Charge-Transfer Excited States and Proton Transfer in Model Guanine

Jul 19, 2013 - Yuyuan Zhang , Xi-Bo Li , Aaron M. Fleming , Jordan Dood , Ashley A. Beckstead , Anita M. Orendt , Cynthia J. Burrows , and Bern Kohler...
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Charge-Transfer Excited States and Proton Transfer in Model Guanine-Cytosine DNA Duplexes in Water Chaehyuk Ko and Sharon Hammes-Schiffer* Department of Chemistry, University of Illinois at Urbana−Champaign, 600 South Mathews Avenue, Urbana, Illinois 61801, United States S Supporting Information *

ABSTRACT: Characterization of the excited electronic states and relaxation processes in DNA systems is critical for understanding the physical basis of radiation damage. Spectroscopic studies have shown evidence of coupling between the relaxation dynamics of photoinduced charge-transfer states and interstrand proton transfer in DNA duplexes, where a deuterium isotope effect was observed for duplexes with alternating sequences but not with nonalternating sequences. We performed quantum mechanical/molecular mechanical (QM/MM) calculations of the vertical excitation energies and excited state proton potential energy curves for model DNA duplexes comprised of three guaninecytosine pairs with alternating and nonalternating sequences in aqueous solution. Our calculations indicate that the intrastrand charge-transfer states are lower in energy for the alternating sequence than for the nonalternating sequence. The more accessible intrastrand charge-transfer states could provide a relaxation pathway coupled to interstrand proton transfer, thereby providing a possible explanation for the experimentally observed deuterium isotope effect in duplexes with alternating sequences. SECTION: Biophysical Chemistry and Biomolecules

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In the present work, we characterize the excited electronic states in model DNA duplexes comprised of three G-C pairs with alternating and nonalternating sequences in aqueous solution. Our objective is to identify qualitative differences in the nature of the CT states upon initial photoexcitation and the behavior of these states upon interstrand PT. Schematic diagrams of these two model systems are depicted in Figure 1. In this study, we use a quantum mechanical/molecular mechanical (QM/MM) approach, where the DNA duplex is described by long-range corrected time-dependent density functional theory (LRC-TDDFT),12 and the aqueous solvent environment is described by a molecular mechanical (MM) force field. Although these calculations do not provide a definitive explanation for the deuterium isotope effects observed in alternating but not in nonalternating sequences, our studies illuminate qualitative differences between these two types of sequences in terms of the interstrand and intrastrand CT states and their relation to interstrand PT. Such differences are expected to influence the long-time dynamics and could potentially lead to different isotope effects. The first step of our study was to calculate the vertical excitation energies of the model DNA duplexes in solution and characterize the low-lying singlet excited states. The geometries of the three G-C base pairs in alternating and nonalternating sequences were chosen to be those of canonical B-DNA. These geometries were obtained using a web-based DNA analysis

haracterization of the excited electronic states and relaxation processes in DNA systems is of vital importance for understanding the genetic damage caused by UV radiation, and a wide range of experimental and theoretical studies have been directed toward this characterization.1−8 Recently, a photoprotective role of proton transfer (PT) within DNA base pairs has been suggested.5−7 On the basis of theoretical calculations, PT has been found to facilitate the ultrafast decay of electronic excitation in a single base pair in the gas phase, thereby enhancing the photostability of this species.5−7 Additionally, transient absorption spectroscopic studies on single-stranded DNA systems have illustrated that the stacking interactions lead to long-lived excited states that do not exist in monomeric bases.9 These long-lived excited states were proposed to be of intrastrand charge-transfer (CT) character.10 The dynamics of these long-lived excited states was not significantly affected by base pairing in the duplex systems.9 Furthermore, for both adenine-thymine (A-T)9 and guaninecytosine (G-C)11 DNA duplex systems, a deuterium isotope effect was observed for the long-time decays in the duplexes with alternating sequences but not in the duplexes with nonalternating sequences. This type of isotope effect was also not observed in single-stranded DNA, suggesting that the isotope effect could arise from an interstrand PT process. A proposed interpretation of these isotope effects is that the intrastrand CT state enables interstrand PT in the alternating sequence but not in the nonalternating sequence duplex because of the stronger CT character in the alternating sequence duplex.11 © 2013 American Chemical Society

