Polarity-Induced Surface Recognition and Self-Assembly of

Feb 6, 2018 - Polarity-Induced Surface Recognition and Self-Assembly of Noncanonical DNA Nucleobases on h-BN Monolayer. Nabanita Saikia and Ravindra P...
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Cite This: J. Phys. Chem. C 2018, 122, 3915−3925

Polarity-Induced Surface Recognition and Self-Assembly of Noncanonical DNA Nucleobases on h‑BN Monolayer Nabanita Saikia* and Ravindra Pandey* Department of Physics, Michigan Technological University, 1400 Townsend Drive, Houghton, Michigan 49931, United States S Supporting Information *

ABSTRACT: A systematic understanding of the self-assembly of DNA nucleobases is essential for biomolecular recognition on surfaces of novel 2D materials. Using atomistic molecular dynamics (MD) simulations, we investigate the self-assembly of guanine and cytosine nucleobases on the hexagonal boron nitride (h-BN) monolayer. We find that the self-assembly is driven by the inherent polarity of the bases determining the nature of molecular ordering and growth patterns: guanine into 2D aggregates and cytosine into 1D linear arrays and interconnected molecular chains. The base−base H-bond interactions guide the self-assembly, and the base-surface interactions facilitate surface recognition and monolayer adsorption. Simulations at elevated temperatures find reconstruction at the surface with cytosine forming distinct 1D chains and guanine forming an extended network. We propose that the distinctive patterns in assembly, unique to the DNA nucleobases, would serve as fingerprints for biomolecular recognition at the solid/liquid interface. The ability to control the assembly into well-defined (ordered) patterns would constitute the first step toward integrating self-organized hierarchical nanostructures in DNA based devices at the nanoscale.

1. INTRODUCTION “Sequence complementarity” of nucleic acids owing to its remarkable molecular recognition ability guides the design of programmable self-assembled structural motifs with welldefined periodicity.1 Molecular flexibility and the base-specific H-bond interaction of nucleic acids have facilitated applications in biosensing,2,3 cell-signaling pathways,4,5 and as platforms for the development of molecular machinery.6−8 The instructions to molecular recognition, which are central to self-assembly, are encoded in the structural motifs of the constituent molecules and define the subtle balance in structure−property of selfassembled heterostructures. Molecular self-assembly of DNA nucleobases on 2D materials and surfaces is a rapid, inexpensive, and scalable technique toward the formation of highly ordered hierarchical nanostructures. Compared to nanoparticles, the surface mediated 2D assembly is governed by the internal mismatch between base pairs, molecular cooperativity, noncovalent interactions, and lateral variation in the base-surface interactions.9−12 The noncovalent interactions control molecular orientation and packing, while the electronic properties of 2D materials and growth temperatures determine the assembly and adsorption/desorption limit on surfaces. A rational design of DNA assemblies on 2D materials would, in turn, serve as the Lego (or building blocks) for the formation of DNA based hybrid structures at the nanoscale. Hitherto, graphene has been one of the versatile intermediaries in ultrasensitive detection of nucleic acids, © 2018 American Chemical Society

DNA sequencing, and development of graphene-based sensors for biomedical applications.13−17 Recent advancements in application of graphene has enabled extensive research on the assimilation of alternative 2D materials like graphene oxide,18−20 highly ordered pyrolytic graphite (HOPG), MoS2,21,22 WS2,23 and solid substrates for realizing molecular assembly within the desired functionality.24,25 As an emergent 2D material, a hexagonal boron nitride (hBN) monolayer, also referred to as “white graphene”, is a structural analog of graphene in which alternating B and N atoms substitute C atoms in the atomic lattice.26,27 The electronegativity difference between B and N atoms leads to the localization of π-electrons around N atoms and polarity of B−N bond underlie the charge transfer between B and N atoms. The novel properties of h-BN have attracted research interest in boron neutron capture therapy, biosensing, and DNA sequencing applications.28−31 The DNA-BNNT biofunctional hybrids were exploited for constructing BNNT nematic ordered ensembles.32 The improved wettability (hydrophilicity) of hBN by UV-ozone (UVO) treatment for the translocation of DNA and the fabrication of solid state nanopores are reported.33 Calculations based on first-principles methods on physisorption of DNA nucleobases on h-BN and graphene Received: December 5, 2017 Revised: February 4, 2018 Published: February 6, 2018 3915

