Conductance through Short DNA Molecules - American Chemical

Feb 7, 2011 - approach was used by Kasumov et al.,1 and superconducting ... to provide answers for the conductance mechanism, through- bond or ...
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Conductance through Short DNA Molecules Aleksandar Staykov, Yuta Tsuji, and Kazunari Yoshizawa* Institute for Materials Chemistry and Engineering and International Research Center for Molecular Systems, Kyushu University, Fukuoka 819-0395, Japan

bS Supporting Information ABSTRACT: The conductance through short DNA molecules connected to gold electrodes is studied with density functional theory and nonequilibrium Green’s function method combined with density functional theory. The anchoring of the molecules to the electrodes is investigated, and in addition to the covalent SAu bond, weak interactions between the aromatic heterocyclic bases and the electrodes are found. These weak interactions are important for the electron transport through DNA molecules. A tunneling mechanism is suggested, and the conductive properties of the nucleotides in a metal-molecule-metal junction are compared. Different four-nucleotide DNA sequences are investigated. A significant value for the current, 20 pA, is calculated for 1.5 V applied bias for a DNA sequence consisting of guanine and cytosine nucleotides. It is shown that adenine-thymine nucleotide pairs introduce potential barriers for the electron transport and therefore significantly decline the conductance. The obtained results are compared with recent experimental observations (Nanotechnology 2009, 20, 115502) and confirm the possibility for electron transport through DNA molecules as well as provide an explanation for the reduced conductance through DNA sequences, which contain adenine-thymine nucleotide pairs. The results are compared with a previous theoretical study, performed with the extended H€uckel method (ChemPhysChem 2003, 4, 1256), which reports low conductance for DNA molecules. The difference in the conclusions is due to the applied bias self-consistent field calculations used in the recent study, which take into account the changes of the transmission probabilities with the bias.

1. INTRODUCTION The electron transport through the DNA molecule is unspecific and unrelated to its biological functionality phenomenon, which has attracted significant scientific attention in the past decade. DNA conductance was measured experimentally1-7 and investigated theoretically8-12 at different levels of theory. Contradicting results for its electron transport properties were reported. The obtained experimental data vary from good conducting properties2,3,5 and superconductivity1 to semiconducting behavior4 and a large band gap insulator.13-15 Different techniques were applied in the experiments leading to different experimental results. The electrodes were often fabricated using electron-beam lithography followed by subsequent liftoff5,14 or a mechanically controllable break junction technique.1,2,16 These methods are capable of producing a nanogap, which varies from a few hundred5,14 to less than 10 nm.2,4 The actual trapping of DNA molecules within the nanogap is verified with the atomic force microscope techinique14 or the scanning electron microscope technique.4 Experiments were carried out for DNA molecules with different lengths,1,4,14 nucleotide sequences,2,14,15 and electrode-molecule connecting sites.3 Among the different authors exists increasing consensus about the length dependence of the conductance. Long DNA molecules exceeding 40 nm are considered to be insulators14,15 while shorter DNA molecules show significant conductance.1,2,4 However, exceptions were reported; de Pablo et al.13 obtained resistance of 3 GΩ for 2 V r 2011 American Chemical Society

applied bias for a 10 nm long DNA molecule, while Okahata et al.3 reported good conductance for DNA molecules exceeding 100 nm. The length dependence of DNA conductance is an important clue for the nature of the electron transport mechanism. A coherent-tunneling transport mechanism is characterized with significant length dependence of conductance, while an incoherent hopping mechanism has small length dependence.9,17 The conflicting experimental data show that neither of the mechanisms can be neglected; however, the length dependence suggested in most experimental works favors the coherenttunneling electron transport.1,2,4,14,15 The analysis of the experimental data shows that beside the DNA length the anchoring site between the molecule and the electrodes plays an important role. Okahata et al.3 have shown 2 orders of magnitude resistance difference for DNA molecules oriented parallel and perpendicular to the electrodes. They have concluded that DNA molecules can conduct along the double helix axis, while perpendicular to it the DNA is an insulator.3 The actual bonding of the DNA molecule to the electrodes is crucial for the obtained conductance. Inappropriate bonding can result in insulating contact.15 Two main techniques were employed in the experimental studies. The first is direct physical contact with Received: November 12, 2010 Revised: January 11, 2011 Published: February 07, 2011 3481

