Noncovalent Interaction of Single-Walled Carbon Nanotubes with 1

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Noncovalent Interaction of Single-Walled Carbon Nanotubes with 1-Pyrenebutanoic Acid Succinimide Ester and Glucoseoxidase Victor A. Karachevtsev,† Stepan G. Stepanian,*,† Alexander Yu. Glamazda,† Maksym V. Karachevtsev,† Victor V. Eremenko,† Oksana S. Lytvyn,‡ and Ludwik Adamowicz§ †

B. Verkin Institute for Low Temperature Physics and Engineering, National Academy of Science of Ukraine, 47, Lenin Ave., Kharkov, 61103, Ukraine ‡ V. Lashkaryov Institute of Semiconductor Physics, Kyiv, 03028, Ukraine § Department of Chemistry and Biochemistry, University of Arizona, Tucson, Arizona 85721, United States

bS Supporting Information ABSTRACT: Peculiarities of the interface interactions of 1-pyrenebutanoic acid N-hydroxysuccinimide ester (PSE) with single-walled carbon nanotubes (SWCNTs) and enzyme glucoseoxidase (GOX) have been studied with the resonance Raman spectroscopy and theoretical calculations employing the DFT method and the molecular dynamics (MD) simulation. The interaction of a nanotube with PSE leads to a downshift of the band assigned in the Raman spectrum to the tangential mode of the hybrid with respect to the position of this mode in the spectrum of the pristine SWCNT. The MD simulation demonstrates that the direct interaction between SWCNT and GOX is very strong. This interaction can be expected to change the structure of the enzyme and to significantly affect its activity. The MD simulation also shows that only one PSE molecule used as a linker between SWCNT and GOX is enough to keep GOX near the nanotube surface in the water surrounding and to prevent strong interaction between SWCNT and GOX. However, to stabilize this nanobiohybrid in water at least two PSE linkers are needed. The molecular structure of PSE is determined using the density functional theory approach (DFT/B3LYP/6-31++G(d,p). The geometries and the relative stabilities of all possible PSE conformers are characterized in the calculations. High structural flexibility of the PSE molecule is demonstrated. Calculations (at the M05-2X level of theory) have also been performed on the structures and the interaction energies of complexes formed by various SWCNTs with PSE and pyrene. Pyrene interacts strongly with the surface of carbon nanotubes with different chiralities, but the interaction with zigzag nanotubes is stronger than with armchair ones of the same diameter. Increasing the diameter of the SWCNTs leads to a higher adsorption energy, reaching the maximum value for graphene ( 20.8 kcal/mol).

1. INTRODUCTION Due to their unusual physical, optical, thermal, and electronic properties, single-walled carbon nanotubes (SWCNTs) are one of the most promising nanomaterials for biosensing applications1 3 including genosensors and biosensors for detection of glucose, lactate, and other compounds. Current methods of biosensing with carbon nanotubes have mainly focused on electrochemical detection,4 on optical detection,5 7 on using single-carbonnanotube field-effect transistors with immobilized biomolecules,8,9 on networking nanotube-field-effect transistors,10 on using quantum-dot-modified nanotubes,11 etc. In elaboration of biological sensors involving carbon nanotubes, one of the important problems that needs to be solved is related to immobilization of the recognizing molecule on the nanotube surface. As enzymes are often exploited as possible recognition elements in biosensors, their immobilization on the nanotube surface needs to be investigated in detail. There are works where the immobilization was achieved by direct deposition of the enzymes onto the nanotube surface.5 However, in the paper where r 2011 American Chemical Society

this procedure was discussed,12 it was shown that the activity of the enzyme (R-chymotrypsin and soybean peroxidase) decreases significantly after its adsorption onto the SWCNT surface. The decrease of the enzymatic activity of GOX absorbed onto the nanotube surface was experimentally observed by Tsai et al.13 Thus, a procedure for enzyme immobilization on a nanotube that does not lower the enzyme native activity needs to be found. For this purpose, nanotube functionalization can be utilized. Some success in this direction was achieved with the use of molecular anchors14 and the polymer wrapping of the nanotubes.15 Chen and co-workers suggested an effective noncovalent way of carbon-nanotube functionalization by organic molecules for biocompatibility testing.14 Their approach utilizes a bifunctional molecule containing succinylimide ester and a pyrene moiety to bind proteins to the nanotube surface. Pyrene attaches to the nanotube surface by means of the π π stacking or hydrophobic Received: August 17, 2011 Published: September 19, 2011 21072

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The Journal of Physical Chemistry C interactions and does not significantly disturb the electronic structure of the nanotube. This approach enables development of a specifically programmed chemical functionality of the system. Different derivatives of the pyrene molecule,16,17 as well as pyrene-functionalized block copolymers,18 20 were synthesized and investigated for their ability to provide an effective noncovalent functionalization of SWCNTs and multiwalled carbon nanotubes. SWCNT noncovalent functionalization using pyrenecarboxylic acid, which allows for the formation of stable SWCNT aqueous dispersions, was also suggested as an alternative to the oxidative acid treatment particularly for applications involving polymer composites.21 Density functional theory (DFT) calculations confirmed that the aromatic compounds and carbon nanotubes strongly interact and form stable hybrids.22,23This suggests that noncovalent functionalization of carbon nanotubes by pyrene derivatives can be an efficient way to modify the chemical and electronic properties of the nanotubes. To develop an effective approach for enzyme immobilization on nanotubes using molecular interfacing, the interaction between the enzyme molecules and SWCNTs needs to be studied in detail. Some work has already been done in this area. For example, the role of the length of alkyl chains forming bridges between amide groups and pyrene moieties was investigated.24 In spite of numerous evidence of the interaction between the nanotube sidewall and pyrene derivatives by different experimental and theoretical methods, a more fundamental understanding of the interaction between carbon nanotubes and 1-pyrenebutanoic acid N-hydroxysuccinimide ester (PSE) is still lacking. This includes the interaction of nanotubes with glucoseoxidase (GOX) in the water environment. Elucidation of this interaction would permit understanding of the operation of a nanotube GOX hybrid in a real bionanoenvironment. In this work, Raman spectroscopy is employed to study the interaction between PSE and SWCNTs. The investigation involves monitoring the shifting of the tangential mode occurring upon formation of PSE SWCNT complexes. Quantum-chemical calculations performed at the M05-2X/6-31++G(d,p) level of theory in this work have demonstrated that the hybrids formed by SWCNTs with PSE molecules are stabilized due to strong π π interactions between the pyrene fragment of the PSE molecule and the nanotube surface. A detailed analysis of the PSE molecule conformers, as well as of the interaction of the pyrene molecule with a nanotube of different chiralities and with graphene, has been carried out. MD simulations have shown that one PSE molecule is sufficient to form a stable triple SWCNT PSE GOX hybrid in the surrounding water. The interaction energies between the pyrene fragment of PSE and SWCNT (with one and two PSE molecules) and between the GOX part of the complex and SWCNT are estimated.

