RNA

Subscriber access provided by - Access paid by the | UCSB Libraries

Article

Phosphorene as a Template Material for Physisorption of DNA/RNA Nucleobases and Resembling of Base Pairs: A Cluster DFT Study and Comparisons with Graphene Diego Cortés-Arriagada J. Phys. Chem. C, Just Accepted Manuscript • DOI: 10.1021/acs.jpcc.7b11268 • Publication Date (Web): 20 Feb 2018 Downloaded from http://pubs.acs.org on February 26, 2018

Just Accepted “Just Accepted” manuscripts have been peer-reviewed and accepted for publication. They are posted online prior to technical editing, formatting for publication and author proofing. The American Chemical Society provides “Just Accepted” as a service to the research community to expedite the dissemination of scientific material as soon as possible after acceptance. “Just Accepted” manuscripts appear in full in PDF format accompanied by an HTML abstract. “Just Accepted” manuscripts have been fully peer reviewed, but should not be considered the official version of record. They are citable by the Digital Object Identifier (DOI®). “Just Accepted” is an optional service offered to authors. Therefore, the “Just Accepted” Web site may not include all articles that will be published in the journal. After a manuscript is technically edited and formatted, it will be removed from the “Just Accepted” Web site and published as an ASAP article. Note that technical editing may introduce minor changes to the manuscript text and/or graphics which could affect content, and all legal disclaimers and ethical guidelines that apply to the journal pertain. ACS cannot be held responsible for errors or consequences arising from the use of information contained in these “Just Accepted” manuscripts.

The Journal of Physical Chemistry C is published by the American Chemical Society. 1155 Sixteenth Street N.W., Washington, DC 20036 Published by American Chemical Society. Copyright © American Chemical Society. However, no copyright claim is made to original U.S. Government works, or works produced by employees of any Commonwealth realm Crown government in the course of their duties.

Page 1 of 37 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

The Journal of Physical Chemistry

Phosphorene as a Template Material for Physisorption of DNA/RNA Nucleobases and Resembling of Base Pairs: A Cluster DFT Study and Comparisons with Graphene Diego Cortés-Arriagada1,* 1

Programa Institucional de Fomento a la Investigación, Desarrollo e Innovación.

Universidad Tecnológica Metropolitana. Ignacio Valdivieso 2409, P.O. Box 8940577, San Joaquín, Santiago, Chile. *E-mail address: [email protected] Abstract. A quantum chemistry study was performed to study the interaction of single deoxyribonucleic/ribonucleic acid (DNA/RNA) nucleobases and hydrogen-bonded base pairs onto a phosphorene nanosheet. Adenine (A), cytosine (C), guanine (G), thymine (T) and uracyl (U) were considered as the adsorbates that are physisorbed onto phosphorene in stacking patterns, reaching adsorption energies of 0.64−0.94 eV, and sorting the physisorption stability as G>C>A>T>U. The structure and aromaticity of all the 1 ACS Paragon Plus Environment

The Journal of Physical Chemistry 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Page 2 of 37

nucleobases is not affected upon complexation. Likewise, the hydrogen-bonded base-pairs (CG, AT and AU) are adsorbed in the armchair plane of phosphorene with high adsorption energies of 1.28−1.44 eV, and sorting the physisorption stability as CG>AT>AU. The hydrogen bond energies of the base-pairs are slightly affected by binding on phosphorene, retaining its stability at room temperature (300 K). Furthermore, comparison analyses showed that phosphorene is better suited for physisorption of nucleobases and base-pairs than graphene, improving the stability in up to 27%. This improvement is based on the interplay between enhanced dispersion and electrostatic interactions. Otherwise, all the nucleobases behave as mild n-dopants, introducing up to ∼0.1 e/molecule in phosphorene. The charge doping and bandgap changes suggest that the phosphorene conductance could be sensitive to the physisorption of nucleobases and base-pairs. Finally, the new insights from this work shed light into the physisorption phenomena of biomolecules occurring at phosphorene interfaces, indicating that phosphorene emerges as a promising template for self-assembly of nucleobases in nanobiological devices. INTRODUCTION Phosphorene has recently emerged as a new alternative to graphene because of its potential applications in electronics and nanodevices, and due to its stability as a bidimensional material1. Phosphorene is entirely composed of phosphorous atoms with a strong in-plane covalent binding. Among the interesting properties of phosphorene are its high charge carrier mobility (1000 cm2/Vs), high mechanical strength (Young' modulus 44−166 GPa), and tunable bandgap (0.3-2.0 eV)2. The applications of phosphorene have been mainly proposed for use in field effect transistors, Li-ion batteries, spintronic, gas sensors, and water splitting1-5. Nevertheless, like the case of graphene, theoretical studies 2 ACS Paragon Plus Environment

Page 3 of 37 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


have predicted the interesting sorption properties of phosphorene, which are promising for technologies related to the adsorption, storage, removal, detection or analysis of different chemical species. For instance, small molecules (such as SO2, CO, H2O, H2, NH3, NO, NO2, PH3 and AsH3) are physisorbed onto phosphorene with adsorption energies ranging from 0.1 to 1.0 eV, where the adsorption strength is improved with respect to the physisorption onto MoS2 and graphene6-9. Theoretical studies have recently explored the interaction of phosphorene with biomolecules (glycine, leucine, glutamic acid, histidine and phenylalanine), which are physisorbed with a high stability (adsorption energies of up to ∼0.7 eV)10-11. These studies give evidence that phosphorene could be implemented as part of bioinorganic interfaces1011

. The latter turns important because of phosphorene is a more biologically-friendly

material than graphene, causing a lower disruption in the structure of proteins12-13. Furthermore, the high biocompatibility of phosphorene is also addressed by its high stability in water and organic solvents14-16, in addition to the biocompatibility of its degrading compounds (phosphate and phosphite)14. In this regard, nucleobases such as adenine (A), cytosine (C), guanine (G), thymine (T) and uracyl (U) are important biomolecules because of they are the fundamental constituents of the deoxyribonucleic (DNA) and ribonucleic (RNA) acids, storing the genetic information. Since it is known that purine and pyrimidine bases can self-assemble onto crystalline solids17, its interaction onto layered materials is of importance due to its potential biotechnological applications, this is to develop biological-friendly interfaces and materials for resembling, sensing and/or sequencing of DNA/RNA. In this regard, it has been studied the interaction of nucleobases with layered materials such as intrinsic and doped graphene18-24, transition-metal 3 ACS Paragon Plus Environment


Page 4 of 37

dichalcogenides25, graphynes23, BC3, and boron-nitride sheets21, 26; these studies allow to understand the adsorption phenomena at nanobiological interfaces. Taking graphene as a representative class of adsorbent material, experimental and theoretical analyses have shown that nucleobases are highly stable onto its surface (even in aqueous conditions), giving insights into as these biomolecules interacts at graphene interfaces18, 20, 22, 27-28. The adsorption energies of nucleobases onto graphene are on the range of 0.4−1.1 eV, depending on the different nucleobases and theoretical methodologies11, 18, 20-23, 27-30. The order of stability among all the nucleobases follows the order of G>C≥A≥T>U, where the stability of C, A and T can change according with the different theoretical aproaches11, 18, 2023, 27-30

