Nature of the Interaction between Natural and Size-Expanded

Nov 6, 2012 - In this paper, we study the interaction of natural and size-expanded guanine molecules with small gold clusters, to shed light on the na...
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Nature of the Interaction between Natural and Size-Expanded Guanine with Gold Clusters: A Density Functional Theory Study Wenming Sun* and Rosa Di Felice* CNR Institute of Nanoscience, S3 Center, Via Campi 213/A, 41125 Modena, Italy S Supporting Information *

ABSTRACT: In this paper, we study the interaction of natural and size-expanded guanine molecules with small gold clusters, to shed light on the nature of the N/O− Au bonds and of the unconventional NH···Au hydrogen bonds, as well as on the dependence of these bonds on the charge state of the systems. Based on density functional theory results, it is found that the nature of the N/O−Au bonds between both guanine and its size-expanded form and three- and four-atom Au clusters is covalent in the neutral systems. In the −1 charged systems, the binding energy decreases by almost 50% with a significant change of geometry. Although the NH site in the spacer ring of size-expanded guanine may supply a new acceptor opportunity for forming an additional NH···Au hydrogen bond, this hardly emerges because of the nonplanarity and the large steric effect. The introduction of a spacer ring in guanine decreases the highest occupied molecular orbital−lowest unoccupied molecular orbital gap and expands the spatial distribution of electron wave functions, which make size-expanded guanine appealing for charge transfer performance. At the same time, it increases the steric hindrance, making the adsorption process more orderly, which is also good in view of molecular electronic devices.

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transition metals found in different systems.5 In fact, the unconventional hydrogen bond for the XH···M complex (M = transition metal) has been originally introduced by Brammer6 and has been investigated experimentally and theoretically. In 2009, Shukla and co-workers investigated the interactions of the guanine base and the Watson−Crick guanine−cytosine base pair with larger gold clusters Aun (n = 2, 4, 6, 8, 10, 12): their results confirmed the bonding between N and Au atoms.7 Other groups investigated the interactions between the DNA bases or base pairs with gold clusters,8 even for a Au20 cluster.9 Recently, Cao and co-workers studied the nucleobase−gold complexes with anion photoelectron spectroscopy and DFT calculations and confirmed the existence of NH···Au hydrogen bonds through experimental measurements.10 Another class of studies tackles the adsorption of nucleobases on extended inorganic surfaces or nanoparticles. In 2006, Piana and Bilic11 investigated the nature of the adsorption of nucleobases on the Au(111) surface, assuming that, at a low coverage in vacuum, the preferred configuration for the hybrid system is a flat orientation of each base on the surface. They concluded that the coupling is dominated by dispersion interactions for all the bases while an appreciable degree of chemisorption occurs for adenine only. Apparently, this is inconsistent with the chemisorption regime found for nucleobases on small gold clusters.4,12 Furthermore, there are discrepancies about the binding orientation of DNA nucleosides relative to gold flat surfaces and the surfaces of gold

INTRODUCTION The interaction between biomolecules and inorganic surfaces and nanoparticles is of great importance in natural systems and for the design of bionanomolecular devices. Due to its chemical inertness and biocompatibility, gold could be utilized in several bioelectronic and biomedical applications. Experimental studies have shown that the DNA bases and proteins interact with gold surfaces and clusters and adsorb at electrodes in a complex and sequence-dependent manner.1−3 The investigation of the nature of these interactions is essential for understanding the physisorption/chemisorption regime, which influences the transport, catalytic, and sensing mechanisms of gold-supported devices, and could shed more light on these controversial issues. Few-atom clusters have been widely exploited to investigate some properties of molecular adsorption on surfaces with computational approaches, due to the convenience of using small-size systems for grasping basic mechanisms. In 2005, Kryachko and Remacle4 investigated the interactions between DNA bases and two types of gold clusters, Au3 and Au4, by a computational approach within density functional theory (DFT). They determined that the bonding occurs via the N and O atoms in the bases and one gold atom. They also showed that this chemical bonding could be reinforced by the NH···Au unconventional hydrogen bonds nearby. In Kryachko’s work on the DNA@Au complexes, the authors compared the geometrical parameters, the vibrational frequencies, and the NMR signatures of the molecule−metal H bond with the prerequisites of conventional weak hydrogen bonds. They labeled the NH···Au bonds with the adjective “unconventional” by analogy with other unconventional hydrogen bonds with © 2012 American Chemical Society