Received: June 3, 2013 Accepted: July 19, 2013 Published: July 19, 2013 2540

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Å beyond the duplex. We also tested larger QM regions that included the 10 or 20 closest water molecules, as well as the DNA duplex. The larger QM regions resulted in similar excitation energies for the CT states, as shown in Table S1 of the Supporting Information; therefore, we performed our full analysis on the smaller QM region consisting of only the DNA duplex. The QM/MM interaction energy was calculated with the electronic embedding scheme, in which the QM electronic density is polarized by the MM point charges (i.e., the TIP3P charges for the water molecules). The excited states were characterized using the natural transition orbital (NTO)17 analysis. The MD simulations on the water were performed with AMBER11,18 and the QM/MM calculations were performed with the Q-Chem package.19 Figure 2 compares the vertical excitation energies of the intrastrand and interstrand singlet CT states calculated for the

Figure 1. Schematic diagrams of the model DNA duplex structures studied in the present work: (a) nonalternating sequence and (b) alternating sequence. G and C denote guanine and cytosine bases, respectively, and each column represents a single strand with the hydrogen bonds indicated by dashed lines. The phospho-deoxyribose backbones are removed. (c) The Watson−Crick base pairing between guanine and cytosine. The proton in the red box is displaced from G to C of the middle pair in (a) and (b) to generate the potential energy curves along the proton coordinate.

application, Web 3DNA,13 with the missing hydrogen atoms added by MolProbity.14 The sugar−phosphate backbones were removed, and the N-glycosidic bonds were capped with hydrogen atoms. A previous study showed that this kind of modification affects the vertical excitation energies by only ∼0.1 eV.15 The positions of the hydrogen atoms were optimized at the DFT/B3LYP/6-31G* level of theory with all other atomic positions fixed. Each DNA duplex was immersed in a rectangular box of water molecules extending at least 20 Å beyond the duplex in all directions. With the DNA duplex geometries fixed, the box of water was equilibrated at 300 K in the NVT ensemble for 300 ps using classical molecular dynamics (MD) simulations with periodic boundary conditions and the AMBER99 and TIP3P force fields for the base pairs and water molecules, respectively. After equilibration, 11 snapshots of water configurations were obtained at 10 ps intervals from a 100 ps MD trajectory. Note that these water configurations were obtained from equilibrium MD simulations of the ground state, corresponding to the situation prior to photoexcitation (i.e., at the Franck−Condon point). The vertical excitation energies were calculated for each of these snapshots using QM/MM methods. The QM region was described by TDDFT using the long-range corrected functional PBE12 (denoted LRC-ωPBE in ref 15) in an effort to avoid known difficulties such as underestimation of the CT state energies. We used the same range partitioning parameter (0.3 bohr−1) and basis set (6-31G*) as those used in a previous study on A-T model systems.15,16 This previous study compared the excitation energies for nucleobase dimers calculated with TDDFT/LRC-ωPBE to those calculated with correlated wave function methods, such as CC2 and CIS(D), and showed that this level of TDDFT theory provides qualitatively reasonable excitation energies for these types of systems. Multiconfigurational wave function methods could potentially provide more quantitatively accurate energetics of CT states but are computationally expensive for these large systems and are beyond the scope of the qualitative analysis herein. The QM region included all atoms in the DNA duplex, and the MM region included all water molecules extending 10