. Moreover, the high physisorption stability of nucleobases onto graphene indicates

that its hydrogen-bonded base pairs can spontaneously self-assemble on its surface, especially because of the hydrogen bonds are merely affected by binding on graphene22-23. Nevertheless, to the best of our knowledge, there are no major reports dealing on the interaction stability of nucleobases with phosphorene. Taking into account that phosphorene could serve as a promising new layered substrate for biomolecules in biotechnological devices, in addition to its advantages over graphene, this work characterizes the physisorption stability of nucleobases and hydrogenbonded base-pairs onto phosphorene. A dispersion corrected Density Functional Theory (DFT) methodology is implemented to obtain the structure, binding modes, energetic and stability of the nucleobase−phosphorene and base-pair−phosphorene complexes, studying also the effect of the physisorption into the hydrogen bond of the base-pairs. Additionally, the results are compared against those obtained for graphene as a reference substrate with high sorption properties towards biomolecules. 4 ACS Paragon Plus Environment

Page 5 of 37 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


COMPUTATIONAL METODOLOGY Finite phosphorene (P88H26) and graphene (C96H26) sheets were implemented, where the dangling bonds at the edges were saturated with hydrogen atoms; these models were selected according to well converged adsorption energies as the surface size increases and a rigid cluster structure (see the Supporting Information for details). Note that finite phosphorene models have been implemented to analyze its interactions with molecules such as CO2, CH4, NH3, and pirazinamide31-33, and also to study its electronic properties in nanosheets34. Likewise, finite graphene models have been used to study its interactions with nucleobases and base-pairs19-20, 22. All the DFT calculations were performed in the ORCA 4.0 program35-36. The PBE37 functional was used, which has been widely implemented to characterize the structural, electronic and sorption properties of phosphorene and graphene10-11, 21, 27, 31-32. Geometry optimizations were performed with the all-electron def2-SVP basis sets38, while all the electronic properties were obtained with the def2-TZVP basis sets38; the auxiliary basis def2/J was adopted for the resolution-of-identity procedure in the ORCA program39. The DFT-D3 method (including the Becke-Johnson damping function) was used to include the dispersion energy corrections in the SCF energies (ESCF-PBE) and gradients40-41; the latter results in the PBE-D3 method. Accordingly, the total energy (EPBE−D3) is expressed as a sum of electronic (ESCF-PBE) and dispersion contributions (Edisp): EPBE−D3=ESCF−PBE+Edisp. The use of dispersion corrections for the PBE functional is necessary as shown in the analysis of nucleobase−graphene systems, the latter in order to avoid overestimated binding distances and inaccurate adsorption energies21. Basis set superposition errors were corrected by the geometrical counterpoise correction (gCP)42. Note that the gCP-PBE-D3 5 ACS Paragon Plus Environment


Page 6 of 37

methodology has been determined as a reliable method to study the adsorption of aromatic molecules onto nanosheets such as graphene and graphyne, even with best results compared to the B97-D3 approach43. Wavefunction and Atoms-in-Molecules (AIM) analyses were performed in the Multiwfn program44. The isotropic first electric dipole polarizabilities were analytically obtained through solution of the coupled-perturbed SCF equations in the ORCA program and with the conjugate gradient solver. The physisorption stability was evaluated by means of the adsorption energies (Eads) as:

E ads = E adsorbent + E adsorbate − E adsorbent − adsorbate

(1)

where, Eadsorbent, Eadsorbate and Eadsorbent−adsorbate correspond to the total energies of the adsorbent, adsorbate, and adsorbent−adsorbate systems, respectively. The more positive values of Eads, the more stable the adsorbed structures are. The contribution of dispersion interactions was also assessed by decomposing the total adsorption energies into the sum of electronic and dispersion contributions as: Eads=Eads-SCF-PBE+EvdW. In this equation, Eads-SCFPBE

is the electronic contribution to the adsorption energy (this is without dispersion

corrections), and EvdW is the dispersion contribution. EvdW is computed as:

where

Edisp(i) are

EvdW=Edisp(adsorbent)+Edisp(adsorbate)−Edisp(adsorbent−adsorbate)

(2)

the

and

dispersion

corrections

of

the

isolated

fragments

adsorbent−adsorbate system. Although this study is focused in the gas phase DFT computations at 0 K, exploratory ab-initio molecular dynamic trajectories were performed in order to get insights 6 ACS Paragon Plus Environment

Page 7 of 37 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


into the structural stability of the adsorbed base-pairs onto phosphorene. Equations of motion were resolved via the Verlet velocity algorithm at 300 K, and using the Berendsen thermostat for the temperature control45-46 (canonical ensemble). The potential was determined "on-the-fly" through the semiempirical PM6 Hamiltonian in the MOPAC2016 program47. Corrections to dispersion and hydrogen bonding were included by the D3H4 correction48, which includes: i) the dispersion correction by the Grimme's D3 method with specific parameters for PM640; ii) the H4 hydrogen-bond function developed by Řezáč and Hobza; and iii) a correction to account by hydrogen-hydrogen steric repulsive interactions in PM649. The PM6-D3H4 method was selected due to its performance to reproduce the adsorption energies at the semiempirical level with respect to those obtained at the DFT level, showing low deviations in the range of 0.07-0.30 eV. The input geometries for the trajectories involve the base-pairs interacting onto a P126H30 cluster, which show the same ground state adsorption configuration as in the P88H26 cluster. A more extended cluster model was adopted in these cases to allow more flexibility in the molecular motions of the adsorbate onto the adsorbent. The time step in all the simulations was of 1.0 fs; data were collected after 1000 fs of both heating and equilibrium; statistics were obtained by 33 ps of production. RESULTS AND DISCUSSION Physisorption of single nucleobases Fig. 1 shows the optimized adsorption configurations of nucleobases onto phosphorene, and their properties (and comparisons with graphene) are summarized in Table 1.

7 ACS Paragon Plus Environment


Page 8 of 37

Figure 1. Minimum energy adsorption configurations of nucleobases (A, C, G, T and U) onto phosphorene. Table 1. Adsorption energies (Eads, in eV), contribution of dispersion energies (EvdW) and intermolecular

distances

(dinter,

in

Å)

of

the

nucleobase−phosphorene

and

nucleobase−graphene complexes. nucleobase A C G T U

phosphorene Eads EvdW dinter

graphene Eads EvdW dinter

0.76 0.79 0.94 0.72 0.64

0.63 0.63 0.81 0.61 0.54

0.89 0.75 0.97 0.79 0.69

3.13 3.07 3.21 3.13 3.14

0.67 0.57 0.74 0.61 0.54

3.40 3.36 3.33 3.38 3.32

All the nucleobases are physisorbed onto phosphorene; the physisorption strength follows the order of G>C>A>T>U. Guanine reaches the largest adsorption energy among all the nucleobases (0.94 eV), which has also been determined with the largest stability onto graphyne-based surfaces23, carbon nanotubes50, transition-metal dichalcogenides25, and boron-nitride sheets21, 51. The larger adsorption energy of guanine in these surfaces can be explained due to its relative high polarizability compared to other nucleobases50, 52, this is a


Page 9 of 37 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


larger tendency to displace the charge density upon interaction. The latter increases the magnitude of induction and electrostatic terms in the interaction energy as determined from Energy Decomposition Analyses22, allowing to compensate (in addition to the dispersion contribution) the destabilizing exchange repulsion interactions as found in non-covalent nucleobase-graphene complexes. By comparison with graphene, the adsorption energies are improved onto phosphorene in the range of ∼17-27%. Besides, the average intermolecular distances of the adsorbates with respect to the adsorbent plane (Table 1) show that nucleobases are adsorbed at shorter intermolecular distances on phosphorene (3.1−3.2 Å) compared to those reached on graphene (3.3−3.4 Å), qualitatively indicating the enhanced binding ability of phosphorene. Thus, phosphorene is best suited for physisorption of nucleobases and base pairs than graphene. In this regard, the increased sorption performance of phosphorene is different of related layered materials such as graphyne, graphdiyne, tungsten disulfide (WS2) and molybdenum disulfide (MoS2), where the physisorption strength of nucleobases is decreased compared to graphene as determined from DFT calculations23,

25

. Note that the order of binding strength on graphene was

computed to be G>A≈C>T>U, which is in agreement with previous theoretical studies11, 18, 20-23, 27-30

(see the Supporting Information for details).

