DOI: 10.1002/cphc.201500040


Hydrated Electron Transfer to Nucleobases in Aqueous Solutions Revealed by Ab Initio Molecular Dynamics Simulations Jing Zhao,[a, b] Mei Wang,[a] Aiyun Fu,[b] Hongfang Yang,[a] and Yuxiang Bu*[a] We present an ab initio molecular dynamics (AIMD) simulation study into the transfer dynamics of an excess electron from its cavity-shaped hydrated electron state to a hydrated nucleobase (NB)-bound state. In contrast to the traditional view that electron localization at NBs (G/A/C/T), which is the first step for electron-induced DNA damage, is related only to dry or prehydrated electrons, and a fully hydrated electron no longer transfers to NBs, our AIMD simulations indicate that a fully hydrated electron can still transfer to NBs. We monitored the transfer dynamics of fully hydrated electrons towards hydrated NBs in aqueous solutions by using AIMD simulations and found that due to solution-structure fluctuation and attraction of NBs, a fully hydrated electron can transfer to a NB gradually over time. Concurrently, the hydrated electron cavity gradually reor-

ganizes, distorts, and even breaks. The transfer could be completed in about 120–200 fs in four aqueous NB solutions, depending on the electron-binding ability of hydrated NBs and the structural fluctuation of the solution. The transferring electron resides in the p*-type lowest unoccupied molecular orbital of the NB, which leads to a hydrated NB anion. Clearly, the observed transfer of hydrated electrons can be attributed to the strong electron-binding ability of hydrated NBs over the hydrated electron cavity, which is the driving force, and the transfer dynamics is structure-fluctuation controlled. This work provides new insights into the evolution dynamics of hydrated electrons and provides some helpful information for understanding the DNA-damage mechanism in solution.

1. Introduction In living organisms, ionizing radiation brings about deleterious biological effects in biomolecules, such as mutations, cancer, and cell death.[1–4] DNA damage induced by low-energy excess electrons (EEs) has attracted increasing attention mainly because EEs are created in large amounts by ionizing radiation and they are thought to play an important role in radiation-induced DNA damage.[5–7] Both experimental and theoretical studies have shown that EEs are responsible for a variety of damage types within DNA, such as strand breaks, nucleobase (NB) damage, base release, and base modification.[8–10] Thus, a firm understanding of the effect of EEs in biological matter is extremely important to fully assess radiation-induced dangers and develop highly efficient anticancer drugs and clinical protocols. Recently, by using model DNA, experimental and theoretical investigations have both shown that low-energy EEs may induce single- and double-strand breaks in DNA through disso[a] Dr. J. Zhao, Dr. M. Wang, Dr. H. Yang, Prof. Dr. Y. Bu School of Chemistry and Chemical Engineering Institute of Theoretical Chemistry, Shandong University Jinan, 250100 (P. R. China) E-mail: [email protected] [b] Dr. J. Zhao, Prof. Dr. A. Fu Shandong Collegial Key Laboratory of Biotechnology and Utilization of Biological Resources, College of Life Science Dezhou University, Dezhou 253023 (P. R. China) Supporting Information for this article is available on the WWW under

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ciative electron attachment.[3, 11–19] Furthermore, the reactivity of EEs with DNA was also conducted with dry DNA or DNA in more realistic biological environments (e.g. sparse water, salts, and proteins).[5, 17–19] For example, a theoretical study for the gas-phase system has proved that 2’-deoxycytidine-3’-monophosphate is able to capture a EE of almost 0 eV to form a stable radical anion.[12] By using condensed-phase models, ab initio molecular dynamics (AIMD) simulations reveal that an EE can localize at the hydrated NB in aqueous solution.[17] That is, a vertically injected EE initially distributes in the water region in a delocalized state, but within 15 to 25 fs the EE can rapidly localize around the NB to form a hydrated NB anion initially, then transfers to and breaks the P¢O bonds.[17] Clearly, these studies have shown that an EE can effectively attach to NBs to form anionic species whether in the gas phase or in solution. Additionally, some relevant studies suggest that the EEs that cause DNA damage are in their dry or prehydrated forms, instead of a fully hydrated form.[5, 18] In other words, radiationgenerated dry or prehydrated EEs can localize at NBs to form transient NB anions, but the fully hydrated EEs do not. In this damage mechanism, dry or prehydrated EEs attach or transfer to NBs to form radical anions. The formed transient anions may then further dissociate, couple, or release the bound EE to the DNA backbone to cause strand breaks. Of course, EEs can also react with the water molecules that surround DNA and create reactive species to produce indirect damage.[19] As is known, injection of EEs into water leads to the formation of hydrated electrons that first pass through dry and pre-


