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. 2020 Jul 20;5(30):18808–18817. doi: 10.1021/acsomega.0c01931

Nucleobase Pair–Metal Dimer/Dinuclear Metal Cation Interaction: A Theoretical Study

Ruby Srivastava 1,*
PMCID: PMC7408194  PMID: 32775882

Abstract

graphic file with name ao0c01931_0003.jpg

Nucleobase pair–metal dimer/dinuclear metal cation interactions play an important role in biological applications because of their highly symmetrical structures and high stabilities. In this work, we have selected five adenine–adenine hydrogen bonding, adenine–thymine (AT), adenine–uracil, adenine–adenine stacking pairs, and Watson–Crick AT stacking pairs and studied their interaction with the coinage metal dimer M2 and M22+ metal cations, where M = Ag, Au, and Cu. Quantum chemical calculations have been carried out with density functional theory (DFT) and time-dependent DFT (TDDFT) methods. Electronic structures were analyzed by the partial density of states method. During interactions, we find that M–M distances are shorter than the sum of van der Waals radii of the corresponding two homocoinage metal atoms, which show the existence of significant metallophilic interactions. Results indicated that nucleobase–M22+ complexes are stronger as compared to nucleobase–M2 complexes. Also, the replacement of the hydrogen bond by the dinuclear metal cation-coordinated bond forms more stable alternative metallo-DNA sequences in AAST base pairs. TDDFT calculations reveal that nucleobase–Cu2 complexes and nucleobase–Ag22+/Au22+ complexes can be used for fluorescent markers and logic gate applications. Atom-in-molecules analysis predicted the noncovalent interaction in these complexes.

Introduction

Nucleobase pair–metal ion complexes have attracted tremendous attention because of their conductive behavior and significant thermal duplex stabilization.1−7 These complexes can be used as nanowires,1 sensors,8 bifacial nucleobases,9 and logic gates.10 Logic gate applications used for digital decision of living organisms are aimed to program cells for environmental sensing and medicinal applications.11−13 As DNA acts as a carrier of genetic information, its regular and canonical structure can be used for the generation of new bioinspired functionalized molecular structures.

DNA computers have attracted extensive research interest for their massive parallel operations and high computational speed.14 Dinuclear metal ion–base pairs have become an interesting class of metal-ion–base pair complexes in recent years. Studies have been carried out on artificial bases that form metal-mediated pairs bridged by AgI, CuII, and PdII.4−6 The structural analysis of these complexes shows that the complex formation is possible without major conformational changes in the base structures, though metal-modified nucleic acids may acquire the nonhelical topologies. The most recent applications include charge-transfer dynamics in metal-modified DNA,15−17 recognition of specific nucleic acid sequences,18−20 dynamic and switchable DNA nanostructure creation,21,22 and utilization of their processing by polymerases.23−26 Various nanobioconjugate-linked functional nanoparticles are used in diagnostics, treatment, therapeutics, sensing, and bioengineering. The detection methods based on these nanobioconjugates show increased selectivity and sensitivity.

Many theoretical and experimental investigations have been carried out on nucleobases and coinage metal cations,27 nucleobases and coinage metal anions,28,29 dinuclear silver ion-mismatched base pairs, dinuclear CuII and HgII complexes with artificial base pairs,30−33 which are considered as the new generation nucleoside mimics. The planarity of these artificial DNA base pairs ensures their proper intercalation within the DNA base stack. Another remarkable feature is the strongly intensified thermal stability of the duplex as compared to the normal hydrogen-bond interactions.

Schmidbaur et al. introduced the term “aurophilic” bonding or interactions for the gold clusters. The metallophilic interactions are very close to the hydrogen bonding, which is stronger than van der Waals forces but weaker than covalent bonding. Therefore, these structures and the complex characteristics are significantly influenced by the interactions. The aurophilic interactions are stronger than argentophilic bonding because of the strong relativistic effects of gold.34 The argentophilic metal bonding is also unique as it binds exclusively to the bases rather than the backbone of DNA and also nontoxic in nature. The fluorescent DNA-stabilized silver clusters35 are used for novel chemical- and biochemical-sensing schemes.36

Shionoya et al. included several metal ions adjacent to each other in an artificial DNA framework to form a self-assembled metal array.4,9 These DNA–metal complexes form a magnetic chain by the self-assembled alignment of metal centers and form novel nanodevices such as semiconductors, molecular magnets, and wires. DNA is also considered as an excellent building material for logic gates because of its compatibility, nontoxic nature, biodegradability, and its usefulness for analysis of metal ions in biological RNAs. It was reported in an experimental study that a number of gates were produced based on the DNA polymerization reactions producing an output signal of the G quadruplex DNA sequence.37 Furthermore, the production cost of logic gates was reduced by designing gates, which do not require labeled oligonucleotide probes to generate the fluorescent signal.38,39 Mandal et al. studied for the first time the transformed mononuclear or dinuclear base pairs, which depend on the relative orientation of the DNA duplex.30 Fully artificial metal-mediated base pairs were developed by the complexation of metals with monomeric ligand-bearing nucleosides, and it was first reported by Tanaka and Shionaya.4 Studies were conducted on DNA base pair stacks to accommodate the transition metal ions Cu2+, Ni2+, and Pd2+, in which Cu2+ was utilized more widely. It was seen that the resulting metallobase pairs became flat and most of them have no net charge as these metallonucleobase complexes conduct the deprotonation of the coordinating groups, giving possible benefit for molecular electronics.40−42 As the characteristics of nucleic acid base (NAB)–M2/M22+ complexes are highly influenced by the interactions and their applicability in molecular electronics, we have selected a few NAB pairs and studied their interactions with M2 and M22+ to find their application in biosensors and bioelectronics. For this purpose, we have selected different combinations of NAB pairs, which are adenine–adenine hydrogen bonding (AAHB), adenine–thymine (AT), adenine–uracil (AU), adenine–adenine stacking pairs (AAST), and Watson–Crick (ATAT) (WCST) stacking pairs.