Received: August 9, 2012 Revised: November 2, 2012 Published: November 6, 2012 24954

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The interaction of the x-bases with small metal clusters was also investigated. Sharma et al. utilized a DFT method to investigate the interaction between the x-bases (xA, xT, xC, xG) and Au6 clusters to inquire on the possibility of enhancing conductivity in size-expanded nucleic acids tagged by gold atoms.25 Bu’s group did some work on the rational design of heteroring-expanded DNA base analogues and determined that the expanded bases may be considered as DNA genetic motifs and serve as building blocks in the development of molecular electronic devices.26,27 They investigated various xGs in which the spacer ring has different conjugation, for example, π66conjugated and π68-conjugated bonding. They found that the HOMO−LUMO gap of xG4 (with π68-conjugated bonding spacer) is significantly lower than that of natural G and standard xG, decreasing by 1.75 and 0.75 eV, respectively. Due to its small HOMO−LUMO gap and the presence of two NH sites in the expanded spacer ring, xG4 may offer optimized bonding opportunity and better charge transfer performance. We investigate here the adsorption of xG4, xG6, and xG8 (all labels are consistent with ref 26) on gold clusters by DFT: these model systems would allow us to answer more questions on the suitability of the new designed heteroring-expanded DNA base analogues tagged on gold clusters for molecular conduction applications. We wish to understand if and how chemical modifications of the bases affect the DNA@Au binding and in particular the unconventional H bonding. This issue is relevant for revealing the interaction between biomolecules and gold surfaces and nanoparticles.28 Progress in this field will offer more information on the potential molecular wire application of natural and modified DNAs.

nanoparticles. This is not surprising, because the properties of clusters and surfaces may be significantly different from each other. Very recently, it was determined that gold clusters (Au18, Au27) tend to pump electrons to the corner and edge sites, making these sites more electronically active than surface sites.13 Accordingly, the different electronic reactivity of gold atoms at surface, corner, or edge sites of nanoparticles may significantly influence the binding orientation of nucleobases on surfaces and nanoparticles and consequently the electronic properties of the resulting systems. Meanwhile, the N/O−Au interaction is dominant in the adsorption process of other biomolecules on gold surfaces or nanoparticles. For example, histidine anchors through its unprotonated nitrogen atom on top of a gold atom at the Au(111) surface.14 Furthermore, the dative bond between a hydroxyl-rich β sheet and a gold surface is the essential component of the recognition mechanism.15 In all the past studies of the binding between DNA bases and Au clusters, the authors characterized the binding sites and electron affinity/ionization processes, while mostly omitting information on the detailed topology of the unconventional NH···Au hydrogen bonding. The adsorption process of biomolecules on gold surfaces/nanoparticles is a dynamic phenomenon, which depends on the molecule coverage and other specific conditions. Different driving factors contribute to determining the geometry. On one hand, π stacking between molecule and surface in a horizontal relative orientation would lead to stability by maximizing orbital mixing. On the other hand, direct N/O−Au bonding between molecule and surface, possibly reinforced by the unconventional NH···Au hydrogen bonding, would play a crucial role in an inclined relative orientation for some special conditions, such as the high coverage on a surface or the self-assembly process of a DNA strand at gold nanoparticles or surfaces.16 A very recent paper reports on the multiple adsorption geometries and electronic properties of DNA bases adsorbed on the Au(100) surface.17 The authors briefly reviewed the inconsistent reports on this topic and determined that a horizontal orientation is favored in ascendant order for dG, GC, and dT while there is negligible difference between horizontal and vertical orientations for dA. However, considering the small difference between horizontal and vertical binding orientations for dA, the flat potential energy surface, and the high mobility of the DNA base on the surface, there are indeed some other unexpected orientations besides the static horizontal and vertical configurations. In the past 10 years, interest in the use of modified analogues of DNA as templates for growing nanoparticle complexes has increased significantly, aiming to investigate whether these new alternative genetic systems could exist for therapeutic and biotechnological applications. Kool and his collaborators did some pioneering work on the synthesis and characterization of size-expanded “stretched-out” DNA bases (xDNA)18,19 that retain the recognition property of natural DNA. Theoretical studies have shown that these x-bases have more electron conjugation than the natural bases in the highest occupied molecular orbital (HOMO) and lowest unoccupied molecular orbital (LUMO), which in turn affects the value of the HOMO−LUMO gap.20−23 It was found that the expanded π conjugation could induce strong π−π coupling between stacked bases and base pairs,24 which would facilitate charge transfer through the double helix when the size-expanded DNA bases are incorporated.

