Transport of Amino Acid Cations through a 2.25-nm-Diameter Carbon

Article pubs.acs.org/JPCC

Cite This: J. Phys. Chem. C XXXX, XXX, XXX−XXX

Transport of Amino Acid Cations through a 2.25-nm-Diameter Carbon Nanotube Nanopore: Electrokinetic Motion and Trapping/ Desorption Mark D. Ellison,*,† Lucas Bricker,† Laura Nebel,† Jessica Miller,†,‡ Samuel Menges,† Gabrielle D’Arcangelo,†,‡ Anna Kramer,†,‡ Lee Drahushuk,§ Jesse Benck,§ Steven Shimizu,§ and Michael S. Strano§ †

Department of Chemistry, Ursinus College, 601 E. Main St., Collegeville, Pennsylvania 19426, United States Department of Chemical Engineering, Massachusetts Institute of Technology, 77 Massachusetts Avenue, Cambridge, Massachusetts 02139, United States

§

S Supporting Information *

ABSTRACT: In this study, we examine the individual ionic transport of four different amino acid cations through a 2.25-nmdiameter, 200-μm-long single-walled carbon nanotube (SWNT) and compare them to previous work on Li+ and methanol in the same SWNT. For the amino acids, the pore-blocking current was found to increase with applied field, from 1 to 100 pA. The observed differences in pore-blocking currents of the different amino acids are mostly explained by a simple model of the volumes of the blockers. A threshold voltage was found for the amino acids to exhibit pore blocking, in agreement with previous results for monatomic ions and molecules which also encounter an energy barrier for entry into an SWNT. The average dwell time for each of the amino acids was found to be relatively constant for applied voltages between 400 and 1000 mV. Additionally, the distribution of dwell times for each amino acid exhibited a tail at long dwell times. These results are well-modeled by an adsorption/desorption model in which the amino acid molecules interact with the nanotube wall as they pass through the tube. Our results suggest that comparisons of conductance changes and mobilities could be used in some cases to identify the type of amino acid, although the identification might not be unambiguous.

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solutions, water can wet and fill a carbon nanotube.39−42 This enables ions and molecules to enter and block proton current through the nanotubes, resulting in a two-state Coulter effect that provides a distinct signature of transport through a nanotube.20−23,43−45 The high aspect ratio of nanotubes allows mass transfer resistance to manifest itself in properties such as conductivity change and ionic mobility,20−23,46 and these transport properties of individual ions provide details about the nature of molecular motion within the nanopore. The flow of a variety of ions and molecules through carbon nanotubes has been studied through both experiments and simulations.20−23,25,46−50 With regard to small molecules, the motion of water has been particularly well-studied,51−61 and recently, we reported the results of studies of the motion of methanol through a single-walled carbon nanotube (SWNT) nanopore.46 On the other hand, with the exception of a study on caffeine,50 little other work has been published about the motion of smallto medium-sized molecules through carbon nanotubes. This exposes a gap in the knowledge about the behavior of molecules whose sizes fall between the extremes of the smallest

INTRODUCTION The transport of ions and molecules, particularly those of biological relevance, through single, isolated, synthetic pores with sub-10-nm diameters is an area of significant interest. Synthetic nanopores have been constructed using a variety of materials, including Si/SiN,1−7 SiC,8−11 polymer track etching,12,13 graphene,14−18 MoS2,19 and carbon nanotubes.20−27 Each of these systems offers its own challenges and advantages. One feature that these different nanopores have in common is an opportunity to enhance our fundamental understanding of flow in a nanoconfined environment. This basic knowledge can then be transferred to applications in the sensing and sequencing of biomolecules. For example, the use of nanopores in the sensing, separation, and identification of even larger biomolecules, such as proteins and DNA, has already been reported.28−33 Moreover, the use of solid-state nanopores to sequence proteins has shown good promise.34−36 These encouraging results demonstrate the importance of further studying the basic science and applications of fabricated nanopores. As a nanopore material, carbon nanotubes offer several advantages. First, physical stability and small diameters enable them to detect and selectively transport small ions or molecules.37,38 In carbon nanotubes immersed in aqueous © XXXX American Chemical Society