We calculated the cooperative energies, reactivity parameters (global hardness and electrophilicity index), ionization potential (IP), electron affinity (EA), and the highest occupied molecular orbital (HOMO)–lowest unoccupied molecular orbital (LUMO) (HL) gap of the studied complexes. Partial density of states (PDOS) studies have been carried out for the electronic structures of NAB–M2 and NAB–M22+ complexes, respectively. As the recent studies have been conducted on Watson–Crick base pairing arabino-furanosyl nucleosides in water,43 we have also reported time-dependent density functional theory (TDDFT) calculations for absorption and excitation energies in water as a solvent.

Computational Method

The geometries of AAHB, AT, and AU are optimized at the DFT (B3LYP)44/6-31G** level and the CAM-B3LYP45/6-31G** method is used for AAST and WCST stacking pairs. Furthermore, the studied complexes were optimized by Los Almos effective-core potential LANL2DZ46 for gold, silver, and copper clusters and the 6-31G** basis set for the other atoms to maintain consistency. The G09 software program47 is employed in the present calculations. As the computation of interaction energy with finite basis sets generates error, we have included BSSE-corrected energy using the Boys–Bernardi counterpoise correction scheme48 in our calculations. Gaussview49 is used for structures and orbital manipulations. We have considered the closed-shell (singlet state) configuration of the complexes; with only even numbers of Au, Ag, and Cu clusters. Numerous structures have been optimized for the interacting sites. Vibrational analysis has been carried out to confirm the stability of these complexes, and it was found that there is no negative frequency for all these reported stable complexes. In order to compute the solvation effect, self-consistent reaction field theory with the polarizable continuum method is used in the water-phase calculations. The dielectric constant was chosen as the standard value for water (ε = 78.39). A conductor-like screening model50 has been used to calculate theoretical absorption wavelength and excitation wavelength in aqueous media.

The total interaction energy for the M2/M22+–base pair complexes is given by

graphic file with name ao0c01931_m001.jpg 1

where ΔEM2–B1 is the pairwise interaction energy between M2 and the nucleobase directly bonded to it (B1); ΔEB1–B2 is the pairwise base–base (B1–B2) interaction energy; ΔEM2–B2 is the interaction between hydrated M2 and the remote base (mostly long-range electrostatics); and ΔE3 is the polarization energy.

The IP and EA have been calculated as

graphic file with name ao0c01931_m002.jpg 2
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where EN–1, EN+1, and EN are the total energies of the anionic, cationic, and neutral clusters, respectively.

The IP (I) and the EA (A) may also be deduced from the frontier orbitals, I = −EHOMO and A = −ELUMO, using the Koopmans’ theorem. The Mulliken electronegativity χ: μ = – χ = −(I + A)/2 and the hardness η: η = (I – A)/2, where μ is the chemical potential. The electrophilicity index is defined by ω = μ2/2η. Both ω and EA are interrelated, because both measure the capability of accepting one electron from the environment. The electrophilicity index measures the energy lowering of the ligand because of the maximal flow of electrons between the donor and the acceptor.

Natural bond orbital (NBO) analysis51,52 was conducted for these complexes in order to obtain the natural charges and to obtain the stabilization energy E(2) for all possible interactions of these substituents between “filled” (donor) Lewis-type NBOs and “empty” (acceptor) non-Lewis NBOs and estimating their energetic importance by second-order perturbation theory. The properties of bond critical points (BCPs) are performed by atom-in-molecules (AIM) analysis with the AIM 2000 package.53,54

First-principles calculations were performed on the optimized geometries of complexes in a solvent using the DFT approach implemented in the SIESTA55 (Spanish Initiative for the Electronic Simulations with Thousands of Atoms) 4.1.b4 program package. The exchange and correction terms were described using generalized gradient approximation in the scheme of the Perdew–Burke–Ernzerhof (PBE) functional. Double-ζ basis set plus polarization function56 is used for all the calculations. A Monkhorst pack of 2 × 2 × 0.5 k-point mesh for Brillouin zone integration, a cutoff of 300 Ry, a lattice constant of 1 AÅ, and a Gaussian smearing of 0.10 eV are used for PDOS calculations.