The effect of the orientation of nucleobases onto phosphorene was studied through the analysis of the potential energy surface as a function of the in-plane rotation of the adsorbates with respect to the phosphorene plane. Starting from the optimized geometries of the complex systems (Fig. 1), the nucleobases were rotated about its centre in steps of 10°, and the single-point energies were computed (Fig. 2). The lowest energy remains in the optimized geometries, hence other conformations are higher in energy. In fact, the in9 ACS Paragon Plus Environment


Page 10 of 37

plane rotation of nucleobases increases the energy in up to ∼8 kcal/mol, decreasing the adsorption energies. Note that the out-of-plane rotations were not computed because of the perpendicular orientations of nucleobases onto two dimensional materials are unfavorable11, 23

. Additionally, it is worth to point out that the structure of the nucleobases is almost

unchanged by binding on phosphorene; indeed, the relaxation energies of nucleobases were found to be lower than ∼0.01 eV (total energy difference between the geometry of the nucleobases in its isolated and physisorbed state).

Figure 2. Relative energy (Erel, in eV) according to the in-plane rotation (θ, in degrees) of nucleobases onto phosphorene. On the other hand, the contribution of dispersion forces (EvdW) in the stability of the nucleobase-phosphorene systems was characterized (Table 1). The dispersion energies are mainly larger (or equal) compared to the adsorption energies (EvdW≥Eads), indicating the electronic part of the interaction is repulsive in nature, and the nucleobase-phosphorene systems are mainly stabilized by dispersion interactions. Indeed, the dispersion interactions contribute ∼1 eV to the adsorption energies, indicating the strong physisorption. Interestingly, the dispersion contribution increases in the range of 28−32% when the nucleobases are adsorbed onto phosphorene compared to graphene. Additionally, the non10 ACS Paragon Plus Environment

Page 11 of 37 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


covalent interaction (NCI)53 analysis was performed to get insights into the qualitative pattern of the weak interactions dominating the physisorption; the NCI analysis is based on the reduced density gradient s and the electron density ρ according to: s=∇ρ/(2(3π2)1/3ρ4/3). This index is associated with the long-range interactions at low electron density regions; the points in the low density region relate to the sign of the second largest eigenvalue of the Hessian matrix of the electron density (λ2) (as in the Bader´s atoms in molecules theory)5354

, where λ2 characterizes the nature of the chemical interactions. In this scheme, weak

interactions are found for λ2≈0, while hydrogen bonds are found for λ20. The NCI analysis is displayed in Fig. 3 for the G−phosphorene system as a representative case.

Figure 3. a) The patterns of the reduced density gradient vs the sign of the second Hessian eigenvalue multiplied by the electron density. Blue and red boxes stand for the regions with the stabilizing dispersion interactions and destabilizing steric interactions, respectively. b) The NCI surface of weak interactions in the G−phosphorene and G−graphene systems. Technical details in the NCI: s=0.7; λ2=[-0.020; 0.010] a.u. All the cases are in the Supporting Information. 11 ACS Paragon Plus Environment


Page 12 of 37

Fig. 3a displays the 2D-NCI surfaces (s function vs the electron density multiplied by λ2). The peaks of the reduced density gradient at λ2≈[−0.020, 0.010] a.u. characterize the intermolecular

dispersion

interactions

in

the

nucleobase−phosphorene(graphene)

complexes. Interestingly, the 3D-NCI surfaces (Fig. 3b) of the these interactions in the G−graphene and G−phosphorene systems show similar patterns, even when phosphorene is not a delocalized system like graphene, and supporting the larger contribution of dispersion forces

in

this

interaction.

Furthermore,

the

2D-NCI

surfaces

of

the

nucleobase−phosphorene complexes show a peak at λ2≈0.08 a.u., which does not appear in graphene. This peak corresponds to the intramolecular dispersion interactions between phosphorous atoms in the phosphorene network as observed at the 3D-NCI surface, which should not be confused with the repulsive intramolecular steric interactions at λ2≈0.13 a.u. Further insights into the contribution of electrostatic interactions to the physisorption stability were addressed by the AIM analyses, where the electron density (ρi) at the bond critical points (BCPs) of intermolecular interactions was studied, this is at the BCPs points in intermolecular bond paths connecting the Nuclear Critical Points (NCP) (Fig. 4). In this scheme, the weak long-range electrostatic closed-shell interactions are associated to low density BCPs (ρi≤0.01e/Bohr3)55. Taking the G−phosphorene system as a representative case (all the cases are in the Supporting Information), it is noted that intermolecular electrostatic interactions play a key role in the physisorption stability like in the graphene case. However, Fig. 4 shows that the magnitude and amount of the intermolecular electrostatic interactions are enhanced onto phosphorene (ρi≈0.003−0.012 e/Bohr3) with respect to those reached onto graphene (ρi≈0.005−0.006 e/Bohr3). Intermolecular bond paths between the pyramidal amino groups of the nucleobases with the 12 ACS Paragon Plus Environment

Page 13 of 37 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


surfaces of both phosphorene and graphene are also observed, which are associated to BCPs of

ρi≈0.004−0.009 e/Bohr3. In the case of graphene, these interactions were

described as weak hydrogen bond-like interactions between the amino groups and the π−centres of the benzene-like rings of graphene29-30, in agreement with the low magnitude of ρi. Interestingly, such interactions are also improved onto phosphorene.

Figure 4. Electron density at intermolecular BCPs (ρi) of the G−graphene and G−phosphorene systems, which is assigned to weak long-range electrostatic interactions; ρi values are in e/Bohr3.

