Stability of Nucleobases and Base Pairs Adsorbed on Graphyne and

Article pubs.acs.org/JPCC

Stability of Nucleobases and Base Pairs Adsorbed on Graphyne and Graphdiyne S. Chandra Shekar and R. S. Swathi* School of Chemistry, Indian Institute of Science Education and Research Thiruvananthapuram (IISER-TVM), Kerala, India 695016 S Supporting Information *

ABSTRACT: A theoretical understanding of the structure and energetics of the interaction of nucleobases (NBs) and amino acids with extended carbon-based network structures is crucial for understanding phenomena occurring at the nanobio interface. Herein, we investigate the adsorption of NBs and base pairs (BPs) on the new network materials in the carbon family, graphyne (GY), and graphdiyne (GDY) using dispersioncorrected density functional theory (ωB97XD functional) with a basis set of triple-ζ quality. Systematic investigations on the orientation dependence of the interaction of each of the NBs with a series of model compounds along with their superstructures reveal that the binding strengths of NBs on GY and GDY follow the order G > A > C > T > U, while those of BPs follow the order GC > AT > AU. The NBs and the BPs are found to adsorb at distances of ∼3 Å from the GY and GDY sheets, and the adsorption strengths are higher for GY than GDY. The small decrease in the hydrogen bond energies of the BPs subsequent to adsorption suggests that GY and GDY can serve as promising templates for the self-assembly of DNA and RNA. Our first-principles studies on how the NBs interact with GY and GDY can serve as a first and significant step toward the aim of understanding the interactions of DNA and RNA with GY and GDY as well as designing biomolecular devices based on GY and GDY. We believe that our findings will motivate several studies toward understanding the interface of biology and the nanoworld.

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reported.26−28 Experimental measurements of the binding energies of the complexes have revealed that among all the NBs guanine has the strongest binding with graphene.28 A large number of theoretical investigations using molecular dynamics29,30 and quantum chemical calculations31−36 have contributed to an understanding of the structure, energetics, and dynamics of the NB−graphene complexes. Adsorption of NBs on a variety of other substrates like graphite,7 boron-nitride sheet,37,38 Cu surface,39,40 and Si nanowires41,42 has also been studied. After the successful isolation of graphene by micromechanical cleavage43 and preparation by chemical methods,44 a plethora of its applications in areas like biosensors,45 photonics,46 energy production, and energy storage47 have emerged. The versatility of carbon atoms to exist in various states of hybridization (sp, sp2, and sp3) has led to the prediction of new forms of carbon. Graphyne (GY) and graphdiyne (GDY) are the new members in the carbon family with large two-dimensional network structures analogous to graphene.48,49 These new layered forms of carbon contain sp- and sp2-hybridized carbon atoms and are based on dehydrobenzo[12]annulene (DBA-12) and dehydrobenzo[18]annulene (DBA-18) frameworks, respectively. A layered structure of DBA-12 was originally predicted theoretically by Baughman et al. in 1987 and is now referred to as γ-GY.50 However, a variety of other network structures were also proposed by Baughman and co-workers, including lattices with

INTRODUCTION Understanding the interactions of biomolecules like DNA, RNA, and proteins with carbon-based systems is crucial for developing novel hybrid materials that could have a wide range of applications from molecular recognition and self-organization to molecular electronics.1−7 Various strategies for functionalizing (covalent and noncovalent) graphene and carbon nanotubes (CNTs) with DNA and proteins have evolved over the years.8−11 The hybrid materials thus obtained were found to be extremely useful in sensing,11−13 bioengineering,14,15 and nanoelectronics.16,17 Several theoretical studies on the adsorption of nucleobases (NBs) and amino acids on graphene and CNTs are already reported.18−21 Interestingly, DNA and carbon-based materials (graphene, graphene oxide, and CNTs) share a synergistic relationship. Graphene and graphene oxide have been demonstrated to be excellent platforms for sequencing DNA22,23 and for studying DNA hybridization.14,24 DNA motifs have found utility in sorting CNTs according to their chiral indices.25 Thus, structural recognition of DNA is possible through graphene and graphene oxide, and that of CNTs is possible through DNA, implying synergy. Adenine (A), guanine (G), thymine (T), cytosine (C), and uracil (U) are the fundamental constituents of DNA and RNA. The genetic information present in the nucleic acids is encoded in terms of these NBs. An understanding of the interactions of NBs with graphene and CNTs can shed light onto the phenomena occurring at the nanobio interface. Novel syntheses of NB−graphene and NB−CNT hybrids are recently © 2014 American Chemical Society

Received: December 31, 2013 Published: January 28, 2014 4516

dx.doi.org/10.1021/jp412791v | J. Phys. Chem. C 2014, 118, 4516−4528

The Journal of Physical Chemistry C

Article

where EBP−MC refers to the energies of the BP−MC complexes, and EBP and EMC refer to the energies of the BPs and MCs, respectively. Further, we calculate the distortion of the BP geometries from the hydrogen-bonded geometries in the presence of MCs. The distortion is estimated by calculating the distortion energy, which is defined as the difference in the energies of the free BP and that of the BP in the complex and is given by

the same hexagonal symmetry of graphene, which are now known as the α- and β-forms of GY. A recent experimental study has reported the preparation of thin films of GDY,51 while the synthesis of GY is still elusive. However, successful synthesis of the annulenic subunits of GY and GDY by Haley and coworkers52 and others53,54 followed by reports of their applications in nonlinear optical studies have provided a great thrust to this area.55,56 We hope that the stage for the experimental realization of monolayers of GY and GDY is not too far. Theoretical studies on the electronic, optical, and mechanical properties of GY and GDY are now reported57−60 with interesting applications for energy storage,61,62 electrode materials,63,64 filters,65 electronics,66 crystal engineering,67 and hydrogen purification.68 For the GY and GDY lattices to be useful as substrates for biological systems like nucleic acids and proteins, an understanding of the underlying interactions of their building blocks, NBs, and amino acids with these layered materials is essential. To the best of our knowledge, there are so far no reports in the literature of studies on the binding of NBs with GY and GDY. We believe that theoretical studies in this direction would help in understanding the energetics and dynamics of these complexes as well as in developing GY- and GDY-based biomolecular devices. In this article, we theoretically investigate the noncovalent interactions of NBs and Watson−Crick base pairs (BPs) with GY and GDY and study the effect of these substrates on the hydrogen bonding in BPs. The results thus obtained are compared with our studies on graphene performed at the same level of calculation as well as with the earlier reports on NB−graphene and BP−graphene interactions.