Atoms-in-Molecules Analysis

The Laplacian of electron density ∇2ρ(r) at the BCP is given by the local expression of virial theorem as53

graphic file with name ao0c01931_m004.jpg 4

where G(r) and V(r) are kinetic and potential energy densities, respectively. A negative value of ∇2ρ(r) shows the excess potential energy at BCP. This is the condition for all shared electron covalent interactions. A positive ∇2ρ(r) value reveals excess kinetic energy and indicates the closed shell electrostatic interaction and the depletion of electronic charge over the bond length. Similarly, the electron density Hamiltonian H(r) follows the equation

graphic file with name ao0c01931_m005.jpg 5

Koch and Popelier54 proposed both ρ(r) > 0 and H(r) > 0 for weak and medium bonds; ∇2ρ (r) > 0 and H(r) < 0 for strong hydrogen bonds and both∇2ρ(r) < 0 and H(r) < 0 for very strong hydrogen bonds. Two of its charge density-based topological descriptors, viz., the presence of a bond path, and the presence of the (3, −1) BCP between interacting atomic basins, have been proved to be very useful in inferring the presence of a chemical bonding in these chemical systems.

NBO Analysis

The donor–acceptor interactions in the NBO basis are evaluated by the second-order perturbation theory analysis of the Fock matrix.51 The interaction results in a loss of occupancy from the localized NBOs of the idealized Lewis structures into the empty non-Lewis orbitals. For each donor, NBO (i), and acceptor (j), the stabilization energy E(2) associated with delocalization i → j is estimated using

graphic file with name ao0c01931_m006.jpg 6

where εiεj are the NBO orbital energies and F is the Fock operator.

The cooperative energies are also calculated by considering the interaction energies between one base and M2 as given in eq 1. Numerous studies have been carried out previously on the metal–nucleobase interactions.57

Results

Studies have been carried out on all nucleobase pair–M2 complexes in both singlet and triplet spin states. Finally, the nucleobase–M2 complexes in the singlet state are studied because of their higher stability. The electronic structure inspection of the studied complexes gives more insights into the effects induced by the complexation of metal clusters, facilitating more detailed analysis of the geometries. It has been observed that atomic charges also represent useful qualitative information on the electronic structure and, in particular, on relative charges when atoms change their ligand coordination.

The optimized structures of the base pairs are reported in Figure 1 and the other parameters such as HL gap (eV), polarizability, dipole moment (Debye), and bond lengths (AÅ) of the isolated base pairs are given in Table S1. The dipole moment is higher for the AT base pair and the HL gap is higher for the reported AAST and WCST base pairs. For (AAHB, AT, and AU)–M2/M22+ complexes, we find the B3lyp/LANL2DZ:6-31G** method to be appropriate57−61 and for (AAST, WCST)–M2/M22+ complexes, we have carried out calculations using CAM-B3LYP/LANL2DZ:6-31G**and PBE1PBE/cc-pVDZ:6-31G** methods and reported the final calculations using the CAM-B3LYP/LANL2DZ:6-31G** method. The comparison of relative energies (au) of the (AAST, WCST)–M22+ complexes is given in Table S2.

Figure 1.

Figure 1

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Optimized structures of the studied nucleobase pairs: AAHB, AT, AU, AAST, and WCST.

In nucleobase–M2 complexes, we found that the metal dimers are attracted to nitrogen (N) atoms of the major groove site of the adenine bases. For nucleobase–M22+ complexes, it is observed that the dinuclear metal cations interact from the outer side with the nucleobase (AAHB, AT, and AU) pairs and (AAST and WCST)–M22+ complexes forming metal-mediated dimer–nucleobase complexes. Nucleobases (AAHB, AT, and AU) have planar geometries, while AAST and WCST stacking pairs form parallel and slightly curved structures, respectively. We found that the metallonucleobase complexes possess strong bonding and exhibit high thermal stability.

The M–N distance is found to be 1.97–2.29 AÅ for all the complexes, which approaches the sum of covalent radii of Ag (1.53 AÅ), Au (1.44 AÅ), Cu (1.38 AÅ), and N (0.75 AÅ), indicating a stronger bond. Cu2 and Au2 are strongly bonded to the nucleobase pairs as compared to the Ag2 interaction. The results of M–N bond distances and the hydrogen bond distances for all the nucleobase–M2 and nucleobase–M22+ complexes are summarized in Table 1a,b, respectively. In nucleobase–M22+ interactions, we observed that the interaction trend is the same for all the complexes except for AAHB–Au22+ interactions. Here, we found that the bond lengths of the AAHB–Au22+ complexes are larger than the bond lengths of the AAHB–Ag22+ complexes. This property can be used to construct or induce higher-order structures. The structural stability of Cu was also observed in H–Cu2+–H and other metallobase pairs in GNA double strands studied by Zimmermann et al.62 All studied complexes formed flat planer structures as observed in the H–Cu2+–H complexes. (AAST, WCST)–M2/M22+ complexes showed curved geometries. The optimized structures of these NAB–M2/M22+ complexes are shown in Figure 2a,b, respectively. In a previous study, it was seen that metal coordination does not induce any charge because of the deprotonation of the R-hydroxyl group, so it is considered as the right choice for the hydrophobic base stacking within the DNA duplexes.63 Also, metallobase complexes increase the duplex stability because of larger bond energies of metallonucleobase complexes as compared to the hydrogen bonds. This interesting feature of these complexes (addition or removal of metal ions) without any changes in temperature can be used in DNA sensors and DNA computer applications. These complexes can also be used in artificial DNAzymes, logic gates, DNA machines, and DNA-based nanomaterials such as electronic wires and magnetic devices.64