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METHOD Geometry optimizations have been done with the B3LYP exchange-correlation functional29 in its restricted and unrestricted forms, employing the LANL2DZ and 6-31+G* basis sets for Au and the guanine/x-guanine, respectively. Frequency calculations at the same level were performed as well, to ensure that the equilibrium systems represent true minima on the potential energy surfaces. No symmetry constraint was imposed during the geometry optimizations. The basis set superposition error (BSSE) was corrected by using the counterpoise procedure of Boys and Bernardi.30 The natural bond orbital (NBO) analysis of charge population and other electronic properties were studied at the B3LYP/LANL2DZU6-311+ +G** level. All calculations have been performed with the Gaussian03 suite of codes.31 The total energies of all the investigated systems are reported in Table S5 of the Supporting Information. We remark that the use of a smaller basis set for structural optimization and a larger basis set to refine the analysis of the electronic structure is a validated procedure for several different materials and systems, both in plane-wave and localized basis sets.32−34 Topological properties of the electron density at the bond critical points (BCPs) of the NH···Au and OH···Au hydrogen bonds were characterized using the atoms in molecules (AIM)35 methodology at the B3LYP/LANL2DZU6-311+ +G** level, choosing the electron density (ρ) and the Laplacian (∇2ρ) of the electron density at the BCPs as criteria. This analysis was used to inquire on the nature of the unconventional hydrogen bonds in the complexes. In fact, in the AIM theory, the atomic and bond properties are defined on the basis of the electron charge density. In general, the sign of ∇2ρBCP is considered to relate to whether the atomic 24955

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Figure 1. Optimized geometry and isosurface plots (s = 0.02 a.u.) of frontier orbitals for the neutral G@Au3 (top) and G@Au4 (bottom) complexes. Color code: white hydrogen, gray carbon, blue nitrogen, red oxygen, yellow gold. Atom labels are defined as used throughout the text.

interaction possesses a dominant character of the sharedelectron (covalent) interaction (∇2ρBCP < 0) or of the closedshell interaction (∇2ρBCP > 0). A positive Laplacian is associated with electron depletion, and a negative Laplacian is associated with electron concentration. The AIM descriptors are listed in the Supporting Information (Table S2). To analyze and visualize the noncovalent interactions in these systems, the noncovalent interaction index (NCI) approach, developed by Yang et al., was adopted.36 In this approach, the reduced density gradient (RDG), defined as 1 4 RDG(r) = (1/(2(3π2) /3))((|∇ρ(r)|)/(ρ(r) /3)), together with the electron density ρ, was used to distinguish the covalent and noncovalent interactions. The noncovalent interactions could be isolated as regions with low density and low RDG. To identify the noncovalent interaction types, the sign of the second largest eigenvalue (λ2) of the electron density Hessian was utilized as a tool to distinguish bonded (λ2 < 0) from nonbonded (λ2 > 0) interactions. The functions RDG and sign(λ2)ρ were calculated with the Multiwfn software.37

Table 1. Some Key Features of Neutral G@Au3 and G@Au4 Complexes neutral G@Au3

Eba (kcal/mol) D(N3−Au1) (Å) ΔR(N9−H9) (Å) r(H9···Au) (Å) ∠N9−H9···Au2 (deg) Δυ (N9−H9) (cm−1) RIRb δσisoc

neutral G@Au4

this work

other theory4

27.2 2.164 0.010 2.810 163.2

20.9 2.146 0.010 2.841 161.8

181.8

181

6.4 −1.6

6.0 −1.8

this work Eb R(O6−Au4) (Å) ΔR(N2−H2) (Å) ΔR(N1−H1) (Å) Δυ(N1−H1) (cm−1) Δυ(N2−H2) (cm−1) RIR (N1−H1) RIR (N2−H1) Δσisoc (N1H) Δσisoc (N2H)

32.01 2.177 0.009 0.008 148.38 150.6 7.6 12.4 −2.4 −5.4

a The binding energy (Eb) includes the BSSE correction. It is computed as the total energy of the complex minus the total energies of the isolated guanine and cluster. bRIR is the ratio of the IR activities of the N−H stretching mode involved in the H bond in the complex and in isolated guanine cΔσiso is the NMR shift (in ppm) taken with respect to the isolated guanine and gold cluster.

