Multi-copper incorporation into ring-expanded base pairs: An ab initio study

Chemical Physics Letters 734 (2019) 136704

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Chemical Physics Letters journal homepage: www.elsevier.com/locate/cplett

Research paper

Multi-copper incorporation into ring-expanded base pairs: An ab initio study a,⁎

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Mei Wang , Jing Zhao , Jing Li , Runxiu Chen , Kai Chen , Shuang Hu , Lijun Wang , Huihe Gaoa, Hui Xua a

School of Physics and Physical Engineering, Shandong Provincial Key Laboratory of Laser Polarization and Information Technology, Qufu Normal University, 273165 Qufu, China Shandong Collegial Key Laboratory of Biotechnology and Utilization of Biological Resources, College of Life Science, Dezhou University, Dezhou 253023, China

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H I GH L IG H T S

four multi-Cu-mediated ring-expanded base pairs designed have good stability. • The rC and rA rT exhibit AFM magnetic exchange interaction. • Trans-rG • These base pairs designed have enhanced transverse electronic communication. 3Cu

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A R T I C LE I N FO

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Keywords: Metal-modified base pair Ring-expanded base pair Transverse electronic communication Diradical character

In this work, we design four multi-copper-mediated ring-expanded base pairs, which possess improved electromagnetic properties due to the introduction of cyclopentadienyl radicals and copper ions. These designed base pairs have smaller HOMO-LUMO gaps and lower ionization potentials than those of the corresponding natural base pairs. Trans-rG3CurC and rA2CurT possess open-shell singlet ground states. They exhibit variable degrees of magnetic exchange interaction. In addition, their transverse electronic communication by the chargetransfer transitions in the UV absorption spectra is enhanced significantly.

1. Introduction In order to explore molecular materials with novel properties, the research of DNA molecules has become a hot topic in recent years [1–5]. The most important characteristics of DNA molecules are its interbase stacking and nano-scale, which is helpful to construct a variety of electronic devices through self-assembly. At present, although the conductivity of DNA is controversial, the study of the electrical conductivity of DNA molecules still continues. Therefore, in order to improve the performance of the device, a lot of work has been done on the modification of nucleobases and base pairs both theoretically and experimentally [6–12]. At present, there are two main methods to modify DNA base, that is, ring-expanded modification [13–18] and adding nanoparticles [19–23] to change their structure. For ring-expanded modification, benzene, naphthalene, pyridine, or pyrrole are inserted into DNA bases to form new base analogues in theory. Some DNA base analogues have also been synthesized in the experiment. For example, Kool’s group has synthesized a series of new ring-expanded nucleobases, such as x-bases [24], y-bases [25] and yy-bases [26]. These novel bases synthesized

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have more unique electronic properties than the natural bases, such as the smaller HOMO−LUMO gap and the stronger stacking interaction. For another modification, some transition metals (Co2+, Fe2+, Cu2+ and Zn2+) have been successfully used in DNA functionalization [27–31]. The results show that DNA can be functionalized through participation of metals and transformed into semiconductors or conductors. Therefore, the modification of doping appropriate metals has been widely carried out in order to design high performance DNA devices. It is well known that the high-spin multiradical molecules have been widely studied because of their novel electromagnetic properties [32–34]. Among them, diradical molecules play an important role in the synthesis of magnetic materials [35–39]. Usually, their inter- and intra-molecular interactions affect the magnetic properties of materials. Now, a lot of couplers connecting two radical centers have been investigated both theoretically and experimentally, and they exhibit different magnetic coupling interactions. Due to the structural characteristics of DNA molecules, the DNA molecules seem to be suitable for the preparation or construction of single-molecule electromagnetic devices with unique properties, such as high-density information storage and

Corresponding author. E-mail address: [email protected] (M. Wang).

https://doi.org/10.1016/j.cplett.2019.136704 Received 18 July 2019; Received in revised form 20 August 2019; Accepted 21 August 2019 Available online 22 August 2019 0009-2614/ © 2019 Elsevier B.V. All rights reserved.