2. METHODS Sample Preparation. In this work, SWCNTs have been produced by the CoMoCAT method25 (SouthWest NanoTechnologies Inc., USA). This method yields nanotubes with narrow diameter (0.75 0.95 nm) and chirality (6,5) distributions. 1-Pyrenebutanoic acid N-hydroxysuccinimide ester (PSE) was purchased from Sigma-Aldrich, Europe. All compounds have been used without additional purification. SWCNTs have been mixed with PSE in methanol (with weight ratio 1:1, 0.3 mg/mL). The mixtures have been treated with sonication (1 W, 44 kHz)

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for 30 min, and then the suspensions have been deposited on a quartz substrate and dried under a stream of warm air. Raman Spectroscopy Studies. The Raman experiments have been performed in the 90° scattering configuration relative to the laser beam using the 632.8 nm (1.96 eV) light from a He Ne laser. The laser beam was focused onto a stripe with dimensions ∼0.1 mm  1 mm to yield the laser power density of 100 W/cm2. The spectra have been analyzed using a Raman double monochromator with the reverse dispersion of 3 Å/mm and have been detected with a thermocooled CCD camera. The peak position of the G band (in the spectral range between 1500 and 1630 cm 1) corresponding to the tangential mode in the nanotube film was determined with the accuracy not worse than 0.3 cm 1. This level of accuracy has been achieved because the frequency positions of the plasma lines from the He Ne laser in the vicinity of the G+ and RBM bands were used in the internal calibration of the spectrometer. Atomic Force Microscopy Experiment. An AFM image of SWCNTs with GOX adsorbed on them was obtained by using a NanoScope III D3000 AFM instrument (Digital Instruments, Santa Barbara, USA) operating in the tapping mode. The measurements have been performed using silicon tips (purchased from NT-MDT, Russia) with the nominal apex radius of ∼10 nm. The samples for the AFM measurements have been obtained with a spray method. 1-Methyl-2-pyrrolidone (NMP) has been used as the solvent for dispersing SWCNTs in the solution. NMP (99% purity; the spectrophotometric grade) was purchased from Sigma-Aldrich (Europe) and used without additional purification. In the sample, preparation of 0.6 mg of the SWCNT powder was first added to 4 mL of NMP and sonicated for 2 h. Next, the SWCNT:NMP solution was centrifuged at 18 000 rpm for 30 min, and the supernatant solution was collected, moved to a vessel of a home-built airbrush, and sprayed onto a freshly cleaved mica surface. Five cycles of the coating were applied, and the sample was dried in an air oven at 80 °C for 10 min after each cycle. Each coating cycle required only 2 s to ensure uniform coverage. Next, the SWCNT-coated mica substrate was immersed in the PSE solution (1 μM) for 10 min to produce SWCNT PSE hybrids and then washed with deionized water with a resistance of 18 MΩ. After washing the mica substrate with SWCNT PSE, the hybrids were immersed in the GOX aqueous solution for 30 min which allowed GOX to covalently link via carboxyl amine coupling reactions to PSE absorbed onto the SWCNT surface. Aqueous solution of glucose oxidase (GOX) from Aspergillus niger (Sigma-Aldrich, Europe) with the concentration of 1 μM (pH = 6.5) was prepared in deionized water. Then the sample was analyzed with AFM. Computational Methods. The geometries of the complexes formed by SWCNTs with PSE and pyrene molecules have been optimized at the DFT level of theory. The M05-2X functional26 has been used. As demonstrated before, this functional shows an excellent performance for stacked complexes of carbon nanotubes and planar organic molecules.27 29 The geometries and the interaction energies obtained with the M05-2X functional for the complexes studied in those works were very close to the ones obtained at the MP2 level of theory. In this work, we use the SLDB (same level different basis) approach to reduce the total number of basis functions in the calculations. We employ the standard STO-3G basis for the terminal hydrogen atoms of the carbon surface. For the nanotube carbon atoms and for all pyrene atoms we use the standard 6-31G(d) and 6-31++G(d,p) basis sets, respectively. 21073