Table 1. (a) Bond Lengths (AÅ) of the Optimized Nucleobase Pair–M2 Complexes (M = Ag, Au, and Cu); (b) Bond Lengths (AÅ) of the Studied Optimized M22+–Nucleobase Pairs for (M = Ag, Au, and Cu).

  bond length (AÅ)
   bond length (AÅ)
complexes M–N N1–H1 N2–H2 complexes M–N
(a)
AAHB–Ag2 2.278 1.686 1.575 AAST–Ag2 2.281
AAHB–Au2 2.115 1.616 1.740 AAST–Au2 2.125
AAHB–Cu2 1.982 1.683 1.571 AAST–Cu2 1.984
  bond length (AÅ)
   bond length (AÅ)
complexes M–N N1–H1 O–H Complexes M–N N1–H1 O–H
(a)
AT–Ag2 2.296 1.816 1.681 WCST–Ag2 2.262 1.800 1.725
AT–Au2 2.130 1.806 1.691 WCST–Au2 2.190 1.841 1.603
AT–Cu2 1.983 1.822 1.682 WCST–Cu2 1.971 1.839 1.599
  bond length (AÅ)
complexes M–N N1–H1 O–H
(a)
AU–Ag2 2.293 1.677 2.659
AU–Au2 2.138 1.666 1.828
AU–Cu2 1.989 1.676 2.655
  bond length (AÅ)
    
complexes M–N N1–H1 N2–H2 complexes M–N
(b)
AAHB–Ag22+ 2.175 1.732   AAST–Ag22+ 2.124
AAHB–Au22+ 2.732 1.569   AAST–Au22+ 2.060
AAHB–Cu22+ 1.908 1.647 1.823 AAST–Cu22+ 1.908
  bond length (AÅ)
        
complexes M–N N1–H1 O–H complexes M–N N1–H1 O–H
(b)
AT–Ag22+ 2.210 1.097   WCST–Ag22+ 2.170 1.727 1.913
AT–Au22+ 2.138 1.771 1.721 WCST–Au22+ 2.009 1.848 1.877
AT–Cu22+ 1.989 1.676 2.655 WCST–Cu22+ 1.891 1.809 1.657
  bond length (AÅ)
complexes M–N N1–H1 O–H
(b)
AU–Ag22+ 2.203 1.796  
AU–Au22+ 2.081   1.906
AU–Cu22+ 1.928 1.725  
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Figure 2.

Figure 2

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(a): Optimized structures of the studied nucleobase pair–M2 complexes (M = Ag, Au, and Cu). (b) Optimized structures of the studied nucleobase pair–M22+ complexes (M = Ag, Au, and Cu).

Though many metal cations usually interact with various parts of the DNA, metal cations such as Hg2+, Ag+, and Pt2+ target specific base motifs in DNA, which led to functional metallic DNA.65−67 This specific property has been observed for our studied complexes also. Furthermore, we observed that M–M distances are shorter than the sum of van der Waals radii of the corresponding two homocoinage metal clusters (Ag-1.66 AÅ), Au (1.72 AÅ), and Cu (1.40 AÅ), reflecting the existence of significant metallophilic interactions in these complexes. Tanaka et al. have arranged Cu2+ ions into a magnetic chain using the artificial DNA.68 In canonical helical conformation of the DNA-like duplexes also, Cu2+–Cu2+ has maintained the regular distance. The experimental studies on the EPR spectra reveal that the Cu2+–Cu2+ distance is 3.7(0.1 AÅ), which is comparable to 3.3–3.4 AÅ for B-DNA between natural base pairs. The hydrogen bond distances show contraction in bond distances as compared to the hydrogen bond distance observed for the isolated NAB pairs except the O–H bond length, which is larger for AU–M2 complexes. For nucleobase–M22+ complexes, we observed that hydrogen bond distances are contracted. The interaction energies are higher for (AAST, WCST)–M2/M22+ complexes as compared to those of the other studied complexes.

A different look at the role of the metal moiety in the electronic structure of these complexes can be given by inspecting the HOMO–LUMO gaps, which are reported in Table 2. The HL energy gap plays an important role in the metal-induced effect in view of nanotechnological applications. The HL gap is larger for all nucleobase–Au2 complexes except for WCST–Au2 complexes, which have a lower HL gap. Because of the larger HL gap (5.80 eV), most of the nucleobase–M2 complexes are considered to be very stable. In some nucleobase–M2 complexes, a large shrinking is observed in the HL gap. As metals play a vital role in the HOMO and the LUMO, we can also predict that the band gap shifts are not only because of the electrostatic effects but also because of the orbital hybridization. The HOMO, being the most chemically active species, is localized on the metal, so the metal can definitely affect the frontier orbitals. AU–Cu22+, AAST–Ag22+, AAST–Cu22+, and WCST–M22+ complexes have a larger HL gap.