Received: September 1, 2017 Revised: November 4, 2017 Published: November 24, 2017 A

DOI: 10.1021/acs.jpcc.7b08727 J. Phys. Chem. C XXXX, XXX, XXX−XXX

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The Journal of Physical Chemistry C particles (alkali metal ions) and very large molecules (biopolymers). In addition to exploring the fundamental science of motion through nanopores, investigations of the motion of amino acids through carbon nanotubes offer an opportunity to assess the potential of applications for nanopores. Although the transport of larger biomolecules, such as proteins and DNA, continues to be studied,24,62,63 analysis and sequencing of larger biomolecules depends on the reliable identification of their constituent units, e.g., amino acids. These molecules are similar in size, shape, and structure, so differentiating among them represents a significant challenge. Several approaches to detecting fundamental biomolecules as they pass through a nanopore have been tried, including current sensing64 and quantum tunneling.33,36,64 Although quantum tunneling detection shows promise for future work, detection of the changes in current flowing through a narrow nanopore could provide a sensitive measurement of the identity of the analyte molecule. For example, for an SWNT nanopore of known diameter and length, certain properties such as the conductance change, velocity, and mobility might be characteristic of and/or unique to a specific amino acid. Therefore, we undertook a study of four small amino acids, namely, glycine, valine, β-alanine, and glutamic acid, through a 2.25-nm-diameter single-walled carbon nanotube nanopore.

Figure 1. (a) SEM image of the multiwell device. The red rectangle shows the area covered by PDMS, and the SWNTs are the two light gray vertical lines. The left SWNT was completely covered by PDMS and not active in these experiments. (b) Optical microscope picture of the multiwell device. The specific reservoirs used in these experiments are highlighted in the red rectangle. The ruler at right has markings in millimeters. Reproduced with permission from ref 46. Copyright 2017 American Chemical Society.

The nanotube devices were mounted on optical mounting hardware on a nitrogen-cushioned vibration isolation table surrounded by a Faraday cage (Kinetic Systems). This lownoise setup allows for the detection of pore-blocking events with amplitudes as low as 2 pA.46 The Ag/AgCl electrodes were formed by immersing Ag wire in bleach for 20 min. The voltage applied across the SWNT was controlled using a Molecular Devices Axopatch 200B amplifier, and the current was collected using a Molecular Devices Digidata 1550 D/A converter. Data collection was performed using Clampex software (Molecular Devices, 2 kHz Bessel low-pass filter, 250 kHz acquisition frequency), whereas pore-blocking current and dwell times were obtained from the current data with ClampFit software (Molecular Devices). Before analysis, the data were filtered in the ClampFit software with a Boxcar low-pass filter using 21 smoothing points. Statistical analysis of the pore-blocking current and dwell-time data was performed in Igor (Wavemetrics). Solutions of the different analytes were made in the following steps: Glycine hydrochloride (Aldrich, >99%) was dissolved in ultrapure water to concentrations of 0.1 and 1.0 M. These solutions had pH values of 3.1 and 2.2, respectively, as measured by a pH meter. β-Alanine hydrochloride (Aldrich, >99.0%) and L-glutamic acid hydrochloride (Aldrich, >99%) were dissolved in ultrapure water to concentrations of 0.1 M. (Although 1.0 M solutions are preferable because pore-blocking events are more frequent at higher concentrations, the solubilities of these amino acids are lower than 1.0 M.) These solutions were each measured to have a pH of 3.2. LValine hydrochloride (Aldrich, >99.5%) was dissolved to a concentration of 1.0 M. Concentrated hydrochloric acid was added in 10 μL increments to the valine solution until the pH was measured to be 3.0 with a pH meter. Separately, lithium chloride (Aldrich, ≥99.99%) was dissolved in ultrapure water, and concentrated hydrochloric acid was added in 10 μL increments until the pH reached 3.0.