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The Journal of Physical Chemistry C The calculations are performed for complexes formed by fragments of the SWCNTs with different chiralities. The geometry of a fragment is determined in a two-step procedure. First we fully optimize the structures of the corresponding SWCNT shortened and terminated at the edges with hydrogen atoms. In the calculation we use the DFT method with the B3LYP functional30 32 and the standard 3-21G basis set. Then we cut out a fragment of the nanotube, terminate the dangling bonds with hydrogens, and optimize the hydrogen positions while keeping the positions of the carbon atoms frozen. In all calculations of SWCNT pyrene and SWCNT PSE complexes that followed, the geometries of the fragments have not been reoptimized. As special attention needs to be paid to the stability of the DFT wave function in the calculation, for each studied system we tested its wave function using the keyword STABLE. Some RHF f UHF instabilities have been found for some isolated nanotube fragments and for some complexes. In such cases, the wave functions were corrected in subsequent calculations using the keyword STABLE = (OPT, QCONLY). All quantum-chemical calculations reported in this work have been performed using the Gaussian 03 program package.33 Calculated Cartesian coordinates are collected in the Supporting Information (Table S1). Molecular Dynamics Simulation Protocol. The SWCNT PSE, SWCNT GOX, SWCNT PSE GOX, and SWCNT (PSE)2 GOX complexes have been simulated with the molecular dynamics method implemented in the program package NAMD.34 The Charmm27 force-field parameter set has been used.35,36 The structure of the GOX enzyme was obtained from the Protein Data Bank.37 The aromatic carbon atom parameters have been used for the carbon atoms of the SWCNTs. The parameters (i.e., the force constants and the equilibrium structure parameters concerning the bond distances, the angles, and the dihedral angles) for the atoms of the PSE molecule were obtained based on the results of quantum-chemical calculations performed at the B3LYP/6-31++G(d) level of theory. Those calculations have also been used to determine the net atomic charges of the PSE molecule. For the van der Waals parameters of the PSE atoms, we use the Charmm27 force field. A complete description of all force-field parameters used for the PSE molecule in the present calculations is available in the Supporting Information (Table S2). In the simulations the complexes are embedded in a cubic box with water molecules. The distance between the complexes and the walls of the box has always been greater than 12 Å for all systems. The NPT ensemble (constant number of molecules and constant pressure and temperature) has been used in the simulations with the temperature and the pressure equal to 293 K and 1 bar, respectively. In the modeling, the periodic boundary conditions are assumed. The lengths and the diameter of the carbon nanotube used in the simulations are 11.0 and 1.27 nm, respectively (for zigzag(16,0) nanotube). In the simulation, the energy of the studied system is first minimized during 1000 steps, and then the system is equilibrated for 20 ns using a 1 fs time step. The visualization and the analysis of the configurations have been performed with the VMD package.38

3. RESULTS AND DISCUSSION 3.1. Raman Spectroscopy of the SWCNT PSE Hybrid. Information about the noncovalent interaction of a SWCNT and an organic molecule can be extracted by comparing the Raman spectrum of the nanotube before and after the absorption of the organic molecule on the SWCNT surface. The molecule

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Figure 1. Raman spectra of SWCNTs (a) and SWCNT PSE (b) in the range of the tangential G mode. Each experimental spectrum (orange curve) obtained at λexc = 632.8 nm laser excitation was fitted with approximated curves (black curve) described with the sum (color lines) of one BWF function and four Lorentzian (high-frequencies ones). Parameter 1/q of the BWF band was 0.16 for two samples. The value of the band peak position and its area (in brackets) is indicated close to the band location. Peaks labeled “*” correspond to the plasma line of the laser.

binding to the tube can lead to a downshift or an upshift of the intensive band corresponding to the high-frequency component of the tangential mode (G+).23,39,40 The fragments of the Raman spectra in the vicinity of the tangential G mode (1500 1650 cm 1) of the SWCNTs and of the SWCNT PSE complexes are shown in Figure 1. Both SWCNT and SWCNT PSE spectra are very similar, but, nevertheless, some differences in the band positions and intensities can be observed. Each experimental spectrum has been fitted with the minimal number of approximation functions (Figure 1) consisting of sums of four Lorentzians and one Breit Wigner Fano (BWF) function, I(ω) = I0{1 + (ω ω0)/qΓ}2/{1 + [(ω ω0)/Γ]2, where I0, ω0, Γ, and q are the intensity, the BWF frequency, the broadening parameter, and the asymmetry parameter, respectively. The BWF function has been used to describe the sloping asymmetric lower-frequency band which appears for metallic nanotubes.41,42 As can be seen in Figure 1, the agreement between the calculated and the experimental data is very good. Each band in the spectrum has been normalized to the total area of four bands, which is assumed to be 100. Besides the peak position of each calculated line shown in the figure, the area of this line is indicated. By using the He Ne laser as the excitation source, the resonance conditions for both the semiconducting and the metallic 21074