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The Journal of Physical Chemistry C the electrodes resulting in weak adhesion between the DNA and the metal electrode surface.1,4,15 This method was applied by Porath et al.4 who reported semiconductive properties with a well-defined conductive high-bias region over 1.5 V. The same approach was used by Kasumov et al.,1 and superconducting properties of 10 nm long DNA were reported. A disadvantage of the weak adhesion bonding is the possible insulating barrier between the DNA and the electrodes15 and the difficult reproduction of the results, due to the difficulty to achieve the same binding between the molecule and the electrodes. To obtain reproductive results, the bonding between the metal and the molecule should be strong enough to withstand the shear forces and to survive the experiment.15 The second approach is to introduce chemical binding between the DNA molecule and the electrodes.2,5,14,15 This can be achieved with propanethiols or hexanethiols connected to the free ends of the molecule. Gold is often used as an electrode,2,5,14,15 and organic thiols are known to build strong covalent bonds to the Au surface.18-21 Conflicting results for the conductance achieved with the SAu bonds were reported. Dulic et al.2 reported good conductance of short DNA molecules attached to Au electrodes with propanethiols in mechanically controllable break junction measurements. However, Storm et al.14 reported insulating properties for DNA molecules attached to Au electrodes with hexanethiols. Zhang et al.15 suggested that the propane and hexane spacers introduce insulating barriers and proposed direct binding of the DNA molecule through S-Au bonds to the gold surface; nevertheless, they obtained insulating properties. A theoretical study of DNA by Tada et al.,11 performed with the extended H€uckel method,22 reported strong conductance dependence from the connecting site. DNA molecules connected to the electrodes through their sugar-phosphate skeleton showed insulating properties.11 That result led to a conclusion that the conductance cannot be achieved through the σ-bond network. DNA molecules connected to the electrodes through the nucleotide bases showed semiconductive properties for applied biases in the range from 4 to 6 V.11 The conductance was achieved through the π-π stacked nucleotide bases. In the experiments,2,5,14,15 the molecules were attached to the electrodes with thiolate bridges connected to the DNA’s deoxyriboses, which should make them potential insulators.11 Despite the important qualitative results, which were obtained with the extended H€uckel theoretical study,11 the method lacks an adequate description of the electrode-molecule coupling and electronic interaction, which would improve the quality of the obtained results. First-principle quantum mechanical calculations and geometry optimization of the bonding site between the DNA molecule and the electrodes would provide important insight into the anchoring sites. Such a theoretical study can provide answers for the binding conditions, which can favor the conductance through DNA molecules. Another important factor for the conductance through DNA molecules is the nucleotide sequence. Several studies reported that DNA conductance is achieved mainly through guanine, due to its lowest ionization potential among the four nucleotides,23 good π-electron delocalization,9 and hole trapping structural distortions.8 A recent study of Dulic et al.2 reported significant conductance difference for short, 12-nucleotide DNA molecules containing more guanine-cytosine base pairs compared to those containing more adenine-thymine base pairs. Because of the short size of the molecules, the coherent-tunneling conductance mechanism can be suggested.17 A theoretical study of tunneling electron transport through short DNA molecules would be able

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to provide answers for the conductance mechanism, throughbond or through-space conductance, as well as to provide explanations for the increased resistance through the adenineand thymine-rich DNA molecules. The obtained theoretical results can be compared with the reported experimental data because of the conceptual similarities between the nonequilibrium Green’s function (NEGF) theory and the mechanically controllable break junction technique.2,16,24 The DNA conductance contributed to DNA analysis23,25 and offered applications of DNA molecules, different from the main information storage purpose.26 The one-dimensional DNA double helix has two bond networks spread throughout the length of the molecule. These are the σ-bond network of the sugar-phosphate skeleton and the intermolecular π-π stacked bases’ p-σ bond network. Each of these polymeric networks could rise conductance bands responsible for the long-distance transport.27 However, the sugar-phosphate skeleton conductance was ruled out by the theoretical studies.11,13 In the last decades, the π-π stacked polycyclic aromatic hydrocarbons’ conductance was investigated intensively, and semiconducting properties were reported in the literature.28 The DNA π-π stacked aromatic bases represent such one-dimensional polymers, to which are addressed the main computational efforts on DNA electron transport.11,13 The aim of this study is to investigate theoretically the coherent-tunneling electron transport in short DNA molecules, whose conductance was measured recently.2 Another important point is to estimate the reasons for the different conductance through DNA molecules rich in guanine and cytosine bases compared to those rich in adenine and thymine bases. On the basis of these results, we can make a conclusion for the type of electron transport through short DNA sequences. The clarified DNA conductance mechanism may significantly improve our understanding for the conductivity of complex bioorganic polymers. Such an electron-transport study would be beneficial for the fields of bioelectronics and nanoelectronics. These fields are expected to play a significant role in the electronic industry once the borders of the nowadays widely used silicon-based conducting and semiconducting devices are reached.29 In the present work, we investigate the bonding of the DNA molecule through a propanethiol spacer to the Au surface, the coherent electron transport through short, 4 nucleotide, DNA sequences, and the conductance through each single nucleotide.