Table 2. BSSE-Corrected Interaction Energy (−Eint, kcal/mol), HL Gap, Dipole Moment (μ, Debye), Cooperative Energies (Ecoop, kcal/mol), and Contribution of the Cooperative Energy to the Total Interaction Energy (% Ecoop) for NAB–M2 Complexes (M = Ag/Au/Cu).

complexes Eint HL gap (eV) Ecoop % Ecoop complexes Eint HL gap (eV)
AAHB–Ag2 67.24 2.61 –11.92 17.73 AAHB–Ag22+ 394.40 0.29
AAHB–Au2 57.11 3.54 –15.94 27.91 AAHB–Au22+ 413.23 0.42
AAHB–Cu2 63.88 2.56 –16.04 25.11 AAHB–Cu22+ 403.32 0.34
AT–Ag2 61.10 2.83 –11.50 18.82 AT–Ag22+ 433.22 0.33
AT–Au2 54.40 4.00 –13.57 24.94 AT–Au22+ 450.23 0.37
AT–Cu2 56.80 2.83 –15.75 27.73 AT–Cu22+ 341.35 5.72
AU–Ag2 46.99 2.92 –12.19 25.94 AU–Ag22+ 422.45 0.37
AU–Au2 38.70 3.99 –11.26 29.10 AU–Au22+ 447.32 0.61
AU–Cu2 40.11 2.76 –10.58 26.38 AU–Cu22+ 451.14 2.48
AAST–Ag2 110.77 3.26 –13.82 12.48 AAST–Ag22+ 456.31 4.93
AAST–Au2 121.91 4.16 –11.82 9.70 AAST–Au22+ 453.22 0.85
AAST–Cu2 119.22 3.13 –16.79 14.08 AAST–Cu22+ 461.22 4.94
WCST–Ag2 155.70 5.25 –12.98 8.32 WCST–Ag22+ 463.41 4.25
WCST–Au2 149.20 3.40 –19.21 12.88 WCST–Au22+ 465.23 4.41
WCST–Cu2 169.10 4.71 –13.65 8.07 WCST–Cu22+ 469.29 6.41
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To justify this statement, we have carried out the PDOS structure analysis of these complexes. The computational details regarding PDOS studies of all complexes are given in the theoretical methods. In individual NAB pairs, we get few peaks for the N 2s orbital at the HOMO, and the p-orbital peaks (C and N) are observed for both the HOMO and LUMO. In AAHB–Ag2 and AAST–Cu2 complexes, the “d” orbital of Ag/Cu has not contributed to the interactions. While in the rest of the complexes, few peaks for “s” orbital peaks of H atoms are observed in the NAB–M2 complexes. The “p” orbital contribution of N and C has been observed in almost all the complexes, see Figure S1a. In NAB–M22+ complexes, the contributions of “s” and “p” orbitals of C and N are observed at the HOMO and LUMO. Few peaks have been observed for the s and d-orbitals of the metal at the HOMO and the LUMO, see Figure S1b. The cubic lattice vectors for AAHB–M2 > AAHB–M22+ complexes and AAST–M2 < AAST–M22+ complexes. For the rest of the other complexes, no trend has been observed for the increase or decrease of cubic unit vector parameters for the individual NAB–M2/M22+ complexes.

The cooperative energies and the % Ecoop of nucleobase pairs–M2 complexes also reflected the stable nature of these complexes. The cooperative effect is calculated to see the strength of the interactions. The BSSE-corrected interaction energy, HL gap, and other parameters are given in Table 2. The estimated negative Ecoop values indicate that the cooperative energies have stabilized the NAB–M2 complexes.

The vertical IP, vertical EA, hardness, and electrophilicity index are shown in Table 3. The computed vertical EA (EAv) is (0.41–2.73 eV) and vertical IPv is (4.9–7.9 eV) for all the complexes. The ω value is higher for (AAST, WCST)–Au2 complexes. EA and ω are interrelated because both measure the capability of accepting one electron from the environment.66−68 The electrophilicity index measures the energy lowering of the ligand due to maximal transfer of electrons between the donor and acceptor. Our results are in agreement with the previous studies.57 It is also in agreement with the rule that electron transfer should proceed from the highest chemical potential to the lowest chemical potential.69 No specific trend has been observed for the dipole moment, which is reported in Table 3. The dipole moment is in the range (2.53–10.35) D.