Figure 2. Vertical excitation energies of intrastrand (blue) and interstrand (red) singlet CT states for DNA duplexes comprised of three G-C base pairs in water with alternating (filled circles) and nonalternating (open circles) sequences. The excitation energies were calculated with a QM/MM approach using TDDFT/LRC-ωPBE/631G* for the DNA duplex and TIP3P for water at water configurations obtained from 11 snapshots along a MD trajectory. Note that the water configurations for each snapshot are different for the alternating and nonalternating sequences because they were generated from independent MD trajectories. The energy range is from S1 to S25. The average excitation energies of the lowest CT states of each type are indicated by the horizontal lines, with solid lines corresponding to the alternating sequence and dashed lines corresponding to the nonalternating sequence. Note that the intrastrand CT states are lower in energy for the alternating sequence (filled blue circles, solid blue line) than those in the nonalternating sequence (open blue circles, dashed blue line).

11 water configuration snapshots described above. The intrastrand and interstrand CT states are shown in blue and red, respectively. The open and filled circles denote the CT states for the DNA duplexes with nonalternating and alternating sequences, respectively. Within the energy range (up to S25) of Figure 2, the intrastrand CT states always correspond to a G → C transition for the alternating sequence and, as dictated by the sequence, a G → G or C → C transition for the nonalternating sequence. The interstrand CT states always correspond to G → C transitions for both alternating and nonalternating systems. Figure 3 depicts the NTOs associated with representative intra- and interstrand CT states for the nonalternating and alternating sequences. The interstrand CT state tends to be delocalized along the C strand for the nonalternating sequence, but the other CT states 2541

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Figure 3. NTOs representing the dominant transitions (>95%) in the (a) nonalternating sequence and (b) alternating sequence of a duplex comprised of three G-C pairs in aqueous solution. The intrastrand and interstrand CT states are depicted on the top and bottom, respectively, with the specific CT states indicated over the arrow. For clarity, the water molecules are not shown.

intrastrand CT character.10 In time-resolved femtosecond transient absorption experiments on the alternating G-C duplex,11 the relaxation process was observed to exhibit a monoexponential decay with a time constant of ∼5 ps in H2O but a biexponential decay with time constants of ∼5 and 22 ps in D2O. This deuterium isotope effect was not observed for the nonalternating duplex or for single-stranded DNAs. Similar results were obtained for A-T duplexes.9 According to Figure 2, the intrastrand CT states of the G-C duplex are accessible with lower-energy photoexcitation for the alternating sequence than for the nonalternating sequence. Similar trends were found in previous TDDFT calculations on a model DNA duplex of three A-T pairs in the gas phase.15 Although these analyses focus on the CT states in the Franck−Condon region (i.e., immediately following photoexcitation), differences in the CT states at early times are expected to influence the long-time dynamics. Thus, the common trends in the relative energetics of the intra- and interstrand CT states found in alternating and nonalternating A-T and G-C duplexes may be related to the deuterium isotope effects for the long-time decays, which are likely associated with the long-lived intrastrand CT states.11 To characterize the intra- and interstrand CT states in relation to interstrand PT, we calculated the excited state potential energy curves of the model DNA duplexes in aqueous solution along a proton displacement coordinate with the other nuclear positions fixed. We used a representative water configuration (i.e., the sixth water configuration from Figure 2) for both the nonalternating and alternating sequences and displaced the proton in the N−H···N hydrogen bond of the middle G-C pair (Figure 1c) to represent a single PT reaction occurring in a nonterminal G-C pair. The proton coordinate is represented by the scalar value α in the following equation