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Articles hydrated stages. The formed hydrated electrons usually possess a cavity-shaped structure that consists of four to six H2O molecules in the first hydration shell with an extremely long lifetime.[20–24] In detail, after electron injection, a rapid rearrangement of the hydrogen-bond network occurs to minimize the system. In the relaxation process, the water molecules reorient and a fully hydrated electron can be formed in approximately 1.6 ps.[25] In fact, in such EE hydration processes, various EE states occur that could be roughly classified as dry, prehydrated, and fully hydrated electrons. In structure, the former two are delocalized, whereas the latter is localized, a cavityshaped structure. Plentiful investigations indicate that such metastable transient EE adducts (hydrated NB anions) are closely associated with many important processes, such as DNA and protein damage.[18, 26] However, compared with dry DNA or gaseous DNA, aqueous DNA has considerable larger electron affinity (EA), as shown in the microsolvation experiments.[17, 27, 28] This implies that hydration of DNA or NBs could improve their electron-capturing ability and thus provide favorable conditions for possible transfers of hydrated electrons towards NBs. In fact, as shown by experimental investigations, fully hydrated electrons can also transfer to NBs and their derivatives and even other organic molecules with different EAs in aqueous solutions.[29] However, no studies have been reported regarding the transfer dynamics of hydrated electrons so far. Inspired by this recent progress, herein we explore the behavior of a fully hydrated electron in aqueous NB solutions. The main objective herein is to learn if a fully hydrated electron can also transfer to a NB in solution to form a hydrated NB anion, which is a precursor state for DNA damage, a new mechanism for which the transfer dynamics have not been reported in previous works. We chose an aqueous NB (G, C, A, or T) system that contains a fully hydrated electron and a hydrated NB, denoted by (e¢)aq···NB, as a simple solution model to clarify some fundamental issues about the structural properties and transfer dynamics of fully hydrated electrons towards hydrated NBs in solutions by using AIMD simulations. Most importantly, we reveal that a fully hydrated electron can still transfer to a hydrated NB in solution and the transfer dynamics are controlled by the solution-structure fluctuation and the electron-binding ability of the NB as the driving force.

Computational Methods To prepare aqueous NB solutions with a cavity-shaped solvated electron (labeled as (e¢)aq···G, (e¢)aq···C, (e¢)aq···A, and (e¢)aq···T), we constructed a periodically repeated cubic cell (14.88 Õ 14.88 Õ 14.88 æ) that consisted of a NB, 100 water molecules, and an auxiliary Cl¢ , which corresponds to a solution density of 1.00 g cm¢1. First, a classical MD simulation was performed for 5 ns for the periodic system to make sure the system reached equilibrium. The time step was set to 1.0 fs to ensure good control of the conserved quantities. The COMPASS force field and the method of Nos¦ and Anderson were employed in the simulation process to make sure that the system could mimic an aqueous NB solution. Simulations were carried out within the canonical NVT ensemble and the temperature was kept at around 300 K by using a Nos¦– ChemPhysChem 2015, 16, 2348 – 2356

Hoover chain of thermostats.[30] All classical molecular dynamics (MD) simulations were conducted by using the Discover package from Accelrys. Subsequently, the auxiliary anion (Cl¢) was removed and replaced by an EE, and the system was further optimized at the first-principles level. The optimized configurations were taken for subsequent AIMD simulations. The electronic structures and evolution dynamics were described by nonlocal density functional theory (DFT) calculations by using the Becke and Lee–Yang–Parr (BLYP)[31, 32] functional, in which the exchange functional and correlation functionals were given by Becke and Lee, Yang, and Parr, respectively. A double numerical plus p-functions (DNP) atomic orbital basis set was employed to provide accurate results. AIMD simulations were carried out also within the canonical (NVT) ensemble, and the system temperature was kept at 300 K by controlling the Nos¦–Hoover chain of thermostats. Self-consistent field calculations were done with a convergence criterion of 10¢6 Hartree on the total energy, and the cutoff of the atomic basis set was 3.3 æ. The accuracy of integration points used to integrate the wavefunction in reciprocal space (k-point) was set to medium and gamma points were used to integrate the wavefunction in reciprocal space. The AIMD simulation time was 1 ps, which has proved to be sufficient for acquiring reasonable information. All procedures were completed with the DMol3 package implemented in the Cerius2 4.6 suite[33, 34] available from Accelrys. Considering that the structure of the hydrated electron cavity could influence subsequent evolution dynamics, we adopted the same procedure to prepare a hydrated electron cavity to reduce the effect of the cavity structures. Additionally, to further confirm that an EE can transfer from a cavity-shaped hydrated electron state to a valence anion state, AIMD simulations on the considered system ((e¢)aq···G) with different starting configurations were also conducted and similar results were obtained, which confirmed our conclusions (Figures S8–13 and Table S1 in the Supporting Information). In addition, to establish a benchmark for comparison and to prove that the disappearance of the hydrated electron cavity is really a consequence of electron attachment to NB, we also simulated the dynamics of cavity-shaped hydrated electrons in water ((e¢)aq···H2O) by using the same computational approach. The effect of the diffuse functional was also examined, and indicated that the diffuse functional basically does not affect the transfer mechanism or dynamics character of hydrated electrons towards NBs in solution (Figure S13).