Figure 5. Electron density at the ring critical points (ρRCP, in e/Bohr3), and multicenter bond order (MCBO, in arbitrary units a.u.) of the pyrimidine and/or imidazole rings of the DNA/RNA nucleobases. The AIM analysis was also implemented to obtain the electron density at the ring critical point (ρRCP) of the pyrimidine and/or imidazole rings of nucleobases. The values of 13 ACS Paragon Plus Environment


Page 14 of 37

the ρRCP have been linked to the aromatic character of rings56. Note that the aromatic character of nucleobases decreases in the order of A>G≥C>T≥U57-60, where A, C and G are described as aromatic systems, while T and U are almost non-aromatic systems57-60. Fig. 5 shows the ρRCP values of the pyrimidine and imidazole rings of the nucleobases in their isolated state, and compared with those upon physisorption onto phosphorene and graphene. By comparison with the free nucleobases, the ρRCP values remain almost unchanged by adsorption onto phosphorene or graphene, suggesting that the aromatic character of the nucleobases is not affected by both adsorbents. These results are consistent taking into account the negligible changes in the molecular structure of the adsorbates after physisorption and its low preparation energy, in addition to the weak electron transfer as will be noted below. These results were also compared against those obtained with the multicenter bond order (MCBO) index61-62, which is based on electron delocalization properties and is in agreement with magnetic and structural aromaticity based indexes63-64. MCBO indicates the strength and the electron delocalization ability of multicenter bonds on rings61. In this regard, the larger MCBO, the larger is the strength of the multicenter bond (aromaticity). In fact, the trend in the MCBO results is the same as obtained by the AIM analysis (Fig. 5). The normalized MCBO indexes of the pyrimidine and imidazole rings in the free nucleobases appear in the range of 0.58 to 0.47; when the physisorption takes place on phosphorene (or graphene), the MCBO indexes remains almost unchanged (change of up to ±0.01), indicating that the aromatic character of the nucleobases is almost not affected by the interaction with the adsorbents. On the other hand, Fig. 6 displays the electron density difference [∆ρ(r)] between the adsorbent-adsorbate fragments after and before the physisorption. In the case of the 14 ACS Paragon Plus Environment

Page 15 of 37 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


G−phosphorene system, ∆ρ(r) shows that an intramolecular charge distribution occurs in phosphorene and guanine upon physisorption; the nucleophilic and electrophilic groups of guanine polarize the adsorbent electron density just below the adsorption site, inducing an intramolecular charge transfer by means of mutual effects. Specifically, the lone pair 3p orbitals of the phosphorous atoms in phosphorene are highly polarized, redistributing its electron density and inducing an enhanced intermolecular interaction compared to graphene as noted above. A similar pattern of electron density redistribution is responsible for the contribution of electrostatic interactions in the stacking of aromatic molecules on graphene, but the electron density of the π bonds of graphene is polarized instead43. Therefore, the improved physisorption stability of nucleobases onto phosphorene compared to graphene is explained by the interplay and improvement of both dispersion and electrostatic interactions as a result of the mutual polarization effects due to the intramolecular electron density redistribution.

Figure 6. Charge density difference [∆ρ(r)] of the G−graphene and G−phosphorene systems; the accumulation and outflow of electron density after physisorption are depicted with sky-blue and yellow color, respectively. Isosurface value of 0.0007 a.u.



Page 16 of 37

Physisorption of hydrogen-bonded base pairs Considering the strong physisorption of single DNA/RNA nucleobases onto phosphorene, it is now characterized the stability of the hydrogen-bonded base-pairs. The Cytosine-Guanine (CG), Adenine-Thymine (AT) and Adenine-Uracyl (AU) base-pairs were firstly optimized and subsequently placed at distances of ∼3.5 Å on phosphorene in several conformations. Fig. 7 displays the computed ground states of these complexes, and Table 2 show the adsorption energies and average intermolecular distances. It is necessary to point out that the choice of the configurations of the base pairs is based on the WatsonCrick complementarity of nucleobases as implemented in related theoretical analyses18, 22, 65

, and other conformations or dimers were not considered in this work.

Figure 7. Minimum energy adsorption configurations of base pairs (CG, AT and AU) onto phosphorene and graphene clusters.


Page 17 of 37 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


Table 2. Adsorption energies (Eads, in eV), contribution of dispersion energies (EvdW, in eV) and intermolecular distances (dinter, in Å) of the base-pair−phosphorene and basepair−graphene complexes. aThe values reported by ref23. bThe values obtained at the CCSD(T) level of theory in this work, including extrapolation to the complete basis set.

base pair

phosphorene

graphene

isolated

Eads

EvdW

EHB

dinter

Eads

EvdW

CG

1.44

1.67

-1.28

3.17

1.22

1.21 -1.39 (1.41)a 3.44

-1.49 [-1.47]a(-1.41)b

AT

1.39

1.61

-0.77

3.18

1.19

1.24 -0.80 (0.75)a 3.44

-0.84 [-0.78]a(-0.74)b

AU

1.28

1.52

-0.78

3.17

1.12

EHB

1.19 -0.81 (0.74)

dinter

a

3.40

EHB

-0.85 [-0.76]a(-0.75)b

All the base-pairs are physisorbed onto phosphorene in a parallel conformation with respect to the adsorbent surface, and at average intermolecular distances of ∼3.2 Å like in the case of the single nucleobases. The CG pair shows the largest adsorption stability onto phosphorene (1.44 eV) as expected by the larger adsorption strength of guanine. AT and AU are adsorbed onto phosphorene with energies of 1.39 and 1.28 eV, respectively. The stability of the base-pair−phosphorene complexes is improved in ∼15−18% compared to that reached through adsorption on graphene, indicating that phosphorene is a good candidate to bind and resemble DNA/RNA nucleobases. In addition, the largest adsorption energy of the CG pair onto layered materials agrees with the isothermal titration calorimetry experiments developed for base-pair−graphene complexes18. The ground state orientation of the base-pair−phosphorene systems is always placed in 45° with respect to the armchair or zigzag direction of phosphorene. The latter is different of graphene, where the base-pairs are preferably adsorbed in the armchair



Page 18 of 37

direction of the surface. In this regard, the in-plane rotation of the adsorbates with respect to phosphorene was found to raise the total energy of the base-pair−phosphorene complexes (Fig. 8). For instance, a rotation of θ≈45° increases the energy in ∼0.4−0.6 eV with respect to the ground state, decreasing the physisorption stability. Hence, another conformations are unfavorable geometries at 0K, and those conformations need to overcome higher energies to be reached. The latter suggest that base-pairs can self-assembly onto phosphorene with high stability in certain planes at lower temperatures, but certainly different adsorption planes could be preferred at higher temperatures in molecular selfassembly of freestanding base pairs. Note that the base pair orientation onto phosphorene is some different of the single nucleobases (see Figs. 1), which slightly decrease the stability of the base-pair−phosphorene complexes, and causing the adsorption energies appear between

the

sum

of

the

component

bases;

for

instance,

Eads(CG−phosphorene)Eads), and the strong physisorption is due to long-range dispersion and electrostatic interactions such as in the case of the single nucleobases. As well, the NCI analysis (Fig. 9) shows that the pattern of intermolecular dispersion interactions reached on phosphorene is similar to those obtained on graphene, supporting the presence of a strong stacking interaction onto both adsorbent materials. Furthermore, when the EvdW values are compared, it is found that the dispersion contribution increases by up to 38% when the base-pairs are adsorbed onto phosphorene compared to that on graphene. For that reason, both single nucleobases and its base-pairs are able to be adsorbed onto phosphorene with high physisorption stability.

