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Binding mechanisms of DNA/RNA nucleobases adsorbed on graphene under charging: first-

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 Mater. Res. Express 4 (2017) 065401 https://doi.org/10.1088/2053-1591/aa6e67

PAPER

Binding mechanisms of DNA/RNA nucleobases adsorbed on

graphene under charging: first-principles van der Waals study
RECEIVED
22 February 2017
RE VISED
30 March 2017
ACCEP TED FOR PUBLICATION
Hikmet Hakan Gürel1 and Bahadır Salmankurt1,2
1
21 April 2017 Technology Faculty, Department of Information Systems Engineering, Kocaeli University, Kocaeli 41380, Turkey
2
PUBLISHED
Department of Physics, Sakarya University, 54187 Sakarya, Turkey
5 June 2017 E-mail: h.hakan.gurel@gmail.com

Keywords: graphene, nucleobases, charging, binding energies, density functional theory

Abstract
Graphene is a 2D material that has attracted much attention due to its outstanding properties. Because
of its high surface area and unique chemical and physical properties, graphene is a good candidate
for biological applications. For this reason, a deep understanding of the mechanism of interaction of
graphene with biomolecules is required. In this study, theoretical investigation of van der Waals effects
has been conducted using density functional theory. Here we show that the order of the binding energies
of five nucleobases with graphene is G  >  A  >  T  >  C  >   U. This trend is in good agreement with most
of the theoretical and experimental data. Also, the effects of charging on the electronic and structural
properties of the graphene-nucleubase systems are studied for the first time. We show that the binding
energy can be changed by adding or removing an electron from the system. The results presented in
this work provide fundamental insights into the quantum interactions of DNA with carbon-based
nanostructures and will be useful for developments in biotechnology and nanotechnology.

1. Introduction

Graphene, a recently discovered nanomaterial, which comprises one layer of sp2 hybridized carbon atoms arranged
in a honeycomb lattice, has attracted many researchers due to its unique properties such as massless Dirac fermions,
high optical transmittance, good electrical and thermal conductivity and abnormal mechanical flexibility [1–6].
Applications in medicine and biology and interactions of molecules (especially DNA and RNA nucleobases) with
graphene have also received attention due to the properties of these molecules such as molecular recognition and
self-assembly [7]. Many important studies have been done to understand the mechanism by which nucleobases
bind to graphene and to discover the binding energy of adenine (A), guanine (G), cytosine (C), thymine (T) and
uracil (U) to graphene and related 2D materials. For example, in the study conducted by Duy Le et al [8], G had
the highest binding energy, with binding energy decreasing in the order G, A, T, C and U, calculated using DFT-D2
[9]. Jun-Ho Lee et al used the Perdew–Burke–Ernzerhof (PBE) and PBE  +  van der Waals (vdW) functionals to
investigate the similar binding mechanism of nucleobases with graphene and hexagonal boron nitride [10]. They
showed a similar order of binding energies. Most recently, Hakkim Vovusha et al made a comparative study using
graphene-based nucleobases [11]. Although interactions between biomolecules and graphene are important, a
detailed understanding of the binding mechanism of biomolecules on graphene is lacking. It is known that this
interaction is long-ranged and very weak, so it would be very desirable to develop new techniques for designing
of bioelectronics sensors and devices.
There have been several theoretical investigations on charged nanosystems [12–18]. These studies have shown
that the physical properties of a system can be affected when it is charged. This charging can be simulated by chang-
ing the number of electrons in the unit cell, and mechanisms of interaction of nucleobases and graphene can be
changed by the applied charge. Thus, we have investigated binding mechanism of DNA/RNA bases with graphene
by using the plane-wave (PW) pseudopotential (PP) approach within the generalized gradient approximation
(GGA) of density functional theory (DFT). We found that the trend of the calculated interaction energies within
the vdW functional [8, 10] verified our results. We also show here how the structural and electronic properties of
nucleobases on graphene are affected by the applied charge.

© 2017 IOP Publishing Ltd

Mater. Res. Express 4 (2017) 065401 H H Gürel and B Salmankurt

Figure 1.  The optimized structures of adsorbed nucleobase adenine (a), guanine (b), cytosine (c), thymine (d) and uracil
(e) on a graphene layer. The circles represent C (brown), N (light blue), O (red), and H (light pink) atoms. For clarity C atoms on the
nucleobases are drawn in a different (green) color.