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The Journal of Physical Chemistry C nanotubes with the 0.7 1.0 nm diameter distribution can be achieved.27 This means that each observed spectrum is a superposition of the spectra of the semiconducting and metallic nanotubes. As can be seen in Figure 1, the low-frequency asymmetric component of the G band in the SWCNT spectrum is very weak. It means that the contribution of the metallic nanotubes in the observed spectrum is very small. Thus, all bands described by the Lorentzians can be assigned to semiconducting nanotubes. The interactions between the nanotubes and the PSE molecules are manifested in the spectra by downshifts of the corresponding SWCNT bands with respect to the positions of those bands in the spectra of the pristine SWCNTs. These shifts vary in the range from 0.6 to 1.5 cm 1 depending on the band (Figure 1). A small downshift of the G band frequency can be explained by a partial electron transfer from the PSE molecule to the nanotube surface. As our calculations indicate, this transfer does not exceed a few percent of an electron. The second reason for the band downshift in the spectrum of SWCNT PSE can be the relatively smaller interaction between the components of the hybrid relative to the intertube interaction in bundles of the pristine nanotubes. In this case, the C C bond force constant in the nanotube complexed with PSE becomes smaller relative to the value of this constant in the bundles. 3.2. AFM Image of the SWCNT PSE GOX Complex. The morphology of the SWCNT PSE GOX complexes was characterized using atomic force microscopy. Although AFM does not provide comprehensive information on the tertiary structure of the enzyme, the method provides a quantitative measurement of the shape of the enzyme adsorbed on SWCNT PSE and gives information about the portion of the nanotube surface covered with GOX. Figure 2 shows AFM images of GOX adsorbed onto PSE-coated SWCNTs deposited on the mica substrate. The wirelike structures are identified as small SWNCT bundles or individual nanotubes around which GOX molecules are adsorbed. As seen in Figure 2, GOX is immobilized specifically on the SWCNT surface, and the major portion of the surface is covered with the enzyme molecules. In aqueous solution at moderate ionic strength, GOX is a dimer protein. The monomer GOX molecule has a distinct globular structure with a height of about 4.5 nm.37 Scanning Tunneling Microscopy (STM) studies of GOX on the gold surface reveal two different shapes of native GOX molecules.43 One is an ellipsoid with dimensions of 10  6 nm, assigned to the lying position of the molecule, while the second is an approximately spherical shape with dimensions of 6.5  5 nm assigned to a standing position. The difference in dimensions is more than 2 nm and exceeds the diameter of CoMoCAT nanotubes used in this work which is about 0.75 0.95 nm. It was also observed that GOX molecules exhibit a tendency to organize themselves into a two-dimensional array or form isolated clusters of five to six GOX molecules.44 In the AFM image, we observed globules with heights close to 4 5 nm (Figure 2). The height of some SWCNT PSE GOX hybrids is about 8 9 nm. This indicates that two GOX monomers are aggregated in the vertical direction. In a few cases, the height of the nanotube enzyme coating is more than 10 nm, indicating aggregation of a few GOX molecules. It should be noted that the structure of GOX aggregates also depends on the ionic strength of solution.44 Aggregation of GOX molecules can be controlled by the enzyme concentration. The AFM imaging allows us to conclude that GOX is intimately associated with the sidewall of the SWCNT. It also shows the important role the

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Figure 2. AFM image of the SWCNT PSE GOX hybrids on the mica substrate, which was obtained by a spray method from the SWCNT solution in 1-methyl-2-pyrrolidone.

linking molecule plays in the immobilization of GOX onto the nanotube surface. 3.3. Structure of 1-Pyrene Butanoic Acid Succinimidyl Ester. In this work, we have used the PSE molecule as a linker between the carbon nanotube and the enzyme (GOX). The PSE molecule includes a pyrene fragment which consists of four condensed six-membered aromatic rings. This fragment interacts with the carbon nanotube surface with a nonbonding π π interaction. On the other hand, the succinimidyl fragment of the PSE molecule can react with amino groups of side residues of the enzyme forming strong covalent bonds. The pyrene and succinimidyl fragments are connected in PSE by an alkyl chain whose structure is highly flexible. To determine the PSE equilibrium molecular structure, we performed quantum-mechanical calculations of the geometries and relative stabilities of all possible PSE conformers. These calculations have been carried out using the density functional theory approach (DFT/B3LYP/6-31++G(d,p)). The total number of possible conformers of the PSE molecule was determined in the following way. The carbon chain which connects pyrene and succinimidyl fragments includes four single C C bonds (Figure 3a). Rotations about two of them (the CH2 CH2 bonds) result in three conformers per one rotation because the dihedral angles of the rotamers differ by 120°. Hence, the energy of the PSE molecule has been determined as a function of the three possible values of these two dihedral angles. Additionally, the rotations around the C(pyrene) CH2 (rotation 1) and CH2 COO (rotation 2) (Figure 3a) bonds have been examined. The results of the calculations presented in Figure 3b show that rotation 1 produces two energy minima. Rotation 2 produces only one minimum corresponding to the dihedral angle value of 0°, but the energy profile for rotation 2 has an almost plane part at the dihedral angle in the range between approximately 70° and 90° (Figure 3b). Although the energy profile calculated for the particular PSE rotamer does not have a minimum in this range, we cannot exclude that for other PSE rotamers an additional minimum may exist in this range. Thus, the total number of possible rotamers of the PSE molecule is 3  3  2  2 = 36. Next we performed full geometry optimization of all those 36 PSE rotamers to determine their relative stabilities. The zeropoint vibration energy correction was included in the calculation. The calculations converged to 22 unique conformers. Structures and relative energies of the PSE conformers are shown in the Supporting Information, Figure S1, and selected structural parameters 21075

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Figure 4. Structure of the pyrene molecule (left) and fragment of the SWCNT (right).

Figure 3. (a) Structure of the most stable conformer of the PSE molecule (B3LYP/6-31++G(d,p)). (b) Relative energy of the PSE molecule as a function of the dihedral angles C(pyrene) CH2 (rotation 1, left scale of the relative energy) and CH2 COO (rotation 2, right scale) calculated at the B3LYP/6-31++G(d,p) level of theory.

of the PSE conformers are collected in Supporting Information, Table S3. The results show that the most stable conformer of the PSE molecule denoted as PSE1 (Figure 3a) has an extended conformation of the carbon side chain. The relative energies of other conformers differ less than 5 kcal/mol from the most stable one. Moreover, the relative stabilities of eight PSE conformers are only within 1 kcal/mol relative to the most stable conformer PSE1. This manifests high structural flexibility of the PSE molecule. 3.4. Interaction Energies and Structure of the Pyrene SWCNT Complexes. The pyrene molecule was used as a model of the PSE molecule interacting with a SWCNT. The geometries of the complexes formed by SWCNTs and pyrene were optimized at the DFT levels of theory. In the DFT calculations, we used the M05-2X density functional. The calculations were performed for complexes formed by pyrene and a fragment of the SWCNT surface which is shown in Figure 4. It includes 96 carbon atoms and 24 terminal hydrogen atoms. To elucidate how the nanotube chirality affects the interaction energies, calculations have been performed for the 18 nanotubes with different chiralities which are shown in the Supporting Information, Table S4. Sixteen of those nanotubes are modeled by the fragment shown in Figure 4. For complexes formed by two small-diameter nanotubes (zigzag(6,0) and armchair(4,4)), the whole nanotubes have been used in the calculations, as it is not possible in those cases to cut out smaller fragments. The interaction energies of the pyrene nanotube and pyrene graphene complexes are collected in Table S4 (Supporting Information). The structures of the pyrene zigzag(10,0) and pyrene armchair(6,6) complexes obtained in the calculations are shown in Figure 5. In both cases, the pyrene molecule is aligned with the main nanotube axes. Such orientation facilitates the maximal