Figure 9. The NCI surface of the weak interactions of base-pairs adsorbed onto phosphorene and graphene. Technical details in the NCI: s=0.7; λ2=[-0.020; 0.010] a.u. 19 ACS Paragon Plus Environment


Page 20 of 37

Regarding the stability of the base-pairs, Table 2 shows its hydrogen bond energies (EHB) in the presence and absence of the adsorbent, which were obtained as previously proposed22-23: EHB=∆E−∆EA−C−∆EB−C

(3)

where A and B represent each nucleobase in the base-pair, and C is the adsorbent material. In addition, ∆E, ∆EAC and ∆EBC are defined as:

∆E=EAB−C−EA−EB−EC ∆EA−C=EAC−EA−EC , ∆EB−C=EBC−EB−EC

(4) (5)

where all the energies are evaluated at the optimized geometries of the base-pair−adsorbent system. Firstly, the hydrogen bond energies of the isolated base-pairs follow the order of CG>AU>AT, where the CG pair is the most stable due to that its structure is stabilized by three hydrogen bonds (with distances of 1.7−1.9 Å), while two hydrogen bonds are involved in the AU and AT pairs. The computed hydrogen bond energies are in agreement with those obtained at the ωB97XD/6-311+G(d,p) level of theory23 (see parenthesis in Table 2); even the difference is not larger than 0.1 eV when compared to those computed in this work at the high level of theory DLPNO-CCSD(T) with extrapolation to the basis set limit by using the procedures described in the ORCA program66 (the def2-SVP and def2TZVP basis sets were used for the extrapolation at the PBE optimized geometries). When adsorbed onto phosphorene, the hydrogen bond energies of the base-pairs slightly decrease in the order of 8−14%, which is comparable to that reached onto graphene (4−6%).


Page 21 of 37 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


Therefore, base-pairs could self-assembly onto phosphorene as noted above, implying that its hydrogen bond interactions are mainly retained with high stability.

Figure 10. Radial pair distribution function [gab(r)] of hydrogen bond distances (HB) in the base-pair−phosphorene systems. 33000 conformations per system were used for statistics. Exploratory ab-initio molecular dynamic trajectories were also performed at 300 K in order to get insights into the stability of the hydrogen bond interactions on the basepair−phosphorene systems at room temperature; this methodology has been implemented in our previous studies67-70. The attention was focused in the radial pair distribution function [gab(r)] of the intermolecular NH⋅⋅⋅N and NH⋅⋅⋅O interactions of the base-pairs in the overall trajectory (Fig. 8), where such as interactions are recognized as hydrogen bonds. The interactions were considered as hydrogen bonds when its distance and angle appears in the range of [1.50-3.15]Å and [145-215]°, respectively. Fig 8 shows that almost all the



Page 22 of 37

hydrogen bonds interactions are retained in the base-pairs at room temperature upon physisorption on phosphorene, even without larger diffusion of the adsorbates from the adsorption site of phosphorene. Indeed, the structural stability is high in the overall trajectory. The gab(r) function shows that the distances of the NH⋅⋅⋅N and NH⋅⋅⋅O intermolecular interactions are mainly retained in the range of 1.6−2.5 Å (within the hydrogen bond range), hence indicating the high stability of the self-assembly of DNA/RNA nucleobases onto phosphorene as noted above. In the case of the CG−phosphorene system, the dynamic conditions caused that 2710 conformations lost the NH(cytosine)⋅⋅⋅N(guanine) hydrogen bond with respect to the tolerance values. However, this decrease in the amount of hydrogen bonds is negligible considering the overall trajectory (33000 conformations). Snapshots for trajectories and RMSD data are included in the Supporting Information for details. Effects into the electronic properties While the main focus of the current study is to investigate the stability of DNA/RNA constituents onto phosphorene, the effects of the adsorbates into some of the electronic properties of phosphorene are depicted in Table 3. Table 3. Electronic properties of the nucleobase−phosphorene and base-pair−phosphorene systems: Mulliken charge of the adsorbate (QA in |e|); molecular dipole moment (µ, in Debye); isotropic first electric dipole polarizability (α, in 10-30esu); HOMO and LUMO energies (εHOMO and εLUMO, in eV) and its energy difference (∆HL, in eV). (a) α values of the isolated adsorbates. (b) ∆HL values determined at the PBE0/def2-TZVP//PBE-D3/def2SVP level of theory. The total energy of free phosphorene is -30044.096052 a.u. 22 ACS Paragon Plus Environment

Page 23 of 37

systems nucleobases A C G T U base-pairs AT AU CG

QA

µ

α

εHOMO

εLUMO

∆HL

0.10 0.09 0.07 0.06 0.04

1.80 3.95 3.30 2.55 2.43

24.25 (0.72)a 24.20 (0.57)a 24.30 (0.77)a 24.20 (0.63)a 24.11 (0.51)a

-5.06 -5.03 -5.03 -5.06 -5.06

-3.64 -3.72 -3.67 -3.67 -3.67

1.42 (2.82)b 1.31 (2.70)b 1.36 (2.74)b 1.39 (2.79)b 1.39 (2.79)b

0.12 0.10 0.13

1.74 24.65 (1.43)a 1.90 24.57 (1.31)a 3.57 24.65 (1.42)a

-5.01 -5.02 -4.89

-3.61 -3.63 -3.64

1.40 (2.80)b 1.40 (2.79)b 1.25 (2.68)b

0.00

-5.09

-3.71

1.38 (2.77)b

Free phosphorene

-

23.84

1.6 R² = 0.9852

1.4

Eads (eV)

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


1.2 1.0 0.8 0.6 24.1

24.2

24.3

24.4

24.5

24.6

24.7

-30

α (1*10 esu)

Figure 11. Adsorption energy (Eads) vs first electric dipole polarizability (α) of the nucleobase-phosphorene and base-pair-phosphorene systems. Table 3 shows that nucleobases and base-pairs act as mild n-dopants, introducing up to ∼0.04−0.13 e/molecule in phosphorene as noted from the QA parameter. The charge transfer is similar as that reached by interaction of phosphorene with pirazinamide and donor gaseous molecules6, 32, and it is different of amino acids where the charge transfer takes place in the phosphorene→molecule direction10. As a consequence of the intramolecular electron density redistribution and polar character of the nucleobases, the



Page 24 of 37

electronic polarization on the complexes increases as observed from the dipole moments compared to the free phosphorene (0 Debye). The first electric dipole polarizability values (α) in Table 3 indicate that the polarizability of phosphorene is increased upon interaction with the nucleobases and its base-pairs, this is the deformability of the electronic charge distribution increases. Moreover, the trend in the electric polarizability is in according with the magnitude of the polarizability in the free adsorbates (see parenthesis in Table 3). Interestingly, the magnitude of the polarizability in the complex systems is in a linear relation to the magnitude of the adsorption energies (Fig. 11, R2≈0.98), indicating the key role of the polarizability of the adsorbates in the magnitude of the long-range dispersion and electrostatic interactions. Thus, the higher the polarizability of the nucleobases, the higher the adsorption energy is. The latter has been also established in the adsorption of nucleic acid bases on carbon nanotubes, which is explained by the fact that in systems stabilized by dispersion interactions, the dispersion energy is proportional to the polarizability of the interacting systems50. It must be noted that the charge transfer processes could be responsible by changes in the conductance of the substrate due to the charge doping, allowing to increase its sensing properties towards DNA/RNA constituents. In this regard, phosphorene is a semiconductor material, then changes in its bandgap could be useful for sensing applications. The computed HOMO-LUMO energy difference of the isolated phosphorene cluster was computed to be of ∼1.4 eV, similar to that of ∼1.5 eV reported for cluster models of phosphorene32. Upon physisorption, there is a slight change in the HOMOLUMO gap value (∆HL) of the adsorbent-adsorbate complexes. The A, T and U increase the