are relatively localized. The localization of the intrastrand CT states involving adjacent stacked base pairs is consistent with the interpretation of recent femtosecond transient absorption experiments.10 Figure 2 indicates that the intrastrand CT states of the alternating sequence (filled blue circles) tend to have lower vertical excitation energies than those of the nonalternating sequence (open blue circles). The average excitation energies of the lowest CT states of each type are indicated by horizontal lines (i.e., solid and dashed blue lines denote intrastrand CT states for alternating and nonalternating sequences, respectively). For the alternating sequence, the lowest intrastrand CT state (filled blue circles) is lower in energy than the lowest interstrand CT state (filled red circles) by more than 0.6 eV for each water configuration snapshot studied. For some of the water configurations, the interstrand CT states are so high in energy that they are not even located in the depicted energy window. In contrast, the intra- and interstrand CT states are typically similar in energy for the nonalternating sequence (open blue and red circles). From a qualitative perspective, the trends in the relative energies of the intrastrand CT states can be related to the differences in the ionization potentials (IPs) of the donors and electron affinities (EAs) of the acceptors in the gas phase when the distances between the base pairs are similar.10 These estimates are based on relatively high-level ab initio calculations on individual bases in the gas phase,20,21 where IP(donor) − EA(acceptor) is associated with electron transfer between the corresponding bases. For example, IP(donor) − EA(acceptor) is 8.78 eV for a G → C transition and 9.87 eV for a C → G transition, which is not found in the energy range of the present work. Moreover, IP(donor) − EA(acceptor) is 9.23 and 9.42 eV for a G → G and C → C transitions, respectively. Although these values are only qualitative approximations for the CT excitation energies, they are consistent with the observation that the intrastrand CT states are lower in energy for the alternating sequence (i.e., G → C transitions, filled blue circles) than those for the nonalternating sequence (G → G and C → C transitions, open blue circles). Note that this qualitative analysis is only applicable to comparisons of similar types of CT states with similar donor−acceptor distances (i.e., between intrastrand states rather than between intra- and interstrand states). As mentioned above, the long-lived excited states (i.e., >1 ps time scale) in DNA duplex systems appear to exhibit

R p = R 0p + α(RA − R D)

(1)

where RD and RA are the coordinates of the donor and acceptor nitrogen atoms, respectively, R0p is the initial position of the proton, and Rp is the position of the proton for a given value of α. At α = 0.00, the distance between the donor nitrogen and the proton is 0.999 Å, and at α = 0.30, the distance between the proton and the acceptor nitrogen is 0.994 Å, which is assumed to represent the product of the PT reaction. To obtain the potential energy curves along the proton coordinate, single point energy QM/MM calculations were performed as α was increased by increments of 0.05 from 0.00 to 0.30. Panels a and 2542

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Figure 4. Excited state potential energy curves of the model DNA duplex systems in aqueous solution along a proton displacement coordinate associated with PT for the middle G-C pair, as indicated in Figure 1c: (a) S1−S25 for the nonalternating sequence; (b) S1−S35 for the alternating sequence. The proton coordinate is defined to be α in eq 1, and all other nuclei are fixed. The water configuration was chosen to be snapshot 6 in Figure 2. The asterisks in cyan denote the bright ππ* states at α = 0.0 (defined as having an oscillator strength greater than 0.1). In (a), the interstrand CT states involving the middle G-C pair are indicated by open red circles, while the intrastrand middle G → 5′G and intrastrand 3′C → middle C CT states are indicated by open blue and green circles, respectively. In (b), the interstrand CT states involving the middle G-C pair are indicated by filled red circles, and the lowest two intrastrand CT states are indicated by filled blue and green circles, which correspond to middle G → 5′C and middle G → 3′C transitions, respectively. Note that the intrastrand CT states are lower in energy in the alternating sequence than those in the nonalternating sequence. The intrastrand CT states (blue and green circles) are less sensitive to the proton displacement than the interstrand CT states (red circles), which decrease in energy along the proton coordinate.