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spin filter effect. DNA molecules have a much higher probability of ionization to become radicals through high linear energy transfer radiation. It can be expected that the diradicals can be formed in DNA base pairs after the radical–radical reactions by ionizing radiation. Peoples et al. [40] reported that the DNA molecule can be doubly oxidized in radiation, but it causes the formation of diamagnetic (nonradical) molecular damage. In the theory, Pottiboyina et al. [41] have declared that the two radicals bases are formed by removing an NeH hydrogen atom, but the two radicals eventually form the hydrazine-like (NeN) bonds eventually, which makes their diradical properties disappear. Therefore, we hope to find other base pairs structures with diradical properties. At present, we have explored the magnetic properties of doubleelectron oxidized natural base pairs and ring base pairs with diradical characteristic, and obtained some meaningful conclusions [42–44]. Some designed base pairs have large magnetic exchange coupling constants (J). On the basis of these studies discussed above, we herein design four multi-copper-mediated ring-expanded base pairs. At first, the cyclopentadiene radical is inserted to DNA bases to form six ringexpanded base analogues. According to the insertion direction of the cyclopentadiene radical, the base analogues are divided into two groups, which are designated r-bases and trans-r-bases respectively (See Fig. 1). These designed radical bases can match the corresponding radical bases to form stable base pairs analogues. Second, similar to the previous work, the copper iron is chosen to replace hydrogen atoms, and bonds with the N or O atom in the Watson–Crick zone. Ultimately, we hope that the insertion of the radicals and copper ions will give these novel base pairs unusual electromagnetic properties. The investigations show that the four modified base pairs are planar. What's more, two of these bases pairs have diradical characteristic. In addition, they have smaller HOMO-LUMO gaps and lower ionization potentials, which can enhance the transverse electronic communication between the two bases. These mean that they have higher efficiency of charge transfer along Cum-DNA. We hope these results can provide valuable theoretical basis for understanding the electromagnetic properties and conduction ability of Cum-DNA double strand constructed by the designed base pair.

2. Computational details All quantum chemical calculations were carried out in the gas phase using the Gaussian 03 program [45]. The hybrid three parameter B3LYP method was used to optimize the geometric structure of these designed four base pairs at the 6-31+G*(H,C,N,O)/LANDL2DZ(Cu) basis set level. This basis set was utilized to perform the harmonic vibrational analysis for confirming that these structures have real minima on potential surface. For each structure, their closed-shell singlet (CS), openshell broken symmetry singlet (OS), and open-shell triplet (T) states are computed. The relevant electronic property, such as spin densities, ionization potentials (IPs) [46], the gap (H-L gap) between the highest occupied molecular orbital (HOMO), were calculated at the B3LYP/6311++G**(H,C,N,O)/LANDL2DZ(Cu) level with the B3LYP/631+G*(H,C,N,O)/LANDL2DZ(Cu) geometries. For confirming the diradical character, the LUMO occupation number were calculated at the CASSCF(10,10)/6-31G*(H,C,N,O)/ LANDL2DZ(Cu) level. The magnetic interactions for these diradicals were determined by evaluating the Heisenberg coupling constant, J. The positive and negative values of the exchange coupling constant (J) reflect anti-ferromagnetic (AFM) and ferromagnetic (FM) interactions between the two unpaired electrons. In the work, the J value was calculated using a broken symmetry approach proposed within an unrestricted DFT framework. In detail, we use the OS formula proposed by Yamaguchi and co-workers [47,48], which has been regarded as the most appropriate one for estimating the exchange coupling constant J. The formula is given as J = (EOS−ET)/(< S2 > T− < S2 > OS) where EOS and ET refer to the energies of the unrestricted open-shell singlet and triplet states, while < S2 > OS and < S2 > T are the corresponding average spin square < S2 > values, respectively. We determined the exited-state properties using the configuration interaction singles (CIS) method [49] with a focus on the charge transfer states. The CIS method has been successfully used to study the properties of the excited state in the similar systems, such as the Watson–Crick base pairs and their analogues. It is well-known that the CIS method can overestimate the energies. Thus, the transition energy should be adjusted by a factor of 0.72, as recommended by Broo and

Fig. 1. Optimized geometries of the designed base pairs with main parameters. The selected bond lengths are given in Å. 2

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Holmen, as this has been found to be close to the experimental value. Electronic absorption spectrum calculations were conducted with the Swizard suite of program (revision 4.5), using the Gaussian model.

