossings were not energetically accessible from the S1 minima in cytosine. A S1/S0 πσ* CI was located in cytosine in a study by Merchan et al.; such a crossing at the CASPT2/6-31G** level was 0.75 eV higher than an energetically preferred S1/S0 ππ* CI of the keto tautomer.25 In summary, the PIDA mechanism also does not explain an easily accessible tautomerization mechanism for cytosine. Tautomerization As an Alternate Pathway in Radiationless Decay through Conical Intersections. The above mechanisms for tautomerization fail to explain the experimental findings of Lapinski and co-workers,15,55,64 where tautomerization in cytosine and cytosine derivative systems has been observed when irradiating with wavelengths near the origin of the keto tautomer (λ = 313−311 nm). In this case tautomerization should be barrierless, which is very different from the results we obtained so far. Li and co-workers49 provide an alternative mechanism for tautomerization in 1-methylcytosine, which involves the same conical intersections as those used for radiationless decay. After excitation of the keto tautomer to the first bright singlet state, relaxation to conical intersections between the S1 state and the ground state occurs through pathways with small barriers, as has been established by numerous studies. At the conical intersection, a subset of the population can go through conformational changes leading to a transition state between the keto and keto-imino tautomers on the ground state PES. Li et al. showed that the pathways between the CI geometries and the transition state geometries have no barriers, and thus they proposed this mechanism as part of the radiationless decay mechanism of 1-methylcytosine and at the same time, to explain the experimentally observed57 tautomerization of the gas phase molecule. Here we are investigating this mechanism in cytosine. However, in order to study this mechanism for canonical cytosine, more pathways have to be considered since tautomerization to the enol form of the molecule is also possible (this reaction is blocked by the methyl group in 1methylcytosine). We used the two keto CIs previously described by Kistler et al. at the MRCI level28 (shown in Figure 8). These CIs were connected via LLM paths to the two S0 transition states shown in Figure 3. As is evident from the ground state energies in Figure 8, there is a barrierless path connecting the twist CI to both the KE and KKI ground state transition states. Although as previously mentioned TDDFT cannot describe conical intersections accurately, at the twist CI geometry (the first point in both a and b) the ground and first excited states are quite close, indicating that the method is capable of describing the energy in this region of the coordinate space. LLM paths connecting the transition states with the ground state minima with no additional barriers are given in Figure S4, Supporting Information. The case of the sofa CI pathways (c and d in Figure 8) is somewhat different. It is clear, given the difference in energy between the S0 and S1 states at this geometry, that the sofa CI is less well described by TDDFT. Furthermore, the LLM pathways to both the KE and KKI transition states have barriers, 0.32 eV in c and 0.08 eV in d. However, these are only upper bounds of the barriers, and in this case they mainly show that these pathways are less favorable compared to the ones

Figure 8. Pathways between the keto CIs and the transition states on the S0 surface. Energies at the TDDFT/6-31+G* level, given relative to the ground state energy of the keto S0 minimum geometry. See Figure S4, Supporting Information, for the LLM paths between the S0 transition states and the ground state minima of the tautomers.

originating from the twist CI. Additionally, in the case of the sofa to KKI pathway, the barrier is slight enough that it may be overcome. This study has established the energetic feasibility of a phototautomeric mechanism for keto cytosine. The mechanism shown in Figure 8 is the most likely explanation of those considered in this work for the tautomerization reported by Lapinski.15 It is notable that the wavelength used in the Lapinski study was high enough that the keto tautomer was selectively excited; the keto population was shown to decrease after irradiation, while the enol and keto-imino populations both increased. Competing tautomeric pathways, which convert the other tautomers to the keto form, may be accessible when the excitation energy is high enough so that the other tautomers may absorb.

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CONCLUSIONS There is clear evidence for the existence of multiple tautomers in gas-phase samples of cytosine. This fact must be taken into account when attempting to characterize the decay pathways that the molecules follow after photoexcitation. Additionally, it is important to establish the source of these tautomers and any tautomerization reactions that may occur after UV perturbation. In this study, we present several tautomerization mechanisms in order to explain the observed phototautomerization of cytosine. ESIPT has the highest barriers of the excited-state mechanisms; PIDA has slightly lower barriers but is still not energetically comparable to radiationless decay and certainly could not explain tautomerization observed after excitation with low-energy light. Finally, a barrierless pathway connecting the keto twist (ethylenic) CI to the ground state transition states to both the keto-imino and enol tautomers has been described. Similar paths from the sofa CI have very low barriers, and it is possible that both contribute to tautomerization. Although the enol and keto-imino tautomers are considered to be less biologically relevant than the canonical tautomer of cytosine, partly because of their decreased stability in vivo and partly because of the inability of the enol tautomer to be 12172