2. Results and Discussion Herein, we constructed a system that contained a cavityshaped hydrated electron, (e¢)aq, and a NB in aqueous solution to inspect the dynamic behavior of the hydrated electron cavity. In particular, we wondered if the cavity-shaped hydrated electron can transfer to other places, for example, by residing at the NB or forming a new hydrated cavity due to solutionstructure fluctuation. To clarify the nature of the states of a cavity-shaped hydrated electron in aqueous NB solutions, the evolution dynamics of the well-hydrated electron in the periodically repeated (e¢)aq···NB systems were explored by using AIMD simulation techniques. The initial cavity sizes of the four systems are very close to each other. In detail, the volumes enclosed by spin-density surfaces of the initial hydration cavities are about 75 æ3 for all cases. Additionally, the separations between the center of the hydration cavity and the center of mass of NBs are about 11 æ in the four model systems


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Articles 2.1. Structural Character and Evolution Dynamics of Hydrated Electrons To date, most efforts have been devoted to hydrated electrons. In particular, Kevan inferred that an electron is captured in a cavity space bounded by six water molecules with an octahedral configuration, in which one ¢ Figure 1. A representative structure of the (e )aq···NB model with geometrical parameters. a) The singly occupied O¢H group of each water molemolecular orbital (SOMO) contours for (e¢)aq···G at 0 fs. The surface is plotted at isovalue = 0.03. b) The distance between the (e¢)aq cavity center and the center of mass of G for (e¢)aq···G. c) The structure of the hydrated electron cule is oriented toward the eleccavity with the distances between each H atom and the center of mass of the cavity marked. The six caging H2O tron cloud center,[20] although molecules are represented as ball-and-stick models. Dark gray, white, and light gray balls denote the O, H, and the number of water molecules dummy (cavity center) atoms, respectively. The center of mass of the hydration cavity was determined by using that form the hydration cavity the Cerius2 4.6 suite of programs. may be as low as four. Now we focus on the states and evolu(Figure 1 and Figure S1). The systems are stabilized by intermotion dynamics of a fully hydrated electron in aqueous NB solulecular hydrogen bonds between water molecules and solvattions. ed NBs. The initial configurations were optimized at the first-princiBefore the dynamics analyses of (e¢)aq···NB (NB = G, C, A, or ples level, as shown in Figure 1 and Figure S1. Typically, an EE T), we studied the structures and electronic properties of negainitially completely locates in a void surrounded by more water tively charged NBs. Because of their unique p-electronic strucmolecules (first hydration shell) as a cavity-shaped hydrated EE. tures, the NBs are not only good hole carriers but also excelIt is worth noting that the water-cavity geometry and electron lent electronic conducting units. Solvation can further improve distribution resemble a typical Kevan-like cavity structure the electron-binding ability of the NBs, as confirmed by experi(Figure 1 and Figure S1). Six H2O molecules point their O¢H hyment and theoretical calculations.[17, 27, 28, 35] For example, drogen ends toward the EE cloud to form a sexamer cavity. Schiedt et al.[35] measured the electron affinity (EA) of uracil·(The structures and geometrical parameters of the six cavityH2O)n, thymine·(H2O)n, and cytosine·(H2O)n (n = 0–5), and indiforming water molecules (labeled as W1, W2, W3, W4, W5, W6) cated that as the number of water molecules increases, the EA are illustrated in Figure 1 and Figure S1, respectively. For simincreases linearly. Smyth and co-workers[17] extracted the plicity, we only analyzed the initial configuration of (e¢)aq···G as NB·(H2O)n (n = 0–15) clusters from periodic microsolvated NBs an example. The key geometrical parameters, the distances beto compute the EA of the hydration clusters, and found that tween a hydrogen atom of the cavity-forming H2O molecules the EAs of NBs increase as the number of water molecules inand the center of the cavity (re¢···HO) and those between the O creases. Although relevant results suggest the EAs of NBs and and the center of the cavity (re¢···OH), are given in Figure 1 and even microhydrated ones are relatively small, their low-lying Table 1. As shown by the singly occupied molecular orbital lowest unoccupied molecular orbitals (LUMOs) endow them (SOMO, Figure 1a), in the initial configuration an EE is well lowith electron-binding ability. The LUMOs for these NBs are p*calized inside a water cavity that consists of six water moletype orbitals over the entire NB, and they are clearly the prefcules. The localized EE has somewhat of a s-type distribution, erential sites for EEs to reside. More importantly, these NBs can which is similar to the widely accepted Kevan structure. In this be further hydrated with different amounts of water molecules case, the hydration cavity acts as a potential electron trap that through hydrogen bonds, which considerably enhances their is deep enough to attract and capture an EE, and the captured electron-capturing ability with different magnitudes. So, we electron is stabilized predominantly by e¢···HO interactions speculate that the hydrated NBs possess considerable electronwith six water molecules, and also electrostatically by the binding ability and thus can effectively attract dry, prehydrated outer hydration shells. and even fully hydrated electrons to reside. In short, a NB in For the hydration cavity, the distances between the center aqueous solution can act as an electron trap that attracts EEs of the cavity and the six hydrogen atoms (e¢···HO) are 2.098, to reside and its attraction to EEs is the original driving force 2.163, 2.612, 2.214, 2.065, and 2.367 æ, which is in reasonable for electron transfer towards it. Certainly, different NBs could agreement with the literature values (2.3 æ).[36] The e¢···OH sepresult in different transfer dynamics of EEs in their aqueous solarations are 3.088, 3.125, 3.501, 3.202, 3.349, and 3.008 æ, and utions. also agree well with the previously reported one (3.5 æ).[36] Additionally, the radius of the hydration cavity is about 3 æ, which is in satisfactory agreement with the literature value ( … 2.5 æ).[36–38] These findings agree with the generally accepted features of hydrated electron cavities reported previously.[39] Clearly, the initial configuration we chose corresponds to ChemPhysChem 2015, 16, 2348 – 2356