Edis = E(BP) − E(BP in complex)

where E(BP) is the energy of the free BP in its optimized geometry and E(BP in complex) is the energy of the BP in the geometry of the BP−MC complex. Subsequently, the hydrogen bonding energies of various BPs in the absence and presence of MCs are analyzed. First, from the optimized geometries of the individual BP (AT, GC, and AU) geometries, their hydrogen bonding energies are evaluated using E HB(BP) = E(BP) − E(Base1) − E(Base2)

where E(BP), E(Base1), and E(Base2) are the energies of the free BP and the individual bases, respectively, in their optimized geometries. We then consider the geometries of the BPs as found in the BP−MC complexes and perform single-point energy calculations (E(BP in complex)) to determine the hydrogen bonding energies in the presence of MCs using E HB(BP in complex) = E(BP in complex) − E(Base1) − E(Base2)

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It has to be however noted that EHB(BP) − EHB(BP in complex) = Edis. The hydrogen bonding energies of various BPs in the presence of MCs are also evaluated by an approach outlined by Grimme and co-workers32 using

METHODOLOGY All the quantum mechanical calculations reported in this article are performed using the dispersion-corrected density functional theory (DFT-D),69 with a Pople basis set of polarized triple-ζ quality using the Gaussian 09 suite of programs.70 The DFT-D functionals provide a good description of the long-range dispersive forces and are now routinely used for analyzing the structures and energetics of weakly bonded systems.69 ωB97XD and M06-2X functionals have earlier been used to model the interactions of NBs with graphene and CNTs.19,33 The results obtained using these functionals are found to be in agreement with experiments. All the computations reported herein are performed using ωB97XD. The initial geometry optimizations of the structures are performed using the functional, ωB97XD at the 6-31G(d,p) level, and are followed by single-point energy calculations at the 6-311+G(d,p) level with the same functional (ωB97XD/6-311+G(d,p)//ωB97XD/6-31G(d,p)). The reported energies are all corrected for basis set superposition errors (BSSEs), using the counterpoise method unless otherwise stated. The interaction energies for the NB−MC complexes are evaluated using the equation

E′HB (BP in complex) = ΔE − ΔEAC − ΔE BC

where A and B refer to the individual bases, while C refers to the MC. ΔE, ΔEAC, and ΔEBC are defined as ΔE = E BP − MC − EA − E B − EC , ΔEAC = EAC − EA − EC and ΔE BC = E BC − E B − EC

The energies, Ei, are all evaluated by performing single-point energy calculations in the geometries of the BP−MC complexes.

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RESULTS AND DISCUSSION The main objective of this work is to study the interactions of NBs and BPs with GY and GDY and compare the results with those of graphene. Coronene (C24H12), DBA-12 (C24H12), and DBA-18 (C30H12) are chosen as the model compounds (MCs) for graphene, GY, and GDY, respectively. Coronene has been earlier used as a MC for graphene in various theoretical studies.32,71 Extended networks of DBA-12 and DBA-18 give rise to GY and GDY, respectively, and hence we use them as the respective MCs. It is interesting to note that coronene and DBA-12 are isomers. Figure 1 shows the optimized geometries of the MCs. Coronene, DBA-12, and DBA-18 are all conjugated molecules. However, coronene and DBA-18 are (4n + 2)π systems, while DBA-12 is a (4n)π system.64,72,73 In coronene, the C−C bonds are all of the sp2−sp2 type, and there are four unique C−C bond lengths, 1.426 Å (a), 1.410 Å (b), 1.423 Å (c), and 1.364 Å (d) (see Figure 1). In contrast, DBA-12 and DBA-18

E int = E NB − MC − (E NB + EMC)

where ENB−MC refers to the energies of the NB−MC complexes and ENB and EMC refer to the energies of free NBs and MCs, respectively. We also calculate the interaction energies of the BP−MC complexes which are evaluated using E int = E BP − MC − (E BP + EMC) 4517



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Figure 1. Optimized geometries of coronene, DBA-12, and DBA-18, the MCs for graphene, graphyne, and graphdiyne, respectively.

consist of three types of C−C bonds of the sp2−sp2, sp−sp2, and sp−sp nature. The unique sp2−sp2 bond lengths are 1.415 Å (e), 1.399 Å (f), 1.388 Å (g), and 1.392 Å (h), while the sp−sp2 bond length is 1.425 Å (i). In DBA-12, the sp−sp bond length is 1.209 Å (j), while in DBA-18, there are two unique sp−sp bond lengths of 1.213 Å (k) and 1.367 Å (l). Since the NBs are aromatic in nature, their interactions with conjugated systems are predominantly governed by π−π stacking. However, the NBs also contain other active centers like −NH2, −CO, and −CH3 groups that play a key role in the metabolism of the cell74 (see Figure 2 for the optimized

and geometry optimizations are performed to obtain the lowestenergy structures. This allows us to probe the orientation dependence of the interaction of NBs with the MCs. The optimized geometries and the interaction energies for the minimum energy structures of the NB−MC complexes of coronene, DBA-12, and DBA-18 with various NBs are shown in Figure 3. In the figure, we also show the electrostatic potential (ESP) surfaces for the complexes, computed at an isovalue of 0.0004 e/au3. ESP surfaces provide a visualization of the charge density in the vicinity of the system of interest and have received the greatest research focus particularly in biological systems. Most negative regions of the ESP surfaces are colored red. It is interesting to note that the stacked initial geometry does not necessarily give rise to the lowest energy structures in all the NB−MC complexes. For instance, the minimum energy structures of A−DBA-18 and G−DBA-18 complexes are obtained from the initial geometries in which the −NH2 groups face the π-systems. Strong NH···π interactions are responsible for the stabilization of such geometries.33 One would have missed these minima if one had started from just the stacked initial geometry, and hence a study of the orientation dependence as performed here is necessary. Further, in some of the complexes (C−DBA-12, C−DBA-18, T−DBA-18, etc.), we also find that the stacked as well as other initial orientations yield optimized geometries with similar interaction energies. In the Supporting Information (Figures S1−S5 of Supporting Information), we show the optimized geometries and the interaction energies of the NB− MC complexes obtained from the various initial geometries of NBs. The computed interaction energies reveal that among all the NBs guanine has the largest interaction energy with all the MCs. Previous reports on NB−graphene complexes have also shown the largest binding energies for guanine.32 Our current results show that guanine has the largest binding energies with GY and GDY too. Guanine has also been found to exhibit the largest binding energies for adsorption on various other substrates like CNTs,78 BN sheets,37 Si networks,42 etc. Higher binding energies of guanine in comparison with other NBs can be attributed to its large polarizability.34 The complexes of coronene with all the NBs have the largest interaction energies compared to those of DBA-12 and DBA-18. This could be attributed to the presence of sp2 carbons in coronene in contrast to that of sp and sp2 carbons in DBA-12 and DBA-18. To explain this, we consider butadiene (C4H6) and 1-butene-3-yne (C4H4) as test cases. Butadiene has sp2-hybridized carbon atoms, while the carbon atoms of C4H4 are of sp and sp2 type. The ESP surfaces of C4H6 and C4H4 shown in Figure 4