2. COMPUTATIONAL DETAILS The study of conductance through short DNA molecules was performed in the framework of the density functional theory (DFT) formalism. DFT offers adequate descriptions of crucial factors for the understanding of electron transport such as geometry optimization, a realistic molecule-electrode coupling model, electron correlation, and correct estimation for the Fermi energy of the electrodes and the molecular orbital (MO) levels of the bridging molecule. Combined with the nonequilibrium Green’s function theory (NEGF-DFT) and Landauer’s formalism, it is a powerful tool for calculation of transmission probability in the electrode-molecule-electrode junctions.16,24,30,31 The transmission probabilities and transmission spectra calculated with NEGF-DFT can clarify the conductance mechanism and the molecular levels, which participate in the electron transport. The peaks in the transmission spectra can provide information for the type of the electron transport: a through-bond tunneling characterized 3482

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The Journal of Physical Chemistry C with broad peaks or through-space resonance tunneling characterized with sharp narrow peaks.24,32 The self-consistent field NEGF-DFT calculation can be performed for applied biases, and thus with the use of Landauer’s formula the current through the junction can be calculated.16,24,30 The calculated current for different applied biases allows us to build the conductance I/V curves, from which we can obtain the electronic properties of the junction, i.e., conductor, semiconductor, or insulator. In addition, we can estimate the junction’s resistance and compare the electron-transport properties for different molecules. The spatial distribution of the molecular orbitals in the junction environment provides evidence for the conductance channels.32 Delocalized orbitals provide effective through-bond conducting channels characterized with broad peaks in the transmission spectra, while localized orbitals are responsible for the resonance throughspace tunneling characterized with sharp narrow peaks.24,32 Orbital analysis has another importance for the proper understanding of molecular conductance. We have shown that the phases and amplitudes on the connecting atoms between the molecule and the electrodes are the discrete chemical property, which governs the probability for electron transport.33 The B3LYP method was used to optimize the geometry of the deoxyribose-propanethiol bond to the gold surface and to verify the existence of σ-type bonding between p-orbitals of the nucleotide bases and d-orbitals of the Au surface.34-36 The geometry optimization was performed for the cytosine nucleoside, deoxycytidine, connected to a cluster of 17 Au atoms with a (111) surface. We applied the 6-31G basis set to all atoms except Au.37 Polarization functions were added to the heavy elements such as C, N, O, and S to improve the estimation of the interaction between the aromatic base atoms and the Au surface. Polarization functions were not added on the H atoms because the model we considered was a single nucleoside, and hydrogen bonds or hydrogen abstractions were not expected. In addition, a single-point calculation was performed for the optimized geometry with diffuse functions added to the heavy atoms. The Au atoms were described with the LANL2DZ basis set for which pseudopotentials were employed. The coordinates of all Au atoms were kept frozen during the optimization. Single-point energy calculations were performed for different sequences of four-nucleotide DNA molecules with the B3LYP method and the 6-31G basis set with polarization on both the heavy elements and hydrogen atoms. In this case the hydrogen bonds between the adenine and thymine as well as between guanine and cytosine were considered. We also considered the intermolecular π-π stacking of the nucleotides within the DNA double helix.38 Geometry optimization and single-point energy calculations were performed with the Gaussian 03 program package.39 Electron transport calculations were performed with the NEGF-DFT method implemented in the ATK program package.24,40 The method allows complete self-consistent field treatment of an electrode-molecule-electrode junction for zero bias and applied biases and incorporates the effect of the external electric field induced from the electrodes on the molecule. The Perdew-Zunger local density approximation method41 was used with single ζ basis set (SZ) for Au atoms and double ζ basis set with polarization (DZP) for all other atoms.24,40 Calculations with the DZP basis set for all atoms were performed for a smaller molecule and crosschecked with the results obtained with the SZ basis set for the electrodes’ atoms. The calculated I/V curves were qualitatively similar. The semi-infinite left and right

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Figure 1. Geometry of the central region of the electrode-moleculeelectrode junction used for electron transport calculations with the ATK program. The model consists of two layers from each of the electrodes and the heterocyclic bases from the nucleotides of the 30 -CCGG-50 DNA sequence. For simplicity, the sugar-phosphate skeleton is omitted in the electron transport calculations.

electrodes were modeled by two Au(111)-(6  6) surfaces (i.e., each layer includes 36 Au atoms). Two layers from each electrode (in total 144 Au atoms) were included in the central region. The complete model, which includes a four-nucleotide DNA sequence and the sugar-phosphate skeleton of the DNA double helix, turned to be complicated from a technical point of view for the electron-transport calculations. The demands for dynamic memory, CPU power, and time requirements significantly exceeded the usual computational equipment, which resulted in simplification of the calculation model. For simplicity, in our model we removed the sugar-phosphate skeleton and performed the NEGF-DFT calculations on the π-π stacked sequence of four-nucleotide base pairs. In this model the base pairs have their original positions from the DNA molecule and are situated at 3.5 Å parallel to each Au surface. In addition, we performed applied bias calculations to these models to build the I/V curves and compare the relative conductance of different sequences. The model of the central region, used for the electron transport calculations, is shown in Figure 1. The simplification of the model is justified from the results in the study of Tada et al.,11 performed with the extended H€uckel method, which has shown that the conductance is achieved through the π-π stacked bases, while the sugar-phosphate skeleton has insulating properties.