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RESULTS AND DISCUSSION Structural and Electronic Properties of Neutral G@Au3 and G@Au4 Complexes. In an early investigation of the GC@Au4 complex, two gold atoms were bonded to the N7 site, and two other gold atoms were bonded to the N3 site of guanine.8 In other reports, individual Au atoms, as well as Au2 and Au3 clusters, were localized alternately near either of the nitrogen atoms in the nucleobase.38,39 We did not adopt any of these structures, because they cannot occur upon adsorption of guanine on gold surfaces or nanoparticles, which is our final target. Our initial neutral G@Au3/Au4 structures were taken from the most stable geometries in Kryachko and Remacle’s report.4 Our B3LYP/LANL2DZU6-31+G* optimized structures of the neutral G@Au3 and G@Au4 complexes are shown in Figure 1. The electronic ground state of the neutral G@Au4 and G@ Au3 complexes is singlet and doublet, respectively. Isosurface plots of the LUMO, HOMO, and HOMO-1 for the two complexes are also presented in Figure 1. In order to assess our method, the neutral G@Au3 complex was also optimized at the MP2/LANL2DZU6-31+G* level. On the basis of the geometries obtained at the higher computational level, we infer that the results captured by the B3LYP method are accurate (see the Supporting Information, Table S1). In Table 1, we present the structural data computed by us for the B3LYP/

LANL2DZU6-31+G* optimized geometries, along with reference data for G@Au3. We find the length of the N3−Au bond to be 2.164 Å, which is only 0.018 Å longer than in previous work.4 The tiny difference stems from the different basis sets for treating gold atoms and is not significant. The results reported in Table 1 overall demonstrate a good agreement with other theoretical data. According to six criteria, applied to hydrogen-bond formation, van der Waals (vdW) cutoff, red shift of infrared intensity (RIR), and downfield shift of nuclear magnetic resonance (σiso), Kryachko and Remacle found out that the unconventional NH···Au bonds obey all the necessary prerequisites of standard H bonds. On the basis of our results in Table 1, we draw the same conclusion. The results of the NBO analysis and the shape of the frontier molecular orbitals (Figure 1) indicate that each anchoring bond (N3−Au in G@Au3 and O6−Au in G@Au4) is obtained by charge transfer from the N or O lone pair (LP) to the antibonding (BD*) orbital of gold. Instead, each unconventional hydrogen bond (one in G@Au3, two in G@Au4) is characterized by charge transfer from the Ls of gold to the BD* orbital of the NH groups. The detailed perturbation theory 24956