Figure 2. Optimized geometries of the NBs, adenine, guanine, thymine, cytosine, and uracil, with their active centers highlighted.

geometries of the NBs with the active centers highlighted). The possibility of the binding of the NBs with the π-systems of the MCs via the −NH2, −CO, and −CH3 groups cannot be ruled out because of potential −NH···π,75 −CH···π,76 and −CO···π77 interactions. Therefore, we consider the geometries in which the NBs are stacked with respect to the MCs as well as those with the active centers facing the π-clouds of the MCs as the initial geometries and perform full geometry optimizations on the NB−MC complexes. For the thymine−MC complexes, for instance, four initial geometries (stacked geometry as well as geometries in which −CH3 end, −2CO end, and −4CO end face the π-systems of MCs) are chosen. The hexagonal rings of the NBs in each orientation are initially kept at a distance of ∼3 Å, 4518



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Figure 3. Optimized geometries, interaction energies, and ESP surfaces for the NB−MC complexes of various NBs with the MCs of graphene, GY, and GDY. Given in parentheses with each structure are the various types of initial geometries that have given rise to the minimum energy geometries.

Table 1. Interaction Energies of the Complexes of NBs with Coronene and DBA-12 Calculated Using the ωB97XD/ cc-pVTZ Level of Theorya interaction energies (kcal mol−1) NBs@MCs

coronene

DBA-12

adenine guanine thymine cytosine uracil

−15.6 −18.1 −15.9 −15.4 −13.5

−12.8 −17.1 −13.6 −12.3

a Note that for the thymine−DBA-12 complex the calculation did not yield a stable geometry.

Table 2. Tilt Angles of the NBs with Respect to the MCs Relative to Their Corresponding Stacked Geometries tilt angles (degrees) NBs@MCs

A

G

T

C

U

coronene DBA-12 DBA-18

2.2 5.6 13.6

3.8 5.3 17.2

6.3 8.9 28.7

2.2 3.4 17.5

4.5 11.7 25.8

reveal that the electron density on the CC bond in C4H4 is higher than that on the carbon atoms in butadiene. This leads to repulsive interactions with the electron density of NBs, as a result

Figure 4. Optimized geometries of C4H6, C4H4, coronene, and DBA-12 with their ESP surfaces. Note that the scale bar is kept uniform for comparison across structures. 4519



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for coronene and DBA-12, as shown in Figure 4 and Figure S6 of the Supporting Information, respectively. Thus, smaller electronic charge density on coronene than DBA-12 leads to its stronger interaction with the NBs. To estimate how the calculated interaction energies depend on the finiteness of the chosen basis set, we also optimized the geometries of the complexes of NBs with coronene and DBA-12 using the Dunning cc-pVTZ basis set with the same functional. The resulting interaction energies are in reasonable agreement with those obtained using the Pople basis (see Figure 3) and are shown in Table 1. However, it is interesting to note that the NB−MC complexes of DBA-12 and DBA-18 exhibit far more distortion in the orientation of the NBs with respect to the π-systems from the stacked geometry than the complexes of coronene. This can be seen from the tilt angles,79 defined by the angle between the aromatic rings of the NBs and the molecular planes of the MCs as

Table 3. Average Interplanar Distances between the NBs and the MCs in the Complexes interplanar distances (Å) NBs@MCs

A

G

T

C

U

coronene DBA-12 DBA-18

3.30 3.30 2.80

3.24 3.19 3.10

3.25 3.21 3.15

3.22 3.22 2.97

3.20 3.17 2.94

of which C4H4 interacts more weakly with NBs than C4H6. Mulliken charge analyses on C4H6 and C4H4 also confirm the most negative charge on the CC bond. The Mulliken charges estimated at the ωB97XD/6-31G(d,p) level for carbon atoms (in au) A, B, C, and D in C4H6 are −0.302, −0.064, −0.064, and −0.302, respectively. For C4H4, the values for A′, B′, C′, and D′ are −0.456, 0.230, −0.159, and −0.257, respectively. Similar variation in the ESP profiles and Mulliken charges is found

Figure 5. Optimized geometries, interplanar distances, and interaction energies of the complexes of NBs with C66H18, a superstructure of DBA-12, and a model compound of GY. The top views as well as the side views of the complexes are shown. 4520



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Figure 6. Optimized geometries, interplanar distances, and interaction energies of the complexes of NBs with C90H18, a superstructure of DBA-18, and a model compound of GDY. The top views as well as the side views of the complexes are shown.

Figure 7. Out-of-plane and in-plane potential energy surface scans for the interaction of various NBs with C66H18. 4521



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Figure 8. Out-of-plane and in-plane potential energy surface scans for the interaction of various NBs with C90H18.

Figure 9. Optimized geometries, interaction energies, and ESP surfaces for the BP−MC complexes of various BPs with the MCs of graphene, GY, and GDY.

To investigate the effect of the size of the MCs used to represent the GY and the GDY lattices on the adsorption and the interaction energies, we have also considered superstructures formed from DBA-12 and DBA-18, namely, C66H18 and C90H18 (see Figures 5 and 6), and studied their binding with various NBs. These superstructures serve as better MCs for GY and GDY. A similar approach had earlier been adopted by Grimme and co-workers,32 wherein various MCs with increasing sizes, starting from coronene, have been used to model the interactions of NBs with graphene. Initial geometries with the NBs placed on top of the central hexagonal rings as well as on the triangular regions of the superstructures at a distance of ∼3 Å are explored to determine the most stable adsorption geometries. The optimized geometries of the various NB−MC complexes of C66H18 and C90H18 along with their interaction energies are shown in Figures 5 and 6, respectively. It is interesting to note that the binding strengths of the NBs with C66H18 and C90H18 follow the order: G > A > C > T > U. However, the orders of binding strength of the NBs with C66H18 and C90H18 are not the same as obtained for DBA-12 and DBA-18, respectively. This is essentially due to the edge effects and similar discrepancies in the order of binding strengths of NBs with the MCs of graphene (C24H12 (coronene), C54H18, and C96H24) are observed.32

Table 4. Distortion Energies of the Nucleic Acid BPs in the BP−MC Complexes Edis (kcal mol−1) BPs@MCs

coronene

DBA-12

DBA-18

A-T G-C A-U

−0.3 −0.8 −0.3

−0.9 −0.9 −0.5

−2.2 −3.0 −0.4

Table 5. Hydrogen Bond Energies of the Nucleic Acid BPs in the Presence of the MCs of Graphene, GY, and GDY HB energies (kcal mol−1) BPs@MCs

coronene

DBA-12

DBA-18

A-T [−16.2 (−17.9)] G-C [−30.2 (−33.9)] A-U [−15.8 (−17.5)]

−15.9 (−17.4) −29.3 (−32.6) −15.5 (−17.0)

−15.3 (−17.3) −29.2 (−32.6) −15.2 (−17.2)

−14.0 (−16.0) −27.2 (−31.7) −15.4 (−17.6)

shown in Table 2. The computed average interplanar distances for the various complexes are shown in Table 3. The NBs adsorb at a distance of ∼3.2 Å away from the molecular planes of the MCs. The interaction energies and the interplanar distances obtained for the NB−coronene complexes are in close agreement with the previous reports.32 4522



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Figure 10. Optimized geometries, interaction energies, and interplanar distances of the complexes of BPs with C66H18, a superstructure of DBA-12, and a model compound of GY. The top views as well as the side views of the complexes are shown.