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Articles Table 1. The separations between H or O atoms of water molecules in the first hydration shell and the center of hydration cavity (re¢···HO, re¢···OH) in (e¢)aq···G, (e¢)aq···C, (e¢)aq···A, and (e¢)aq···T.





Water molecule

r1e¢···HO [æ]

r2e¢···HO [æ]

r3e¢···OH [æ]

W1 W2 W3 W4 W5 W6 W1 W2 W3 W4 W5 W6 W1 W2 W3 W4 W5 W6 W1 W2 W3 W4 W5 W6

2.098 2.163 2.612 2.214 2.367 2.065 2.202 2.164 2.820 2.081 2.541 2.391 2.307 2.259 2.727 2.019 2.451 2.157 2.261 2.177 2.772 2.134 2.397 2.358

3.434 3.655 3.639 3.537 3.615 3.420 3.453 3.670 3.585 3.359 3.961 3.774 3.518 3.715 3.510 3.311 3.869 3.510 3.426 3.668 3.623 3.450 3.834 3.715

3.088 3.125 3.501 3.202 3.349 3.008 3.184 3.119 3.605 3.070 3.525 3.325 3.285 3.231 3.533 3.006 3.439 3.121 3.226 3.144 3.592 3.124 3.382 3.310

Figure 3. Time evolution of the Mulliken charges on the initial six caging H2O molecules for (e¢)aq···H2O.

a well-defined cavity-shaped hydrated electron structure. Similar situations can be observed for the initial configurations of (e¢)aq···C, (e¢)aq···A, and (e¢)aq···T (Figure S1 and Table 1). Overall, an EE is distributed around the dangling hydrogen atoms of six water molecules in the first hydration shell and the e¢···HO interactions are responsible for primary electron stabilization in the hydrated electrons. In short, the above analyses have indicated that the initially prepared hydration cavity really denotes the fully hydrated electrons. Additionally, to characterize the structural change in the hydrated electron cavity over time, we monitored the variation in solvation modes with time. Figure 2 depicts the time evolution of the EE population over the initial six cavity-forming H2O

Figure 2. Spin densities on the initial six caging H2O molecules versus the evolution time for (e¢)aq···H2O, (e¢)aq···G, (e¢)aq···C, (e¢)aq···A, and (e¢)aq···T.