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Scheme 1. (a) Molecular Configurations of Cytosine (C) and Guanine (G), (b) h-BN Monolayer, and (c) Self-Assembly and Growth Patterns of C and G Bases on h-BN

2. COMPUTATIONAL DETAILS The MD simulations were performed in gas and aqueous phases using the all atom CHARMM27 force field 47 implemented in the NAMD program.48 For aqueous phase simulation, the water molecules were modeled by the TIP3P,49 with constraints applied to the bond lengths and angles using the SETTLE algorithm. The dimension of the periodic supercell of h-BN is (61.24 × 63.62 Å2) comprised of 1500 carbon atoms. The partial charges and force field parameters for modeling the h-BN surface were adopted from previous theoretical reports.50 The MD simulations of Cn/h-BN and Gn/h-BN at intermediate and saturated coverage proceeded with 2000 steps of energy minimization followed by production run of 50 ns at a time-step of 1.0 fs. The particle mesh Ewald (PME)51 summation method was considered to calculate the electrostatic interactions with a long-range cutoff of 12.0 Å. The NVT and isothermal−isobaric (NPT) ensembles using the Langevin dynamics and the Langevin piston Nose-Hoover method were employed to maintain the pressure to 101.3 kPa. The convergence of MD simulation and overall stability of the system were confirmed using the root mean-square deviation (RMSD) over the trajectory. The number of Hbonds, base-surface (vertical) π-stacking distance, base−base intermolecular H-bond distance, radial distribution function (RDF), and radius of gyration (Rg) were further analyzed using the VMD plugin.52 The RDF or pairwise correlation function represents the probability to find an atom at a distance r of another reference atom. The base-surface interaction energy of Cn/h-BN and Gn/hBN systems are defined as

show that the binding energy follows the order: G > A > T > C.34,35 Noteworthy, the self-assembly protocols on insulating surfaces like h-BN for the construction of hierarchical nanostructures remains largely unexplored.36 Although there are experimental reports on the assembly of organic molecules into thin films on solid substrates and 2D surfaces, understanding the subtle details of the supramolecular assembly process and a precise control over the resulting phase is rather limited.37 It has been reported that the self-assembly on surfaces can be either reversible and/or irreversible.36,38,39 Complementary to experiment, atomistic MD simulations can provide notable theoretical insights and reinforce our present understanding associated with molecular stability, aggregation dynamics, noncovalent vdW and electrostatic contributions to molecular assembly, and ambient (simulation) conditions for the integration of nucleic acids with h-BN at the solid/liquid interface. Viewed from above, the present study investigates the growth patterns, molecular ordering, and self-assembly of noncanonical DNA nucleobases namely, guanine and cytosine on h-BN. Guanine (G) and cytosine (C) are taken as the representative cases based on the following exclusive considerations: guanine has the highest dimerization energy, low ionization potential, and strong electron-donor/acceptor characteristics,40,41 which enables the formation of supramolecular hierarchical assemblies.42,43 The presence of three H-bond acceptor (N7, N3, and O6) and two H-bond donor (N1, and N2) sites simultaneously behave as Brønsted acid and base, and exhibit an exquisite internal H-bonded motif.44 In cytosine, the donor (N1 and N7) and acceptor (O12 and N10) sites are rather localized,45 which restricts the ability to form long-range ordered arrays, while medium range 1D structural motifs are possible.46 The calculated equilibrium configurations of G and C43 and a schematic illustration of the hierarchical self-assembly patterns on h-BN are shown in Scheme 1. The present study predicts that donor/acceptor sites of the nucleobases mediate the base− base intermolecular interactions and in-turn regulate the distinctive growth patterns on h-BN as illustrated in Scheme 1c.