Figure 11. Optimized geometries, interaction energies, and interplanar distances of the complexes of BPs with C90H18, a superstructure of DBA-18, and a model compound of GDY. The top views as well as the side views of the complexes are shown.

superstructures, C66H18 and C90H18. Starting from the optimized geometries of the complexes of NBs with C66H18 and C90H18 shown earlier, out-of-plane and in-plane rotation of the NBs are performed separately in steps of 10 degrees to compute the single-point energies at every step. Figures 7 and 8 show the resultant PES scans. All single-point energy calculations shown herein are performed using the ωB97XD/6-31G(d,p) level of theory. The out-of-plane rotation of the NBs from the initial geometries has been found to raise the energy of the system, implying that the almost perpendicular orientations of the NBs with respect to MCs are unfavorable. The orientations explored during the in-plane rotations yield multiple geometries with

Table 6. Hydrogen Bond Energies of the Nucleic Acid BPs in the Presence of Superstructures HB energies (kcal mol−1) BPs@ superstructures

A-T [−16.2 (−17.9)]

G-C [−30.2 (−33.9)]

A-U [−15.8 (−17.5)]

C66H18 C90H18

−15.5 (−17.7) −15.7 (−17.5)

−29.4 (−31.8) −29.6 (−32.5)

−15.2 (−16.8) −15.2 (−17.0)

To examine the effect of orientation of the NBs on the surface of MCs, we perform single-point potential energy surface (PES) scans for the out-of-plane and in-plane rotation of the NBs on the 4523



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Figure 12. Optimized geometries of the MCs of other forms of GY and GDY. Hexagon, rhombus, and DA-12 serve as the MCs for GY, and DA-18 serves as the MC for GDY.

Figure 13. Optimized geometries, interaction energies, and ESP surfaces for the NB−MC complexes of various NBs with the MCs of other forms of GY and GDY. Given in parentheses with each structure are the various types of initial geometries that have given rise to the minimum energy geometries.

the π-systems in a stacked orientation and perform full geometry optimizations on the BP−MC complexes. The optimized geometries and the interaction energies of the various BP−MC complexes of nucleic acid BPs with coronene, DBA-12, and DBA-18 are shown in Figure 9. Among the BPs, GC adsorbs strongly over all the MCs. AT adsorbs strongly over DBA-18, while GC and AU adsorb strongly

similar energies. However, as one would expect, the lowest energy geometry has always been the initial optimized geometry in each case. We now study the adsorption of nucleic acid BPs on the MCs of graphene, GY, and GDY. Herein, we first optimize the geometries of the BPs, AT, GC, and AU. Subsequently, we place the BPs at a distance of ∼3 Å from the molecular planes of 4524



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Figure 14. Optimized geometries, interaction energies, and ESP surfaces of the various BPs with the MCs of other forms of GY and GDY.

Table 7. Hydrogen Bond Energies of the Nucleic Acid BPs in the Presence of MCs of Other Forms of GY and GDY HB energies (kcal mol−1) BPs@MCs

hexagon

rhombus

DA-12

DA-18

A-T [−16.2 (−17.9)] G-C [−30.2 (−33.9)] A-U [−15.8 (−17.5)]

−15.5 (−17.1) −29.5 (−32.0) −14.7 (−16.1)

−15.6 (−17.0) −29.4 (−31.6) −15.1 (−16.7)

−15.8 (−17.4) −29.5 (−32.5) −15.4 (−17.1)

−16.0 (−17.7) −29.2 (−32.5) −15.2 (−16.6)

is more favorable on GY than GDY. The energies of interaction of the BPs with C66H18 and C90H18 are larger than those with DBA-12 and DBA-18 by at least ∼5 kcal mol−1. However, this difference was found to be smaller for the complexes of NBs. This arises due to the edge effects that are predominant for the complexes of BPs compared to those of NBs. The hydrogen bonding energies of the BPs in the BP−superstructure complexes are tabulated in Table 6. It is clear that there is a slight decrease in hydrogen bonding energies on adsorption, implying that GY and GDY could serve as promising templates for DNA self-assembly. We now consider the interaction of NBs and BPs with the MCs for the other forms of GY and GDY. γ-GY, an extended network of DBA-12, is the most well-studied form of GY. However, α-GY, β-GY, and (14,14,14)-GY50 are its other known forms. The electronic structure of the various forms of GY has recently been investigated.49 Figure 12 shows the optimized geometries of the MCs for the other forms of GY and GDY that we have considered for our studies. C24H12 (hexagon)80 is chosen as the MC for α-GY. Coronene, DBA-12, and hexagon are isomers with relative energies of 0, 168.3, and 390.6 kcal mol−1, respectively. β-GY, however, can be thought of as a hybrid structure formed as a combination of α- and γ-forms of GY. C16H8 (rhombus) serves as the MC for a yet another known form of GY, (14,14,14)-GY. The effect of the presence of benzene rings and their contribution to the π-electron density of the central rings in DBA-12 and DBA-18 is studied by choosing their corresponding dehydroannulenes, C12H6 (DA-12) and C18H6 (DA-18). Study of the interactions of annulenic systems with NBs is important for two reasons: (i) annulenes serve as the MCs of GY and GDY and (ii) annulenes, by themselves, exhibit selectivity toward DNA and RNA as demonstrated very recently.81

over coronene. Further, there is a significant distortion of the BP geometries from the hydrogen-bonded geometries in the presence of DBA-18. The distortion is estimated by calculating the distortion energy. The distortion energies for the various BP−MC complexes are reported in Table 4. Note that since the complexes of BPs with DBA-18 are associated with a large structural distortion it is important to look at the distortion energy, rather than just the average tilt angle. Subsequently, the hydrogen bonding energies of various BPs in the absence and presence of MCs are analyzed. The procedure to calculate the hydrogen bonding energies is discussed in the Methodology section. Table 5 shows the numerical values of the hydrogen bonding energies for the various BP−MC complexes. For each BP, their hydrogen bonding energies in the absence of MCs are given in parentheses. The values for E′HB shown in parentheses are computed using the Grimme’s approach. The distortion energies as well as hydrogen bonding energies are all evaluated without the counterpoise corrections. The hydrogen bonding energies of BPs are found to decrease in magnitude in the BP−MC complexes in comparison with the free BPs. This is because of the structural distortion in the BPs arising due to their interaction with the MCs. The decrease in hydrogen bonding is greatest for the AT and GC complexes of DBA-18 because of the largest structural distortions found for these complexes. As earlier, we also calculate the interaction of BPs with the superstructures of DBA-12 and DBA-18. Figure 10 and Figure 11 show the optimized geometries, interaction energies, and the interplanar distances for the complexes of the BPs with the superstructures, C66H18 and C90H18. The strengths of binding of the BPs with GY and GDY follow the order: GC > AT > AU. The computed interaction energies reveal that the adsorption of BPs 4525