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EXPERIMENTAL SECTION The SWNT nanopore fabrication process has been previously described,20−22 as has the construction of the particular nanopore device used in this study.46 Details are also given in the Supporting Information (SI). Briefly, a catalyst solution was applied to the edge of a rectangular piece of silicon wafer. SWNTs were grown using a chemical vapor deposition (CVD) process with CH4 as the carbon source. In contrast to previous research,65 our process does not grow closely packed arrays of nanotubes. Rather, it produces individual SWNTs that are typically 50−250 μm from their nearest neighbor. After growth, the SWNTs were located and characterized using scanning electron microscopy and Raman spectroscopy. Next, a multiwell device was created in which a polydimethylsiloxane (PDMS, Dow Sylgard, 1:1 ratio of elastomer to curing agent) mask with regularly arranged openings was glued with PDMS glue (Dow Sylgard, 3:1 ratio of elastomer to curing agent) to the wafer. The glue layer is much thicker than the SWNT, so it encapsulates the SWNT. After the glue had cured, the device was briefly exposed to an oxygen plasma, which removed uncovered sections of the SWNTs and produced carboxylic acid functional groups on the ends of the remaining SWNT segments.66 The reservoirs were then thoroughly rinsed with ultrapure water (Millipore, 18.2 MΩ cm). Two views of the multiwell device are shown in Figure 1. The first panel shows a scanning electron microscopy (SEM) image of the silicon wafer, with the red rectangle showing the area covered by PDMS. The second panel is a light microscopy image of the device with the PDMS overlayer. In experiments using this device, several adjacent reservoir combinations were tested. The combination that reliably gave results was reservoirs separated by a 200 ± 15 μm thick section of PDMS; the SWNT length was assumed to be the same as the width of the PDMS. All results from the device reported in this article were obtained with this 200 ± 15 μm long SWNT under that section of PDMS.

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RESULTS AND DISCUSSION Current traces collected with 0.1 M glycine hydrochloride solutions in the reservoirs are shown in Figure 2a. The data B


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The Journal of Physical Chemistry C

is visualized more clearly in Figure 2b, in which individual points indicate the average PBC and the error bars reflect the standard deviations. At low applied voltages, the PBC was low with little spread in the PBC values of individual events. At higher applied voltages, the PBC generally increased, as did the distribution in values. As shown in Figure 2c, at different applied voltages, the average dwell-time values for glycine were quite similar. The overlap of the error bars across the different voltages indicates that there was no statistically significant difference among the dwell times at different voltages. In other words, the dwell time of glycine in the SWNT was found to be independent of applied voltage. Using data for all voltages, we calculate the average dwell time for 0.1 M glycine to be 82.5 ± 64.7 ms. Current traces, PBCs, and dwell times for valine, β-alanine, and glutamic acid are shown in Figures 3−5, respectively. These data are qualitatively similar to those for glycine: The PBC generally increases with increasing applied voltage, and the dwell times are independent of applied voltage. The PBCs of βalanine and glutamic acid were found to be significantly higher than those of glycine, whereas those of valine were similar to those of glycine. Each of the amino acids exhibited a threshold voltage for pore blocking to be observed. As noted earlier, carboxylic acid groups are expected to be present at the pore mouth. Interaction between the positively charged amino acid and these carboxylic acid groups and/or hydrogen bonding between the amino acid and these carboxylic acid groups present an activation barrier to amino acids trying to enter the SWNT. Only at a sufficiently large voltage is enough electromotive force imparted to the amino acids for them to enter the inside of the nanotube. Because the behavior of alkali metal ions in sub-3-nmdiameter SWNT nanopores is fairly well-understood,20−22,47,48,67−78 the device used in this work was tested with solutions of 0.1 M LiCl, and the results of these experiments have been previously reported in detail elsewhere.46 In that work, the Li+ ions showed a steadily increasing pore-blocking current (PBC, magnitude of current decrease) with applied voltage. This is similar to the results found previously for Li+ in SWNT20,22 and PDMS79 nanopores. Additionally, the dwell times (length in time of the current decrease) for Li+ ions were found to be inversely proportional to the applied voltage, as is characteristic for an ion with a constant electrophoretic mobility. The same type of linear relationship has previously been observed for Li+ in SWNT nanopores.20,22 However, PDMS was used to cover the SWNTs in our device, so it was necessary to consider the possibility that the nanopore was formed by a pathway in the PDMS. Such a pathway could be either entirely through the PDMS or between the SWNT and the PDMS. Li+ ions in PDMS nanopores, however, display dwell times that are basically independent of voltage.79 Thus, the Li+ PBC and dwell-time data provide strong evidence that the nanopore connecting the tested reservoirs was an SWNT. Additional experiments determined that the charge carriers are positively charged, that is, protons and not hydroxide ions. Numerous control experiments were performed to rule out other effects as sources of the current fluctuations and to establish ions as the current blockers. Representative current traces from these control experiments are presented in ref 46. The results of these control experiments support our hypothesis of a proton current through the SWNT that is