3. RESULTS AND DISCUSSION 3.1. Geometry Optimization of Deoxycytidine on a Gold Cluster. The actual bonding between the surfaces of the elec-

trodes and the DNA molecule is crucial for its conducting properties.15 Conductance can be achieved as a result of good overlapping between the orbitals of the electrodes with welldelocalized orbitals of the molecular wire, which have large amplitudes on the connecting sites.33 Experimental studies suggested a covalent S-Au bond that can survive the shear forces during the measurement.2,5,14,15 The sulfur atom is connected to the molecule through a propanethiol or hexanethiol spacer bonded at the free 30 end of the DNA molecule. The frontier orbitals of saturated aliphatic chains are localized on the σ-bonds and do not provide good conductance channels. It was suggested that such aliphatic chains would introduce an insulating barrier and significantly hinder the conductance.15 In our 3483

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Figure 2. Optimized geometry and highest occupied orbitals of deoxycytidine attached by propanethiol to a gold cluster of 17 Au atoms.

study, we optimize the geometry of deoxycytidine attached to a cluster of 17 Au atoms through a S-Au bond and propanethiol spacer. This theoretical model is identical to the experimental conditions in the paper of Dulic et al.2 A B3LYP hybrid functional was used with the 6-31G(d) basis set for H, C, N, O, and S atoms and the LANL2DZ basis set for Au atoms. The coordinates of the Au atoms were kept frozen during the optimization. Single-point calculation was performed for the optimized geometry with diffuse functions added to the heavy atoms (C, N, O, and S). Results of the geometry optimization are summarized in Figure 2. The cytosine base is situated at 3.5 Å nearly planar to the gold surface. The deviation of planarity is mainly due to the stronger interaction of the heteroatoms from the aromatic ring with the surface. This deviation should be avoided in the double helical structure because of the hydrogen bonds with the second nucleotide. Geometry optimization shows that the purpose of the propanethiol spacer is to introduce flexibility in the orientation of the nucleoside instead of increasing the distance between the nucleoside and the surface. Figure 2 shows the four highest occupied frontier orbitals, which are, to a large extent, responsible for the electron density distribution between the molecule and the surface. The spatial distribution of these four orbitals justifies our assumption for two major simultaneous interactions between the molecule and the surface. The first covalent S-Au interaction is responsible for the attachment of the molecule to the surface. The flexible propane spacer allows favorable orientation of the nucleoside by allowing the aromatic ring to arrange parallel to the surface. That parallel arrangement provides favorable conditions for the formation of a second weak molecule-surface interaction, which can be seen in all four frontier orbitals. This weak molecule-surface interaction is similar to the Au-nanographene stacking, used for the experimental fabrication of nanosize diodes and transistors,42 and it can provide a good connecting point for electron transport through the DNA molecule. The geometry optimization shows that the insulating barrier between the surface and the molecule, which should be introduced by the aliphatic spacer, would not affect significantly the conductance due to the second weak molecule-surface interaction, which is a favorable conductance connecting point. The aromatic ring-surface distance of 3.5 Å is optimal for adsorption of polycyclic aromatic hydrocarbons on the Au surface, and it was experimentally shown that electron transport could be achieved through such weak molecule-surface bonds.42 Similar geometry optimization was performed for deoxyguanosine attached to a cluster of 25 Au atoms through a S-Au bond and propanethiol spacer. The B3LYP hybrid functional was used with the 6-31G(d) basis set for H, C, N, O, and S atoms and

the LANL2DZ basis set for Au atoms. The coordinates of the Au atoms were kept frozen during the optimization. Single-point calculation was performed for the optimized geometry with diffuse functions added to the heavy atoms (C, N, O, S). The purpose of this calculation was to compare the molecule-surface interactions for the nucleosides with purine bases, i.e., adenine and guanine, to those with pyrimidine bases, i.e., cytosine and thymine. The purine bases differ from the pyrimidine bases with their electron-rich five-membered rings. The geometry optimization of deoxyguanosine shows very similar structure to that of the optimized deoxycytidine with an aromatic ring-surface distance of 3.5 Å. 3.2. Frontier Orbitals of Insulated Four-Nucleotide DNA Sequences. Highest occupied and lowest unoccupied orbitals can provide important qualitative information for the conductance of metal-molecule-metal junctions. For most organic wires, the Fermi energy of the Au electrodes is situated within the HOMO-LUMO gap which makes the nearest in energy orbitals most suitable for conductance channels. The Fermi energy of the electrodes is -5.31 eV and is estimated with separate periodic calculation of bulk gold. Besides the energy, the spatial distribution of the frontier orbitals is another important factor that provides qualitative information for the conductance. Orbitals’ delocalization is related to the spatial electron density distribution and provides qualitative explanation for the through-bond electron transport. Orbitals of the insulated molecule can be compared and can help in the understanding of the molecular orbitals perturbed by the electrodes within the junction environment. In this work, we investigate the electron transport through two four-nucleotide, double helical DNA sequences. The first contains only guanine (G) and cytosine (C) bases in the following order: 30 -CCGG-50 . Its complementary chain has the following order: 50 -GGCC-30 . It was shown that short DNA molecules containing a high concentration of guanine and cytosine are characterized with good conductance.2,8 The second DNA sequence contains also adenine (A) and thymine (T) in the following order: 30 -CAAG-50 . Its complementary chain has the following order: 50 -GTTC-30 . Short DNA molecules, which contain more adenine and thymine bases, are reported to show poor conductance.2 Figure 2 shows that in the experimentally described model2 two bonding sites exist between the molecule and the surface, a covalent S-Au bond and a weak moleculesurface bond. A previous theoretical study suggested that the conductance could be achieved exactly through such weak molecule-surface bonds.11 It was reported that the conductance channels were the occupied orbitals, while the contribution of the unoccupied orbitals was neglectable.11 Our goal is to analyze the possible conductance channels by looking into the spatial 3484