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As earlier, the interaction of each of the NBs with the abovementioned MCs is studied for various orientations of the NBs. The minimum energy structures along with the interaction energies and ESP surfaces are shown in Figure 13. In the Supporting Information (Figures S1−S5), we show the optimized geometries and the interaction energies of NB−MC complexes obtained from the various initial geometries of NBs. Among the various MCs of GY, DBA-12 and hexagon have large interaction energies with all the NBs, while the rhombic form and DA-12 have lower interaction energies. Adsorption of the NBs on hexagon, rhombus, DA-12, and DA-18 reveals the lowest binding strength for adenine. This is in contrast to adsorption on DBA-12 and DBA-18, wherein uracil has the least binding strength. Stronger binding of adenine with DBA-12 and DBA-18 can be attributed to the extra stability due to the presence of benzene rings around the annulenic rings. The NB−MC complexes of hexagon reveal a rather large distortion in MC geometry in comparison with those of the other forms of GY. However, it is interesting to note that DBA-12 has the largest interaction energies with the DNA-BPs, AT and GC, while hexagon has the largest interaction energy with the RNA-BP, AU, as can be seen from Figures 9 and 14. The interaction energies of NBs and BPs with DA-12 and DA-18 are lower than those with DBA-12 and DBA-18, respectively, implying that the presence of additional benzene rings provides extra stability to the NB−MC and BP−MC complexes. We have also analyzed the hydrogen bonding energies of the BPs with the MCs of other forms of GY and GDY, as can be seen from Table 7.

Figure 16. Summary of the interaction energies for the adsorption of various BPs on the MCs of graphene, GY, and GDY. (i) Coronene (C24H12), (ii) DBA-12 (C24H12), (iii) DBA-18 (C30H12), (iv) hexagon (C24H12), (v) rhombus (C16H8), (vi) DA-12 (C12H6), (vii) DA-18 (C18H6), (viii) superstructure of DBA-12 (C66H18), and (ix) superstructure of DBA-18 (C90H18).

GDY can be useful platforms for biological studies and are the first step toward a deeper understanding of the interactions of DNA and RNA with GY and GDY.

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ASSOCIATED CONTENT

S Supporting Information *

The optimized geometries, interaction energies, and ESP surfaces of the NB−MC complexes obtained from the various initial geometries of NBs. This material is available free of charge via the Internet at http://pubs.acs.org.

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SUMMARY To summarize, we have studied the adsorption of nucleic acid bases and base pairs on graphyne and graphdiyne. A series of model compounds representing various forms of GY and GDY and their superstructures are considered for investigations. Subtle differences in the binding strengths of the NBs for various initial orientations are analyzed. Comparisons with results obtained on coronene, a MC for graphene, as well as with previous theoretical studies on graphene are made. The difference in the interaction of NBs with graphene and GY has been attributed to the presence of carbon atoms in various states of hybridization and is demonstrated using the ESP analysis. A summary of our findings on the strengths of adsorption of NBs and BPs on various MCs is shown in Figures 15 and 16. Our studies demonstrate that GY and

AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS The authors thank IISER-TVM for computational facilities. SCS thanks IISER-TVM for financial support. REFERENCES

(1) Gui, E. L.; Li, L. J.; Zhang, K.; Xu, Y.; Dong, X.; Ho, X.; Lee, P. S.; Kasim, J.; Shen, Z. X.; Rogers, J. A.; Mhaisalkar, S. G. DNA Sensing by Field-Effect Transistors Based on Networks of Carbon Nanotubes. J. Am. Chem. Soc. 2007, 129, 14427−32. (2) Calvaresi, M.; Zerbetto, F. The Devil and Holy Water: Protein and Carbon Nanotube Hybrids. Acc. Chem. Res. 2013, 46, 2454−63. (3) Liu, Y.; Dong, X.; Chen, P. Biological and Chemical Sensors based on Graphene Materials. Chem. Soc. Rev. 2012, 41, 2283−2307. (4) Lu, F.; Zhang, S.; Gao, H.; Jia, H.; Zheng, L. Protein-Decorated Reduced Oxide Graphene Composite and its Application to SERS. ACS Appl. Mater. Interfaces 2012, 4, 3278−3284. (5) Lu, Y.; Lerner, M. B.; John, Q. Z.; Mitala, J. J.; Hsien Lim, J.; Discher, B. M.; Charlie Johnson, A. T. Graphene-Protein Bioelectronic Devices with Wavelength-Dependent Photoresponse. Appl. Phys. Lett. 2012, 100, 033110. (6) Luan, B.; Zhou, R. Nanopore-Based Sensors for Detecting Toxicity of a Carbon Nanotube to Proteins. J. Phys. Chem. Lett. 2012, 3, 2337− 2341. (7) Bald, I.; Weigelt, S.; Ma, X.; Xie, P.; Subramani, R.; Dong, M.; Wang, C.; Mamdouh, W.; Wang, J.; Besenbacher, F. Two-Dimensional Network Stability of Nucleobases and Amino Acids on Graphite under Ambient Conditions: Adenine, L-Serine and L-Tyrosine. Phys. Chem. Chem. Phys. 2010, 12, 3616−3621.