3. Results and discussion 3.1. Relative stability For the four base pairs designed, they all contain two radical moieties, so we calculated their three states, namely, closed-shell singlet, open-shell broken symmetry singlet, and open-shell triplet states. Only rA2CurT and trans-rG3CurC possess OS ground states. rG3CurC has CS ground state, while trans-rA2curT possess T ground states. Both of them have no OS state. The optimized rG3CurC, rA2CurT, trans-rG3CurC and trans-rA2CurT structures are shown in Fig. 1. All four base pairs have planar structure. Their dihedral angles [rC2(rG/rA)-N1(rG/rA)-N3(rC/ rT)-rC4(rC/rT)] are close to 180°. In addition, the angles of Cu1-Cu2Cu3 are 179.675 and 179.613 for the stable rG3CurC and trans-rG3CurC, so that the three copper atoms are essentially in a straight line. Compared with the natural base pairs GC and AT, the distance of two radical moieties rG/rA and rC/rT is longer. The reason is that the radius of Cu (1.17 Å) is large, while the radius of H (0.32 Å) is small. In addition, due to the introducing of the cyclopentadiene radical, the bond lengths in each molecule also vary to some extent. Therefore, in order to explore their sizes quantitatively, the relevant bond lengths are also showed in Fig. 1. For the designed rG3CurC, and trans-rG3CurC, the O6-N4 distance is elongated to be 3.810 and 3.795 Å, while N1(G)-N3(C) and N2(G)O2(C) distances are elongated to 3.835/3.834 Å and 3.795/3.803 Å respectively. Compared with that of GC base pair, the bond length of N1(G)-N3(C) is stretched by 0.879 (rG3CurC) and 0.875 Å (transrG3CurC) Å. For the designed rA2CurT and trans-rA2CurT, the N6-O4 distance is elongated to be 3.794 and 3.791 Å, while N1-N3 distances are all elongated to 3.876 Å. Compared with that of AT base pair, the bond length of N1-N3 is stretched by 0.995 Å. Obviously, the introducing of Cu makes a slight bend toward the minor groove for the designed GC series, and it also makes A and T bend slightly toward the major groove for the designed AT series. For these designed base pairs, the two ring-expanded bases should bind more tightly than those of the natural GC and AT pairs due to the metal-ligand bonds between Cu and its adjacent N/O atom in the Watson–Crick zone. Here, the binding energies of these base pairs were also calculated. We considered some the binding modes, that is, the combination of the radical pyrimidine part and the radical purine part. They are shown in Fig. S1. For each structure, the binding energy varies with different separation modes, which is due to the number of bonds combined by CueO and CueN. We take rG3CurC as an example. As shown in Fig. 2, it has three separation modes, and the corresponding binding energies are −153.36, −155.78, and −144.67 kcal/mol, respectively. Obviously, rG3CurC is more stable than the natural GC base pair, and its binding energy is only −24.74 kcal/mol. In the whole, these designed base pairs become more stable than the natural base pairs. This shows that the binding ability between the two radicals parts is enhanced after the substitution of H by Cu in the Watson-Crick region, which confirms that the Cu-N/O bond is stronger than the H bond. In addition, the calculation shows that there are short Cu···Cu bonds within the four designed base pair, which range from 2.475 to 2.559 Å. As is known to all, the covalent radius of Cu is 1.17 Å, while its van der Waals radii is 2.00–2.27 Å. Therefore, the Cu···Cu interaction in the Watson–Crick zone may be the Cu(d10)-Cu(d10) metallophilic interaction. The natural charge distributions from NBO analysis is shown in Table S1. The positive charge is mainly distributed on the H and C atoms, and the negative charges distribute mainly on the N and O atoms, indicating that N and O atoms can interact with the copper atoms directly. The charge rearrangement mainly occurs in the Watson–Crick zones, which may lead to the structural changes.

Fig. 2. The corresponding binding energies of the designed base pairs in different separation modes. Binding energies of the natural GC and AT base pairs are represented with the two horizontal dashes.