Table 3. Vertical First IP (IPv, eV) and Vertical EA (EAv, eV), Electronegativity (χ), Hardness (η), Electrophilicity Index (ω), and Dipole Moment (Debye) in the Ground State for NAB–M2 Complexes (M = Ag/Au/Cu).

complexes IPv EAv Χ η Ω μD
AAHB–Ag2 6.65 1.69 4.18 2.48 3.52 6.40
AAHB–Au2 7.61 1.38 4.50 3.11 3.25 8.42
AAHB–Cu2 6.58 1.66 4.13 2.46 3.46 6.00
AT–Ag2 5.44 0.64 3.04 2.40 1.93 9.07
AT–Au2 7.79 0.54 4.17 3.63 2.40 10.35
AT–Cu2 6.72 0.59 3.66 3.07 2.18 8.93
AU–Ag2 6.73 0.53 3.63 3.10 2.12 4.51
AU–Au2 7.89 0.41 4.15 3.74 2.31 8.47
AU–Cu2 6.75 0.51 3.63 3.12 2.11 4.15
AAST–Ag2 6.71 1.57 4.14 2.57 3.35 2.53
AAST–Au2 7.77 2.73 5.26 2.52 5.49 4.85
AAST–Cu2 6.83 1.21 4.03 2.81 2.89 3.16
WCST–Ag2 5.68 1.03 3.36 2.32 2.43 7.58
WCST–Au2 4.93 2.30 3.62 1.32 4.98 8.43
WCST–Cu2 6.28 1.03 3.66 2.62 2.55 6.86
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The second-order perturbation energies E(2) represent the nN → nM* transfers. E(2) values and charge transfer have been reported for all the studied complexes by NBO analysis (see Table 4). We observed that the perturbation energies of aurophobic interactions are higher for nucleobase–M2 complexes. In nucleobase–M22+ complexes, dinuclear Cu metal cation complexes have larger energies for AU, AAST, and WCST interactions. No correlation has been observed for the interaction energies and E(2) values.

Table 4. NBO Charge-Transfer Energy (E(2), kcal/mol) Due to the nN → nAu*, Charge (ΔqCT, e) for the Studied NAB–M2 Complexes (M = Ag/Au/Cu).

complexes E(2) ΔqCT complexes E(2) ΔqCT
AAHB–Ag2 16.02 0.089 AAHB–Ag22+ 13.70 0.071
AAHB–Au2 18.02 0.089 AAHB–Au22+ 15.44 0.064
AAHB–Cu2 29.66 0.125 AAHB–Cu22+ 13.36 0.510
AT–Ag2 13.95 0.084 AT–Ag22+ 17.08 0.052
AT–Au2 29.74 0.111 AT–Au22+ 26.06 0.126
AT–Cu2 26.94 0.122 AT–Cu22+ 20.43 0.110
AU–Ag2 12.80 0.62 AU–Ag22+ 12.14 0.067
AU–Au2 28.57 0.106 AU–Au22+ 35.19 0.114
AU–Cu2 14.11 0.076 AU–Cu22+ 53.98 0.136
AAST–Ag2 12.77 0.100 AAST–Ag22+ 16.21 0.052
AAST–Au2 29.14 0.110 AAST–Au22+ 20.83 0.089
AAST–Cu2 15.09 0.125 AAST–Cu22+ 69.43 0.183
WCST–Ag2 18.87 0.106 WCST–Ag22+ 12.31 0.058
WCST–Au2 30.85 0.108 WCST–Au22+ 45.67 0.110
WCST–Cu2 16.56 0.116 WCST–Cu22+ 70.34 0.167
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The calculated electron density ρBCP, its Laplacian ∇2ρBCP, total electron energy density HBCP, and its components (the local kinetic energy density) GBCP, and the local potential energy density VBCP for nucleobase–M2 and nucleobase–M22+ complexes are reported in Table 5a,b, respectively. It can be seen that the ρ values of these complexes are larger, indicating strong interaction of these complexes. Furthermore, the nucleobase–M2 interactions can be classified as closed shell interactions because of the positive Laplacian. In addition, positive HBCP values indicate a dominant closed shell (electrostatic) interaction. H-bond has increased the strength of these complexes. It has been observed in several studies that nature of interactions is determined by the balance between the GBCP and VBCP values. If the absolute ratio of these quantities is less than 0.5, it is a shared interaction. For 0.5 < −GBCP/VBCP < 1 values, the interaction is partly covalent in nature and for −GBCP/VBCP > 1, the interaction is noncovalent in nature. In our studied complexes, these interactions are noncovalent as the absolute values for −GBCP/VBCP > 1.70 The cooperative effects in the H-bonding also tend to decrease −GBCP/VBCP values. HBCP values reveal that the covalency of these NAB–M2 bonds increases the complexation of the NAB pairs. For NAB–M22+ complexes, larger ρ values confirm strong interactions. The positive value of Laplacian in these interactions also classified them as closed shell interactions. Furthermore, the positive HBCP values indicate a dominant closed shell (electrostatic) interaction, and −GBCP/VBCP > 1 indicate noncovalent interactions for these complexes.