E int = Eadsorbed − Enoninteracting

(1)

where Eadsorbed is the potential energy of the system when the bases are in an adsorbed state on h-BN surface and Enoninteracting is the potential energy of the system when the bases are separated from the h-BN surface at a lateral distance of ∼25.0 Å, mimicking a noninteracting system. To evaluate the energetics contribution from the different constituents of the total interaction energy, the calculated basesurface interaction energy defined in eq 1 was further 3916

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Figure 1. Gas phase (intermediate coverage) snapshots of cytosine and guanine self-assemblies on h-BN: (a) C36/h-BN and (b) G36/h-BN. (c) Unit cell parameter of cytosine.

Figure 2. Gas phase (saturated coverage) snapshots of cytosine and guanine self-assemblies on h-BN: (a) C72/h-BN and (b) G72/h-BN. (c) Unit cell parameter of cytosine.

10−4 eV/Å. The convergence criteria in density matrix and total energy were 10−8 and 10−6 eV, respectively.

decoupled into the vdW and electrostatic counterparts. The present generation CHARMM force field no longer includes an explicit H-bonding energy term, because the Coulomb and Lennard-Jones terms account for the H-bonding interactions.52−54 The H-bonds that are observed in NAMD simulations using the CHARMM force field are a result of the electrostatic interactions,55 and the force field does treat the all-atom pairwise ligand−ligand, ligand−water, and water− water interactions in a consistent manner.54 The electronic properties of self-assembled cytosine and guanine nucleobases in the gas phase was investigated within the framework of vDW dispersion-corrected DFT. The exchange correlation was described by the Generalized Gradient Approximation (GGA) using the wB97xD functional56 and a 6-31G (d,p) basis set.42,57,58 All of the calculations were performed using Gaussian 09,59 with the maximum force convergence for geometry optimization set to

3. RESULTS AND DISCUSSION 3.1. Gas-Phase Self-Assembly on h-BN. The selfassembly of cytosine and guanine on h-BN in the gas phase was considered for two surface coverages: (i) intermediate and (ii) saturated, modeled with 36 and 72 bases, respectively. Figure 1a,b shows the snapshots of C36/h-BN and G36/h-BN at intermediate coverage. The assembly of cytosine on h-BN is characterized by interconnected linear 1D arrays at room temperature with well-defined periodicity. The orientation of donor/acceptor sites in cytosine is stabilized by the intermolecular H-bonds as shown in the inset of Figure 1a. This organization maximizes the alignment of polar groups within cytosine. While the parallel orientation of adsorption proffers the base−surface interaction, a tilted orientation is 3917

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Figure 3. (a) Gas phase: Interaction energy and interaction energy/base of Cn/h-BN and Gn/h-BN (for n = 36 and 72) and (b) average number of H-bonds, π-stacking distance, and intermolecular H-bond distance for Cn/h-BN and Gn/h-BN (for n = 36 and 72).

Figure 4. Aqueous phase (intermediate coverage) snapshots of cytosine and guanine self-assemblies on h-BN; (a) C36/h-BN and (b) G36/h-BN. Panels c and d show the intermolecular H-bond interaction between cytosine (c) and guanine (d) bases, respectively. (e) The π-stacking interaction between two guanine bases adsorbed on h-BN.