Figure 5. Structure of the pyrene zigzag(10,0) (a) and pyrene armchair(6,6) (b) complexes calculated at the M05-2X level of theory.

contact between the π systems of the pyrene molecule and the nanotube. The distance between the pyrene molecule and the nanotube surface is about 3.2 Å. The positions of the pyrene molecule in the complexes with the fragments of the nanotubes with different chiralities (zigzag or armchair) are similar to the corresponding structures shown in Figure 5. The data presented in Table S1 (Supporting Information) demonstrate the dependency between the nanotube diameter and the nanotube purene interaction energy. The interaction energies increase from 13.4 kcal/mol for smaller-diameter nanotubes to approximately 20.0 kcal/mol for larger-diameter nanotubes to eventually approach the interaction energy between pyrene and planar graphene which can be viewed as an infinite-diameter nanotube. The interaction energies calculated in this work at the M05-2X level of theory are higher than ones obtained using the MP2 method (7 8 kcal/mol for small diameter nanotubes).23 This difference is due to two reasons: the MP2 interaction energies were calculated without geometry optimization, and the smaller basis set (3-21G) was used in the MP2 calculations. As seen from Table S4 (Supporting Information), the interaction energies strongly depend on the nanotube diameter. The interaction energies 21076

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Figure 6. (a) Dependency of the interaction energy between pyrene and SWCNT fragments calculated at the M05-2X level of theory for zigzag (solid curve) and armchair (dashed curve) nanotubes on the nanotube diameter. Horizontal lines correspond to the interaction energies of the pyrene molecule with planar graphene. Solid and dashed lines correspond to the zigzag-like and armchair-like orientation of pyrene with respect to the graphene surface, respectively. (b) Dependency of the interaction energy between pyrene and SWCNT fragments calculated at the M05-2X level of theory for (n,m) nanotubes on the nanotube diameter.

shown in Figure 6 clearly demonstrate that the interactions between pyrene and zigzag nanotubes are stronger than those between pyrene and armchair nanotubes with similar diameters. This conclusion is in agreement with the trend observed for the interaction energies of different pyrene graphene conformers which differ in terms of the orientation of the pyrene molecule with respect to the graphene surface (see Table S4, Supporting Information). The interaction of pyrene positioned in a “zigzag-like” orientation on the graphene surface is stronger by 0.8 kcal/mol than the pyrene graphene interaction in an “armchair-like” conformation. The stronger interaction for the zigzag orientation may be explained by more energetically favorable positions of the pyrene carbons with respect to the nanotube carbons. It is wellknown that the most optimal mutual orientation in this case should be the one with the carbon atoms of the first system (pyrene) being placed exactly above the centers of the six-membered rings of the second system (graphene) to avoid close contacts between the carbon belonging to the different systems. As seen in Figure 5, the number of close contacts between pyrene and nanotube

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carbons is larger for the pyrene nanotube in the armchair orientation than for the zigzag orientation. This results in a weaker interaction between pyrene and armchair nanotubes than between pyrene and zigzag nanotubes. Modeling of nanotube complexes is usually performed for zigzag(n,0) or armchair(n,n) nanotubes due to their relative simplicity. However, a significant fraction of real SWCNTs have an “irregular” chirality. To investigate complexes of such nanotubes with pyrene, we have calculated the equilibrium structures and the interaction energies for the pyrene (n,m)SWCNT complexes with n + m = 12., i.e., for the nanotubes with the following chiralities: (12,0), (11,1), (10,2), (9,3), (8,4), (7,5), and (6,6). These nanotubes are close in diameter to the SWCNTs produced by the CoMoCat method used in the present experiments.24 Calculated structures of the complexes are shown in the Supporting Information, Figure S2. The dependency of the calculated interaction energies on the nanotube diameter is shown in Figure 6b. As it is seen, this dependency has two almost linear parts. An analysis of the calculated structures of the complexes allows for explaining the dependency. The complexes of pyrene with the (12,0), (11,1), and (10,2) SWCNTs have zigzag-like orientation of pyrene with respect to the nanotube surface (Figure 5a). However, starting from the (9,3) SWCNT, the orientation of pyrene changes to the armchair-like orientation (Figure 5b). This results in the dependency change. Modeling of nanotube complexes is usually performed for zigzag(n,0) or armchair(n,n) nanotubes due to their relative simplicity. However, a significant fraction of real SWCNTs has an “irregular” chirality. To investigate complexes of such nanotubes with pyrene, we have calculated the equilibrium structures and the interaction energies for the pyrene (n,m)SWCNT complexes with n + m = 12, i.e., for the nanotubes with following chiralities: (12,0), (11,1), (10,2), (9,3), (8,4), (7,5), and (6,6). These nanotubes are close in diameter to the SWCNTs produced by the CoMoCat method used in the present experiments.24 Calculated structures of the complexes are shown in the Supporting Information, Figure S2. The dependency of the calculated interaction energies on the nanotube diameter is shown in Figure 6b. As it is seen, this dependency has two almost linear parts. An analysis of the calculated structures of the complexes allows for explaining the dependency. The complexes of pyrene with the (12,0), (11,1), and (10,2) SWCNTs have zigzag-like orientation of pyrene with respect to the nanotube surface (Figure 5a). However, starting from the (9,3)SWCNT, the orientation of pyrene changes to the armchair-like orientation (Figure 5b). This results in the dependency change. In all calculations of the pyrene nanotube and pyrene graphene complexes, the structure of the nanotube surface was frozen. To test how it may have influenced the accuracy of the resulting interaction energies, we have performed an additional calculation involving a full optimization of the structure of a selected pyrene graphene zigzag-like complex. The interaction energy obtained in the calculation is shown in Table S4 (Supporting Information). As it is seen, the relaxation of the surface structure leads to an insignificant change of the interaction energy of 0.4 kcal/mol (from 20.4 to 20.8 kcal/mol). The test demonstrates that the freezing of the carbon surface only marginally influences the pyrene nanotube interaction energy. 3.5. Quantum-Chemical Calculations of the PSE SWCNT Complex. The geometry and the interaction energy of the PSE complex with the fragment of the zigzag(10,0) SWCNT have been calculated at the M05-2X level of theory. The structure is 21077