∆HL values (up to +0.04 eV); consequently, its base-pairs also increase the ∆HL values. 24 ACS Paragon Plus Environment

Page 25 of 37 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


Conversely, C and G decrease the ∆HL values (up to −0.07 eV); as an effect, the CG physisorption causes the largest decrease in the ∆HL index due to the increase of the HOMO energy compared to the free phosphorene. Note that the trend in the ∆HL values is the same when they are obtained with the more accurate hybrid PBE0 functional at the PBE geometries (see Table 3 in parenthesis). The partial density of state (DOS) plots were also inspected to obtain more information about the electronic structure of the nucleobase−phosphorene and basepair−phosphorene systems (Fig. 12). It was observed that nucleobases cause changes in the conduction band near to the HOMO level, but the conduction band of phosphorene is not affected by the physisorption. Taking into account the G−phosphorene system as a representative case, the 2p states of the C, N and/or O atoms of the nucleobases hybridize with the 3p states of phosphorene near to the HOMO level in the valence band (∼-5 eV). No appreciable hybridization and/or contribution from the nucleobases is observed in the conduction band near to the Fermi level, which only appears above -3 eV in the conduction band. In the case of the CG−phosphorene complex, the base-pair decreases the bandgap because of a new peak in the valence band is appearing at higher energies than the Fermi level of free phosphorene, which is due to the contribution of the 2p states in the nucleobases; then, the HOMO of the cluster system is almost a contribution from the hydrogen-bonded base-pair. Besides, the 2p and 3p states of the base-pairs and phosphorene hybridizes below of -5.5 eV in the valence band of phosphorene.



Page 26 of 37

Figure 12. Total (TDOS) and partial density of states (PDOS) of the G−phosphorene and CG−phosphorene systems; the green line indicates the position of the HOMO level. All the DOS plots are in the Supporting Information. In summary, the effects of charge doping and bandgap changes into the electronic structure of phosphorene through physisorption of nucleobases and base-pairs suggest that changes in its electric conductance could be implemented for the fast sensing/sequencing of DNA/RNA constituents, where the response of the adsorbent electronic properties is required. Indeed, the bandgap value is directly proportional to the conductance (σ∝∆HL/kT, where k is the Boltzmann constant and T the temperature). The sensing applications need to be computationally explored in deep by means of electron transmission/transport studies as those based on the non-equilibrium Green Function formalism71-72, where the effects of the chemical potential and bias should be evaluated. In this regard, the changes in the conductance of graphene upon the strong physisorption of nucleobases and nucleic acids have allowed the proposal and preparation of DNA/RNA sensing/sequencing devices71-74. 26 ACS Paragon Plus Environment

Page 27 of 37 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


CONCLUSIONS It was demonstrated by dispersion corrected DFT calculations that single DNA/RNA nucleobases are strongly physisorbed onto phosphorene in highly stable stacking patterns, with adsorption energies in the range of 0.64−0.94 eV. The physisorption strength was sorted as G>C>A>T>U. The physisorption does not affect the structure and aromaticity of the nucleobases. Otherwise, the hydrogen-bonded base pairs (CG, AT and AU) are preferably adsorbed in the armchair plane of phosphorene with adsorption energies of 1.28−1.44 eV. The hydrogen bonds of the base pairs remain almost unchanged by binding on phosphorene, even with high stability at room temperature. Furthermore, phosphorene is best suited for physisorption of DNA/RNA constituent compared to graphene, improving the adsorption stability in up to 27% due to the interplay between enhanced dispersion and electrostatic interactions. Therefore, phosphorene emerges as a promising template for self-assembly of DNA/RNA constituents, with an improved adsorption affinity compared to graphene. Additionally, the charge doping and bandgap changes into the electronic structure of phosphorene through physisorption of nucleobases suggest applications in the fast sensing/sequencing of DNA/RNA constituents. ASSOCIATED CONTENT Supporting Information. Complementary data to the main article: XYZ coordinates of all the systems, convergence tests, nucleobase−graphene optimized geometries, and additional data of AIM, NCI, DOS, and molecular dynamics analyses. The Supporting Information is available free of charge on the ACS Publications website.



Page 28 of 37

AUTHOR INFORMATION Corresponding Author *[email protected] Notes The authors declare the absence of any competing financial interests. ACKNOWLEDGMENT Powered@NLHPC: This research was partially supported by the supercomputing infrastructure of the NLHPC (ECM-02). REFERENCES 1.

Li, L.; Yu, Y.; Ye, G. J.; Ge, Q.; Ou, X.; Wu, H.; Feng, D.; Chen, X. H.; Zhang, Y.,

Black Phosphorus Field-Effect Transistors. Nat. Nanotechnol. 2014, 9, 372-377. 2.

Bagheri, S.; Mansouri, N.; Aghaie, E., Phosphorene: A New Competitor for

Graphene. Int. J. Hydrogen Energy 2016, 41, 4085-4095. 3.

Suvansinpan, N.; Hussain, F.; Zhang, G.; Chiu, C. H.; Cai, Y.; Zhang, Y.-W.,

Substitutionally

Doped

Phosphorene:

Electronic

Properties

and

Gas

Sensing.

Nanotechnology 2016, 27, 065708. 4.

Sui, X.; Si, C.; Shao, B.; Zou, X.; Wu, J.; Gu, B.-L.; Duan, W., Tunable Magnetism

in Transition-Metal-Decorated Phosphorene. J. Phys. Chem. C 2015, 119, 10059-10063. 5.

Rahman, M. Z.; Kwong, C. W.; Davey, K.; Qiao, S. Z., 2d Phosphorene as a Water

Splitting Photocatalyst: Fundamentals to Applications. Energy Environ. Sci. 2016, 9, 709728.


Page 29 of 37 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


6.

Cai, Y.; Ke, Q.; Zhang, G.; Zhang, Y.-W., Energetics, Charge Transfer, and

Magnetism of Small Molecules Physisorbed on Phosphorene. J. Phys. Chem. C 2015, 119, 3102-3110. 7.

Yang, Q.; Meng, R.-S.; Jiang, J.-K.; Liang, Q.-H.; Tan, C.-J.; Cai, M.; Sun, X.;

Yang, D.-G.; Ren, T.-L.; Chen, X.-P., First-Principles Study of Sulfur Dioxide Sensor Based on Phosphorenes. IEEE Electron Device Lett. 2016, 37, 660-662. 8.

Mahabal, M. S.; Deshpande, M. D.; Hussain, T.; Ahuja, R., Sensing Characteristics

of Phosphorene Monolayers toward Ph3 and Ash3 Gases Upon the Introduction of Vacancy Defects. J. Phys. Chem. C 2016, 120, 20428-20436. 9.

Ray, S., First-Principles Study of Mos 2, Phosphorene and Graphene Based Single

Electron Transistor for Gas Sensing Applications. Sens. Actuators, B 2016, 222, 492-498. 10.

Rubio-Pereda, P.; H. Cocoletzi, G., Density Functional Theory Calculations of

Biomolecules Adsorption on Phosphorene for Biomedical Applications. Appl. Surf. Sci. 2018, 427, 1227-1234. 11.

Gürel, H. H.; Salmankurt, B., Interaction Mechanism of Biomolecules on Vacancy

Defected 2d Materials. AIP Conf. Proc. 2017, 1815, 050005. 12.