surface60 and G-quartet motifs on Au (111) surface where a single guanine interacts via three intermolecular H-bonds per molecule.61 The STM imaging on the self-assembly of DNA bases on Cu (111) substrate demonstrates a similar patterning for cytosine and guanine with an increased intermolecular Hbond stabilization facilitating molecular aggregation with islandsized distribution.62 The saturated surface coverage modeled with 72 bases depicts 1D linear arrays for cytosine and a 2D aggregated network for guanine as shown in Figure 2a,b. The unit cell for cytosine is projected in Figure 2c and consists of four bases per unit cell with lattice parameters a = 6.90 Å, b = 6.60 Å, α = 58.9°, and β = 121.1°, which is comparable to the cell parameters calculated for the intermediate coverage. For guanine, we could not characterize a unit cell due to the absence of periodicity in self-assembly at both the intermediate and high coverage levels. The base−surface interaction energy and interaction energy/ base between Cn/Gn and h-BN (for n = 36 and 72) are provided in Figure 3a. The interaction energy for a cytosine and guanine monomer adsorbed on h-BN is also drawn for comparison. The Gn/h-BN has higher interaction energy values compared to Cn/h-BN at the intermediate and saturated coverages. This may be attributed to (i) molecular geometry,

observed at the intersection between two linear arrays (labeled by red arrows in Figure 1a). The in-plane dipole moment causes a tilt in orientation of cytosine, and stabilization is rendered from the intermolecular H-bonds between the bases, rather than the base−surface interaction (unpublished results). The unit cell for cytosine is depicted in Figure 1c and consists of four bases per unit cell with lattice parameters a = 7.06 Å, b = 6.40 Å, α = 60.05°, and β = 119.95°. The guanine bases prefer to assemble in a square 2D lattice with no well-defined periodicity as shown in Figure 1b and inset panel. A close inspection of the extended assembly reveals random clustering of guanine in a condensed 2D network. The formation of 2D supramolecular network can be associated with the highest G-G dimerization energy (−1.48 eV) > G-C (Watson Crick base pair) dimerization energy of −1.16 eV.43 The growth patterns of cytosine and guanine on h-BN are distinctive of the underlying surface and are in stark contrast to those reported on graphene, highly ordered pyrolytic graphite (HOPG), Au (111), and Cu (111) surfaces. On graphene, MD studies predict guanine to aggregate in a highly condensed 2D network with the formation of G-quartet domains at intermediate coverage.42 The scanning tunneling microscopy (STM) imaging studies under ultrahigh vacuum (UHV) conditions suggest a quasi-square arrangement on the HOPG 3918

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Figure 5. (a) Aqueous phase: interaction energy and interaction energy/base of Cn/h-BN and Gn/h-BN (for n = 36 and 72) and (b) average number of H-bonds, π-stacking distance, and intermolecular H-bond distance of Cn/h-BN and Gn/h-BN (for n = 36 and 72). The RDF of (c) C36/h-BN and G36/h-BN and (d) h-BN with oxygen and hydrogen atoms of water.

3.2. Aqueous-Phase Self-Assembly on h-BN. The selfassembly of cytosine and guanine on h-BN is shown in Figure 4a,b. In going from gas phase to aqueous phase, there exists disruption in the base−base interaction leading to a higher degree of immobilization on h-BN. At intermediate coverage, cytosine forms loosely connected linear arrays (see Figure 4a), and the cytosine−cytosine aggregation is facilitated by the intermolecular H-bond interactions. Each cytosine is stabilized by ∼2 H-bonds as shown in Figure 4c. For guanine, both the base−surface and base−base π-stacked domains are observed as shown in Figure 4b,e. The intermolecular H-bond interaction between guanine is quite random due to a higher degree of immobilization at intermediate coverage. One of the preferential modes of the intermolecular H-bond interaction is depicted in Figure 4d wherein each guanine is stabilized by ∼4 H-bonds. At saturated coverage, snapshots exhibit a similar assembly pattern with random dispersion of the bases as shown in Supporting Information, Figure S1a,b, respectively. We find that the growth patterns of cytosine and guanine are dependent on the simulation conditions (gas vs aqueous) at both intermediate and saturated coverages and the solvent polarity affects the self-assembled structures; the high dielectric constant of water (∼80) destabilizes the intermolecular H-bond or dipole−dipole interactions between the bases with formation of water hydration spheres around the bases as shown in Figure 4e. Note that solvophobicity and polarity can affect self-