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energy analysis is reported in Table S2 of the Supporting Information. The analysis of the charge density and its Laplacian at the bond critical points sheds more light into the nature of the unconventional hydrogen bonds in the complexes. Our results indicate that the (3, −1) CP exists in the NH···Au hydrogen bonds and in the N/O−Au bonds. It is easy to comprehend that the nature of the NH···Au is a hydrogen bond. What is the nature however of the N/O−Au bonds? To answer this question, we introduce the local energy density E(r) to distinguish the two types of bonds. The local energy density is related to the Laplacian of the electron density by the following equation: E(r) = (1/4)∇2ρ − G(r), where G(r) denotes the kinetic energy density, which is always positive. Generally speaking, a covalent interaction is characterized by a negative Laplacian, a negative E(r), and a large ρ. A closed-shell interaction is represented by a positive Laplacian, a positive E(r), and a small ρ. The intermediate regime is represented by a positive Laplacian, a negative E(r), and a moderate ρ. According to the sign of E(r), we could determine that the N/ O−Au bonds are covalent. To assess the bonding energy between nitrogen and gold atoms in the G@Au3 neutral complex, we artificially constrained the complex to a different geometry. Specifically, we moved the Au3 cluster so that the Au3 triangle becomes perpendicular to the guanine plane, without changing the internal geometry of the cluster and the guanine or the N3− Au1 distance. After this, the N9H···Au3 bond is broken while the N3−Au1 bond is kept. For this geometry, the BSSE corrected binding energy is 21.35 kcal/mol, so the approximate N9H···Au3 bonding energy is 5.85 kcal/mol. The BSSE corrected binding energy for the G−C base pair at the B3LYP/6-311++G**//B3LYP/6-31+G* is 28.4 kcal/mol, so the average contribution of each of the three hydrogen bonds in the G−C pair is about 9.5 kcal/mol. Hence, we find that the unconventional hydrogen bond in the neutral G@Au3 complex is weaker than that in a Watson−Crick H bond in the GC pair. It is noteworthy that, in the neutral G@Au4 complex, according to the AIM analysis, there is no hydrogen bond between N1H and the middle Au2 atom, namely, no (3, −1) BCPs. However, according to the same rule, we find a hydrogen bond between N1H and the Au4 atom. This is somewhat strange in terms of the atomic distances. In fact, the distance N1H···Au2 in the neutral G@Au4 complex is 2.875 Å, larger than the N1H···Au4 distance in the same complex but comparable to the N9H···Au2 distance in the G@Au3 complex, and the latter contact was found compatible with H bonding through the AIM analysis. To further explore the nature of the N1H···Au2 contact, we utilized Yang’s approach,36 according to which one can use the sign of λ2 to distinguish bonded (λ2 < 0) from nonbonded (λ2 > 0) interactions. The results of this analysis are presented in Figure 2. In the bottom of Figure 2, the gradient isosurfaces are colored according to the corresponding values of sign(λ2)ρ, which is found to be a good indicator of interaction strength. Large negative values of sign(λ2)ρ are indicative of attractive interactions (such as dipole−dipole or hydrogen bonding). Large negative values of sign(λ2)ρ are indicative of nonbonding interactions. Values of sign(λ2)ρ close to zero indicate weak van der Waals interactions. The visualization of the isosurfaces of the reduced density gradient is an effective tool that characterizes noncovalent interactions as distributed over broad regions of the real space, rather than simple pairwise contacts between

Figure 2. Isosurface plots of the electron density difference (top, s = 0.005 au) and of the reduced density gradient (bottom, s = 0.500 au) for the neutral G@Au3 and G@Au4 complexes. The green and cyan isosurfaces in the top plots identify the regions in which the electron density is increased and decreased, respectively, upon complex formation. The isosurfaces of the reduced density gradient in the bottom plots are colored according to the values of the quantity sign(λ2)ρ, and the RGB scale is indicated.

atoms. The isosurface plots shown in Figure 2 indicate the existence of a H bond between N1H and the Au2 atom in the neutral G@Au4 complex, which instead does not emerge from the BCP analysis. This is a genuine result of our work, which goes beyond previous descriptions. Essentially, we find that Yang’s approach performs better than AIM theory in treating this system, and this conclusion was proved recently.40 The blind point of AIM in the description of the G@Au4 complex may arise from the use of pseudopotientials.41 If electron transfer occurs during the formation of the complex from the isolated components, this can be inspected by visualizing the electron density difference, namely, the total charge density of the complex minus the electron density of the gold cluster and the guanine molecule in their standalone states. This is shown in the top of Figure 2. We find that, in the neutral G@Au3 complex, the charge variation is mostly due to the covalent N3−Au1 bonding, with minor contributions from the hydrogen bonds. According to the NBO analysis, the amount of charge transfer from the guanine molecule to the gold cluster is −0.117e and −0.073e in G@Au3 and G@Au4, respectively. Namely, during complex formation, electrons are transferred from the molecule to the cluster. The amount of electronic charge transferred to the Au3 cluster is larger than that transferred to the Au4 cluster. This difference can be ascribed to the different anchoring sites in the two complexes. In the G@ Au4 complex, the gold cluster anchors to the oxygen atom of guanine, which has larger electronegativity than the nitrogen anchoring site in the G@Au3 complex. Furthermore, the amount of charge transfer has the same trend as the electron affinity (EA) of the Au3 (3.85 eV) and Au4 (2.77 eV) clusters.42 Our result obtained by the NBO method is consistent with the statement found elsewhere that “gold clusters with an odd number of atoms are better electron acceptors and better electron donors than clusters with an even number of atoms.”9 However, a different picture is obtained through the Mulliken population analysis, according to which the value of charge transfer is −0.187e and −0.602e in the G@Au3 and G@Au4 complexes, respectively (Figure S2, Supporting Information). This erroneous behavior could be due to the high sensitivity of Mulliken charge population analysis to the choice of basis sets, 24957