Zhang, W.; Huynh, T.; Xiu, P.; Zhou, B.; Ye, C.; Luan, B.; Zhou, R., Revealing the

Importance of Surface Morphology of Nanomaterials to Biological Responses: Adsorption of the Villin Headpiece onto Graphene and Phosphorene. Carbon 2015, 94, 895-902. 13.

Zhang, W.; Ye, C.; De Luna, P.; Zhou, R., Snatching the Ligand or Destroying the

Structure: Disruption of Ww Domain by Phosphorene. J. Phys. Chem. C 2017, 121, 13621370. 14.

Hanlon, D., et al., Liquid Exfoliation of Solvent-Stabilized Few-Layer Black

Phosphorus for Applications Beyond Electronics. Nat. Commun. 2015, 6, 8563(1-11). 29 ACS Paragon Plus Environment


15.

Page 30 of 37

Yasaei, P.; Kumar, B.; Foroozan, T.; Wang, C.; Asadi, M.; Tuschel, D.; Indacochea,

J. E.; Klie, R. F.; Salehi‐Khojin, A., High‐Quality Black Phosphorus Atomic Layers by Liquid‐Phase Exfoliation. Adv. Mater. 2015, 27, 1887-1892. 16.

Kang, J.; Wood, J. D.; Wells, S. A.; Lee, J.-H.; Liu, X.; Chen, K.-S.; Hersam, M. C.,

Solvent Exfoliation of Electronic-Grade, Two-Dimensional Black Phosphorus. ACS nano 2015, 9, 3596-3604. 17.

Sowerby, S. J.; Stockwell, P. A.; Heckl, W. M.; Petersen, G. B., Self-

Programmable, Self-Assembling Two-Dimensional Genetic Matter. Orig. Life Evol. Biosph. 2000, 30, 81-99. 18.

Varghese, N.; Mogera, U.; Govindaraj, A.; Das, A.; Maiti, P. K.; Sood, A. K.; Rao,

C., Binding of DNA Nucleobases and Nucleosides with Graphene. ChemPhysChem 2009, 10, 206-210. 19.

Mudedla, S.; Balamurugan, K.; Subramanian, V., Computational Study on the

Interaction of Modified Nucleobases with Graphene and Doped Graphenes. J. Phys. Chem. C 2014, 118, 16165-16174. 20.

Mudedla, S. K.; Balamurugan, K.; Kamaraj, M.; Subramanian, V., Interaction of

Nucleobases with Silicon Doped and Defective Silicon Doped Graphene and Optical Properties. Phys. Chem. Chem. Phys. 2016, 18, 295-309. 21.

Lee, J.-H.; Choi, Y.-K.; Kim, H.-J.; Scheicher, R. H.; Cho, J.-H., Physisorption of

DNA Nucleobases on H-Bn and Graphene: Vdw-Corrected Dft Calculations. J. Phys. Chem. C 2013, 117, 13435-13441. 22.

Antony, J.; Grimme, S., Structures and Interaction Energies of Stacked Graphene-

Nucleobase Complexes. Phys. Chem. Chem. Phys. 2008, 10, 2722-2729.


Page 31 of 37 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


23.

Chandra Shekar, S.; Swathi, R., Stability of Nucleobases and Base Pairs Adsorbed

on Graphyne and Graphdiyne. J. Phys. Chem. C 2014, 118, 4516-4528. 24.

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. 25.

Vovusha, H.; Sanyal, B., Adsorption of Nucleobases on 2d Transition-Metal

Dichalcogenides and Graphene Sheet: A First Principles Density Functional Theory Study. RSC Adv. 2015, 5, 67427-67434. 26.

Eslami, M.; Peyghan, A. A., DNA Nucleobase Interaction with Graphene Like Bc 3

Nano-Sheet Based on Density Functional Theory Calculations. Thin Solid Films 2015, 589, 52-56. 27.

Le, D.; Kara, A.; Schröder, E.; Hyldgaard, P.; Rahman, T. S., Physisorption of

Nucleobases on Graphene: A Comparative Van Der Waals Study. J. Phys.: Condens. Matter 2012, 24, 424210. 28.

Gowtham, S.; Scheicher, R. H.; Ahuja, R.; Pandey, R.; Karna, S. P., Physisorption

of Nucleobases on Graphene: Density-Functional Calculations. Phys. Rev. B 2007, 76, 033401. 29.

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. 30.

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.



31.

Page 32 of 37

Arabieh, M.; Azar, Y. T., In Silico Insight into Ammonia Adsorption on Pristine

and X-Doped Phosphorene (X=B, C, N, O, Si, and Ni). Appl. Surf. Sci. 2017, 396, 14111419. 32.

Saikia, N.; Seel, M.; Pandey, R., Stability and Electronic Properties of 2d

Nanomaterials Conjugated with Pyrazinamide Chemotherapeutic: A First-Principles Cluster Study. J. Phys. Chem. C 2016, 120, 20323-20332. 33.

Zhang, Y.; Liu, C.; Hao, F.; Xiao, H.; Zhang, S.; Chen, X., Co2 Adsorption and

Separation from Natural Gason Phosphorene Surface: Combining Dft and Gcmc Calculations. Appl. Surf. Sci. 2017, 397, 206-212. 34.

Zhou, S.; Liu, N.; Zhao, J., Phosphorus Quantum Dots as Visible-Light

Photocatalyst for Water Splitting. Comput. Mater. Sci. 2017, 130, 56-63. 35.

Neese, F., The Orca Program System. Wiley Interdiscip. Rev.: Comput. Mol. Sci.

2012, 2, 73-78. 36.

Neese, F., Software Update: The Orca Program System, Version 4.0. Wiley

Interdiscip. Rev.: Comput. Mol. Sci. 2017, DOI: 10.1002/wcms.1327. 37.

Perdew, J. P.; Burke, K.; Wang, Y., Generalized Gradient Approximation for the

Exchange-Correlation Hole of a Many-Electron System. Phys. Rev. B 1996, 54, 1653316539. 38.

Weigend, F.; Ahlrichs, R., Balanced Basis Sets of Split Valence, Triple Zeta

Valence and Quadruple Zeta Valence Quality for H to Rn: Design and Assessment of Accuracy. Phys. Chem. Chem. Phys. 2005, 7, 3297-3305. 39.

Weigend, F., Accurate Coulomb-Fitting Basis Sets for H to Rn. Phys. Chem. Chem.

Phys. 2006, 8, 1057-1065.


Page 33 of 37 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


40.

Grimme, S.; Antony, J.; Ehrlich, S.; Krieg, H., A Consistent and Accurate Ab Initio

Parametrization of Density Functional Dispersion Correction (Dft-D) for the 94 Elements H-Pu. J. Chem. Phys. 2010, 132, 154104. 41.

Grimme, S.; Ehrlich, S.; Goerigk, L., Effect of the Damping Function in Dispersion

Corrected Density Functional Theory. J. Comput. Chem. 2011, 32, 1456-1465. 42.

Kruse, H.; Grimme, S., A Geometrical Correction for the Inter- and Intra-Molecular

Basis Set Superposition Error in Hartree-Fock and Density Functional Theory Calculations for Large Systems. J. Chem. Phys. 2012, 136, 154101. 43.

Cortés-Arriagada, D., Adsorption of Polycyclic Aromatic Hydrocarbons onto

Graphyne: Comparisons with Graphene. Int. J. Quantum Chem. 2017, 117, e25346. 44.