(ii) donor−acceptor interacting sites, and (iii) the ability for enhanced π-orbital overlap on the h-BN surface. Guanine and cytosine favor the parallel orientation of adsorption on h-BN maximizing the base-surface interactions, though a slightly titled orientation can be seen for cytosine (Figures 1a and 2a). The steric interactions between cytosine lead to titling of some of the bases with the dipole moment vector aligned normal to hBN surface. The interaction energy/base at the two coverage levels is consistent with a single base molecule adsorbed on hBN with G/h-BN > C/h-BN. The average base−base intermolecular H-bond distance is ∼1.70−1.73 Å, while the average base-surface π-stacking distance is ∼3.25−3.40 Å (see Figure 3b). The calculated πstacking distance agrees well with the DFT studies on physisorption of DNA bases on the h-BN cluster.34 Recent vdW-corrected DFT studies investigating the adsorption of DNA nucleobases on graphene, MoS2, and WS2 reported the vertical separation to be in the range of 3.54−3.58 Å for graphene, 3.52−3.64 Å for MoS2, and 3.53−3.61 Å for WS2.63 Figure 3b shows the average number of H-bonds at intermediate and saturated coverages which are comparable for Cn/h-BN and Gn/h-BN; C36/h-BN (24), G36/h-BN (27), C72/h-BN (50), and G36/h-BN (49). On an average, a slightly higher count of the intermolecular H-bonds in guanine at intermediate coverage can be correlated to the formation of an aggregated 2D network, thereby maximizing the base−base Hbond interactions via the donor−acceptor sites. 3919

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Figure 6. (a) Geometry of a cytosine unit cell, (b) ESP of a cytosine unit cell, and (c) ESP of an extended linear array of cytosine modeled with seven bases. The frontier molecular orbitals corresponding to HOMO (d) and LUMO (e) of an extended linear array of cytosine.

assembly,64 as a nonpolar molecule will have higher propensity to form close-packed assemblies in the presence of polar solvent.65,66 In our study, both the DNA bases and water are polar molecules which do not promote a close-packed assembly but rather disrupt the base−base interactions in aqueous phase. The base−surface interaction energy and interaction energy/ base between Cn/Gn and h-BN (for n = 36 and 72) in the aqueous phase is shown in Figure 5a. To provide a qualitative estimate of the stability lost or gained for a cytosine and guanine nucleobase adsorbed on h-BN in the presence of water, we compared the difference in the base−surface interaction energy of Cn/h-BN and Gn/h-BN systems in gas and aqueous phases. The presence of water enhances the stability of the system as shown in Figures 3a and 5a; for Cn/h-BN, the aqueous stability increases by ∼25−30%, while for Gn/h-BN, the aqueous phase stability increases by ∼38−43%. The higher net gain in stability of guanine over cytosine can be correlated to the higher polarizability and the availability of H-bond donor and acceptor sites in guanine. The change in base−surface vdW and electrostatic interaction energy for C36/h-BN and G36/h-BN systems in gas and aqueous phases is provided in Figures S2a,b of the Supporting Information. In the gas phase, the vdW interaction energy is calculated to be higher than the electrostatic interaction contributing to the overall stabilization of the system. Guanine has a higher per base vdW interaction energy of ∼−0.65 eV compared to that for cytosine (∼−0.36 eV) as shown in Figure S2a. Additionally, the base−base intermolecular interaction induces electrostatic interaction: ∼−0.11 eV for Cn/h-BN and ∼−0.16 eV for Gn/h-BN. Likewise, in the aqueous phase, in addition to the base−surface interactions, the base−water, h-BN−water, and water−water interactions also contribute to the total interaction energy of the system. Similar to the gas phase, the vdW energy is found to be predominant in stabilizing the system. The presence of water leads to an increase in the electrostatic interaction energy; guanine has higher values of both vdW and electrostatic interaction energies compared to cytosine (see Figure S2b). For Cn/h-BN, the increase in stability is ∼37% for vdW interaction and ∼24% for