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molecules for the (e¢)aq···H2O, (e¢)aq···G, (e¢)aq···C, (e¢)aq···A, and (e¢)aq···T systems. The charges of the initial six caging H2O were calculated for the (e¢)aq···H2O system and its time course is displayed in Figure 3. As shown in Figures 2 and 3, the spin densities and Mulliken charges of the initial six caging H2O essentially remain constant (about 0.85 and ¢0.60) from 0 to 180 fs, which indicates that the EE can stably localize in the hexamer cavity and maintain that position for a period of time. The spin-density distributions of the snapshot configurations further reveal that in 180 fs the EE is still in the hydration cavity and exhibits as a traditional cavity-shaped hydrated electron (Figure 3). Although solution-structure fluctuation and molecular motion can affect the solvent cavity, the cavity does not break and still holds the EE over time. However, for (e¢)aq···G, (e¢)aq···C, (e¢)aq···A, and (e¢)aq···T, in the first 50 to 100 fs the electron distribution on the initial six caging H2O decreases rapidly, and in this short time period the hydrated electron affects the intermolecular interactions of solvent molecules, which leads to structural reorganization and electron redistribution. Overall, spin densities on the initial six caging H2O molecules show an obvious lowering trend over time. At the same time, as shown in Figure 2, in the initial stage, the total spin densities on the initial six caging H2O are about 0.86, 0.84, 0.84, and 0.85 for (e¢)aq···G, (e¢)aq···C, (e¢)aq···A, and (e¢)aq···T, respectively, which indicates that the hydrated EE is mainly captured by six water molecules at first, as mentioned above. However, at 180 fs, the total spin densities on the initial six caging H2O become approximately 0.1 to 0.2 and at about 300 fs they basically become 0 for all the (e¢)aq···G, (e¢)aq···C, (e¢)aq···A, and (e¢)aq···T systems (Figure 2). In addition, it should be noted that because the surroundings of the water molecules differ slightly from each other for the four solutions, spin densities on the six water molecules are somewhat different from each other. Spin densities summarized into the six water molecules are plotted in Figure 4 as a function of time. Taking (e¢)aq···G as an example, Figure 4 shows that the changes in electron-spin densities distributed on the six H2O molecules can be divided into two groups. The spin densities on W1, W2, W3, and W4 continuously decrease and finally


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Articles Overall, the spin densities on NBs increase significantly, whereas those on the initial six cavityshell H2O molecules show an obvious downward trend. When the cavity-shaped hydrated electrons transfer to the hydrated NBs, the cavity structures gradually disappear along their respective (e¢)aq···G, (e¢)aq···C, (e¢)aq···A, and (e¢)aq···T trajectories, and ultimately the EEs reside in the NB p*-type orbitals. In addition, by monitoring the trajectories (Figures S2–5), we noted that after a short time the hexamer cavity decomposes and degrades to a pentamer, tetramer, and oligomer ( … 2–3 mer) cavity for hydrated electrons, and finally the hydration cavities fade and the EEs transfer out of the cavity Figure 4. Time evolutions of the spin density of six H2O molecules in the first hydration shell at the initial stage region. for (e¢)aq···G, (e¢)aq···C, (e¢)aq···A, and (e¢)aq···T. These curves indicate different contributions and variations of each In a word, for (e¢)aq···G, caging H2O in binding EE in each NB solution. ¢ (e )aq···C, and (e¢)aq···A, the EE is initially distributed spherically on reach small values (< 0.01), whereas those on W5 and W6 inthe hydrogen atoms of six cavity-forming water molecules, crease initially, but decrease subsequently and become stable and the hydrated electron cavities finally disappear in a short along the evolution time. At time zero, the total spin densities time (< 180 fs). on the water molecules (W1, W2, W3, W4, W5, W6) were calculated to be about 0.183, 0.114, 0.083, 0.162, 0.174, and 0.147, 2.2. Evolution Dynamics of Excess Electrons on Hydrated respectively (Figure 4). At 100 fs, the EE is concentrated on Nucleobases two water molecules (W5 and W6). At this time, the spin densities on W1, W2, W3, W4, W5, and W6 are 0.047, 0.003, 0.006, The disappearance of the original hydrated electron cavity im0.046, 0.152, and 0.270, respectively. After 150 fs, the spin denplies a transfer of the hydrated EE. To clarify if the original hysities on the six caging H2Os are small (Figure 4) and the total drated electron moves to a new place to form a new hydrated amount on the six caging H2O molecules is less than 0.2 electron cavity or to NB to form a hydrated valence anion, (Figure 2), which means that only a very small portion of the Figure 5 presents the spin-density surfaces for some representative structures. Additionally, variations in spin densities on EE is on these six H2O molecules. The changes in spin density should be related to the rearrangement of the hydrated elecNBs with respect to the evolution time are displayed in Figure 6. For (e¢)aq···G, the EE localizes mainly in the hydrated tron cavity. Similar phenomena can be observed in (e¢)aq···C, ¢ ¢ electron cavity in the beginning (Figure 1a). Figure 5 shows (e )aq···A, and (e )aq···T. From the changes in spin density on the six H2O molecules, we can predict that the original hydrated that the EE starts to flow to the G in about 16 fs. At this time, electron cavities basically disappear at about 180 fs in the four spin-density analysis reveals that the unpaired electron resides NB solutions. Clearly, these observations in four NB solutions mainly on the water cavity (90 %) and partly on G (10 %), are distinctly different from that in water for which the hydratwhich implies that a part of the EE transfers from the water cavity to G (Figure 6). The hydrated electron cavity actually ed electron cavity is maintained, which indicates an important role of NBs in affecting the structure and stability of hydrated acts as the electron donor, whereas G acts the electron acceptelectron cavities. In addition, different evolution dynamics of or. After a short relaxation, further EE transfer takes place. As the hydrated EEs in water and four NB solutions also prove the simulation progresses, at 140 fs the distributions of the EE that the disappearance of the hydrated EE cavity is really a conon the initial six caging H2O molecules and G are 32 and 28 %, sequence of EE attachment to NBs. respectively (Figures 2 and 6). With molecular rearrangement, Figure 5 shows some representative snapshots of spin-densiafter 178 fs the EE is mainly distributed over the G (> 50 %) to ty contours for the four NB solutions and thus the behavior of form a G valence anion. It is worth noting that the hydration the initial six cavity-shell H2O molecules visually and intuitively. cavity disappears and the transferred EE no longer returns to It can be found that electron migration phenomena may take the original place, recovering its cavity-shaped hydrated strucplace between the cavity-making H2O molecules and NBs. ture. Similar evolution characters are observed for (e¢)aq···C, ChemPhysChem 2015, 16, 2348 – 2356