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Table 1. Interaction Energies (IE, kcal/mol) of the Pyrene, PSE, 1-Methylpyrene, and 1-Ethylpyrene with Fragment of Zigzag(10,0) SWCNTs Calculated at the M05-2X Level of Theory molecule pyrene

Figure 7. Structure of the PSE zigzag(10,0) complex calculated at the M05-2X level of theory: side view (a), top view (b), and view along the main axes of the nanotube (c).

shown in Figure 7. A comparison of the structure with the structure of the pyrene SWCNT complex reveals their similarity. In both complexes, the pyrene core is stacked above the nanotube surface, and its orientation with respect to the nanotube atoms is almost identical. Thus, we conclude that the side residue of the PSE molecule affects little the geometry of the complex. On the other hand, the interaction energy between the PSE molecule and the nanotube is 2.8 kcal/mol (in absolute value; see Table 1) higher than the interaction energies of 15.7 and 18.5 kcal/mol for the pyrene zigzag(10,0) and PSE zigzag(10,0) complexes, respectively. As seen from Figure 7, there is an additional contact between the nanotube surface and the PSE molecule in the PSE nanotube complex as compared to the pyrene nanotube complex. This contact is between the CH2 group of the PSE side residue and the nanotube surface. To elucidate the nature of this interaction, we performed additional calculations of the zigzag(10,0) nanotube complexes with 1-methylpyrene and 1-ethylpyrene. The methyl and ethyl groups mimic the PSE side chain. The structures of the complexes

IE

ΔIE

15.7

PSE

18.5

2.8

1-methylpyrene

17.5

1.8

1-ethylpyrene

18.1

2.4

obtained in the calculations are identical to the PSE zigzag(10,0) complex. The calculated interaction energies are presented in Table 1. As seen, the addition of the methyl or the ethyl group increases the interaction energy (in absolute values). The interaction energy difference between the PSE nanotube and 1-ethylpyrene nanotube complexes is only 0.4 kcal/mol. This demonstrates that the influence of the remaining part of the PSE side residue (other than the ethyl fragment) on the interaction with the nanotube surface is negligible. The above allows us to conclude that the similarity between the structures and the interaction energies of the pyrene SWCNT and PSE SWCNT complexes makes pyrene a good model to study the PSE interaction with carbon nanotubes. We have determined that pyrene strongly interacts with the surface of the carbon nanotubes with different chiralities. As shown in Table 1 and Figure 6, this interaction is stronger for zigzag nanotubes than for armchair nanotubes with similar diameters. Taking into account that all armchair nanotubes are metallic and only 1/3 of all zigzag nanotubes are metallic and the rest are semiconducting, we conclude that pyrene should preferably attach to semiconducting SWCNTs rather than to conducting ones. 3.6. Molecular Dynamics Modeling of the SWCNT PSE GOX Hybrids in the Water Environment. MD modeling of various hybrids formed by SWCNT, PSE, and GOX molecules was performed to determine their stabilities and estimate their interaction energies in the water environment. We modeled twocomponent hybrids, SWCNT GOX and SWCNT PSE, as well as three- and four-component hybrids, SWCNT PSE GOX and SWCNT (PSE)2 GOX. First, the modeling has been performed for the SWCNT GOX and SWCNT PSE dimers. In the SWCNT PSE structure used to initiate the MD simulation, the PSE molecule was placed 3.4 3.5 Å above the carbon nanotube surface, the pyrene fragment of PSE placed parallel to the nanotube main axes, and the PSE side residue directed away from the nanotube. The SWCNT PSE complex was then placed inside a water box with the dimensions 41  45  135 Å containing about 9100 water molecules. The system was then optimized for 1000 iterations and equilibrated for 10 ns. In the modeling of the SWCNT GOX complex, the system was placed inside a water box with the dimensions 92  92  125 Å containing approximately 30 000 water molecules. The results of the modeling, i.e., the PSE SWCNT interaction energy and the structures of the SWCNT PSE and SWCNT GOX complexes, are shown in the Supporting Information, Figure S3 and S4, respectively. The MD modeling of the SWCNT GOX complex demonstrates its stability in water. This complex is characterized by a high interaction energy between GOX and the nanotube surface which, as seen from Figure S4 (Supporting Information), is about 65 kcal/mol. This high value may be explained by a large 21078

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Figure 8. (a) Interaction energies between the pyrene fragment and SWCNT (1) and the PSE GOX part and SWCNT (2). (b) Equilibrated structure of the SWCNT PSE GOX complex. Water molecules are not shown.