electrostatic interactions in aqueous phase, while for Gn/h-BN, the vdW contribution is ∼33% and electrostatic contribution is ∼25%. This suggests that the vdW along with electrostatic interaction energy contribute to the stabilization of the nucleobases on the h-BN surface in both gas and aqueous phases. A recent MD study on the interaction of polyaniline with boron-nitride sheet reported the vdW dispersion term to be dominant in stabilizing polyaniline on the surface.67 The MD results were compared with the DFT calculations at the BLYPD/TZP level of theory, which further supports that the dispersion energy predominantly contributes to the interaction energy. On the other hand, for single walled carbon nanotubes (CNTs), the vdW interaction energy becomes favorable with a decrease in the curvature of the nanotube.68 The loss in electrostatic contribution of peptide is compensated by the increase in the vdW energy component in the complex. Similarly, MD study of DNA nucleobases conjugated h-BN suggested that the electrostatic interaction determines the interfacial interaction with h-BN, while the vdW interaction contributes as the dominant term in the net stabilization of the system.69 It has also been reported that, for nonpolar molecules, the phase transition to an ordered state is governed by the intermolecular vdW interactions rather than electrostatic interactions, while for polar molecules, both vdW and electrostatic interactions simultaneously control the assembly process.70 For example, in the tetracyanoquinodimethane (TCNQ)−phosphorene system, when the vdW interaction was reduced to half, the 2D lattice of TCNQ was completely disrupted after removing the partial charges, thereby confirming the importance of the electrostatic interaction in the 2D lattice formation.69 A lowering of the average number of H-bonds between the bases in aqueous phase is due to the water induced disruption in base−base aggregation on h-BN (see Figure 5b). At intermediate and saturated coverages, cytosine has higher Hbonds compared to guanine. The formation of linear arrays and localized clusters between cytosine as opposed to the 3920

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Figure 7. (a) Geometry of a condensed guanine network modeled with 12 bases and (b) ESP of corresponding guanine network.

Figure 8. Snapshots of C36/h-BN and G36/h-BN systems at elevated temperatures ranging from 450 to 700 K. (a−d) C36/h-BN and (e−h) G36/hBN.

preferentiality of guanine to form π-stacked domains within itself, along with monolayer adsorption is ascribed to a lower number of H-bonds in the latter. On an average, the calculated base−surface (π-stacking) distance is consistent with the gasphase results, while the intermolecular H-bond distance increases to ∼1.79−1.87 Å which is due to water-induced perturbation in the base−base aggregation. The radial distribution function of cytosine and guanine at intermediate coverage is shown in Figure 5c. A single broad RDF for C36/h-BN and G36/h-BN at ∼3.5 Å corresponds to the vertical interacting distance of the bases on h-BN, in agreement with the calculated π-stacking distance. Note that the RDF of water on h-BN shows two broad peaks. The first broad peak slightly below 4.0 Å, denoted by (1), corresponds to the first water ordering distance on h-BN as shown in the inset of Figure 5d. The second broad RDF, denoted by (2), corresponds to the second water ordering distance on h-BN. Previous MD studies on the self-assembly of cytosine and guanine on graphene predict the RDF of graphene−water slightly above 4.0 Å,42,47 while on h-BN it is below 4.0 Å, which is ascribed to the ionic nature of B−N bonds. 3.3. Self-Assembly Mechanisms on h-BN: DFT Calculations. To ascertain the detailed insights on the intermo-