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Figure 3. Geometry and isosurface plots of frontier orbitals for the anionic G@Au3− (top) and G@Au4− (bottom) complexes.

bond, because the gold cluster slides to the N1 and N2 sites of guanine. Hence, there is only hydrogen bonding in the G@ Au4− cluster, no covalent bonding. It should be noted that both anionic complexes keep a nonplanar geometry (Figure S5, Supporting Information). The analysis of the frontier molecular orbitals (Figure 3) indicates that both HOMO and LUMO in the anionic complexes are localized on the gold cluster moiety, which could be expected on the basis of the large electron affinity of the gold cluster. The NBO charge population analysis shows that the amount of gold-localized charge in the G@Au3− and G@Au4− complexes is −0.927e and −0.936e, respectively (the BCP analysis is reported in Table S4 in the Supporting Information). Also, in this case, we find a blind point among the BCPs, which can be corrected through Yang’s approach; in fact, Figure 4 shows the existence of a hydrogen bond between N2H and the Au2 atom in the G@Au4− anionic complex.

especially for large basis sets with diffuse functions, such as the 6-311++G** set that we adopted. Structural and Electronic Properties of Anionic G@ Au3− and G@Au4− Complexes. It is well known that a small gold cluster has a large electron affinity, which means that it would like to accept an excess electron to be in a more stable ́ anionic state. In 2009, Martinez investigated anionic gold clusters attached to an adenine−uracil base pair and obtained some interesting conclusions.42 Based on the results presented above for the neutral clusters, we now want to explore whether the excess electron would increase or decrease the binding between gold clusters and the guanine molecule and modify the process of charge transfer in the system. We optimized the atomic coordinates of the G@Au3− and G@Au4− complexes starting from the equilibrium structures of the corresponding neutral complexes, with one net negative charge added to each system. The optimization process was implemented at the B3LYP/LANL2DZU6-31+G* level as used in the neutral complexes. The BSSE corrected binding energy is 14.24 and 15.37 kcal/mol for the G@Au3− and G@Au4− complex, respectively. These values are about 50% smaller than those found for the neutral complexes. It means that the excess electron decreases the binding strength, in agreement with previous indications for different nucleobases.29 The optimized geometries and frontier orbital plots are presented in Figure 3. In the G@Au3− complex, the shape of the gold cluster changes from triangular to linear: the angle between the three gold atoms is 178.5°. The distances between gold atoms and the neighboring hydrogen and nitrogen atoms are reported in Figure 3. The N3−Au1 distance increases significantly as compared to neutral G@Au3, by about 1.25 Å. The N9H···Au2 distance increases by 0.2 Å, and another N2H···Au3 hydrogen bond forms. To determine the binding energy of the elongated N3−Au1 bond, we adopted the same procedure as described for the neutral complexes, namely, we rotated the gold rod 90°, while keeping the coordinates of guanine and of the Au1 atom fixed. Thus, the gold rod becomes perpendicular to the guanine plane and the H bonds are broken. The BSSE corrected binding energy for this structure is 9.56 kcal/mol, which is significantly smaller than its counterpart in the neutral complex (21.53 kcal/mol). Therefore, the elongated N3−Au1 bond in the G@Au3− complex is weaker by ∼12 kcal/mol than the corresponding bond in the neutral G@Au3 complex. In the G@Au4− anionic complex, the T shape of the gold cluster does not change significantly as compared to the G@ Au4 neutral system. However, the relative cluster/guanine orientation changes. We do not find in G@Au4− the O6−Au1

Figure 4. Isosurface plots of the density gradient (s = 0.500 au) for the anionic G@Au3− (left) and G@Au4− (right) complexes. The isosurfaces of the reduced density gradient are colored according to the values of the quantity sign(λ2)ρ, and the RGB scale is indicated.