3.2. Electronic properties and diradical characters In order to further explore the potential application of these four designed ring-expanded copper-modified base pairs, we calculated the adiabatic and vertical ionization potentials (AIP and VIP) and tried to obtain some interesting results. For GC series, the AIP and VIP values of the rG3CurC (trans-rG3CurC) are 127.712 (128.873) and 132.119 (131.704) kcal/mol, respectively, which are lower than those of the natural GC (159.683 and 167.991 kcal/mol). The same thing also happens with the AT series. Their AIP and VIP values are 152.071 (151.645) and 155.361 (154.232) kcal/mol for rA2CurT (trans-rA2CurT), respectively, which are smaller than those of the natural AT (178.564 and 184.048 kcal/mol). Obviously, our designed copper-modified ringexpanded base pairs have lower IP, which means that they are easier to oxidize and produce electron-loss centers. The spin density distributions and the frontier molecular orbitals of the designed base pairs are shown in Fig. 3. For rG3CurC base pair with CS ground state, the HOMO-LUMO gap is reduced to 0.480 eV, which is much smaller than that (3.805 eV) of the natural GC base pair. For other designed base pairs, the singly occupied molecular orbitals (SOMOs) are shown. For trans-rA2CurT, the spin orientations are in the same direction, but for rA2CurT and trans-rG3CurC, their spin orientations are opposite, which indicates that both base pairs have the open-shell single state character. To better understand this phenomenon, Fig. 4 presents the HOMO and LUMO of their CS state and the SOMOs of their OS state. For comparison, the HOMO−LUMO gaps of the natural base pairs, GC and AT, are also presented. Obviously, the HOMO–LUMO gaps of trans-rG3CurC and rA2CurT also become very small, and decrease to 0.452 eV and 0.363 eV. We think that the introduction of the radicals will lead to the rapid decrease of the HOMO–LUMO gap. As is known, the narrower gaps make it easier for electrons to promote from the HOMO to the LUMO. Therefore, the SOMOs of trans-rG3CurC and rA2CurT should be a mixture of HOMO and LUMO. Fig. 4 also shows the HOMO and LUMO can reorganize to form two lower energy SOMOs. Here, we use the CASSCF(10,10) method to calculate the number of electrons outside the closed-shell bonding orbitals, the LUMO occupation number, which is widely used to characterize diradical properties. The corresponding parameters are shown in Table 1. The occupation numbers of LUMO of rA2CurT (< S2 > = 1.024), are close to one (0.998), and the percentage of the diradical character is about 99.8%. Clearly, the rA2CurT base pair possess large diradical character. For trans-rG3CurC (< S2 > = 0.584), its LUMO occupation number is relatively small, and only 0.361. Therefore, the amounts of diradical character is only 36.1%, which implies that its SOMOs is a bad mixture 3

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Fig. 3. The plots of the spin density surfaces (SP), highest doubly occupied molecular orbital (HDMO), and singly occupied molecular orbital (SOMO) for the ground states of the designed base pairs.

of HOMO and LUMO. In order to understand the diradical character, we also calculate the magnetic exchange coupling constant (J) to evaluate the internal interaction of the radical centers. The constant (J) can characterize ferromagnetism (FM, positive) and antiferromagnetism (AFM, negative). The corresponding parameters are tabulated in Table S2. For rA2CurT and trans-rG3CurC, the energy of the singlet is lower than that of the triplet, which indicates both base pairs have antiferromagnetic character. For the rA2CurT base pair, its energy differences between the singlet and triplet are very small and the J value is only −1.689 cm−1. Therefore, its magnetic coupling interaction is very weak. For the trans-

Table 1 Number of electrons outside closed-shell bonding orbitals (BO), occupation number of LUMO and the amounts of the diradical character of the open-shell BS singlet states of the designed diradical base pairs. Base Pair

Total occupancy outside BO

Occupation number of LUMO

Diradical percentage

trans- rG3CurC rA2CurT

0.584 1.177

0.361 0.998

36.1% 99.8%

Fig. 4. Molecular orbital energy levels of the natural and diradical (rA2CurT and trans-rG3CurC) base pairs. The HOMO-LUMO gaps of the natural and closed-shell diradicals are labeled. 4

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Fig. 5. Absorption spectrum of the natural and designed base pairs in the ultraviolet region obtained by the CIS method (half-bandwidths: 500 cm−1). The charge transfer transitions and first excited states are identified with arrows.

rG3CurC base pair, the J value of the trans-rG3CurC is −969.592 cm−1, which indicates it have possesses strong antiferromagnetic coupling interactions. That is to say, the internal interaction between two radical centers is very strong.