lecular H-bond stabilized organization in the assembly of cytosine, the electrostatic potential (ESP) isosurface was studied for a fragment of 1D aligned cytosine, at the DFT (wB97xD/6-31G (d,p)) level of theory. We considered two representative units for cytosine: (1) tetramer cytosine bases and (2) a linear 1D array comprising of seven base molecules, as shown in Figure 6. The ESP demonstrates a uniform charge distribution within cytosine (see Figure 6b,c). The regions with negative and positive electron density reside along the two extremes with the intermediate charge density in the central region. This affirms the predicted molecular ordering and growth pattern of cytosine on h-BN. Likewise, the frontier molecular orbitals corresponding to HOMO and LUMO represent states which are localized on the terminal cytosine molecules within the linear array as shown in Figure 6d,e. The absence of electronic charge distribution on the other cytosine molecules might explain the preferentiality in formation of the linear 1D network. The geometry and ESP isosurface of a condensed guanine network modeled with 12 bases are shown in Figure 7a,b. The anisotropic ESP is observed for guanine, with regions of negative to positive charge density distributed within the 2D network as shown in Figure 7b. The lack of molecular 3921

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Figure 9. Gas-phase radius of gyration (Rg) of (a) C36 and (b) G36 bases. (c) The number of H-bonds in C36 and G36 bases for temperatures in the range of 298−700 K.

Simulations at elevated temperature lead to the formation of extended guanine arrays on h-BN (see Figures 8e−h and 1b for a comparison). The coupling between guanine bases, irrespective of thermal annealing, is rather random on the hBN surface. Annealing, thus, leads to a less dense assembly in guanine and does not induce any corrugation within the h-BN monolayer. The radius of gyration (Rg) of cytosine and guanine in C36/hBN and G36/h-BN as a function of temperature are further considered to understand the structural stability (or compactness) of the bases adsorbed on h-BN. The fluctuations in Rg are found to be uniform for temperatures between 400 and 520 K, as shown in Figure 9a,b. Although molecular assembly on h-BN is predicted to be spontaneous in the gas phase, high molecular flexibility and thermal fluctuations at elevated temperature contribute to the prominent oscillations in Rg values over the trajectory at 650 and 700 K. For cytosine, at 650 K, Rg demonstrates an abrupt increase from 25 to 30 Å at ∼10 ns (see Figure 9a). Likewise at 700 K, the fluctuations in Rg are prominent over the trajectory, which corresponds to the random oscillation of cytosine 1D arrays on h-BN. On the other hand, variation in Rg of guanine is calculated at ∼20−25 Å (see Figure 9b), with high temperature induced thermal fluctutations at 650 and 700 K. Interestingly, the Rg of guanine is observed to be somewhat uniform (except at 650 and 700 K) which can be correlated to the extended 2D network, in contrast to distinct 1D linear chains in cytosine. We believe that molecular geometry, polarity, and ability for an enhanced π-orbital overlap of guanine on h-BN attributes to the uniform variation in Rg, signaling toward more compact selfassembled heterostructures. In addition, the number of Hbonds between cytosine and guanine bases at intermediate coverage decreases with elevation of temperature, suggesting a lowering in intermolecular interactions between the base pairs

periodicity and localized charge density regions within the assembly mediates the random alignment of guanine, wherein each guanine is stabilized by ∼4−5 intermolecular H-bonds and has ∼4−5 guanine neighbors. With the growth of the 2D aggregated network of guanine on h-BN, an increase in anisotropic ESP distribution is observed (see the Supporting Information, Figure S4a,b for a comparison). The previously reported theoretical and experimental studies have focused extensively on the self-assembly of nonpolar, symmetric organic molecules at the solid/liquid interface showing a well-defined long-range molecular ordering and growth patterns. However, in the present study, the results obtained for DNA nucleobases are quite striking, in the sense that the inherent polarity, lack of molecular symmetry, and the influence of underlying surface lead to a higher flexibility in molecular orientation and formation of myriad self-assembled structural motifs. 3.4. Temperature Dependence on Molecular SelfAssembly. MD simulations at elevated temperatures were considered to investigate the growth patterns, aggregation dynamics, and phase-transition in the self-assembly process. We focused on the gas-phase intermediate coverage for C36/h-BN and G36/h-BN as it is much easier to monitor the events in the assembly process with thermal annealing. The annealing temperatures are based on a previous experimental study on the self-assembly of graphene nanoribbons on Au (111).71 For C36/h-BN, annealing the system at temperatures in the range of 450−700 K promotes the formation of elongated 1D chains as shown in Figure 8a−d. The 1D network of cytosine splits into distinct linear chains, accompanied by an asymmetric unzipping of the interconnected 1D arrays as observed in the room temperature simulations (see Figure 1a). For G36/h-BN, thermal annealing does not render any well-defined periodicity within the 2D condensed network as shown in Figure 8e−h. 3922

