Stabilization of Graphene Nanopore

Stabilization of graphene nanopore

Jaekwang Leea,b,1, Zhiqing Yangc, Wu Zhoua, Stephen J. Pennycookb,d, Sokrates T. Pantelidesa,b, and Matthew F. Chisholma,d,1

aMaterials Science and Technology Division, Oak Ridge National Laboratory, Oak Ridge, TN 37831; bDepartment of Physics and Astronomy, Vanderbilt University, Nashville, TN 37235; cShenyang National Laboratory for Material Science, Institute of Metal Research, Chinese Academy of Science, Shenyang 110016, China; and dDepartment of Materials Science and Engineering, University of Tennessee, Knoxville, TN 37996

Edited by Jisoon Ihm, Seoul National University, Seoul, Republic of Korea, and approved April 22, 2014 (received for review January 14, 2014) Graphene is an ultrathin, impervious membrane. The controlled that graphene edges can be terminated by mono- and di-hydro- introduction of nanoscale pores in graphene would lead to applica- gen (24). Recent muon spectroscopy investigations have con- tions that involve water purification, chemical separation, and DNA firmed the existence of C—H bonds at graphene defects (25). sequencing. However, graphene nanopores are unstable against There is no report, however, of intentional hydrogenation of filling by carbon adatoms. Here, using aberration-corrected scanning nanopores in graphene to determine whether hydrogen passiv- transmission electron microscopy and density-functional calculations, ation prevents filling. To explore how hydrogen passivation we report that Si atoms stabilize graphene nanopores by bridging affects carbon filling, Born–Oppenheimer MD simulations were the dangling bonds around the perimeter of the hole. Si‐passivated done in the microcanonical ensemble (NVE), where the number pores remain intact even under intense electron beam irradiation, of particles (N), the volume (V), and the energy are conserved. and they were observed several months after the sample fabrication, (Details of the MD simulations are provided in Methods.) The demonstrating that these structures are intrinsically robust and sta- MD simulations show that carbon adatoms interact strongly with ble against carbon filling. Theoretical calculations reveal the under- H-passivated nanopores and form a planar network that fills the lying mechanism for this stabilization effect: Si atoms bond strongly nanopore (Fig. 1 A–D and Movie S1). Thus, hydrogen passiv- to the graphene edge, and their preference for tetrahedral coordi- ation of the carbon edge atoms is not expected to prevent filling nation forces C adatoms to form dendrites sticking out of the gra- of graphene nanopores by carbon. phene plane, instead of filling the nanopore. Our results provide