To summarize the main differences between the anionic and neutral complexes with the same atomic composition, we note that the excess electron (i) destroys the triangular shape of the Au3 cluster, while it has little influence on the T shape of the Au4 cluster and (ii) makes the complexes less stable by breaking the O6−Au bond in G@Au4− and weakening the N3−Au interaction in G@Au3−. Moreover, because of the large electron affinity, the excess electron almost localizes on the gold cluster moiety in the anionic complexes. In the Supporting Information, Table S6, we report geometrical parameters for the gas-phase neutral and anionic guanines and compare the behavior of the complexes to that of the molecules upon the addition of one electron. Structural and Electronic Properties of Neutral xGn@ Au3 (n = 4, 6, and 8) Complexes. Three initial structures were designed for the xG4@Au3 complex (see Figure 5): the 24958

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Figure 6. Geometries of (a) the neutral gas-phase xG6 molecule and (b−d) the neutral xG6@Au3 complexes. Panel c illustrates the lowestenergy xG6@Au3 complex after atom relaxation.

Figure 5. Geometries of (a) the neutral gas-phase xG4 molecule and (b−d) the neutral xG4@Au3 complexes. Panel b illustrates the lowestenergy xG4@Au3 complex after atom relaxation.

Au3 cluster has a triangular shape; one Au atom binds to either N7 (Figure 5b) or N3 (Figure 5c, d). A NH···Au hydrogen bond was designed in all the initial structures. After atomic optimization, we could not obtain a stable isomer with gold attaching to the oxygen atom of xG4. The three optimized isomers for the xG4@Au3 complex are shown in Figure 5, along with optimized gas-phase xG4. It should be noted that, for the complexes in which the gold−molecule contact is through the N3 site of xG4 (Figure 5c, d), the initial geometries are essentially maintained, including the presence of the NH···Au hydrogen bond. However, for the complex in which the gold− molecule contact is through the N7 site of xG4, after optimization, the NH···Au hydrogen bond is broken. Among the three xG4@Au3 isomers, the one of Figure 5b has the lowest total energy, which could be partly explained by the torsion of the xG4 molecule. The xG4 molecule in the gas phase is not exactly planar, with a 166.9° folding angle. The folding angles of xG4 in the three xG4@Au3 isomers are 168.9°, 169.6°, and 173.3°, respectively. The BSSE corrected binding energy for it is 27.90 kcal/mol. The energy difference between isomers c and d is only 0.19 kcal/mol. The fact that the most stable xG4@Au3 isomer is the one in which the gold−molecule contact is through the N7 site of xG4 and no unconventional hydrogen bond is formed contradicts the expectation that NH···Au hydrogen bonding would reinforce the N/O−Au bond during the combination of cluster and molecule, as we found in the G@Au3 cluster with natural guanine. We infer that this peculiar behavior of xG4 in complex formation with a small gold cluster is due to the steric effect caused by the spacer ring. In order to confirm our speculation, we also considered the complex formation between Au3 clusters and expanded guanines with different spacer rings, namely, xG6 and xG8.26 The names of xG with spacer rings of different symmetries were defined elsewhere,26 and we follow the same labeling rules. Compared with xG4, one NH is replaced by oxygen in the spacer ring of xG6. Introducing one oxygen atom in the spacer ring could in principle increase the planarity, but in our results, the optimized xG6 is still not planar. xG8 has instead a fivemembered spacer ring, which should also facilitate planarity. Interestingly, xG6 has the second lowest HOMO−LUMO gap in the series of size-expanded guanines.26 We obtained three stable isomers for each of the xG6@Au3 and xG8@Au3 complexes, as shown in Figures 6 and 7,

Figure 7. Geometries of (a) the neutral gas-phase xG8 molecule and (b−d) the neutral xG8@Au3 complexes. Panel b illustrates the lowestenergy xG8@Au3 complex after atom relaxation. This complex has the highest binding energy of all the computed xG@Au3 complexes.

respectively. The isomer in Figure 6c is the most favorable among the three xG6@Au3 complexes. The BSSE corrected binding energy is 27.04 kcal/mol, which is very similar to the binding energy of the lowest-energy xG4@Au3 cluster (lower by less than 1 kcal/mol). The binding pattern is also similar, with gold−molecule contact occurring at the N7 site of xG6. The isomer in Figure 7b is the most favorable among the three xG8@Au3 complexes. The BSSE corrected binding energy is 30.42 kcal/mol, which is higher than that of xG4@Au3 by 2.52 kcal/mol. In this structure, due to the overall good planarity and a reduced steric hindrance, a NH···Au can be established to reinforce the N−Au covalent bonding. The xG8@Au3 complex has the largest binding strength of all the xG@Au3 sampled complexes because of the minor molecular torsion, which in turn enables the formation of a NH···Au hydrogen bond. The HOMO−LUMO gap for the three xG4@Au3 isomers (b, c, and d) is 2.40, 2.22, and 2.45 eV, respectively, which is slightly lower than that of the G@Au3 complex (2.46 eV). The HOMO and LUMO isosurfaces for the most stable xG4@Au3, xG6@Au3, and xG8@Au3 isomers are shown in Figure 8. Comparing the three types of novel size-expanded guanine molecules, we can draw some interesting conclusions. Although the NH site in the spacer ring may supply a new opportunity for forming NH···Au hydrogen bonds in complexes of sizeexpanded guanine with small gold clusters, this does not occur, because of significant steric effects that hinder further 24959