Figure 2. (a) Current traces of 0.1 M glycine hydrochloride solution at pH = 3.1 in the device at various voltages, showing pore-blocking events. Inset are the structure of the glycine molecule-ion and a zoomed-in view of a section the 1000 mV data, showing individual pore-blocking events (b) Dependence of pore-blocking current on applied voltage for 0.1 M glycine hydrochloride. No pore blocking was observed below 400 mV. (c) Dependence of dwell time of 0.1 M glycine on the applied voltage. Data points indicate the average value at each voltage, and error bars show the standard deviations of all events recorded at each voltage.

show that no pore blocking occurred below 400 mV and that the PBC generally increased with increasing voltage. This result C


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Figure 4. (a) Current traces of 0.1 M L-β-alanine hydrochloride solution at pH = 3.2 in the device at various voltages, showing poreblocking events. Inset are the structure of the β-alanine molecule-ion and a zoomed-in view of a section the 1000 mV data, showing individual pore-blocking events. (b) Dependence of pore-blocking current on applied voltage for 0.1 M L-β-alanine hydrochloride. No pore blocking was observed below 600 mV. (c) Dependence of dwell time of 0.1 M β-alanine on the applied voltage. Data points indicate the average value at each voltage, and error bars show the standard deviations of all events recorded at each voltage.

Figure 3. (a) Current traces of 1.0 M L-valine hydrochloride solution at pH = 3.0 in the device at various voltages, showing pore-blocking events. Inset are the structure of the valine molecule-ion and a zoomed-in view of a section the 1000 mV data, showing individual pore-blocking events. (b) Dependence of pore-blocking current on applied voltage for 1.0 M valine hydrochloride. No pore blocking was observed below 700 mV. (c) Dependence of dwell time of 1.0 M valine on the applied voltage. Data points indicate the average value at each voltage, and error bars show the standard deviations of all events recorded at each voltage.

and with previous studies that found hydrogen ions to be the primary current carriers.20,22 We therefore conclude that hydrogen ions were the chief current carriers in the amino acid solutions used in this research. ΔI PBC Conductance changes, ΔG = V = V , were calculated for all events of each amino acid, and a histogram of the

blocked when an amino acid ion enters the nanotube. For all four of the amino acids studied, the PBC generally increased with increasing voltage, which is in agreement with the Li+ data D