Figure 15. Summary of the interaction energies for the adsorption of various NBs on the MCs of graphene, GY, and GDY. (i) Coronene (C24H12), (ii) DBA-12 (C24H12), (iii) DBA-18 (C30H12), (iv) hexagon (C24H12), (v) rhombus (C16H8), (vi) DA-12 (C12H6), (vii) DA-18 (C18H6), (viii) superstructure of DBA-12 (C66H18), and (ix) superstructure of DBA-18 (C90H18). 4526



Article

(29) Bobadilla, A. D.; Seminario, J. M. DNA−CNT Interactions and Gating Mechanism Using MD and DFT. J. Phys. Chem. C 2011, 115, 3466−3474. (30) Manohar, S.; Tang, T.; Jagota, A. Structure of Homopolymer DNA−CNT Hybrids. J. Phys. Chem. C 2007, 111, 17835−17845. (31) Cho, Y.; Min, S. K.; Yun, J.; Kim, W. Y.; Tkatchenko, A.; Kim, K. S. Noncovalent Interactions of DNA Bases with Naphthalene and Graphene. J. Chem. Theory Comput. 2013, 9, 2090−2096. (32) Antony, J.; Grimme, S. Structures and Interaction Energies of Stacked Graphene-Nucleobase Complexes. Phys. Chem. Chem. Phys. 2008, 10, 2722−9. (33) Panigrahi, S.; Bhattacharya, A.; Banerjee, S.; Bhattacharyya, D. Interaction of Nucleobases with Wrinkled Graphene Surface: Dispersion Corrected DFT and AFM Studies. J. Phys. Chem. C 2012, 116, 4374−4379. (34) Gowtham, S.; Scheicher, R.; Ahuja, R.; Pandey, R.; Karna, S. Physisorption of Nucleobases on Graphene: Density-Functional Calculations. Phys. Rev. B 2007, 76, 033401. (35) Le, D.; Kara, A.; Schroder, E.; Hyldgaard, P.; Rahman, T. S. Physisorption of Nucleobases on Graphene: A Comparative van der Waals Study. J. Phys.: Condens. Matter 2012, 24, 424210. (36) Jurecka, P.; Sponer, J.; Cerny, J.; Hobza, P. Benchmark Database of Accurate (MP2 and CCSD(T) Complete Basis Set Limit) Interaction Energies of Small Model Complexes, DNA Base Pairs, and Amino Acid Pairs. Phys. Chem. Chem. Phys. 2006, 8, 1985−93. (37) Lin, Q.; Zou, X.; Zhou, G.; Liu, R.; Wu, J.; Li, J.; Duan, W. Adsorption of DNA/RNA Nucleobases on Hexagonal Boron Nitride Sheet: An Ab Initio Study. Phys. Chem. Chem. Phys. 2011, 13, 12225−30. (38) Lee, J.-H.; Choi, Y.-K.; Kim, H.-J.; Scheicher, R. H.; Cho, J.-H. Physisorption of DNA Nucleobases on h-BN and Graphene: vdWCorrected DFT Calculations. J. Phys. Chem. C 2013, 117, 13435−13441. (39) Kilina, S.; Tretiak, S.; Yarotski, D. A.; Zhu, J. X.; Modine, N.; Taylor, A.; Balatsky, A. V. Electronic Properties of DNA Base Molecules Adsorbed on a Metallic Surface. J. Phys. Chem. C 2007, 111, 14541− 14551. (40) Bogdan, D.; Morari, C. Effect of van der Waals Interaction on the Geometric and Electronic Properties of DNA Nucleosides Adsorbed on Cu(111) Surface: A DFT Study. J. Phys. Chem. A 2013, 117, 4669−78. (41) Haldar, S.; Spiwok, V.; Hobza, P. On the Association of the Base Pairs on the Silica Surface Based on Free Energy Biased Molecular Dynamics Simulation and Quantum Mechanical Calculations. J. Phys. Chem. C 2013, 117, 11066−11075. (42) Zhong, X.; Slough, W. J.; Pandey, R.; Friedrich, C. Interaction of Nucleobases with Silicon Nanowires: A First-Principles Study. Chem. Phys. Lett. 2012, 553, 55−58. (43) Geim, A. K. Graphene: Status and Prospects. Science 2009, 324, 1530−4. (44) Stankovich, S.; Dikin, D. A.; Piner, R. D.; Kohlhaas, K. A.; Kleinhammes, A.; Jia, Y.; Wu, Y.; Nguyen, S. T.; Ruoff, R. S. Synthesis of Graphene-based Nanosheets via Chemical Reduction of Exfoliated Graphite Oxide. Carbon 2007, 45, 1558−1565. (45) Pumera, M. Graphene in Biosensing. Mater. Today 2011, 14, 308−315. (46) Bonaccorso, F.; Sun, Z.; Hasan, T.; Ferrari, A. C. Graphene Photonics and Optoelectronics. Nat. Photon. 2010, 4, 611−622. (47) Brownson, D. A. C.; Kampouris, D. K.; Banks, C. E. An Overview of Graphene in Energy Production and Storage Applications. J. Power Sources 2011, 196, 4873−4885. (48) Ivanovskii, A. L. Graphynes and Graphdiynes. Prog. Solid State Chem. 2013, 41, 1−19. (49) Liu, Z.; Yu, G.; Yao, H.; Liu, L.; Jiang, L.; Zheng, Y. A Simple Tight-Binding Model for Typical Graphyne Structures. New J. Phys. 2012, 14, 113007. (50) Baughman, R. H.; Eckhardt, H.; Kertesz, M. Structure-Property Predictions for New Planar forms of Carbon: Layered Phases Containing sp2 and sp Atoms. J. Chem. Phys. 1987, 87, 6687. (51) Li, G.; Li, Y.; Liu, H.; Guo, Y.; Li, Y.; Zhu, D. Architecture of Graphdiyne Nanoscale Films. Chem. Commun. 2010, 46, 3256−8.