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Figure 3. Highest occupied orbitals of the insulated 30 -CCGG-50 DNA sequence. Gold electrodes are not considered. All energies are in absolute values.

Figure 4. Highest occupied orbitals of the insulated 30 -CAAG-50 DNA sequence. Gold electrodes are not considered. All energies are in absolute values.

distribution of the molecular orbitals close to the Fermi energy and compare the orbitals’ delocalization of both investigated DNA sequences. We consider the highest-occupied orbitals because it was suggested that the conductance was achieved through them.11 Due to the large size of the molecules, only single-point energy calculations were performed. A B3LYP hybrid functional was used with the 6-31G(d, p) basis set. The obtained eight highest-occupied orbitals of 30 -CCGG-50 are shown in Figure 3. As expected, no delocalized orbitals are calculated for the sugar-phosphate skeleton, and there are no significant orbitals’ amplitudes at the connecting 30 sites. Thus, it is unlikely to expect significant electron transport though the covalent σ-bonds.33 Large orbital amplitudes are calculated for the terminating aromatic heterocyclic bases of HOMO, HOMO5, and HOMO-6, which are the second connecting site characterized with weak molecule-surface bonds. In several theoretical studies, it was shown that large orbital amplitudes at the connecting sites play a crucial role in the electron transport.33,43,44 Thus, there is a high probability to observe electron transport through the π-π stacked bases of the 30 -CCGG-50 DNA molecule. The HOMO is the closest occupied orbital to the

Fermi level. It is characterized with orbital amplitudes on the terminating bases as well as on the inner bases. This good delocalization along the π-π stack suggests a through-bond conducting channel. HOMO-5 and HOMO-6 are also well delocalized along the π-π stacks and are considered as good through-bond conducting channels. In Figure 4 are shown the calculated eight highest occupied orbitals of 30 -CAAG-50 . The main difference between the HOMOs of 30 -CCGG-50 and 30 -CAAG-50 is in the orbitals’ amplitudes within the two inner nucleotide pairs. While significant amplitudes were calculated for the 30 -CCGG-50 sequence, in the case of the 30 -CAAG-50 sequence no amplitudes were calculated for the adenine and thymine nucleotide pairs. The delocalization of the frontier orbitals is important for the electron transport properties. In the case of 30 -CAAG-50 , the inner pairs introduce an effective potential barrier, and the electron transport can be achieved only after resonance tunneling through this barrier. The highest well delocalized orbital along the π-π stack orbital of 30 -CAAG-50 is HOMO-6. Its energy is lower than the conductance channels of 30 -CCGG-50 (i.e., HOMO, HOMO-5, and HOMO-6), and electron transport through it would require 3485

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Figure 5. Transmission spectra obtained from the zero-bias calculations for the investigated electrode-molecule-electrode DNA sequences. (A) Transmission spectra in the range from -4 to 4 eV. (B) Transmission spectra in the range from -3.3 to -2.3 eV. The MPSH states responsible for the peaks in the transmission spectra are indicated with numbers. All energies are relative to the Fermi energy of the electrodes.