Our experimental data and density-functional calculations both SCIENCES a novel way to develop stable nanopores, which is a major step demonstrate that Si atoms can passivate nanopore rims very ef- toward reliable graphene-based molecular translocation devices. fectively. Silicon is one of the most common impurities in graphene APPLIED PHYSICAL grown by chemical vapor deposition (CVD). During the high-tem- self-healing process | nanopore stabilization | STEM imaging | perature CVD growth process, it is most likely that Si impurities are density-functional theory introduced into the graphene layer due to the presence of a Si source (the quartz tube) (26, 27). xtensive experimental and theoretical work has been done on Fig. 2 A–C shows annular dark-field (ADF) Z-contrast images Evacancy clusters and nanopores in graphene (1–6). In par- of Si atoms decorating graphene multivacancies. For a hex- ticular, nanopore technology has emerged as a powerful tool for avacancy, the addition of three Si atoms can effectively stabilize single-ion channels, single-molecule detection, and liquid puri- the defect structure by bridging the dangling bonds on neigh- fication. A monolayer graphene nanopore (7–9) compared with a boring perimeter C atoms, forming characteristic five-member typical solid-state nanopore of a 30-nm thickness (10–14) provides rings (4 C + 1 Si). Precisely the same arrangement occurs nat- an optimal approach for very high-resolution, high-throughput, urally in a decavacancy where just four Si atoms provide optimal rapid DNA sequencing. passivation. Calculated lowest-energy atomic configurations are Rapid progress has been made in experimental studies ex- overlaid on the observed images (Fig. 2 D–F). The relaxed ploring a wide variety of methods for introducing nanopores in structural models of V6-Si3 and V10-Si4, where V indicates the graphene. The most recent methods have used diblock copolymer templating, helium-ion beam drilling, and chemical etching to Significance achieve both higher porosity and a more precise pore size control (15–18). However, it is observed that small holes in graphene are The key driving force for nanopore research has been the subject to reconstruction and partial or total filling by diffusing prospect of DNA sequencing, which requires small, thin pores carbon or other adatoms (known as the self-healing process) (19– for highest resolution. The length of the pore channel can be 21). Stabilization of pores for extended periods of time has not reduced to a single layer of atoms through the use of gra- been achieved so far. phene. However, it is known that tiny holes in graphene are Here, we report that Si atoms stabilize graphene nanopores by unstable against filling by carbon adatoms. Thus, the stabili- bridging the dangling bonds around the perimeter of the hole. zation of such holes is a critical issue to be resolved to enable Without passivation, we find that small pores in graphene fill applications. We demonstrate the existence of stabilized holes within hours even under ultrahigh-vacuum conditions. This pore in graphene and theoretical understanding of why they are stabilization is understood in terms of the fact that Si atoms stable. Our discoveries are a major step toward the develop- prefer tetrahedral coordination so that C adatoms that might ment of robust and reliable graphene-based molecular trans- bond to them would not lie in the graphene plane (22, 23). Our location devices. molecular-dynamics (MD) simulations show that the C adatoms would form dendrites sticking out of the graphene plane, instead Author contributions: J.L., Z.Y., and M.F.C. designed research; J.L., Z.Y., and W.Z. per- of filling the nanopore, suggesting that Si passivation is indeed ef- formed research; J.L. contributed new reagents/analytic tools; J.L., S.J.P., S.T.P., and fective in preventing the self-healing process. Furthermore, exper- M.F.C. analyzed data; and J.L., Z.Y., W.Z., S.J.P., S.T.P., and M.F.C. wrote the paper. imental and theoretical evidence suggests that Si-stabilized The authors declare no conflict of interest. nanopores are stable in ambient atmosphere and liquids. This article is a PNAS Direct Submission. 1To whom correspondence may be addressed. E-mail: [email protected] or chisholmmf@ Results ornl.gov. Hydrogen may be expected to stabilize pores in graphene by This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. passivating dangling bonds at the pore rim. It has been reported 1073/pnas.1400767111/-/DCSupplemental.

www.pnas.org/cgi/doi/10.1073/pnas.1400767111 PNAS Early Edition | 1of5 Downloaded by guest on September 25, 2021 Fig. 1. Intermediate snapshots of ab initio MD simulations of H- and Si-passivated nanopores. (A–D) Snapshots of MD simulations of a H-passivated nanopore at varying transient states at 0, 0.1, 0.2, and 0.3 ps. C dangling bonds around the pore rim are initially terminated by 12 monohydrogen atoms (green color). Thirty-four C atoms (orange color) are inserted near the pore, and their coordinates are randomly chosen. Carbon adatoms interact strongly with the H-passivated nanopore, filling it with a planar network. (E–H) Snapshots of MD simulations of a Si-passivated nanopore at the same times. Si dangling bonds around the pore rim are initially terminated by six di-hydrogens. Twelve C atoms are inserted near the pore and their coordinates are again randomly chosen. The preference of Si atoms for tetrahedral coordination prevents the formation of a planar C network inside the nanopore. Instead, C atoms form dendrites sticking out of the graphene plane.