Table 5. Electron Density (ρBCP, au), Its Laplacian (∇2ρBCP, au), Kinetic Electron Energy Density (GBCP, au), Potential Electron Energy Density (VBCP, au), Total Electron Energy Density (HBCP, au), and the Absolute Ratio of the Kinetic and Potential Electron Energy Densities (−GBCP/VBCP) for (a) NAB–M2 and (b) NAB–M22+ Complexes (M = Ag/Au/Cu).

complexes ρBCP ∇2ρBCP GBCP VBCP HBCP –GBCP/VBCP
(a)
AAHB–Ag2 0.0828 0.0947 0.1107 –0.1059 0.0048 1.0453
AAHB–Au2 0.2164 0.0196 0.1236 –0.1233 0.0003 1.0024
AAHB–Cu2 0.2365 0.0419 0.1727 –0.1546 0.0181 1.1170
AT–Ag2 0.1877 0.0012 0.1952 –0.1943 0.0009 1.0046
AT–Au2 0.5883 0.0220 0.3842 –0.3622 0.0220 1.0607
AT–Cu2 0.4533 0.7870 0.0231 –0.0221 0.0009 1.0407
AU–Ag2 0.1084 –0.0910 0.1249 –0.0338 0.1587 3.6890
AU–Au2 0.1247 –0.1575 0.1999 –0.0423 0.2422 4.7250
AU–Cu2 0.3166 0.1700 0.1391 –0.3091 0.4482 0.4501
AAST–Ag2 0.0033 –0.0022 0.0019 –0.0013 0.0006 1.4615
AAST–Au2 0.0388 –0.0326 0.0414 –0.0398 0.0016 1.0402
AAST–Cu2 0.0289 0.0301 0.0316 –0.0376 0.0014 1.0398
WCST–Ag2 0.0063 –0.0063 0.0048 –0.0045 0.0003 1.0666
WCST–Au2 0.0819 –0.0376 0.0316 –0.0249 0.0067 1.2690
WCST–Cu2 0.0014 –0.0014 0.0111 –0.0104 0.0007 1.0670
(b)
AAHB–Ag22+ 0.05431 –0.07243 0.00744 –0.00197 0.07636 3.7766
AAHB–Au22+ 0.00549 –0.00429 0.0034 –0.00090 0.00249 3.7777
AAHB–Cu22+ 0.2068 –0.00148 0.12245 –0.12097 0.24342 1.0122
AT–Ag22+ 0.01305 –0.00614 0.00659 –0.00145 0.00704 4.5448
AT–Au22+ 0.06326 –0.03758 0.05646 –0.01888 0.07534 2.9905
AT–Cu22+ 0.0188 –0.00566 0.01025 –0.00459 0.01485 2.2331
AA–Ag22+ 0.03498 –0.03258 0.00378 –0.00120 0.03498 3.1500
AA–Au22+ 0.00931 –0.01069 0.00834 –0.00235 0.00599 3.5489
AA–Cu22+ 0.23646 –0.04981 0.41348 –0.36367 0.77715 1.1369
AU–Ag22+ 0.01764 –0.01955 0.00712 –0.00243 0.01469 2.9300
AU–Au22+ 0.38082 –0.45908 0.89764 –0.43855 1.33619 2.0468
AU–Cu22+ 0.14280 –0.09767 0.16308 –0.06541 0.22848 2.4932
WCST–Ag22+ 0.00198 –0.0021 0.00158 –0.00052 0.00107 3.0385
WCST–Au22+ 0.01592 –0.02448 0.02064 –0.00384 0.0168 5.3750
WCST–Cu22+ 0.02958 –0.02334 0.002534 –0.00200 0.02734 1.2670
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In recent studies, Ag+ were found to form C–Ag(I)–C pairs at cytosine mismatches in antiparallel B-DNA,71 so we also anticipated that selected metallobase pairs can be used to build new DNA-based assemblies. The selection of silver is due to its lower toxicity in humans as an antimicrobial agent.72 Another important property of silver-mediated nucleobases is its control over size and optical properties of fluorescent DNA-templated silver clusters.73 Few experimental studies also predict silver cation–nucleobase pair complexes in the formation of silver nanowires.74,75 Interestingly, by adjusting some external experimental conditions, the size and the packing density of the Au nanocrystals are controlled when gold ions interact with the imidazole and amine groups of the sequenced peptides on the nanotubes. Furthermore, the orthogonal metal-binding affinity of the nucleobases led to the site-selective and “full-match” metallobase pairing. These essential features of complexes are used for information storage.

The TDDFT calculations are carried out to study the optical properties of the studied complexes. The absorption wavelength (nm) and emission wavelength (nm) in water as the solvent, oscillatory strength and Δλ (nm) of the isolated nucleobase pairs, nucleobase pair–M2, and nucleobase pair–M22+ complexes are reported in Table 6. In a recent study related to the optical properties of DNA-linked gold nanoparticles, it was observed that the absorption wavelength in the UV region is ∼260 nm and the excitation wavelength is ∼520 nm.76 On comparing our TDDFT results, we found that almost all nucleobase pair–M2 complexes show excitation wavelength in the visible region. Nucleobase pair–Cu2 complexes have excitation wavelength in the range of 489–619 nm, which can be used in the application of fluorescent biomarkers and logic gates. Interestingly, nucleobase pair–M22+ complexes showed a different trend. All the aurophilic and argentophilic complexes show excitation wavelength in the visible region. For nucleobase pair–M22+ complexes, only the WCST–Cu22+ complex with excitation wavelength near the visible region is reported.