(8) Husale, B. S.; Sahoo, S.; Radenovic, A.; Traversi, F.; Annibale, P.; Kis, A. ssDNA Binding Reveals the Atomic Structure of Graphene. Langmuir 2010, 26, 18078−18082. (9) Lu, C. H.; Li, J.; Zhang, X. L.; Zheng, A. X.; Yang, H. H.; Chen, X.; Chen, G. N. General Approach for Monitoring Peptide-Protein Interactions Based on Graphene-Peptide Complex. Anal. Chem. 2011, 83, 7276−82. (10) Weizmann, Y.; Chenoweth, D. M.; Swager, T. M. DNA-CNT Nanowire Networks for DNA Detection. J. Am. Chem. Soc. 2011, 133, 3238−41. (11) Liu, X.; Wang, F.; Aizen, R.; Yehezkeli, O.; Willner, I. Graphene Oxide/Nucleic-Acid-Stabilized Silver Nanoclusters: Functional Hybrid Materials for Optical Aptamer Sensing and Multiplexed Analysis of Pathogenic DNAs. J. Am. Chem. Soc. 2013, 135, 11832−9. (12) Lu, Y.; Goldsmith, B. R.; Kybert, N. J.; Johnson, A. T. C. DNADecorated Graphene Chemical Sensors. Appl. Phys. Lett. 2010, 97, 083107. (13) Chang, H.; Tang, L.; Wang, Y.; Jiang, J.; Li, J. Graphene Fluorescence Resonance Energy Transfer Aptasensor for the Thrombin Detection. Anal. Chem. 2010, 82, 2341−2346. (14) He, S.; Song, B.; Li, D.; Zhu, C.; Qi, W.; Wen, Y.; Wang, L.; Song, S.; Fang, H.; Fan, C. A Graphene Nanoprobe for Rapid, Sensitive, and Multicolor Fluorescent DNA Analysis. Adv. Funct. Mater. 2010, 20, 453−459. (15) Hilder, T. A.; Hill, J. M. Modeling the Loading and Unloading of Drugs into Nanotubes. Small 2009, 5, 300−308. (16) Jin, Z.; Sun, W.; Ke, Y.; Shih, C. J.; Paulus, G. L.; Hua Wang, Q.; Mu, B.; Yin, P.; Strano, M. S. Metallized DNA Nanolithography for Encoding and Transferring Spatial Information for Graphene Patterning. Nat. Commun. 2013, 4, 1663. (17) Prasongkit, J.; Grigoriev, A.; Pathak, B.; Ahuja, R.; Scheicher, R. H. Theoretical Study of Electronic Transport through DNA Nucleotides in a Double-Functionalized Graphene Nanogap. J. Phys. Chem. C 2013, 117, 15421−15428. (18) Rajesh, C.; Majumder, C.; Mizuseki, H.; Kawazoe, Y. A Theoretical Study on the Interaction of Aromatic Amino Acids with Graphene and Single Walled Carbon Nanotube. J. Chem. Phys. 2009, 130, 124911. (19) Umadevi, D.; Sastry, G. N. Quantum Mechanical Study of Physisorption of Nucleobases on Carbon Materials: Graphene versus Carbon Nanotubes. J. Phys. Chem. Lett. 2011, 2, 1572−1576. (20) Cazorla, C.; Rojas-Cervellera, V.; Rovira, C. Calcium-based Functionalization of Carbon Nanostructures for Peptide Immobilization in Aqueous Media. J. Mater. Chem. 2012, 22, 19684−19693. (21) Cazorla, C. Ab Initio Study of the Binding of Collagen Amino Acids to Graphene and A-doped (AH, Ca) Graphene. Thin Solid Films 2010, 518, 6951−6961. (22) Avdoshenko, S. M.; Nozaki, D.; Gomes da Rocha, C.; Gonzalez, J. W.; Lee, M. H.; Gutierrez, R.; Cuniberti, G. Dynamic and Electronic Transport Properties of DNA Translocation through Graphene Nanopores. Nano Lett. 2013, 13, 1969−76. (23) Garaj, S.; Liu, S.; Golovchenko, J. A.; Branton, D. MoleculeHugging Graphene Nanopores. Proc. Natl. Acad. Sci. U.S.A. 2013, 110, 12192−6. (24) Jang, H.; Kim, Y. K.; Kwon, H. M.; Yeo, W. S.; Kim, D. E.; Min, D. H. A Graphene-based Platform for the Assay of Duplex-DNA Unwinding by Helicase. Angew. Chem., Int. Ed. 2010, 49, 5703−7. (25) Tu, X.; Manohar, S.; Jagota, A.; Zheng, M. DNA Sequence Motifs for Structure-Specific Recognition and Separation of Carbon Nanotubes. Nature 2009, 460, 250−253. (26) Cao, H.; Wu, X.; Yin, G.; Warner, J. H. Synthesis of AdenineModified Reduced Graphene Oxide Nanosheets. Inorg. Chem. 2012, 51, 2954−60. (27) Singh, P.; Kumar, J.; Toma, F. M.; Raya, J.; Prato, M.; Fabre, B.; Verma, S.; Bianco, A. Synthesis and Characterization of Nucleobase− Carbon Nanotube Hybrids. J. Am. Chem. Soc. 2009, 131, 13555−13562. (28) Varghese, N.; Mogera, U.; Govindaraj, A.; Das, A.; Maiti, P. K.; Sood, A. K.; Rao, C. N. Binding of DNA Nucleobases and Nucleosides with Graphene. Chem. Phys. Chem. 2009, 10, 206−210. 4527