number of carbon vacancies, are depicted in Fig. 2 G and H. V(14n-18)-Si2n (n ≥ 2) (Fig. S2). In the round pores, some Si atoms ∼ ∼ Small pores with diameters of 0.2 and 0.4 nm are formed with form single bonds with C atoms (zigzag sites) from V54-Si12, curved armchair-type edges (indicated in red) passivated by whereas in the rectangular pores all Si atoms bridge pairs of C Si atoms. atoms (armchair sites) at the perimeter. The binding energy of Si atoms is calculated to be larger than Calculated binding energies of bridge-bonded Si atoms in 8 eV. This large binding energy is consistent with the experimental different pores are shown in Fig. 5C. These binding energies are fact that the V6-Si3 structure is stable under prolonged exposure for all larger than 8 eV, which appears to be a saturation value for 169 s to the high-energy (60-keV) electron beam in the electron microscope (Fig. 3). ADF Z-contrast images of the V6-Si3 structure shows that the Si atoms around the perimeter spin without enlarging the hole, forming defects or ripping off atoms under the ABC long consecutive electron beam irradiation (Fig. 3) (28, 29). We find that the energy barrier for the rotation is about 2.0 eV. Under the 60-keV electron beam irradiation, the maximum energy transfer to a Si atom is 4.67 eV (30), which is lower than the binding energy of Si atoms, but higher than the energy for rotation. That is why we observed only the rotation instead of ejection of Si atoms from the V6-Si3 structure. V4-Si2 V6-Si3 V10-Si4 Fig. 4A shows a larger pore passivated by 17 Si atoms. A total of 68 carbon atoms are missing. From the lowest-energy atomic DEF configurations (Fig. 4B), we see that all carbon dangling bonds at the pore rim are completely passivated by Si atoms. Although there is a variety of bonding configurations, all Si atoms have binding energies larger than 5 eV as shown in Fig. 4C. The observation of a large Si-passivated pore several months after the sample was fabricated suggests that such structures are intrinsically stable against carbon filling [carbon adatoms usually fill pores within several hours even under ultrahigh vacuum (19)]. This stability can be understood in terms of the fact that Si G V -Si H V -Si atoms prefer tetrahedral coordination so that C adatoms that 6 3 10 4 might bond to them would not lie in the graphene plane (22, 23). To further confirm this conjecture, we performed MD simulations by adding C adatoms to a Si-passivated 24-vacancy nanopore. We arm find that the C adatoms tend to form dendrites sticking out of the chair E–H graphene plane, instead of filling into the nanopore (Fig. 1 D~2Å D~4Å and Movie S2), suggesting that Si passivation is very effective in preventing the self-healing process. Translocation of molecules through nanopores for various applications would require the deliberate fabrication of holes of specific sizes and shapes. We, therefore, explored two types of nanopores that are larger versions of those observed in Fig. 2 Fig. 2. Atomic structures for Si atoms decorating graphene multivacancies. (V6-Si3 and V10-Si4). Round pores are shown in Fig. 5A. Their (A–C) Experimental STEM-ADF Z-contrast images of Si atoms (2, 3, and 4, re- rims could contain both armchair and zigzag edge portions, and – 2 spectively) in graphene multivacancies (4, 6, and 10, respectively). (D F)Sche- the number of Si atoms obeys the formula V(6m ) -Simax{6m-6,3} ≥ matics of the structure models, overlaid on the corresponding ADF images, for (m 1) (Fig. S1). In contrast, pores constituted of purely curved the defect structures shown in A–C, respectively. (G and H)Detailedschematics

armchair edges would have rectangular shapes as shown in of the structure models of V6-Si3 and V10-Si4, where V denotes the number of C Fig. 5B. These rectangular-shaped pores can be described as vacancies. Each armchair edge is indicated in red. (Scale bar: 0.2 nm.)

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Fig. 3. STEM-ADF Z-contrast images of the V6-Si3 structure. Forty-eight consecutive Z-contrast images of the V6-Si3 while being irradiated by the electron beam for 169 s. The Si atoms move around the perimeter of the hole without enlarging it, or forming defects. The white arrow represents the rotation of Si atoms.

large pores. In contrast, the binding energy of the Si atoms water and Cl ions, which are very reactive. To explore stability bonded to a single C atom in a round pore (e.g., V54-Si12, rect- against oxygen, Si dangling bonds around the pore rim were angular orange) is 5.5 eV, which is still large enough for a robust terminated by oxygen atoms, as shown in Fig. S4, and then MD passivation. Therefore, we expect that fabricated pores with simulations were carried out in the canonical ensemble at 300 K. jagged edges can still be robustly passivated by Si atoms. C adatoms were inserted near the pore and their initial coordinates were chosen randomly. The MD results confirm that Si Discussion passivation of the rim still remains stable, whereas volatile CO We have shown that it is possible to passivate the chemical bonds and CO2 molecules are generated from reactions between C around the perimeter of pores in graphene. However, our results adatoms and oxygen. This phenomenon can be explained by the have shown that not all elements are effective in this role. For fact that the reactions between that C adatoms and oxygen have example, hydrogen bonds at pore edges, but it does not stop significantly higher energy gain than oxygen reactions with Si carbon adatoms from filling small holes in graphene. Our ex- atoms. These results are consistent with a previous study on the perimental and theoretical investigations demonstrate that Si is oxidation resistance of bonded Si atoms in a graphene lattice particularly effective in this role. This stability can be understood (31). The net conclusion is that the Si-passivated graphene pores in terms of the fact that Si atoms strongly prefer tetrahedral are stable in ambient condition. coordination so that C adatoms that might bond to them would We propose that a technology can be developed for the fab- not lie in the graphene plane. rication of stable nanopores in graphene. Pores of desirable size, Si atoms at the pore edges are reactive because of the pres- shape, and pattern can be fabricated by focused electron or ion ence of Si dangling bonds pointing out of the graphene plane. beams (18) or by chemical etching using masks. Subsequent However, hydrogen can passivate these dangling bonds (Fig. S3). supply of Si atoms would naturally passivate the rims of the as- The calculated H binding energy is ∼3.0 eV, which means that H fabricated nanopores. If the graphene layers can be kept clean, passivation of the Si-terminated edges is also robust, leading to the resulting stabilized pores would be suitable for a wide range highly inert and stable nanopores in graphene. Finally, Si pas- of applications. In particular, robust graphene nanopores of sivation of the pore rim is stable against ambient atmosphere as specific size and shape (Fig. S5) can provide an “optimal” ap- the samples were stored in air for months before the present proach for very high-resolution, high-throughput, single‐mole- investigation. In addition, the Si-terminated pores remained in- cule detection and rapid DNA sequencing. This discovery is tact during the removal of monolayer graphene from the Cu a major step toward the development of stable and reliable substrate when they are bathed in liquid FeCl3, i.e., exposed to graphene-based molecular translocation devices (32–35).