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(12) Nir, E.; Müller, M.; Grace, L. I.; de Vries, M. S. REMPI Spectroscopy of Cytosine. Chem. Phys. Lett. 2002, 355, 59−64. (13) Nir, E.; Hünig, I.; Kleinermanns, K.; de Vries, M. S. The Nucleobase Cytosine and the Cytosine Dimer Investigated by Double Resonance Laser Spectroscopy and ab Initio Calculations. Phys. Chem. Chem. Phys. 2003, 5, 4780−4785. (14) Lobsiger, S.; Trachsel, M. A.; Frey, H.-M.; Leutwyler, S. ExcitedState Structure and Dynamics of Keto-Amino Cytosine: The 1ππ* State is Nonplanar and its Radiationless Decay Is Not Ultrafast. J. Phys. Chem. B 2013, 117, 6106−6115. (15) Lapinski, L.; Reva, I.; Nowak, M. J.; Fausto, R. Five Isomers of Monomeric Cytosine and Their Interconversions Induced by Tunable UV Laser Light. Phys. Chem. Chem. Phys. 2011, 13, 9676−9684. (16) Wolken, J. K.; Yao, C.; Tureček, F.; Polce, M. J.; Wesdemiotis, C. Cytosine Neutral Molecules and Cation-Radicals in the Gas-phase. Int. J. Mass Spectrom. 2007, 267, 30−42. (17) Trygubenko, S. A.; Bogdan, T. V.; Rueda, M.; Orozco, M.; Luque, F. J.; Šponer, J.; Slavíček, P.; Hobza, P. Correlated ab Initio Study of Nucleic Acid Bases and Their Tautomers in the Gas Phase, in a Microhydrated Environment and in Aqueous Solution Part 1. Cytosine. Phys. Chem. Chem. Phys. 2002, 4, 4192−4203. (18) Feyer, V.; Plekan, O.; Richter, R.; Coreno, M.; Vall-llosera, G.; Prince, K. C.; Trofimov, A. B.; Zaytseva, I. L.; Moskovskaya, T. E.; Gromov, E. V.; et al. Tautomerism in Cytosine and Uracil: an Experimental and Theoretical Core Level Spectroscopic Study. J. Phys. Chem. A 2009, 113, 5736−5742. (19) Radchenko, E. D.; Sheina, G. G.; Smorygo, N. A.; Blagoi, Y. P. Experimental and Theoretical Studies of Molecular Structure Features of Cytosine. J. Mol. Struct. 1984, 116, 387−396. (20) Bazsó, G.; Tarczay, G.; Fogarasi, G.; Szalay, P. G. Tautomers of Cytosine and Their Excited Electronic States: a Matrix Isolation Spectroscopic and Quantum Chemical Study. Phys. Chem. Chem. Phys. 2011, 13, 6799−6807. (21) Kobayashi, R. A CCSD(T) Study of the Relative Stabilities of Cytosine Tautomers. J. Phys. Chem. A 1998, 102, 10813−10817. (22) Fogarasi, G. High-Level Electron Correlation Calculations on Some Tautomers of Cytosine. J. Mol. Struct. 1997, 414, 271−278. (23) Tajti, A.; Fogarasi, G.; Szalay, P. G. Reinterpretation of the UV Spectrum of Cytosine: Only Two Electronic Transitions? ChemPhysChem 2009, 10, 1603−1606. (24) Tomić, K.; Tatchen, J.; Marian, C. M. Quantum Chemical Investigation of the Electronic Spectra of the Keto, Enol, and KetoImine Tautomers of Cytosine. J. Phys. Chem. A 2005, 109, 8410−8418. (25) Merchán, M.; Serrano-Andrés, L. Ultrafast Internal Conversion of Excited Cytosine via the Lowest ππ* Electronic Singlet State. J. Am. Chem. Soc. 2003, 125, 8108−8109. (26) Ismail, N.; Blancafort, L.; Olivucci, M.; Kohler, B.; Robb, M. A. Ultrafast Decay of Electronically Excited Singlet Cytosine via a π,π* to nO,π* State Switch. J. Am. Chem. Soc. 2002, 124, 6818−6819. (27) Merchán, M.; Gonzalez-Luque, R.; Climent, T.; Serrano-Andrés, L.; Rodriuguez, E.; Reguero, M.; Pelaez, D. Unified Model for the Ultrafast Decay of Pyrimidine Nucleobases. J. Phys. Chem. B 2006, 110, 26471−26476. (28) Kistler, K. A.; Matsika, S. Radiationless Decay Mechanism of Cytosine: an ab Initio Study with Comparisons to the Fluorescent Analogue 5-Methyl-2-pyrimidinone. J. Phys. Chem. A 2007, 111, 2650−2661. (29) Hudock, H. R.; Martnez, T. J. Excited-State Dynamics of Cytosine Reveal Multiple Intrinsic Subpicosecond Pathways. ChemPhysChem 2008, 9, 2486−2490. (30) Kistler, K. A.; Matsika, S. Three-State Conical Intersections in Cytosine and Pyrimidinone Bases. J. Chem. Phys. 2008, 128, 215102. (31) Blancafort, L. Energetics of Cytosine Singlet Excited-State Decay Paths: A Difficult Case for CASSCF and CASPT2. Photochem. Photobiol. 2007, 83, 603−610. (32) Blancafort, L.; Robb, M. A. Key Role of a Threefold State Crossing in the Ultrafast Decay of Electronically Excited Cytosine. J. Phys. Chem. A 2004, 108, 10609−10614.

formed when N1 is attached to a ribose moiety as is found in native DNA, the study of their interconversion and differing excited-state behavior contributes to the overall knowledge of the nucleobase, particularly in the gas phase. Comparisons between gas-phase and solvated behavior can be better accomplished as well. Finally, the study of cytosine tautomers and tautomerization reactions may provide insight into other molecules in which tautomerism is possible.

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ASSOCIATED CONTENT

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AUTHOR INFORMATION

S Supporting Information *

Additional figures of structures and LLM paths as described in the text, and Cartesian coordinates. This material is available free of charge via the Internet at http://pubs.acs.org. Corresponding Author

*(S.M.) E-mail: [email protected]. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work was supported by the National Science Foundation under grant CHE-1213614. C.G.T. was partly supported by an Undergraduate Research Program at Temple University.

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REFERENCES

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