are indicated by filled red circles, and the lowest two intrastrand CT states are indicated by filled blue and green circles. As in the nonalternating case, the interstrand CT state involving the middle G-C pair decreases in energy as the proton is displaced from G to C (filled red circles). The intrastrand CT states (blue and green circles) are less sensitive to the displacement of the proton. These qualitative trends are also observed for a second water configuration for each system, as shown in Figure S1 of the Supporting Information. Although only the proton displacement is currently considered, Figure 4b indicates that the intrastrand CT state becomes of similar energy as the interstrand CT state along this coordinate in the alternating sequence duplex. As mentioned above, the long-lived excited states appear to exhibit intrastrand CT character10 (blue and green circles) and might undergo a nonradiative transition to the interstrand CT state (red circles) as the proton transfers along the proton coordinate depicted in Figure 4b. This type of diabatic curve crossing (i.e., avoided crossing in one dimension and conical intersection in many dimensions) and associated nonadiabatic transition may be responsible for the appearance of the slower (∼22 ps) decay observed for the alternating sequence in D2O. In particular, this pathway may be isotopically sensitive due to a barrier along the PT coordinate (i.e., zero point energy and/or tunneling effects) or isotopic differences in the vibronic coupling at the conical intersection. Note that the nonalternating sequence does not exhibit this type of diabatic curve crossing in the energy range considered (Figure 4a, where the intrastrand states remain significantly higher in energy than the middle G → middle C interstrand CT state), possibly prohibiting facile PT from an intrastrand CT state. The results depicted in Figure 4 do not provide a complete picture for understanding the experimental results but nevertheless provide useful insight. One hypothesis that is consistent with the calculations and the experimental data is that two relaxation channels are possible for the alternating sequence. In the first channel, photoexcitation leads to a long-lived CT state that does not involve PT or involves PT that is not isotopically

b of Figure 4 depict the resulting potential energy curves for the nonalternating and alternating sequences, respectively. In addition, we generated these potential energy curves for a second water configuration for each system and, as illustrated in Figure S1 of the Supporting Information, observed the same qualitative trends discussed below. Note that the TDDFT method is not expected to be as accurate far from the Franck− Condon point;22,23 therefore, these curves are only qualitatively meaningful. Moreover, this study does not account for solute and solvent dynamics, which will impact the barriers along the proton coordinate.24 The excited states from S1 to S25 were calculated for the nonalternating sequence, and the excited states from S1 to S35 were calculated for the alternating sequence to locate the interstrand CT states involving the middle G-C pair at the initial geometry. The intra- and interstrand CT states are identified at selected points along the proton displacement coordinate in Figure 4. The optically bright ππ* states, defined as having an oscillator strength greater than 0.1, are indicated by cyan asterisks at the initial geometry and are of similar energies as some of the CT states. Characterization of all 25 or 35 excited states at the Franck−Condon point is provided in Tables S2 and S3 of the Supporting Information. After photoexcitation to a bright state, the system could evolve to a CT state along the PT coordinate or other coordinates not shown in Figure 4. For the nonalternating sequence (Figure 4a), the interstrand CT states involving the middle G-C pair are indicated by red circles, while the intrastrand CT states are indicated by blue and green circles. At the proton coordinate corresponding to α = 0.0 (i.e., the initial geometry), no intrastrand CT states were located up to S25. The intrastrand CT states (open blue and green circles) appear at relatively high energies as the proton is displaced from G to C. The interstrand CT states (open red circles) are found to decrease in energy along the proton coordinate, as observed for a single G-C pair in the gas phase,7 although solvent effects could lead to a barrier.24 For the alternating sequence (Figure 4b), the interstrand CT states involving the middle G-C pair 2543