2.  Computational details

We used DFT methods to explore the adsorption geometries, energies and dynamics of nucleobases (model
biomolecule)/graphene composite systems. Our calculations were made using the PW-PP approach within DFT
as implemented in the QUANTUM ESPRESSO code [19]. The DFT has been realized in the GGA, using the PBE
method [20] with DFT-D2 [9] to define vdW interactions. Electron–ion interactions are described using ultrasoft
PP [21]. The Brodyden–Fletcher–Goldfarb–Shanno (BFGS) [22] minimization scheme was used in geometric
optimization. In order to mimic a 2D system, we employ a 5  ×  5 supercell geometry (figure 1) with a vacuum space
of about 19 Å in the z-direction so that the interaction between two adjacent unit cells in the periodic arrangement
is negligible. To investigate the effects of larger supercell geometry, we checked the interaction energy between
two periodic molecules along the xy plane for a 5  ×  5 supercell; this was found to be about 10 meV. Thus, it is a
computationally effective strategy to perform calculations with 5  ×  5 supercell geometry.
For Brillouin zone integration, we used a 3  ×  3  ×  1 k-point mesh [23]. The maximum PW cutoff energy is
taken as 35 Ry, while the electronic charge density is expanded in a basis cutoff up to 380 Ry. Integration up to the
Fermi surface is done by a smearing technique using a Methfessel–Paxton (MP) smearing of 0.005 Ry. The starting
point of the relaxation was determined to be in the middle of the supercell on the xy plane. For the band structure

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Mater. Res. Express 4 (2017) 065401 H H Gürel and B Salmankurt

Table 1.  Calculated binding energies compared with previous studies (in eV).

G A T C U

Without vdW
Present 0.082 0.049 0.043 0.052 0.045
PBE [10] 0.14 0.06 0.08 0.13
PBE [11] 0.099 0.052 0.052 0.072 0.041

With vdW
Present 0.70 0.59 0.57 0.52 0.50
PBE  +  vdW [10] 1.18 1.00 0.95 0.93
vdW-DF [10] 0.74 0.63 0.60 0.58
PBE  +  vdW [10] 0.99 0.85 0.76 0.76
DFT-D2 [8] 0.77 0.64 0.58 0.57 0.52

Table 2.  Calculated average distance from graphene (in Å).

G A T C U

Without vdW
Present 3.38 4.09 4.10 3.99 3.96
PBE [10] 3.95 4.00 4.02 3.97
With vdW
Present 3.15 3.20 3.19 3.17 3.14
PBE  +  vdW [10] 3.26 3.29 3.29 3.27
DF-D2 [8] 3.13 3.18 3.22 3.20 3.20

calculations we used the special 60 k-points along the high-symmetry directions. The geometric structures were
drawn using Vesta software [24].

2.1.  Binding energies

The binding energy, Eb, can be calculated from the expression
Eb =  Egraphene +  EM –  EM+grapheme
(1)
in terms of the total energies of pristine graphene and of the molecule M (M  =  A, G, C, T or U), and the total energy
of M adsorbed to each graphene supercell, respectively.

3.  Results and discussions

3.1.  Comparison of adsorption geometries and binding energies

The optimized geometries of DNA/RNA nucleobases physisorbed on a graphene sheet are presented in figure 1.
We examined the several different orientations (including tilted orientations) of nucleobases on graphene. The
most favorable binding energies and average vertical distances are presented in tables 1 and 2, respectively.
Our calculated distances between graphene and nucleobases are in good agreement with previous reports [
10, 11]. All nucleobases are placed parallel to the graphene layer because of π–π interactions. According to our
analysis, unlike silicene [25], there is no significant relation between the distances between graphene and the nucle-
obases and the binding energies [11]. Also, we conclude that PBE results give lower binding energies of less than
0.2 eV (table 1), and thus larger interaction distances of about 4.0 Å (table 2). Interactions between nucleobases and
the graphene layer cannot be correctly described by the PBE results, as in the local density approximation (LDA)
[8]. These results indicate that dispersion correction is necessary. When the dispersion correction of Grimme
(vdW-D2) is included, the binding energies increase as expected. It should be noted that adsorption of the mol-
ecules on the monolayer is mainly due to vdW interaction. Our DFT-D2 results are in good agreement with the
previous vdW studies [8, 10].
We also show the closest distances from the graphene plane in table 3 and the closest atoms to graphene in
figure 2. According to Bader charge analysis [26, 27], for G, A, C and U, hydrogen atoms bonded with N have less
charge than H atoms bonded to other atoms due to the electronegativity of the N atom. So, those atoms move closer
to the graphene plane than other H to get more charge. This is also seen in the H atom of four-bonded carbon in
the T molecule. This is also seen in the H atom of four-bonded carbon in the T molecule.
We compared our results with experimental data. First, we performed the calculations using a pristine graphene
structure. Second, the interaction between nucleobases and graphene in this work was calculated in a vacuum, so