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Figure 5. Some representative snapshots of spin-density contours (isovalue = 0.003) in the time evolution for the four NB solutions ((e¢)aq···G, (e¢)aq···C, (e¢)aq···A, and (e¢)aq···T), which show the transfer processes of a hydrated electron from its cavity-shaped hydrated state to a NB-bound state. In the first row, the spin density localized on the NB is 0.1; in the second row, the electrons on the NB are equal to those of the initial six caging H2O; and in the third row, the EE mainly resides on the NB and only a little on the caging H2O molecules.

Figure 6. Time evolution of spin density on NBs for (e¢)aq···G, (e¢)aq···C, (e¢)aq···A, and (e¢)aq···T.

(e¢)aq···A, and (e¢)aq···T. That is, similar to (e¢)aq···G, for (e¢)aq···C, (e¢)aq···A, and (e¢)aq···T, an EE is completely localized in the hyChemPhysChem 2015, 16, 2348 – 2356

dration cavity at the beginning. Subsequently, the EE starts to transfer from the H2O cavity to C, A, and T at 30, 28, and 12 fs, respectively. In the successive time evolution, the amounts of the EE distributed on the initial six caging H2O molecules and NBs are nearly equal (38 versus 42 % for (e¢)aq···C at 63 fs; 34 versus 30 % for (e¢)aq···A at 120 fs; 40 versus 40 % for (e¢)aq···T at 120 fs). With the continuing structural rearrangement of the system, finally the EE is mainly localized on the p* antibonding orbitals of these three NBs. In addition, it should be noted that the four NBs have different EAs and thus the hydrated EEs should have different transfer dynamics in four NB solutions. However, surprisingly, the EA differences do not noticeably affect the transfer dynamics of the hydrated EEs in such solutions. That is, the observed dependences of evolution dynamics on the EAs of NBs are slightly different from the intuitive expectation, and the transfer of the hydrated EEs towards four NBs exhibits analogous dynamics. Clearly, this observation should be attributed to three fac-