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The Journal of Physical Chemistry C equation μ =

v E

=

d V

τ d

=

d2 , Vτ

where d is the SWNT length, V is

the applied voltage, and τ is the dwell time. For 0.1 M glycine, the distribution of mobilities is shown in Figure 6b, and the average mobility was found to be 1.2 × 10−6 ± 8.6 × 10−7 m2 V−1 s−1. This is somewhat larger than the mobility of Li+ in the very same SWNT, 1.6 × 10−7 m2 V−1 s−1, but similar to the mobilities of alkali metal ions in other SWNTs.20,22 The conductance changes for valine, β-alanine, and glutamic acid are shown in panels c, e, and g, respectively, of Figure 6, and the corresponding mobilities are shown in panels d, f, and h of Figure 6. The average conductance changes and mobilities are summarized in Table 1. For comparison, the Li+ control data and the data for methanol in the same SWNT are also presented in Table 1. Also included in Table 1 are data for a 1.0 M solution of glycine. (Full data for 1.0 M glycine are provided in the Supporting Information.) The increased concentration of this amino acid resulted in a lower pH: about 2.2 versus 3.0 for 0.1 M concentration. The effect of pH is most noticeable for the conductance change: 11.3 pS for 1.0 M glycine versus 1.6 pS for 0.1 M glycine. These values are consistent with previous observations that the PBC strongly depends on pH and further evidence that protons are the predominant charge carriers in the system.20 The increased concentration of glycine does not significantly change its dwell time, threshold voltage, mobility, or velocity, which is expected because those quantities are not dependent upon concentration. These results illustrate that pH is important for the PBC and conductance change and that the other parameters are mostly unaffected by the pH of the solution. Also reported in Table 1 are the volumes and surface areas of the species, computed with the computational program Spartan ’16 (Wavefunction, Inc.), which uses van der Waals radii to compute those quantities. For the amino acids, a trend of increasing conductance change with increasing volume can be observed, with the exception of valine. The discrepancy shown by valine could be related to its dynamical behavior during transit, as discussed below. The overall trend matches what was observed for Li+ and methanol, suggesting that the space occupied by the ions breaks the chains of water molecules within the SWNT and disrupts the proton flow. Figures S3−S6 in the Supporting Information show space-filling molecular diagrams of each of the amino acids in a (16,16) SWNT segment, illustrating the relationship between size and conductance change. There are several explanations for the fact that each of the amino acids exhibits dwell times that do not depend on voltage. The Li+ data indicate that an alkali metal cation in the same SWNT does exhibit the expected inverse relationship between dwell time and voltage.20−22,80 On the other hand, the constant dwell times exhibited by the amino acids are similar to the behavior of the neutral molecule methanol in the same SWNT.46 Therefore, one possible explanation for the voltageindependent dwell times is that the amino acid ions deprotonate in the SWNT, losing their charge and behaving like methanol. We explored the likelihood of such a deprotonation of amino acids in an SWNT by performing multilevel ONIOM calculations in Gaussian 09, Revision E.01.81 A 5-nm-long segment of a (16,16) SWNT (2.25 nm in diameter) was constructed, and 96 water molecules and one amino acid ion were placed inside. The amino acid molecule and seven immediately adjacent water molecules were treated

Figure 5. (a) Current traces of 1.0 M L-glutamic acid hydrochloride solution at pH = 3.2 in the device at various voltages, showing poreblocking events. Inset are the structure of the glutamic acid moleculeion and a zoomed-in view of a section of the 1000 mV data, showing individual pore-blocking events. (b) Dependence of pore-blocking current on applied voltage for 0.1 M glutamic acid hydrochloride. No pore blocking was observed below 600 mV. (c) Dependence of dwell time of 1.0 M glutamic acid on the applied voltage. Data points indicate the average value at each voltage, and error bars show the standard deviations of all events recorded at each voltage.

distribution of values for 0.1 M glycine is shown in Figure 6a. The average conductance change was found to be 1.6 ± 1.2 pS. Assuming that the molecule remained protonated and therefore charged, its electrophoretic mobility was calculated using the E