Lee et al. PNAS Early Edition | 3of5 Downloaded by guest on September 25, 2021 thickness was used as the growth substrate and was placed directly in the A quartz tube. During the growth, the temperature was first raised to 950 °C under 10 torr Ar/H gas flow. Once the temperature reached 950 °C, the Ar/H V -Si 2 2 68 17 gas was cut off and 4 s.c.c.m. CH4 was introduced into quartz tube for graphene growth. The reaction time is typically 10 min. The system was then

cooled down at a rate of 50 °C/min under the protection of a 500 mtorr Ar/H2 atmosphere. The graphene layers were then extracted from the copper film

via chemical etching by FeCl3 and deposited onto a 2,000-mesh copper grid. The sample contained both monolayer and multilayer graphene.

Scanning Transmission Electron Microscopy ADF Z-Contrast Imaging Experiments and Impurity Identification. Aberration-corrected scanning transmission electron microscopy (STEM) ADF imaging was performed with a Nion UltraSTEM- 100. The microscope was operated at 60-kV accelerating voltage, which is below the knock-on radiation damage threshold of graphene. The convergence semiangle of the incident probe was set to ∼30 mrad, and the ADF images were collected using a ∼54- to 200-mrad detector half-angle. The probe current was set to ∼100 pA, contained in a probe of 1.3 Å in diameter. The ADF images 0.3 nm shown in the manuscript have been deconvolved following the method described in ref. 30, which allows atom-by-atom chemical analysis based on quantitative image intensity analysis (37). The intensity from the impurity BCatoms is about 3.83 times the intensity obtained from the carbon atoms, which is close to the Z1.6 ratio of 1:3.87 for Z = 6(C)andZ = 14 (Si), respectively. 11 Furthermore, electron energy-loss spectroscopy analysis from a substitutional impurity atom with the same ADF image intensity ratio confirms that the 15 12 impurities seen passivating the pores in graphene are Si atoms (Fig. S6). The 2 3 6 9 contrast variation within the graphene lattice in Fig. 4A is due to residual 11 1 9 17 (eV) aberration and astigmatism during the acquisition of this image. Si 16 b

E 7 First-Principles Calculations and MD Simulations. First-principles calculations, 10 14 based on density-functional theory (DFT) (38, 39), were performed using the 4 5 8 5 Vienna ab initio simulation package (VASP) (40). The projector augmented 13 7 0 3 6 9 121518 wave (PAW) method was used to mimic the ionic cores (41), whereas the Si site index generalized gradient approximation (GGA) in the Perdew–Burke–Ernzerhof (PBE) parameterization was used for the exchange and correlation functional (42). Atomic positions, as well as lattice parameters, were optimized Fig. 4. Atomic structure of the V68-Si17 structure and the binding energy of using a conjugate gradient algorithm. Ionic and electronic relaxations were − the Si atoms. (A) STEM-ADF Z-contrast image of a graphene nanopore pas- performed by applying a convergence criterion of 5 × 10 2 eV/Å per ion and − sivated by 17 Si atoms. (B) Structure model for the Si-passivated nanopore. 10 4 eV per electronic step, respectively. The size of the graphene supercell is (C) Binding energy distributions of the 17 Si atoms. 2.47 × 2.57 nm for the binding energy calculations and ab initio MD simulations. A rectangular graphene nanopore containing 250 C atoms (graphene pore consists of 216 C atoms and 34 C adatoms) and 12 H atoms was considered to conduct the MD simulation for the H-passivated pore at 300 K. Methods Another rectangular graphene nanopore containing 228 C atoms (graphene Sample Preparation. The graphene material was grown on a copper film pore consists of 216 C atoms and 12 C adatoms), 6 Si, and 12 H atoms was following a CVD method reported in the literature (36). Cu foil of 100-μm considered to conduct the MD simulation for the Si-passivated pore at 300 K.