4. Conclusions In the present work, a comprehensive theoretical study of the electromagnetic properties of the four base pairs designed, namely, rG3CurC, trans-rG3CurC, rA2CurT, and trans-rA2CurT, was performed using density functional theory calculations. For the four multi-Cumediated ring-expanded base pairs, they all maintain planarity, and have good stability due to the metal-ligand bonds between Cu and its adjacent N/O atom and the Cu···Cu metallophilic interaction in the Watson-Crick zone. What’s more, they all possess smaller HOMO-LUMO gaps and lower ionization potentials than those of the corresponding natural base pairs after modification. Using unrestricted DFT and CASSCF calculations, the results show trans-rG3CurC and rA2CurT possess OS diradical ground states, which exhibit varying degrees of AFM coupling interaction. Their HOMO and LUMO tend to recombine to generate two lower SOMOs to reduce the energies of systems through possible structural reorganization. For the four base pairs designed, the UV absorption spectra show that the first excited state transition and the charge-transfer transitions are greatly red-shifted compared with natural base pairs. They all have stronger transverse base-to-base electronic communication than the natural base pairs, which indicates an enhancement of the transverse conductivity. This work shows that the multi-copper-mediated ring-expanded base pairs have better electromagnetic properties, and we hope these can provide a theoretical basis for their potential application as molecular electronic devices.

3.3. Transverse electronic communication The charge transfer transition is an important feature of transverse electronic communication between two bases. Therefore, we study their electron absorption spectra. It is well known TD-DFT and CIS are two relatively effective methods and have been widely applied to the studies of excited-state of the molecular systems. However, TD-DFT method can seriously underestimate the charge-transfer state energy, and find some useless charge-transfer state. CIS method proposed by Yanai et al. has overcome the shortcomings mentioned above and successfully study the transition state to get reasonable energy values, which are consistent with the experimental values. Therefore, we use CIS method to calculate the UV absorption spectra using the Gaussian mode. Fig. 5 shows the UV absorption spectra of rG3CurC, trans-rG3CurC, rA2CurT, trans-rA2CurT and the natural base pairs. The relevant absorption bands of charge transfer are marked with an arrow. In here, we investigate these charge-transfer transitions, from purine (π ) to pyrimidine (π * ), from pyrimidine (π ) to Cu (d * ), from purine (π ) to Cu (d * ), and their reverse processes. For GC base pair, the lowest transition located at 5.34 eV (232.2 nm) possesses πC πG* character. As we can see, charge-transfer transitions of rG3CurC are red-shifted relative to those of the natural GC base pair. The onset absorption peak is at 329.7 nm, and the corresponding excitation energy is 3.76 eV. For trans-rG3CurC base pair, its first excitation energy is 3.54 eV (350.3 nm). Both excited states * character. Moreover, the number of charge-transfer possess πC dCu transitions after modification has increased markedly. There are 7 and 4 for rG3CurC and trans-rG3CurC respectively, while there are only 3 for the GC base pair. Obviously, the first absorption peaks of rG3CurC and trans- rG3CurC show a red-shifted and their energies are reduced correspondingly. For AT series, charge-transfer transitions of rA2CurT and trans-rA2CurT are also red-shifted compared with those of the natural AT base pair. The delocalized transitions have increased in number. There are two transfers for the natural AT base pair, whereas each of them has 5 transfers for rA2CurT and trans-rA2CurT. Obviously, our modification has significantly improved the transverse electronic conductivity between two bases, compared to the natural GC and AT base pairs, which will be helpful to charge migration and the transduction of electrical signals along the DNA nanowires in the application.

Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgments This work was supported by the National Natural Science Foundation of China (11504200, 11604179, 11705101). Part of the calculations was carried out at High Performance Computing Center of Qufu Normal University.

Appendix A. Supplementary material Supplementary data to this article can be found online at https:// doi.org/10.1016/j.cplett.2019.136704. 5

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