contact area between SWCNT and GOX in the complex. Approximately 15 20 side residues of GOX have been in contact with the SWCNT surface during the modeling. The strong GOX SWCNT interaction and the direct contact of the two systems are likely to affect the enzyme structure and lower its activity.12 To make the interaction smaller, a molecular linker can be placed between SWCNT and GOX. This point will be discussed next, and the possibility of one or two PSE molecules being such links will be examined. As seen from Figure S3 (Supporting Information), at the beginning of the modeling the interaction energy between PSE and SWCNT was approximately 25 kcal/mol, but after 2 ns of the modeling it decreased to 35 kcal/mol. It happened because in the initial structure of the complex SWCNT was connected to PSE only via the pyrene fragment. During the first two nanoseconds of the modeling the PSE molecule had the structure of conformer PSE1, but after that the structure of the PSE molecule switched to the conformer PSE2 structure. Structures of the conformers PSE1 and PSE2 are shown in the Supporting Information,

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Figure S1. With the structure transformation, a new contact between the PSE side chain and the SWCNT surface appeared. It resulted in the change of the PSE SWCNT interaction energy. As seen from Figure 8, in the equilibrated structure of the complex both fragments of the PSE molecule have contacts with SWCNT. Thus, we can conclude that the interaction energy between the pyrene fragment of PSE and the nanotube surface is about 25 kcal/mol, but the total interaction energy between PSE and SWCNT is about 35 kcal/mol. Next we performed additional calculations at the M05-2X level of theory of the interaction energies in complexes of PSE conformers PSE1 and PSE2 with the zigzag(10,0) SWCNT surface. The structures of the complexes, the interaction energies, and the relative stabilities obtained in the calculations are shown in Supporting Information, Figure S5. The difference between the M05-2X interaction energies calculated for the PSE1 SWCNT and PSE2 SWCNT complexes ( 9.9 kcal/mol) is in good agreement with the difference obtained in the MD calculations. On the other hand, the MD simulation produced higher (in absolute values) interaction energy between PSE and SWCNT with respect to the M05-2X result. The difference is about 6 kcal/mol and is due to the additional stabilization of the complex in water with respect to the gas-phase environment which is assumed in the standard DFT calculations. In the next step, we modeled the SWCNT PSE GOX complex. We aimed to ascertain the capability of a PSE molecule to hold a covalently bonded GOX molecule near the nanotube surface and to determine the interaction energy between the PSE GOX complex and the SWCNT. The PSE molecule can bind to NH2 groups involved in the peptide CO NH bonds of the side residues of GOX. For example, such a bond can be formed between PSE and the LYS372 residue of the peptide chain of GOX. In this way, a new molecule (called PSE GOX) is formed. It involves the pyrene fragment of PSE connecting to the GOX molecule by a linker. The PSE GOX complex is connected to the SWCNT surface by the pyrene fragment at the distance of 3.5 Å. In the modeling the whole complex was placed in a water box with the dimensions 100  75  139 Å containing about 29 600 water molecules. The system was optimized during 1000 steps and then equilibrated for 20 ns with a 1 fs time step. After the modeling was completed, we calculated the total interaction energy between PSE GOX and SWCNT and the interaction energies between SWCNT and different parts of PSE GOX. These data are presented in Figure 8a, and the equilibrated structure of the SWCNT PSE GOX complex is shown in Figure 8b. As seen in Figure 8, in the SWCNT PSE GOX complex the interaction energy between the pyrene fragment and the nanotube surface has been in the range 25 to 28 kcal/mol during the whole modeling. This is in good agreement with the pyrene nanotube interaction energy obtained for the SWCNT -PSE complex. It shows that, first, during the whole modeling the pyrene fragment has been strongly bonded to the nanotube and, second, even a single pyrene anchor is capable of effectively holding the GOX enzyme attached to the nanotube surface. The total interaction energy between the nanotube and the PSE GOX complex (curve 2 in Figure 8a) is the sum of the interaction energies between PSE and the nanotube and between GOX and the nanotube. Thus, we may determine the interaction energy between GOX and the nanotube by extracting the PSE nanotube interaction energy (curve 1 in Figure 8a) from the total SWCNT PES GOX interaction energy. The interaction energy between GOX and the nanotube has varied from 15 to 10 kcal/mol 21079

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also have modeled a complex formed by SWCNT and GOX covalently bonded to two PSE molecules: SWCNT (PSE)2 GOX. In this complex, two PSE molecules are bonded to the LYS306 and LYS372 residues of the peptide chains of GOX. The (PSE)2 GOX complex was then stacked onto the SWCNT surface by two pyrene fragments at the distance of 3.5 Å in the way described above. The whole complex was placed in a water box with the dimensions 100  75  139 Å containing about 29 800 water molecules, and the whole system was optimized during 1000 steps and then equilibrated during 20 ns with a 1 fs time step. Results of the modeling are presented in the Supporting Information, Animation S2. After the modeling, the total interaction energy between (PSE)2 GOX and SWCNT was calculated. We also calculated the interaction energies between SWCNT and each PSE fragment and between SWCNT and GOX. The results are presented in Figure 9a, and the equilibrated structure of the SWCNT (PSE)2 GOX complex is shown in Figure 9b. We found that the interaction energies of the two PSE fragments and the nanotube surface (approximately 25 kcal/mol, as seen in Figure 9a, curves 1 and 2) are similar to the corresponding interaction energies in the SWCNT PSE and SWCNT PSE GOX complexes. By subtracting the sum of the interaction energies between the two PSE molecules and the SWCNT surface, which is about 50 kcal/mol, from the total (PSE)2 GOX SWCNT interaction energy (curve 3 in Figure 9a), we can determine the interaction energy between the nanotube surface and the GOX molecule. This energy is about 5 kcal/mol during most of the modeling time and increases to 10 kcal/mol for only a very short interval at the end of the simulation. It attests to a weaker interaction between GOX and the nanotube in the SWCNT (PSE)2 GOX complex than in the SWCNT PSE GOX complex. Thus, we can conclude that two PSE molecules attached to GOX provide a stronger binding of the whole complex to SWCNT and better protect the GOX molecule from distortions and activity loss due to the interaction with the nanotube surface. Figure 9. (a) Interaction energies between the first and second pyrene fragments and SWCNT (curves 1 and 2) and the (PSE)2 GOX part and SWCNT (3). (b) Equilibrated structure of the SWCNT (PSE)2 GOX complex. Water molecules are not shown.