higher applied bias. Within the highest eight occupied orbitals shown in Figure 3 and Figure 4, three well-delocalized conductance channels were found for 30 -CCGG-50 (i.e., HOMO, HOMO-5, and HOMO-6), while only one was found for 30 CAAG-50 (i.e., HOMO-6). The orbital pictures are in agreement with the experimental work of Dulic et al.2 that reported better conductance for molecules containing more cytosine and guanine nucleotides compared to those containing more adenine and thymine nucleotides. The delocalized orbitals introduce through-bond conductance channels. Such channels result in broadened peaks in the transmission spectra and bigger values of the calculated current. The spatial distribution of the frontier orbitals reveals that the reason for the conductance difference is the potential barrier introduced by the adenine and thymine nucleotides in the HOMO of 30 -CAAG-50 . Thus, HOMO does not provide a good conductance channel for the electron transport. Another reason is the fact that less delocalized conductance channels are available among the highest occupied orbitals that can take part in the through-bond conductance. The analysis of the frontier orbitals is a powerful chemical tool, which can provide us with useful insight into the conductance phenomenon, which is often missing in the trivial physical treatment of electron transport problems concentrated mainly on the transmission probabilities.33 In addition, we performed calculations in the presence of an external electric field oriented along the main axis of the helical structure.45 Such an external field is induced between the electrodes and can significantly alter the energies and the spatial distribution of the frontier orbitals. The effect is especially strong in conjugated asymmetric πelectron molecules, which have donor and acceptor groups, where it was found to be responsible for current rectification.45-47 The external electric field has to be considered for the accuracy of the orbital analysis.48,49 However, in the π-π stack systems the external field effect can be neglected due to the potential barriers introduced by the interplanar space. The field is strong enough to alter the orbitals only within the planes, but because of its orientation this effect can also be neglected.45 3.3. Zero Bias Electron-Transport Calculations. The qualitative conclusions obtained from the study of the highest occupied orbitals are verified with more quantitative calculations of electrode-molecule-electrode junctions performed with the NEGF-DFT method. The Perdew-Zunger local density approximation method was used with the SZ basis set for Au atoms and the DZP basis set for all other atoms. These calculations provided the exact (within the method’s framework) physical quantities of

the electron transport such as the electron’s transmission probabilities and the current. The investigated model for the electrontransport calculations was simplified because of computational limitations. The orbital analysis performed here and the previous extended H€uckel study11 have shown that the electron transport is achieved through the aromatic π-π stacked bases, and the sugar-phosphate skeleton has only mechanical bonding character. In the electron-transport calculations we considered only the aromatic heterocyclic stacks, while the sugar-phosphate skeleton was not considered for simplicity, as shown in Figure 1. The central region also includes two layers with 36 Au atoms from each electrode. Zero-bias calculations were performed for the 30 -CCGG-50 and 30 -CAAG-50 sequences, and the transmission spectra are shown in Figure 5. The transmission spectra are aligned to the Fermi energy of the electrodes, which is located at the origin of the energy (E = 0). Thus, all energies in Figure 5 are relative to the Fermi energy. Figure 5A shows the calculated transmission spectra in the range from -4 to 4 eV electron energies. Both investigated DNA sequences show conductance through the highest occupied orbitals in the range between -3.3 and -2.3 eV. Those orbitals can be considered as the important conductance channels for the electron transport. The calculated LUMO conductance is characterized with very low transmission probability values. According to the zero-bias spectra, a significant current for both sequences should be observed for biases exceeding 4 V. This result is in agreement with the previous extended H€uckel study.11 The analysis is concentrated on the conducting region between -3.3 and -2.3 eV, shown in Figure 5B, to provide a better insight into the electron-transport properties. The 30 -CAAG-50 spectrum is characterized with less intensive peaks compared to those of 30 -CCGG-50 . The peaks in the spectrum of 30 -CAAG-50 are observed for lower electron energies than those for 30 CCGG-50 , which means that higher applied bias would be required to initiate electron transport. The peaks in the spectra can be related to the orbitals of the insulated molecules shown in Figure 3 and Figure 4. In Figure 5B, it can be seen that the closest peaks of 30 -CCGG-50 to the Fermi level have higher energy than the peaks of 30 -CAAG-50 which can be related to the energies of the delocalized orbitals, shown in Figure 3 and Figure 4, and discussed earlier in the manuscript. A more realistic view can be obtained by looking at the MPSH (molecular projected selfconsistent Hamiltonian) states. The MPSH states approximate the molecular orbitals in the junction environment and include the influence of the electrodes on the molecular wire. MPSH analysis helps in the qualitative understanding of the transmissions 3486

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Figure 6. MPSH states of 30 -CCGG-50 and 30 -CAAG-50 related to the peaks in the zero-bias transmission spectra. The energies of the 30 -CCGG-50 MPSH states are given in blue, and the energies of the 30 -CAAG-50 MPSH states are given in red. All energies are relative to the Fermi energy of the electrodes.