Table 6. Absorption Wavelength (nm) and Emission Wavelength (nm), Oscillatory Strength, and Δλ (nm) of Isolated NAB Base Pairs and Nucleobase–M2/M22+ Complexes in Water as the Solventa.

complexes λabs f λems f complexes λabs f λems f
AAHB 251.0 0.1016 295.12 0.0113          
AAHB–Ag2 308.9 0.0023 505.7 0.0006 AAHB–Ag22+ 547.37 0.0013 869.45 0.0007
AAHB–Au2 327.8 0.0049 423.8 0.1662 AAHB–Au22+ 460.4 0.208 463.43 0.191
AAHB–Cu2 322.9 0.1528 619.4 0.0004          
AT 201.61 0.3074 275.66 0.0017          
AT–Ag2 385.3 0.0006 441.7 0.0019 AT–Ag22+ 361.64 0.0039 475.59 0.0092
AT–Au2 273.2 0.1045 339.3 0.2610 AT–Au22+ 339.3 0.261 387.8 0.0195
AT–Cu2 325.6 0.0929 532.6 0.0007          
AU 245.75 0.2474 289.53 0.0008          
AU–Ag2 371.5 0.5530 504.2 0.0008 AU–Ag22+ 492.60 0.0154 648.94 0.0025
AU–Au2 337.6 0.1488 363.9 0.0080          
AU–Cu2 322.8 0.1180 540.8 0.0010          
AAST 236.60 0.2277 306.16 0.0002          
AAST–Ag2 341.9 0.2031 461.99 0.0011 AAST–Ag22+ 311.95 0.272 461.99 0.0011
AAST–Au2 336.1 0.0051 359.56 0.1554 AAST–Au22+ 282.69 0.1537 359.56 0.155
AAST–Cu2 312.8 0.0677 489.16 0.0074          
WCST 241.68 0.202 320.38 0.0007          
WCST–Ag2 433.2 0.0025 512.6 0.0011 WCST–Ag22+ 425.87 0.273 512.61 0.0011
WCST–Au2 268.9 0.1093 420.4 0.1931          
WCST–Cu2 323.9 0.0475 552.3 0.0003 WCST–Cu22+ 552.29 0.0003 569.88 0.0003
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a

The complexes with excitation wavelength < 900 nm are reported for nucleobase–M22+ complexes.

In a recent study, 450 nm excitation wavelengths were selected for Ag-mediated complexes.21 It was observed that the melting properties were controlled by interatomic distances. As gold particles are linked together via DNA hybridization, remarkable damping occurs upon the electromagnetic coupling between these gold particles at their surface plasmon resonances. The same properties have been observed for quantum-dot nanocrystals also that the emission wavelength can be continuously tuned by changing the particle size and by the use of monochromatic light for simultaneous excitation of different-sized dots.77 Studies revealed that each complex has a selective nature regarding the properties. We can also conclude that because each complex has its own unique properties, judgement cannot be made merely on the basis of previous studies.

Conclusions

DNA acts as a promising material in biomolecular technology because of its unique properties such as recognition capabilities, physicochemical stability, mechanical rigidity, and high-precision processability. Various DNA-based structures and DNA-functionalized metal nanoparticles will find an application in the technological world. These novel complexes will continuously emerge and provide valuable fundamental information about the physicochemical properties of the metallonucleobase complexes and become useful as electronic and photonic materials. In our studies, we observed that because of the interaction of NAB pairs with the coinage metal dimers and dinuclear metal clusters, these complexes have a slightly contracted hydrogen bond distance toward the major groove site of nucleobases. The obvious cooperative effect has been observed by the relative shift in IPs caused by π-stacking and H-bonding interactions. PDOS analysis has been carried out to study the contribution of different valence orbitals of elements to the HOMO and the LUMO. The band gap shrinking along with the metal–base coupling suggests interesting consequences for electron transfer through DNA duplexes. Persistent planarity (except stacking models) of these complexes indicated the structures to be energetically more stable. We anticipate that these design electronic modifications can be applied in various nanoelectronic models. NAB–Cu2 complexes can be used as the best candidates for nanowires because of their conducting properties. Finally, our work will provide a reliable and efficient theoretical tool to describe the structural electron attachment and detachment abilities of NAB–metal interactions, which can be potentially used for exploring long DNA strand models.

Acknowledgments

R.S. acknowledges the financial assistance by DST WOS A project (SR/WOS A/CS-69/2018). R.S. is also thankful to her Mentor Dr. Shrish Tiwari, Bioinformatics, CSIR-Center for Cellular and Molecular Biology and Dr. G. Narahari Sastry, Director, CSIR-NEIST for the technical support.

Supporting Information Available

The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/acsomega.0c01931.

  • HL gap (eV), polarizability, dipole moment (Debye), and bond lengths (AÅ) of the studied base pairs; comparison of relative energies (au) using two different functional and basis sets for (AAST, WCST)–M2/M22+ complexes; and PDOS analysis of isolated NAB pairs and NAB–M2 complexes (M = Ag, Au, and Cu) (PDF)

The author declares no competing financial interest.

Supplementary Material

ao0c01931_si_001.pdf (2.7MB, pdf)

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