ABV -Si V -Si C 6 3 10 4 12

Si (armchair) V4-Si2 11 Si (zigzag) V10-Si4 C 10

9 V24-Si6

V52-Si10 (eV) V6-Si3

V -Si Si 8 24 6 V24-Si6 b E V38-Si8 V66-Si12 7

5 V54-Si12

V38-Si8 V54-Si12 Fig. 5. Calculated sequence of stable nanopores 4 and the binding energy for the Si passivating atoms. 0 10203040506070 (A) Calculated sequence of round pores. (B) Calcu- Number of vacancies lated sequence of rectangular-shaped pores. (C) Binding energy of bridge-bonded Si atoms (armchair V-Si, n2≥ sites). Additionally, the binding energy of a Si atom ()14n-18 2n V-Si , m1≥ bonded to a single C atom (zigzag site) in a round ()6m2 max{} 6m-6,3 pore (V54-Si12) is indicated by the orange square.

4of5 | www.pnas.org/cgi/doi/10.1073/pnas.1400767111 Lee et al. Downloaded by guest on September 25, 2021 The Born–Oppenheimer MD simulations were done in the NVE, where the perature is clearly stabilized within 800 steps (0.4 ps) for both cases (Figs. S7 number of particles (N), the volume (V), and the energy (E) are conserved. and S8). There are no significant changes in temperature when a planar The NVE ensemble is suitable for simulating the self-healing phenomenon network consisting of carbon adatoms is formed in the graphene nanopore because it is experimentally observed in an isolated ultrahigh vacuum where for a H-passivated pore (Movie S1), or when dendrites are formed out of the total energy of system is assumed to be constant. Initially, C adatoms are graphene plane (Movie S2). The total simulation time spans are about 0.5 ps. randomly distributed around the pore. To avoid the short-range repulsive interactions, C adatoms are separated by, at least, 1.7 Å (distance between ACKNOWLEDGMENTS. We are grateful to Dr. Suk-kyun Ahn [Oak Ridge each C atom in graphene is about 1.43 Å). We intentionally place C adatoms National Laboratory (ORNL)] for helpful comments. This research was supported by the Office of Basic Energy Sciences, Materials Sciences and within 2 Å out of plane to expedite reaction near the graphene pore. Two Engineering Division, US Department of Energy (DOE) (J.L., Z.Y., M.F.C., S.J.P., different initial configurations are simulated, but they did not change our and S.T.P.), by DOE Grant DE-FG02-09ER46554 (to S.T.P. and J.L.), by a Wigner main results. Time step of 0.5 fs is taken to track the positions of all of the Fellowship through the Laboratory Directed Research and Development atoms as precise as possible including hydrogen (the lightest element on the Program of ORNL, managed by UT-Battelle, LLC, for the DOE (to W.Z.), by the periodic table). Increasing the time step (1 or 2 fs) does not change our main McMinn Endowment (S.T.P.) at Vanderbilt University, and through a user project ’ results but hides the details of dynamics. The temperature was initialized at supported by ORNL s Center for Nanophase Materials Sciences, which is spon- sored by the Scientific User Facilities Division, Office of Basic Energy Sciences, 300 K (temperature in NVE ensemble is defined by the equipartition theorem). DOE. This research used resources of the National Energy Research Scientific ∼ ∼ After an equilibration time (of 150 fs), the temperature is stabilized at 824.4 K Computing Center, which is supported by the Office of Science of the DOE under for the H-passivated pore (Fig. S7) and 1,071.9 K for the Si-passivated pore Contract DE-AC02-05CH11231. Z.Y. is supported in part by National Natural Sci- (Fig. S8). Even though they are around the stable temperature, the tem- ence Foundation of China Grants 51371178 and 51390473.

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