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Articles tors: the EAs of NBs as the driving force of EE transfer, the inhibiting role of the hydration cavity, and the promoting role of solution-structure fluctuation. The EE transfer dynamics depends not only on the attraction of NBs but also on hydration stabilization of the EE and structural fluctuation of solution. Because the well-localized cavity-shaped hydrated EE has considerably high stability and the NBs have relatively weak electronbinding ability, the stabilization by the hydration cavity plays a dominant role in affecting the hydrated EE transfer, especially at the initial stage in the time evolution. In other words, the structural-fluctuation-induced breakage of the hydrated EE cavity is the rate-determining step in the EE transfer process for all solution cases. Upon breakage of the cavity, the EE rapidly transfers to the NBs. Thus, the hydrated EE transfers towards NBs exhibit similar dynamics in solutions. Overall, the transfer process of the EE in the four systems can be divided into three stages. In the first stage, an EE is completely bound in a hydration cavity. In the second stage, with structure fluctuation of the solution system, the EE redistributes and a part of it resides in both the water cavities and NBs, which exhibits a trend to transfer from the hydration cavity. In the third stage, the EE largely localizes on NB and only a little is on the original caging water molecules. From this we can conclude that the hydrated electrons can convert to the NB (G/C/A/T) valence anion states after a period of relaxation due to structure fluctuation. It is clear that, in the beginning, the LUMO of the six water cavity dominantly contributes to the (e¢)aq···NB LUMO. That is, an EE is initially trapped in a H2O molecule cavity. After a short time, the LUMOs of these water cavity and NB contribute to the (e¢)aq···NB LUMO, and thus an EE distributes on both the NB and the water region that consists of some H2O molecules. As the evolution process proceeds, the continuous (e¢)aq···NB solution structure fluctuation leads to structural reorganization of the water cavity and NB, and eventually an EE occupies the solution LUMO that originates from the LUMO (p*) of the NB. Another notable observation is that after the EE is mainly localized on the NB, the EE never returns to the original water zone and also never goes to another place to form a new hydration cavity during the entire simulation. That is to say, the presence of NBs accelerates the rearrangement of the solution structure, especially the hydrated electron cavity, which further causes the EE transfer to NB to form the NB anion at last. In the evolution process of an EE from the hydrated state to anion state, the e¢···HO interaction plays an inhibiting role and the NB attraction is the main driving force that promotes the EE transfer from its cavity-shaped hydrated cavity to the NB. Additionally, we also calculated the volumes surrounded by the spin-density isovalue (0.003) surfaces of an EE in these (e¢)aq···G, (e¢)aq···C, (e¢)aq···A, and (e¢)aq···T systems (Figure 7). Because at the beginning the EE entirely localizes on the caging water molecules, the spin density surface encapsulated volume is 75 æ3. In the (e¢)aq···G case, the volume decreases from 75 æ3 at 0 fs to approximately 40 æ3 at about 160 fs, and remains roughly constant afterward. For (e¢)aq···C, the spin density surface encapsulated volume is almost invariant (about 35 æ3) after 90 fs. For both (e¢)aq···A and (e¢)aq···T, the volumes stay esChemPhysChem 2015, 16, 2348 – 2356

Figure 7. Time evolution of the volume surrounded by the spin density isovalue (0.003) surface of the bound EE for (e¢)aq···G, (e¢)aq···C, (e¢)aq···A, and (e¢)aq···T. The corresponding spin density contours are also displayed as insets for three snapshots that are taken from (e¢)aq···G at 0, 160, and 300 fs.

sentially constant ( … 40 and 30 æ3, respectively) when the evolution time reaches 130 and 155 fs, respectively. After the cavities disappear, the spin density surface encapsulated volumes stay almost unchanged for all four cases. To obtain further insights into electron hydration character in the four aqueous NB solutions, we monitor the time evolution of the Mulliken charges on the NBs. The Mulliken charges of NBs along the (e¢)aq···NB AIMD trajectories are presented in Figure 8. In general, at first the charges of the NBs are about 0 and rise with increasing evolution time. After a certain time, the charges localized on the NBs are almost unchanged. In addition, the fluctuation curves in Figure 8 reflect the electron exchange between the NBs and water region. Along the course of the AIMD simulation, due to solution-structure fluctuation, the EE tends to move to the NB or the original hydration cavity zone, which features as a low potential well, instead of to other water zones for stabilization. For simplicity, we only analyze (e¢)aq···G as an example. According to Figure 8, at time zero, the charge on G is 0, which indicates that an EE is not localized on the G at the beginning. After a short time, a small fraction of charge is distributed on G, which reflects that electron transfer occurs from the hydrated cavity to G. At about 175 fs, the charge distribution indicates that the EE is located mostly on the G (60 %). Similar trends appear for (e¢)aq···C, (e¢)aq···A, and (e¢)aq···T. These observations indicate that initially the EEs distribute mostly on the water molecules in the cavity zone rather than the NBs (G, A, C, or T), and finally they are located mostly on the NB ( … 60 % for G, … 80 % for C, A, and T), which is in good agreement with spin-density distributions of (e¢)aq···NB discussed above. Figure 9 displays a schematic profile for the EE transfer process from the hydration cavity to a NB in solution. We only take the (e¢)aq···G system as an example in this picture to illustrate the mechanism, which is also applicable for other three NB solutions. Initially, the well-formed hydration cavity as a deep trap can bind an EE in a very short time. The antibonding orbital energy of NB is lower than the energy of the O¢H s*-type orbitals over the water molecules. As the evolution