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Mater. Res. Express 4 (2017) 065401 H H Gürel and B Salmankurt

Table 3.  For each nucleobase (G, A, T, C or U) the closest pair of atoms between the graphene sheet (C) and the base (only H) is given along
with their respective distance (in Å).

Nucleobases Closest atoms Distance C–base

G C–H 2.705
A C–H 3.015
T C–H 2.614
C C–H 2.946
U C–H 2.998

Figure 2.  Top view of (a) guanine, (b) adenine, (c) thymine, (d) cytosine and (e) uracil. C, N, O and H atoms are shown as brown,
blue, red and pink, respectively. The green atoms indicate the H which is the closest atom to the graphene sheet (refers to table 3).

Figure 3.  Charge density spatial distribution of (a) adenine and (b) uracil on graphene. Yellow indicates the spatial distribution of
positive charge density.

these interaction energies may change in a different environment, such as in water. For example, the study in [28]
indicates that graphene–nucleobase interaction energies in an alkaline solution are in the order G  >  A  >  C  >  T,
but the trend in water is G  >  A  >  T  >  C, although the positions of C and T seem to be interchangeable. In the
same study the authors imply that this difference may be attributable to the processes used to produce graphene
and the different concentrations of solutions. Another experimental study conducted by Sowerby et al [29] shows
that nucleic acids in water on the surface of crystalline graphite are in the order G  >  A  >  T  >  C  >  U, which is
good agreement with our study. So, the results we obtained obey the general trend for binding energies in most
theoretical [8, 10, 30–34] and experimental [28, 29] studies.

3.2.  Charge density redistribution

To understand in detail the interaction between nucleobases with graphene we calculated how the charge density
of the system changes. As an example, the charge distribution of A and U on graphene is shown in figure 3.

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Mater. Res. Express 4 (2017) 065401 H H Gürel and B Salmankurt

Figure 4.  Band structure of (a) and (b) adenine and (c) and (d) uracil. The green line indicates the neutral Q  =  0; blue indicates
Q  =  −1 e/cell; red indicates Q  =  +1 e/cell.

In addition to this, we performed charge transfer analysis. According to Bader charge analysis, we observed a
charge transfer of 0.08e from graphene to the molecules, and charge accumulation was mostly localized on the
molecules. Here, we simply say that the nucleobases act as charge acceptors when they adsorbed on a graphene
sheet.

3.3.  Effects of charging on bandstructure

We performed ab initio PW calculations and investigated the effects of charging on DNA/RNA nucleobases on the
graphene layer. We simply define the charging as follows: Q  >  0 indicates a missing electron in the unit cell, while
Q  <  0 indicates an extra electron per unit cell. Q  =  0 is the neutral case. We show the band structures of A and U
on a graphene layer for neutral Q  =  0 e/cell, Q  =  −1 e/cell and Q  =  +1 e/cell in figure 4 as an example of the band
structures of DNA/RNA nucleobases. It can be seen that in figure 4 the Fermi level shifts down for Q  =  +1 e/cell
and up for Q  =  −1 e/cell. The same behavior is also observed for the other nucleobases.
The Dirac semimetal character of the graphene was not broken, even when there were nucleobases adsorbed
on the graphene. But the Dirac semimetal character was changed when we added/removed an electron to/from
the system. In the charged system, the bands crossed the Fermi level, which indicates the deterioration of the
Dirac semimetal character of the graphene. Hence, we can change the electronic properties of the DNA/RNA
nucleobase–graphene system by adding or removing an electron from the system in a controlled manner.