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4. CONCLUSIONS In summary, self-assembly and growth patterns of guanine and cytosine nucleobases on h-BN as a function of molecular surface coverage are investigated using atomistic MD simulations. The noncovalent interactions central to selfassembly can collectively generate stable assemblies and define the subtle balance in the structure−property of self-assembled heterostructures. We find that polarity of nucleobases guides the molecular ordering and growth patterns on h-BN: guanine into a 2D aggregated network and cytosine into short- to medium-order 1D linear arrays and interconnected molecular chains. The base−base interactions via the intermolecular Hbonds are crucial in guiding the self-assembly while the base− surface interactions facilitate surface recognition and monolayer adsorption on h-BN. The molecular orientation of guanine on h-BN is found to be random in both gas and aqueous phases, which is correlated to the donor−acceptor sites and an enhanced intermolecular Hbond interaction. Cytosine, on the other hand, demonstrates periodicity in self-assembly on h-BN at both intermediate and saturated coverage with medium-range molecular ordering. The growth patterns of cytosine and guanine were further supported by the vdW corrected DFT calculations which illustrate the ESP charge density distribution over the assembled molecular arrays. Aqueous phase screens the base−base intermolecular interactions followed by reduction in the H-bonds at both intermediate and saturated coverage. Thermal annealing at elevated temperature promotes the enhanced mobility of nucleobases on h-BN: cytosine forms distinct 1D linear chains while guanine forms an extended 2D network. Compared to room temperature, annealing at higher temperatures predicts a decrease in the base−base intermolecular H-bonds, and the conformational flexibility toward the aggregation dynamics of the base pairs is substantiated from the radius of gyration. We propose that the distinctive patterns in assembly on the h-BN monolayer would serve as fingerprints for biomolecular recognition at the solid/liquid interface. The self-assembly of DNA bases would provide a unique route in the design of hierarchical nanostructures and growth of thin films with medium- to long-range molecular ordering. The inherent electronic properties of the underlying surface (inorganic vs metallic), in turn can tune the molecular epitaxy toward the assembly process. Realizing how the self-assembly on h-BN compares to those on 2D materials like graphene and/or MoS2 would help in elucidating the factors that correlate to the formation of well-defined (ordered) arrangements on 2D surfaces. The formation of stable 2D DNA/h-BN hybrid nanostructures possibly will open new avenues in research for the design and application of novel DNA based biosensors and biocompatible nanoelectronic devices.

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400 K. The vdW and electrostatic interaction energy values of C36/h-BN and G36/h-BN in gas and aqueous phases. The equilibrium geometry, ESP isosurface, and frontier orbitals corresponding to HOMO and LUMO of a guanine network modeled with six bases. (PDF)

AUTHOR INFORMATION

Corresponding Authors

*E-mail: [email protected]. *E-mail: [email protected]. ORCID

Nabanita Saikia: 0000-0001-9648-2363 Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS Helpful discussions with Kevin Waters, Max Seel, and S. Gowtham of Michigan Technological University are kindly acknowledged. N.S. acknowledges financial support from Michigan Technological University. The Superior highperformance computing cluster at Michigan Technological University was utilized in obtaining the results presented in the study.

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ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.jpcc.7b11993. Snapshots of C72/h-BN and G72/h-BN in aqueous phase. Snapshots of C36/h-BN and G36/h-BN in gas phase at 3923

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