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NH site in the spacer ring may supply a new opportunity for forming a NH···Au hydrogen bond, it is not effective because of the large steric effect. The introduction of the spacer ring decreases the HOMO−LUMO gap and expands the πconjugation area, while increasing the steric hindrance. The size-expansion design would make the adsorption process between DNA bases and gold surface/nanoparticle more orderly. This property, together with the reduced HOMO− LUMO gap and high charge conjugation that likely enhance electron transfer, makes xG an appealing candidate for molecular electronics applications.

Figure 8. Isosurface plots of the HOMO and LUMO for the most stable neutral isomers of xG4@Au3, xG6@Au3, and xG8@Au3.

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molecule−gold contacts. The introduction of a spacer ring in guanine is an effective tool to decrease the HOMO−LUMO gap and expand the π-conjugation area. These electronic effects were already discussed by other authors.21−24 The new characteristic that we find in our work, namely, the enhanced steric hindrance, may have other appealing consequences for surface-immobilized DNA-based devices. In fact, our results indicate that the size-expanded guanine molecule favors an adsorption orientation on gold that conduces to π−π stacking, rather than a configuration that maximizes the number of point contacts. The size-expanded design would make the adsorption or assembly process between DNA bases and gold surface/ nanoparticle more orderly. As a consequence of all of this evidence, we suggest that the new designed size-expanded guanine molecules should have an optimal performance in DNA-based devices because of (1) the good inherent charge transfer24 capabilities imparted by the low HOMO−LUMO gap and large π-conjugation area and (2) the highly uniform adsorption orientation caused by the enhanced steric hindrance. The latter issue deserves further attention and is the object of ongoing studies. It means that not only the inherent molecular properties are important to develop molecular devices but also the interaction of the molecules with the inorganic components. Both aspects can be exploited to improve the current state-of-the-art.

ASSOCIATED CONTENT

S Supporting Information *

More details on the atomic structures and on the electronic properties. This material is available free of charge via the Internet at http://pubs.acs.org.

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AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected] (R.D.F.); wenming.sun@ unimore.it (W.S.). Phone: +39-059-205-5320. Fax: +39-059205-5651. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work was funded by the European Commission through project “DNA-Nanodevices” (contract no. FP6-029192), by the ESF through the COST Action MP0802, by the Italian Institute of Technology through project MOPROSURF and the Computational Platform, by Fondazione Cassa di Risparmio di Modena through Progetto Internazionalizzazione 2011. The ISCRA staff at CINECA (Bologna, Italy) is acknowledged for computational facilities and technical support.

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SUMMARY We investigated the nature of the interaction between the guanine molecule and small gold clusters. Our results reveal that the nature of N/O−Au bonds is covalent, with lone pair (LP) electrons of O and N atoms transferred to the antibonding (BD*) orbitals of gold. This covalent bonding is reinforced by the NH···Au unconventional hydrogen bonding. The H bonding may be relevant for adsorption of DNA bases at gold nanoparticles and defective surfaces. When an excess electron is injected into the system, the extra electron localizes on the gold cluster moiety with significantly change of the geometry and reduction of the binding energy. Because of the use of pseudopotentials for treating the core electrons of the gold atoms, blind points occur in BCPs from the AIM theory analysis, while this shortcoming is overcome by the NCI approach developed by Yang’s group. This is an important result of our work: on one hand, the NCI approach sheds light on the interaction mechanisms, to an extent beyond the level of understanding reached before for similar systems; on the other hand, it has methodological implications, meaning that one should be cautious when analyzing electronic structure descriptors. We also surveyed the interaction between the Au3 cluster and three size-expanded guanine molecules with different symmetries (xG4, xG6, and xG8). The results reveal that, although the

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