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The Journal of Physical Chemistry Letters sensitive because it is barrierless or has an extremely low barrier. In the second channel, which is isotopically sensitive, photoexcitation leads to a long-lived intrastrand CT state that enables PT and possibly a nonadiabatic transition to an interstrand CT state. The first channel is associated with the ∼5 ps decay in both H2O and D2O, while the second channel is associated with the ∼5 ps decay in H2O and the ∼22 ps decay in D2O. In H2O, the time scales associated with the two channels may be similar enough that they are not distinguishable experimentally, and the decay appears monoexponential. In contrast, in D2O, the time scales for the two channels are apparently different enough to lead to a clearly biexponential decay. For the nonalternating sequence, only the first channel is available because the intrastrand CT states are higher in energy at the initial geometry. Note that other hypotheses could be utilized to explain these data, and other coordinates may provide different relaxation pathways. Moreover, if the relaxation process involves PT, the proton is expected to transfer back to the donor upon further relaxation to the ground state on some time scale.7 In summary, we have found that the intrastrand CT states have lower excitation energies in the alternating sequence than in the nonalternating sequence for DNA duplexes comprised of three G-C DNA pairs in water. In addition, the interstrand CT state decreases in energy as the proton is displaced from G to C in these duplexes, although a barrier may appear when effects of other solute coordinates and solvent are included. In contrast, the intrastrand CT states are less sensitive to the proton displacement. For the alternating sequence duplex, photoexcitation could lead to an intrastrand CT state, which could enable PT and possibly a nonadiabatic transition from this intrastrand CT state to an interstrand CT state via a conical intersection. This pathway is expected to be isotopically sensitive and unavailable for the nonalternating sequence due to the relatively high energies of the intrastrand CT states. Thus, these calculations provide a possible explanation for the longer-time decay in D2O observed for the alternating sequence but not for the nonalternating sequence. A complete study of this relaxation process would require nonadiabatic dynamics simulations in conjunction with a more quantitatively accurate description of the excited state surfaces.

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ACKNOWLEDGMENTS

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REFERENCES

This material is based upon work supported by the National Science Foundation under CHE-10-57875. MacMolPlt25 was used for visualization of the NTOs.

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ASSOCIATED CONTENT

* Supporting Information S

Vertical excitation energies with varying numbers of water molecules in the QM region; analogue of Figure 4 for an additional water configuration; and characterization of excited electronic states at the effective Franck−Condon point coordinates of the model DNA duplexes comprised of three G-C pairs in nonalternating and alternating sequences. This material is available free of charge via the Internet at http:// pubs.acs.org.

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AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. Notes

The authors declare no competing financial interest. 2544

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M.; et al. AMBER11, University of California: San Francisco, CA, 2010. (19) Shao, Y.; Molnar, L. F.; Jung, Y.; Kussmann, J.; Ochsenfeld, C.; Brown, S. T.; Gilbert, A. T. B.; Slipchenko, L. V.; Levchenko, S. V.; O’Neill, D. P.; et al. Advances in Methods and Algorithms in a Modern Quantum Chemistry Program Package. Phys. Chem. Chem. Phys. 2006, 8, 3172−3191. (20) Roca-Sanjuan, D.; Rubio, M.; Merchan, M.; Serrano-Andres, L. Ab Initio Determination of the Ionization Potentials of DNA and RNA Nucleobases. J. Chem. Phys. 2006, 125, 084302/1−084302/7. (21) Roca-Sanjuan, D.; Merchan, M.; Serrano-Andres, L.; Rubio, M. Ab Initio Determination of the Electron Affinities of DNA and RNA Nucleobases. J. Chem. Phys. 2008, 129, 095104/1−095104/11. (22) Levine, B. G.; Ko, C.; Quenneville, J.; Martínez, T. J. Conical Intersections and Double Excitations in Time-Dependent Density Functional Theory. Mol. Phys. 2006, 104, 1039−1051. (23) Cordova, F.; Doriol, L. J.; Ipatov, A.; Casida, M. E.; Filippi, C.; Vela, A. Troubleshooting Time-Dependent Density-Functional Theory for Photochemical Applications: Oxirane. J. Chem. Phys. 2007, 127, 164111−164118. (24) Dargiewicz, M.; Biczysko, M.; Improta, R.; Barone, V. Solvent Effects on Electron-Driven Proton-Transfer Processes: AdenineThymine Base Pairs. Phys. Chem. Chem. Phys. 2012, 14, 8981−8989. (25) Bode, B. M.; Gordon, M. S. MacMolPlt: A Graphical User Interface for GAMESS. J. Mol. Graphics Modell. 1998, 16, 133−138.

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