Lu, T.; Chen, F., Multiwfn: A Multifunctional Wavefunction Analyzer. J. Comput.

Chem. 2012, 33, 580-592. 45.

Verlet, L., Computer "Experiments" on Classical Fluids. I. Thermodynamical

Properties of Lennard-Jones Molecules. Phys. Rev. 1967, 159, 98. 46.

Berendsen, H. J.; Postma, J. v.; van Gunsteren, W. F.; DiNola, A.; Haak, J.,

Molecular Dynamics with Coupling to an External Bath. J. Chem. Phys. 1984, 81, 36843690. 47.

Stewart, J. J., Optimization of Parameters for Semiempirical Methods V:

Modification of Nddo Approximations and Application to 70 Elements. J. Mol. Model. 2007, 13, 1173-1213. 48.

Řezáč, J.; Hobza, P., Advanced Corrections of Hydrogen Bonding and Dispersion

for Semiempirical Quantum Mechanical Methods. J. Chem. Theory Comput. 2011, 8, 141151.



49.

Page 34 of 37

Vorlová, B.; Nachtigallová, D.; Jirásková-Vaníčková, J.; Ajani, H.; Jansa, P.; Řezáč,

J.; Fanfrlík, J.; Otyepka, M.; Hobza, P.; Konvalinka, J., Malonate-Based Inhibitors of Mammalian

Serine

Racemase:

Kinetic

Characterization

and

Structure-Based

Computational Study. Eur. J. Med. Chem. 2015, 89, 189-197. 50.

Gowtham, S.; Scheicher, R. H.; Pandey, R.; Karna, S. P.; Ahuja, R., First-Principles

Study of Physisorption of Nucleic Acid Bases on Small-Diameter Carbon Nanotubes. Nanotechnology 2008, 19, 125701. 51.

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, 12225-12230. 52.

Jasien, P. G.; Fitzgerald, G., Molecular Dipole Moments and Polarizabilities from

Local Density Functional Calculations: Application to DNA Base Pairs. J. Chem. Phys. 1990, 93, 2554-2560. 53.

Johnson, E. R.; Keinan, S.; Mori-Sánchez, P.; Contreras-García, J.; Cohen, A. J.;

Yang, W., Revealing Noncovalent Interactions. J. Am. Chem. Soc. 2010, 132, 6498-6506. 54.

Bader, R. F., Atoms in Molecules; Wiley Online Library, 1990.

55.

Becke, A.; Matta, C. F.; Boyd, R. J., The Quantum Theory of Atoms in Molecules:

From Solid State to DNA and Drug Design; John Wiley & Sons: Weinheim, Germany, 2007. 56.

Noorizadeh, S.; Shakerzadeh, E., Shannon Entropy as a New Measure of

Aromaticity, Shannon Aromaticity. Phys. Chem. Chem. Phys. 2010, 12, 4742-4749. 57.

Cysewski, P., An Ab Initio Study on Nucleic Acid Bases Aromaticities. J. Mol.

Struct.: THEOCHEM 2005, 714, 29-34.


Page 35 of 37 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


58.

Huertas, O.; Poater, J.; Fuentes-Cabrera, M.; Orozco, M.; Solà, M.; Luque, F. J.,

Local Aromaticity in Natural Nucleobases and Their Size-Expanded Benzo-Fused Derivatives. J. Phys. Chem. A 2006, 110, 12249-12258. 59.

Trujillo, C.; Sánchez‐Sanz, G., A Study of Π–Π Stacking Interactions and

Aromaticity in Polycyclic Aromatic Hydrocarbon/Nucleobase Complexes. ChemPhysChem 2016, 17, 395-405. 60.

Udagawa, T., Theoretical Analysis on the Aromaticity of Uracil: Important

Electronic Configurations and Solvent Effect on the Aromaticity. Chem. Phys. Lett. 2015, 637, 115-119. 61.

Giambiagi, M.; de Giambiagi, M. S.; Mundim, K. C., Definition of a Multicenter

Bond Index. Struct. Chem. 1990, 1, 423-427. 62.

Ponec, R.; Mayer, I., Investigation of Some Properties of Multicenter Bond Indices.

J. Phys. Chem. A 1997, 101, 1738-1741. 63.

Giambiagi, M.; de Giambiagi, M. S.; dos Santos Silva, C. D.; de Figueiredo, A. P.,

Multicenter Bond Indices as a Measure of Aromaticity. Phys. Chem. Chem. Phys. 2000, 2, 3381-3392. 64.

Bultinck, P.; Ponec, R.; Van Damme, S., Multicenter Bond Indices as a New

Measure of Aromaticity in Polycyclic Aromatic Hydrocarbons. J. Phys. Org. Chem. 2005, 18, 706-718. 65.

Shukla, M. K.; Dubey, M.; Zakar, E.; Namburu, R.; Leszczynski, J., Density

Functional Theory Investigation of Interaction of Zigzag (7, 0) Single-Walled Carbon Nanotube with Watson–Crick DNA Base Pairs. Chem. Phys. Lett. 2010, 496, 128-132.



66.

Neese,

F.; Wennmohs, F.; Hansen,

A.,

Page 36 of 37

Efficient and

Accurate Local

Approximations to Coupled-Electron Pair Approaches: An Attempt to Revive the Pair Natural Orbital Method. J. Chem. Phys. 2009, 130, 114108. 67.

Cortés-Arriagada,

D.;

Sanhueza,

L.;

Santander-Nelli,

M.,

Modeling

the

Physisorption of Bisphenol a on Graphene and Graphene Oxide. J. Mol. Model. 2013, 19, 3569-3580. 68.

Cortés-Arriagada, D.; Toro-Labbé, A., Improving as (Iii) Adsorption on Graphene

Based Surfaces: Impact of Chemical Doping. Phys. Chem. Chem. Phys. 2015, 17, 1205612064. 69.

Cortes-Arriagada, D.; Miranda-Rojas, S.; Ortega, D. E.; Toro-Labbe, A., Oxidized

and Si-Doped Graphene: Emerging Adsorbents for Removal of Dioxane. Phys. Chem. Chem. Phys. 2017, 19, 17587-17597. 70.

Cortés-Arriagada, D.; Toro-Labbé, A., Aluminum and Iron Doped Graphene for

Adsorption of Methylated Arsenic Pollutants. Appl. Surf. Sci. 2016, 386, 84-95. 71.

Min, S. K.; Kim, W. Y.; Cho, Y.; Kim, K. S., Fast DNA Sequencing with a

Graphene-Based Nanochannel Device. Nat. Nanotechnol. 2011, 6, 162-165. 72.

Heerema, S. J.; Dekker, C., Graphene Nanodevices for DNA Sequencing. Nat.

Nanotechnol. 2016, 11, 127-136. 73.

Ambrosi, A.; Pumera, M., Stacked Graphene Nanofibers for Electrochemical

Oxidation of DNA Bases. Phys. Chem. Chem. Phys. 2010, 12, 8943-8947. 74.

Cho, Y.; Min, S. K.; Kim, W. Y.; Kim, K. S., The Origin of Dips for the Graphene-

Based DNA Sequencing Device. Phys. Chem. Chem. Phys. 2011, 13, 14293-14296.


Page 37 of 37 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


TOC Graphic


RNA

Recommend Documents