during the modeling. This variation is due to the changing interaction between the nanotube and outer residues of the GOX molecule. The changes occurring to the structure of the SWCNT PSE GOX complex during the MD modeling are shown in Supporting Information, Animation S1. As it can be seen, the mutual orientation of GOX and the nanotube surface slowly changes, and the GOX nanotube interaction energy varies. This result shows that there is no strong interaction between the nanotube surface and GOX, and the GOX activity is likely affected very little by this interaction. GOX is a rather large and heavy molecule, and holding it near the nanotube by means of only one linker formed by C C (each involving two rotation sites) and C N bonds can be difficult. There is some probability that GOX can also reach the nanotube sidewall even without the help of the PSE linker due to the GOX large size. This situation can be prevented if an additional PSE molecule attached to the tube surface binds with GOX. As GOX includes a large number of side residues containing amino groups, it can react with more than one PSE molecule. That is why we

4. CONCLUSIONS The interaction of PSE with carbon nanotubes results in a downshift of the intensive band corresponding to the tangential mode in the nanotube Raman spectrum with respect to the position of this band in the spectrum of the pristine SWCNTs. The magnitude of this downshift varies in the range 0.6 1.5 cm 1. The shift can be explained by a partial electron transfer from the PSE molecule to the nanotube surface or by the weaker interaction between PSE and the nanotube than the intertube interaction in bundles of the pristine nanotubes. Molecular dynamics modeling showed that the interaction energy between the pyrene fragment of PSE and the nanotube surface is about 25 kcal/mol, and the total PSE SWCNT interaction energy is about 35 kcal/mol. In the SWCNT PSE GOX complex, the interaction energy between the pyrene fragment with the nanotube surface, which is in the range 25 to 28 kcal/mol during modeling, is in good agreement with the pyrene nanotube interation energy calculated for the SWCNT PSE complex. We found that during the whole time of the modeling the pyrene fragment is strongly bonded to the nanotube. It shows that a single pyrene anchor may be sufficient to effectively hold the GOX enzyme attached to the nanotube surface. The interaction energy between GOX and the nanotube varies from 15 to 10 kcal/mol during the modeling. 21080

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The Journal of Physical Chemistry C In the SWCNT (PSE)2 GOX complex, the interaction energies between each PSE fragment and the nanotube surface (of approximately 25 kcal/mol) are similar to the corresponding interaction energies in the SWCNT PSE and SWCNT PSE GOX complexes. The interaction energy for the nanotube surface interacting with GOX is about 5 kcal/mol during most of the simulation. It is determined that two PSE molecules attached to GOX provide stronger binding of the whole complex to the SWCNT and better protect the GOX molecule from distortions due to the interaction with the nanotube surface.

’ ASSOCIATED CONTENT

bS

Supporting Information. Structure and relative stabilities of the PSE conformers (Figure S1); Structure of the pyrene (n,m)SWCNT complexes (Figure S2); Results of the MD modeling (Figures S3 and S4); Structure and interaction energies of the PSE1 zigzag(10,0)SWCNT and PSE2 zigzag(10,0)SWCNT complexes (Figure S5); Calculated geometries (Cartesian coordinates) (Table S1); Parameter set of the PSE molecule (Table S2); Geometry parameters of the PSE conformers (Table S3); Interaction energies of the pyrene with SWCNTs and graphene Table S4); Visualization of the MD modeling of the SWCNT PSE GOX and SWCNT (PSE)2 GOX complexes (Animation S1 and Animation S2, respectively). This material is available free of charge via the Internet at http://pubs.acs.org.

’ AUTHOR INFORMATION Corresponding Author

*E-mail: [email protected]. Phone: +380 57 341 0938. Fax: +380 57 340 3370.

’ ACKNOWLEDGMENT This work has been partially supported by Grants N 4950 of the Science and Technology Center in Ukraine and National Academy of Sciences of Ukraine. The authors acknowledge the Computational Centers at Institute for Low Temperature Physics and Engineering and at the University of Arizona for providing computer time for this work. We are grateful to V.S. Leontiev and A.S. Linnik for sample preparation and characterization. ’ REFERENCES (1) Harris, P. J. F. Carbon Nanotube Science; Cambridge University Press: UK, 2009. (2) Kumar, C. Nanomaterials for Biosensors; Wiley-VCH Verlag GmbH&Co./KGaA: Weinheim, 2007. (3) Balasubramanian, K.; Burghard, M. Biosensors Based on Carbon Nanotubes. Anal. Bioanal. Chem. 2006, 385, 452–468. (4) Yang, Y.; Wang, Zh.; Yang, M.; Li, J.; Zheng, F.; Shen, G.; Yu, R. Electrical Detection of Deoxyribonucleic Acid Hybridization Based on Carbon-Nanotubes/Nano Zirconium Dioxide/Chitosan-Modified Electrodes. Anal. Chim. Acta 2007, 584, 268–274. (5) Barone, P. W.; Baik, S.; Heller, D. A.; Strano, M. S. Near-Infrared Optical Sensors Based on Single-Walled Carbon Nanotubes. Nat. Mater. 2005, 4, 86–92. (6) Hazani, M.; Naaman, R.; Hennrich, F.; Kappes, M. M. Confocal Fluorescence Imaging of DNA-Functionalized Carbon Nanotubes. Nano Lett. 2003, 3, 153–155. (7) Jeng, E. S.; Moll, A. E.; Roy, A. C.; Gastala, J. B.; Strano, M. S. Detection of DNA Hybridization Using the Near-Infrared Band-Gap

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