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Figure 9. Schematic profile for the electron-transfer process from the hydration cavity to NB (here G, as an example). Top: The EE is stabilized in a deep trap as a cavity-shaped hydrated EE. Middle: As the simulation progresses, transfer of the EE takes place partly from the hydration cavity to NB, and the electron distributes both in the cavity and on the NB. Bottom: Shallowing of the hydration cavity trap and increase in the EA of the NB further promotes the transfer of the hydrated EE from the water cavity region to the hydrated NB. After a certain time, the EE mainly localizes on the NB, which leads to the formation of a transient anion. The EE cloud is illustrated in gray.

Figure 8. Top: Time evolution of the Mulliken charge on NBs in (e¢)aq···G, (e¢)aq···C, (e¢)aq···A, and (e¢)aq···T. Bottom: The evolution behavior in the initial stage (up to 300 fs) for magnification.

proceeds, it is easy for an EE to transfer from the water cavity to the G p* orbital because the energies of the EE in these two states could be close to each other and can be further modified by the structure fluctuation of hydrated G and rearrangement of the water cavity. In addition, due to the modification of the adiabatic EAs of NBs by surrounding water molecules, the EE in a shallow trap would rapidly transfer to the hydrated NBs. As a result, the EE resides on the NB and forms a new localized state (the NB valence anion). In short, as the simulation proceeds, the initial sexamer hydration cavity gradually decomposes and the EE transfers cooperatively from the water cavity zone to the NB (G, C, A, or T). Finally, the EE almost entirely localizes on the NB and occupies the p*-type LUMO over the whole NB ring to form a localized state (valence anion). Finally, the localized EE on the NB no longer returns to the original water cavity zone to recover its hydration cavity, and also never transfers to other places to form a new hydration cavity through solution reorganization.

3. Conclusions Herein, the structure and electronic properties of cavityshaped hydrated electrons in aqueous NB solutions were explored by using AIMD simulations to reveal the states and evolution dynamics of hydrated electrons. As the main aspect of this work, the AIMD simulations demonstrate that a fully hydrated EE can also transfer to NBs in solution. Over time, the ChemPhysChem 2015, 16, 2348 – 2356

hydrogen-bond network gradually reorganizes, the potentials of the hydrated electron cavity and hydrated NB incessantly modulate, and the EE tends to stay at the side that has a lower potential. Due to solution-structure fluctuation, the hydrated electron cavity gradually splits and the hydrated electron transfers to the hydrated NB; ultimately, the hydrated electron occupies the p*-antibonding orbital of the NB. That is to say, solution-structure fluctuation can cause hydrated electron transfer from the water cavity zone to the NB to form a hydrated NB anion. Notably, once the hydrated electron cavity breaks, a new hydration cavity never forms either in the original hydration zone or in other zones. These phenomena could be attributed to the special structures, the electronic properties of the NBs, and the nature of the (e¢)aq cavity. The present study supports the hypothesis that low-energy electrons, which are responsible for the DNA damage, include dry and prehydrated and even fully hydrated ones. Clearly, this work provides an extended study of the solvation of nucleotides and also an understanding of the interaction of the radiation-generated EEs with biological molecules in solution.

Acknowledgements This work was supported by the Natural Science Foundation of China (NSFC) (20633060, 20973101, 21373123, 21171031), the


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Articles Natural Science Foundation of Shandong province (ZR2013M027), and the Youth Scientist (Doctoral) Foundation of Shandong Province of China (BS2014SW006). A portion of the calculations were carried out at the National Supercomputer Center in Jinan, the Shanghai Supercomputer Center, and the High-Performance Computer Center at Shandong University.

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Keywords: ab initio calculations · electron transfer · hydrated electrons · nucleobases · valence anions


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Received: January 15, 2015 Published online on May 28, 2015


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Hydrated Electron Transfer to Nucleobases in Aqueous Solutions Revealed by Ab Initio Molecular Dynamics Simulations.

We present an ab initio molecular dynamics (AIMD) simulation study into the transfer dynamics of an excess electron from its cavity-shaped hydrated el...
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