3.4.  Pulling of nucleobases

To better understand the binding mechanism under charging, we focused on the pulling energies. We calculated
the total energies of the optimized structures of nucleobases and the graphene system when a nucleobase is pulled
out along the z direction perpendicular the graphene plane. In order to prevent the graphene from being moved
while pulling, we fixed the carbon atoms at the corner of the graphene. The energy related to pulling Ep  =  ET
[M  +  graphene; Q; d]  −  ET [M  +  graphene; Q; d  =  0], increases with increasing d. Ep has a maximum value
denoted by Epmax. Our pulling energy analyses are shown in figures 5 and 6. Our calculations confirm that Epmax can
be taken as a measure of the strength of the binding between the nucleobase and graphene. Epmax, in other words,
is the energy barrier to pulling out the adsorbed nucleobases from the graphene surface. For Q  =  0, Epmax, is 0.64
(0.70), 0.53 (0.59), 0.55 (0.57), 0.47 (0.52) and 0.47 (0.50) eV for G, A, T, C and U, respectively and these energies

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Mater. Res. Express 4 (2017) 065401 H H Gürel and B Salmankurt

Figure 5.  Pulling mechanism of a nucleobase from graphene (a). Pulling of adenine (b), guanine (c), cytosine (c), thymine (d) and
uracil (e) from the graphene plane. Green indicates the neutral Q  =  0; blue indicates Q  =  −1 e/cell; red indicates Q  =  +1 e/cell.

Figure 6.  Pulling energies of guanine, adenine, thymine, cytosine and uracil from the graphene plane. The green bar indicates the
neutral Q  =  0; blue indicates Q  =  −1 e/cell; red indicates Q  =  +1 e/cell.

are consistent with the calculated binding energy (shown in parentheses) Eb of the nucleobases. The obtained
results show that the dependence of Epmax on the charging is strong. When Q  <  0, Epmax increases. But when
Q  >  0 a decrease in Epmax is observed. For example, in the A–graphene system, Epmax is 0.33 eV for Q  =  +1 e/cell.
However, this energy increases to 0.72 eV when Q  =  −1 e/cell. On the other hand, in the U–graphene system, the

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Mater. Res. Express 4 (2017) 065401 H H Gürel and B Salmankurt

Epmax energies are found to be 0.47 eV and 0.53 eV in the case of Q  =  +1 e/cell and Q  =  −1 e/cell, respectively.
The amount by which Epmax increases is different for different nucleobases. This difference is due to the amount
of charge on the nucleobases and graphene. According to the Bader charge analysis, when we add an electron
to the system charge redistribution between graphene and A is much lower than in the U–graphene system so
electrostatic repulsion is much stronger for the U–graphene system than A–graphene. For this reason, when we
add an electron to the system, it is harder to pull A out from the graphene plane than U. Alternatively, when we
remove an electron from the system it is harder to pull U out from the graphene plane than A.
We also calculated the magnetic moments of both the neutral and the charged systems. It is possible to tune
the magnetic moment of a monolayer when it has adsorbed molecules/atoms or when electron(s) are added to/
removed from the systems. However, according to our spin polarized calculations we did not observe any magnetic
moment (μ  =  0) in any of the calculations conducted in this study.

4. Summary

In conclusion, the mechanism of adsorption of DNA/RNA nucleobases on 2D graphene layer has been studied
using first-principles DFT and the vdW-DF2 scheme to include the vdW interaction. Our calculations show
that all DNA/RNA nucleobases are physisorbed on graphene. Adsorption occurs due to vdW interactions, and
the order of interaction is G  >  A  >  T  >  C  >  U. There is very little charge transfer between the nucleobases and
graphene. We also calculated the geometric, electronic and magnetic properties of graphene decorated by DNA/
RNA nucleobases as a function of charging, and investigated how the electronic properties of graphene are affected
by the adsorption of nucleobases under charging. We showed that changing the total number of charges in the
system can change the electronic properties of graphene decorated by DNA/RNA nucleobases. Due to fact that
the Fermi level shifts down for Q  =  +1 e/cell and up for Q  =  −1 e/cell, DNA/RNA nucleobase–graphene system
show a metallic character under charging. Binding and pulling energies and electronic properties strongly depend
on the total number of charges in the system. One may conclude from the present study of geometries, energetics,
electronic structures, charging analysis and pulling properties of the above-mentioned systems that surfaces
similar to graphene may act as potential candidates for sensing the nucleobases in DNA sequencing and other
biomolecules. Also, our results can provide insight into experimental works and could be useful for developments
in biotechnology and nanotechnology.

Acknowledgments

This work was supported by the Scientific and Research Council of Turkey (TÜBİTAK) under grant no. 114F453.

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