peaks’ origin. The MPSH states which are related to the peaks in the spectra, plotted in Figure 5B, are shown in Figure 6. Those MPSH states are well delocalized along the π-π stacks, which emphasize the importance of the through-bond conductance. All energies in Figure 6 are relative to the Fermi energy of the electrodes. According to Landauer’s formula given in eq 1, the current is obtained after integration of a finite part of the transmission spectra called bias window.31 The bias window includes only energies close to the Fermi level in the interval from -EV/2 to EV/2.17,24 Z 2e dETðE, V Þ ð1Þ IðV Þ ¼ h Integration of narrow sharp peaks does not contribute significantly to the value of the calculated current. Broadened peaks in the transmission spectra provide significant contribution to the current. Integration along the whole spectrum in the interval from -4 to 4 eV results in 8.69 for the 30 -CCGG-50 sequence and 5.33 for the 30 -CAAG-50 sequence. As a strong approximation, these values can be related to the current, which shows that 30 CCGG-50 is 60% more conductive than 30 -CAAG-50 . In this way, the zero-bias transmission spectra support the conclusions obtained from the orbitals’ analysis and provide an explanation for the experimentally observed conductance difference between DNA molecules containing a different number of adeninethymine nucleotide pairs.2 In general, the peaks in the transmission spectra of systems characterized with intermolecular bonds are significantly narrower than those of π-conjugated materials. A reason for that is the interplanar tunneling barriers, which significantly increase the resistance in such materials. These potential barriers can statistically reduce the number of tunneling particles, resulting in much lower transmission probabilities. These features make systems with intermolecular bonding, to which the DNA molecules belong, less suitable for electron transport than the chain πconjugated organic polymers. However, the resistance induced by the interplanar tunneling adds interesting semiconductive properties to the materials making them valuable candidates for current-controlling molecular devices. 3.4. Applied Bias Electron-Transport Calculations. To obtain the I/V curves for the both DNA sequences, we performed

current calculations for applied biases in the interval from 0.0 to 1.5 V. The algorithm implemented in ATK allows complete SCF treatment of electrode-molecule-electrode junctions for applied biases taking into account the important factors which govern the electron transport such as the effect of the external electric field induced by the electrodes.24 The only significant approximation is the effect of the field on the junction geometry. However, for systems with intermolecular π-π stacking this effect can be neglected.45,48,49 The bias calculations can significantly alter the transmission spectra and, for systems with external electric field dependence, can raise rectifying properties.45-47,50 A consequence of the applied bias calculation is the narrowing of the HOMOLUMO gap and conductive properties for lower biases than those predicted by the zero-bias calculation.45 These reasons make the applied bias calculations an important factor for the electrontransport studies. The obtained I/V curves are summarized in Figure 7A. 30 CCGG-50 is characterized with very low values of the computed current for biases lower than 1.0 V. However, for applied biases over 1.0 V, the calculated current goes up significantly with 2 orders of magnitude. This result is lower than that predicted from the analysis of the zero-bias transmission spectra and the previous extended H€uckel study,11 which predict significant conductance for biases exceeding 4 V. Thus, the NEGF-DFT calculations demonstrate the relatively good conductance of the short DNA molecules, which was also estimated experimentally.2 The main deviation from the experiment is the shape of the I/V curve. While in the experimental results the I/V curves show metallic character with current,2 which is increasing with the bias, the theoretically obtained curves show semiconductor character with a nonconductive low bias region. A possible reason for this deviation is the simplification of the theoretical model, which neglects the molecule-surface covalent σ-bond. The I/V curve of 30 -CAAG-50 shows lower conductance compared to that of 30 CCGG-50 , which is expected from the orbital analysis and is in agreement with the experimental results.2 An important conclusion from the performed calculations is the increased resistance in some DNA molecules, due to the presence of adenine and thymine nucleotides. The orbital analysis shows that these pairs introduce a tunneling barrier, but this intuitive conclusion requires a deeper understanding of 3487

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Figure 7. I/V curves obtained from the applied-bias NEGF-DFT calculations. (A) I/V curves of the investigated DNA sequences. (B) I/V curves of the four nucleotides.

Figure 8. Transmission probability and I/V curves for the 30 -CCGG-50 four-nucleotide sequence and the sugar-phosphate skeleton. (A) Model of the nucleotides. (B) Model of the sugar-phosphate skeleton. (C) Zero-bias transmission spectra. (D) I/V curves obtained from the applied-bias NEGFDFT calculations.

the nature of electron transport through the nucleotides. We performed NEGF-DFT calculations for each of the four nucleotides, base, and sugar-phosphate, within the nanogap between the electrodes. Besides the transmission spectra, the I/V curves in the low bias region between 0.0 and 0.4 V were calculated. The obtained results are plotted in Figure 7B. The four nucleotides show 4 orders of magnitude higher conductance than the 30 CCGG-50 and 30 -CAAG-50 DNA sequences. This result shows the significant conductance length dependence through DNA molecules as well as the importance of the coherent transport mechanism. The increased resistance in longer DNA molecules is a result of the reduced probability for an electron to tunnel through a large number of sequential potential barriers induced by the intermolecular stacking. As demonstrated in Figure 7B, guanine and cytosine show better conductance than adenine and thymine in the low bias region. Figure 7B provides additional important information for the conductance through the nucleo-

tides. The I/V curves of guanine and cytosine show metallic character with current increasing with the bias within the investigated interval. The I/V curves of adenine and thymine show a semiconducting behavior with clearly defined nonconductive low bias region between 0.0 and 0.1 V and sudden current jump for biases exceeding 0.1 V. The different character, metallic or semiconductive, of the nucleotide pairs demonstrates the complexity of DNA molecules as conducting devices. Within the DNA, electronic elements with metallic character are linked through potential barriers to semiconducting elements. Using our ability to design different DNA sequences, we can build short molecular wires with desired resistance for the needs of the semiconductor electronics. In this study of electron-transport through short DNA molecules, one important approximation was made, which could eventually alter the obtained results, the omitting of the sugar-phosphate 3488