Article

(52) Marsden, J. A.; Haley, M. M. Carbon Networks Based on Dehydrobenzoannulenes. 5. Extension of Two-Dimensional Conjugation in Graphdiyne Nanoarchitectures. J. Org. Chem. 2005, 70, 10213− 10226. (53) Diederich, F. Carbon Scaffolding: Building Acetylenic all-Carbon and Carbon-Rich Compounds. Nature 1994, 369, 199−207. (54) Bunz, U. H. F.; Rubin, Y.; Tobe, Y. Polyethynylated Cyclic [small pi]-Systems: Scaffoldings for Novel Two and Three-Dimensional Carbon Networks. Chem. Soc. Rev. 1999, 28, 107−119. (55) Haley, M. M. Synthesis and Properties of Annulenic Subunits of Graphyne and Graphdiyne Nanoarchitectures. Pure Appl. Chem. 2008, 80, 519−532. (56) Sarkar, A.; Pak, J. J.; Rayfield, G. W.; Haley, M. M. Nonlinear Optical Properties of Dehydrobenzo[18]annulenes: Expanded TwoDimensional Dipolar and Octupolar NLO Chromophores. J. Mater. Chem. 2001, 11, 2943−2945. (57) Luo, G.; Zheng, Q.; Mei, W.-N.; Lu, J.; Nagase, S. Structural, Electronic, and Optical Properties of Bulk Graphdiyne. J. Phys. Chem. C 2013, 117, 13072−13079. (58) He, X.; Tan, J.; Bu, H.; Zhang, H.; Zhao, M. The Roles of π Electrons in the Electronic Structures and Optical Properties of Graphyne. Chin. Sci. Bull. 2012, 57, 3080−3085. (59) Cranford, S. W.; Buehler, M. J. Mechanical Properties of Graphyne. Carbon 2011, 49, 4111−4121. (60) Narita, N.; Nagai, S.; Suzuki, S.; Nakao, K. Optimized Geometries and Electronic Structures of Graphyne and its Family. Phys. Rev. B 1998, 58, 11009−11014. (61) Srinivasu, K.; Ghosh, S. K. Graphyne and Graphdiyne: Promising Materials for Nanoelectronics and Energy Storage Applications. J. Phys. Chem. C 2012, 116, 5951−5956. (62) Guo, Y.; Lan, X.; Cao, J.; Xu, B.; Xia, Y.; Yin, J.; Liu, Z. A Comparative Study of the Reversible Hydrogen Storage Behavior in Several Metal Decorated Graphyne. Int. J. Hydrogen Energy 2013, 38, 3987−3993. (63) Zhang, H.; Zhao, M.; He, X.; Wang, Z.; Zhang, X.; Liu, X. High Mobility and High Storage Capacity of Lithium in sp−sp2 Hybridized Carbon Network: The Case of Graphyne. J. Phys. Chem. C 2011, 115, 8845−8850. (64) Chandra Shekar, S.; Swathi, R. S. Rattling Motion of Alkali Metal Ions through the Cavities of Model Compounds of Graphyne and Graphdiyne. J. Phys. Chem. A 2013, 117, 8632−41. (65) Zhu, C.; Li, H.; Zeng, X. C.; Meng, S. Ideal Desalination through Graphyne-4 Membrane: Nanopores for Quantized Water Transport. Condens. Matter Mater. Sci. 2013, DOI: arxiv:1307.0208. (66) Soodchomshom, B.; Tang, I. M.; Hoonsawat, R. Directional Quantum Transport in Graphyne p-n Junction. J. Appl. Phys. 2013, 113, 073710. (67) Furukawa, S.; Uji-i, H.; Tahara, K.; Ichikawa, T.; Sonoda, M.; De Schryver, F. C.; Tobe, Y.; De Feyter, S. Molecular Geometry Directed Kagomé and Honeycomb Networks: Toward Two-Dimensional Crystal Engineering. J. Am. Chem. Soc. 2006, 128, 3502−3503. (68) Jiao, Y.; Du, A.; Hankel, M.; Zhu, Z.; Rudolph, V.; Smith, S. C. Graphdiyne: A Versatile Nanomaterial for Electronics and Hydrogen Purification. Chem. Commun. 2011, 47, 11843−5. (69) Chai, J.-D.; Head-Gordon, M. Long-Range Corrected Hybrid Density Functionals with Damped Atom-Atom Dispersion Corrections. Phys. Chem. Chem. Phys. 2008, 10, 6615−6620. (70) Frisch, M. J.; Trucks, G. W.; Schlegel, H. B.; Scuseria, G. E.; Robb, M. A.; Cheeseman, J. R.; Scalmani, G.; Barone, V.; Mennucci, B.; Petersson, G. A.; Nakatsuji, H.; Caricato, M.; Li, X.; Hratchian, H. P.; Izmaylov, A. F.; Bloino, J.; Zheng, G.; Sonnenberg, J. L.; Hada, M.; Ehara, M.; Toyota, K.; Fukuda, R.; Hasegawa, J.; Ishida, M.; Nakajima, T.; Honda, Y.; Kitao, O.; Nakai, H.; Vreven, T.; Montgomery, J. A.; Peralta, J. E.; Ogliaro, F.; Bearpark, M.; Heyd, J. J.; Brothers, E.; Kudin, K. N.; Staroverov, V. N.; Kobayashi, R.; Normand, J.; Raghavachari, K.; Rendell, A.; Burant, J. C.; Iyengar, S. S.; Tomasi, J.; Cossi, M.; Rega, N.; Millam, J. M.; Klene, M.; Knox, J. E.; Cross, J. B.; Bakken, V.; Adamo, C.; Jaramillo, J.; Gomperts, R.; Stratmann, R. E.; Yazyev, O.; Austin, A. J.; Cammi, R.; Pomelli, C.; Ochterski, J. W.; Martin, R. L.; Morokuma, K.;

Zakrzewski, V. G.; Voth, G. A.; Salvador, P.; Dannenberg, J. J.; Dapprich, S.; Daniels, A. D.; Farkas; Foresman, J. B.; Ortiz, J. V.; Cioslowski, J.; Fox, D. J. Gaussian 09, Revision B.01; Gaussian Inc.: Wallingford CT, 2009. (71) Zhao, Y.; Truhlar, D. G. A Prototype for Graphene Material Simulation: Structures and Interaction Potentials of Coronene Dimers. J. Phys. Chem. C 2008, 112, 4061−4067. (72) Kimball, D. B.; Haley, M. M.; Mitchell, R. H.; Ward, T. R. Dehydrobenzoannulene−Dimethyl- dihydropyrene Hybrids: Model Systems for the Synthesis of Molecular Aromatic Probes. Org. Lett. 2001, 3, 1709−1711. (73) Jusélius, J.; Sundholm, D. The Aromaticity and Antiaromaticity of Dehydroannulenes. Phys. Chem. Chem. Phys. 2001, 3, 2433−2437. (74) Brown, R. C.; Silver, A. C.; Woodhead, J. S. Binding and Degradation of NH2-terminal Parathyroid Hormone by Opossum Kidney Cells. Am. J. Physiol. 1991, 260, E544−52. (75) Vaupel, S.; Brutschy, B.; Tarakeshwar, P.; Kim, K. S. Characterization of Weak NH-pi Intermolecular Interactions of Ammonia with Various Substituted pi-Systems. J. Am. Chem. Soc. 2006, 128, 5416−26. (76) Tsuzuki, S. CH/π interactions. Ann. Rep. Sect. ″C″ (Phys. Chem.) 2012, 108, 69. (77) Santos-Contreras, R. J.; Martinez-Martinez, F. J.; Garcia-Baez, E. V.; Padilla-Martinez, I. I.; Peraza, A. L.; Hopfl, H. Carbonyl-Carbonyl, Carbonyl-[pi] and Carbonyl-Halogen Dipolar Interactions as the Directing Motifs of the Supramolecular Structure of Ethyl 6-Chloro-2Oxo-2H-Chromene-3-Carboxylate and Ethyl 6-Bromo-2-Oxo-2HChromene-3-Carboxylate. Acta. Crystallogr. C 2007, 63, o239−o242. (78) Das, A.; Sood, A. K.; Maiti, P. K.; Das, M.; Varadarajan, R.; Rao, C. N. R. Binding of Nucleobases with Single-walled Carbon Nanotubes: Theory and Experiment. Chem. Phys. Lett. 2008, 453, 266−273. (79) Pettersen, E. F.; Goddard, T. D.; Huang, C. C.; Couch, G. S.; Greenblatt, D. M.; Meng, E. C.; Ferrin, T. E. UCSF Chimera- A Visualization System for Exploratory Research and Analysis. J. Comput. Chem. 2004, 25, 1605−1612. (80) Baglai, I.; Maraval, V.; Bijani, C.; Saffon-Merceron, N.; Voitenko, Z.; Volovenko, Y. M.; Chauvin, R. Enhanced pi-Frustration in CarboBenzenic Chromophores. Chem. Commun. 2013, 49, 8374−8376. (81) Radic Stojkovic, M.; Skugor, M.; Tomic, S.; Grabar, M.; Smrecki, V.; Dudek, L.; Grolik, J.; Eilmes, J.; Piantanida, I. Dibenzotetraaza[14]annulene-Adenine Conjugate Recognizes Complementary Poly dT Among ss-DNA/ss-RNA Sequences. Org. Biomol. Chem. 2013, 11, 4077−85.

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Stability of Nucleobases and Base Pairs Adsorbed on Graphyne and

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