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The Journal of Physical Chemistry C skeleton of the DNA for the electron-transport calculation. That approximation was justified because the aromatic bases are π-π stacks with mobile electrons within the π-conjugated system, while the sugar-phosphate skeleton is built by σ-bonds with electrons localized between the nucleuses. However, a recent theoretical study reveals the possibility for electron transport through polypeptides in R-helix conformation.51 The electron transport is achieved through the hydrogen bonds. Those helical polypeptides are similar to the sugar-phosphate skeleton of the DNA molecules. We performed electron-transport calculations for two models of the 30 -CCGG-50 four-nucleotide sequence. In the first model, shown in Figure 8 A, the sugar-phosphate skeleton is omitted, and in the second model, shown in Figure 8 B, the nucleotide bases are omitted. In Figure 8 C the calculated zero-bias transmission spectra are compared for both structures. In Figure 8 D the calculated I/V curves are compared for both structures. The calculated current through the sugar-phosphate skeleton is several orders of magnitude lower compared to that through the nucleotides. That result confirms our assumption that the electron transport is achieved through the π-π stacked aromatic bases. The zero-bias transmission spectra reveal that while the electron transport through the sugar-phosphate skeleton is possible it is characterized with lower probability than that through the π-π stacked aromatic bases. This result is not surprising and is in good agreement with previously published studies. The importance of the π-π stacked aromatic bases for the electron transport was first demonstrated with the extended H€uckel method.11 Further investigations were performed by Tsukamoto et al. who demonstrated the importance of the nucleotide base interaction with the gold electrodes in a first-principles method study.52 This interesting topic was also discussed in the work of Haris and coauthors where it was shown that the mechanical distortion of the π-π stacks leads to a significant conductance drop.53 In that study,53 the sugarphosphate skeleton remains unaffected, or slightly distorted in comparison to the π-π stacked aromatic bases. The experimentally reported sequence dependence of the DNA conductance2 is in agreement with the theoretical studies,11,52,53 which report that the electron transport is achieved through the π-π stacked aromatic bases. While the sugar-phosphate skeleton remains unchanged in DNA molecules with different sequences, the ordering of the π-π stacks is the difference, which gives the rise of the conductance change.

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orbitals for biases exceeding 1.0 V. These results were obtained after applied-bias SCF calculations. The zero-bias study is in agreement with previous theoretical results, which report significant conductance for biases exceeding 4 V. That result shows the importance of the applied bias calculations for the detailed understanding of conductance through complex molecules. A major point of this work was to understand the difference of the conductance through DNA molecules containing more adenine and thymine bases and those which lack these nucleotides. Orbital analysis was used to demonstrate that adenine and thymine introduce a tunneling barrier, which increases the resistance in the DNA molecules. That analysis is in agreement with the quantitative NEGF-DFT calculations, which show significantly higher conductance for DNA molecules without adenine and thymine bases. The study of electron transport through single nucleotides demonstrates a semiconductor type I/V curve for adenine and thymine with clearly defined low-bias nonconductive region and high-bias conductive region, while the I/V curves for guanine and cytosine show metallic character.

’ ASSOCIATED CONTENT

bS

Supporting Information. Atomic Cartesian coordinates for the optimized geometries of all investigated structures and complete ref 39. This material is available free of charge via the Internet at http://pubs.acs.org.

’ AUTHOR INFORMATION Corresponding Author

*E-mail: [email protected].

’ ACKNOWLEDGMENT The authors are thankful to Dr. Yoshihito Shiota for useful discussion. K.Y. thanks Grants-in-Aid (Nos. 18066013 and 18GS0207) for Scientific Research from Japan Society for the Promotion of Science (JSPS) and the Ministry of Culture, Sports, Science and Technology of Japan (MEXT), the Nanotechnology Support Project of MEXT, and the Joint Project of Chemical Synthesis Core Research Institutions of MEXT for their support of this work. A.S. acknowledges JSPS for a postdoctoral fellowship. ’ REFERENCES

4. CONCLUSIONS We have investigated the electron transport properties through short DNA molecules with the NEGF-DFT method. Geometry optimization of a nucleoside on a gold surface has shown that besides the covalent S-Au bond a second interaction exists between the aromatic base and the surface. That interaction is responsible for the electron transport between the surface and the molecule, while the covalent S-Au bond plays only a mechanically attaching role. This conclusion helps for the better understanding of electron transport through DNA molecules for which was previously believed to be insulators when connected to the electrodes at the 30 position, due to the insulating character of the sugar-phosphate skeleton. DNA can be considered as a conducting wire consisting of the π-π stacked aromatic heterocyclic bases separated from the environment by the insulating sugar-phosphate skeleton. The electron-transport calculations suggested a conductance mechanism through the highest occupied

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