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Figure 6. Conductance change (pS) distributions for (a) 0.1 M glycine hydrochloride, (c) 1.0 M valine hydrochloride, (e) 0.1 M β-alanine hydrochloride, and (g) 0.1 M glutamic acid hydrochloride. Mobility (m2 V−1 s−1) distributions for (b) 0.1 M glycine hydrochloride, (d) 1.0 M valine hydrochloride, (f) 0.1 M β-alanine hydrochloride, and (h) 0.1 M glutamic acid.

proton-transfer reactions, and carbon-based nanosystems.83−87 Additional details about the calculations and images of the system geometries are presented in the Supporting Information. Finally, a proton was added either to the amine group of the amino acid or to the water molecule adjacent to the amine

with the M06-2X density functional and 6-31G(d) basis set, and the remaining water molecules and SWNT were treated with the AMBER force field,82 which was developed for simulating biomolecules in aqueous environments. The M062X density functional has yielded very good results for a broad range of chemical systems, including noncovalent interactions, F


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Table 1. Average Conductance Changes, Mobilities, Dwell Times, and Velocities for the Four Amino Acids Investigated in this Research, and Li+ and Methanol in the Same SWNT analyte

av conductance change (pS)

glycine (0.1 M) glycine (1.0 M) β-alanine (0.1 M) valine (1.0 M) glutamic acid (0.1 M) Li+ (1.0 M)46 methanol (1.0 M)46

1.6 11.3 5.7 3.5 81.8

± ± ± ± ±

1.2 9.7 4.9 1.0 9.8

6.2 ± 2.4 3.5 ± 1.8

av mobility (m2 V−1 s−1) 1.2 1.3 1.2 1.7 1.1

× × × × ×

10−6 10−6 10−6 10−6 10−6

± ± ± ± ±

8.6 1.1 6.7 6.2 7.6

× × × × ×

10−7 10−6 10−7 10−7 10−7

av dwell time (ms)

threshold voltage (mV)

± ± ± ± ±

400 400 600 700 600

3.9 6.3 4.8 6.7 4.3

200 700

82.5 61.8 68.8 35.9 78.0

1.6 × 10−7 88

V (Å3)

surface area (Å2)

10−3 10−3 10−3 10−3 10−3

72.38 72.38 90.37 127.05 137.04

97.54 97.54 117.98 154.64 168.69

2.3 × 10−3

80.72 40.36

141.08 60.66

× × × × ×

desorbed.92 In that case, the adsorbed/desorbed tail has a characteristic time of 1 τ≈ kdes (2)

group of the amino acid, and the minimum-energy configuration was found. For each amino acid, the minimum-energy configuration was the one with the proton on the amine group of the amino acid, indicating that proton transfer from the amino acid to an adjacent water molecule is energetically unfavorable. The energy of deprotonation of the amino acid was estimated to be ΔE = 380 kJ/mol for glycine, confirming that the amino acid is unlikely to deprotonate within the SWNT. The other three amino acids gave similar results. These results were expected: In the bulk, amino acids are much less acidic than H3O+,88 so proton transfer from the amino acid to a water molecule is unfavorable. However, different chemistry can be exhibited in nanoconfined environments than in bulk solution,87,89,90 so the calculations are a useful check on the deprotonation hypothesis. On the basis of the bulk acid−base properties of amino acids and the calculations we performed, we conclude that it is unlikely that the amino acid molecules lose a proton and become neutral molecules within the SWNT. Furthermore, the average velocities of the amino acids were found to be greater than that of methanol in the same SWNT. (See Table 1.) All of the amino acids tested in this study are larger and more massive than methanol and would therefore be expected to travel more slowly as neutral species than methanol does. Thus, the average velocities of the amino acids suggest that they remain charged inside the SWNT. A trapping-desorption process could explain the voltageinvariant dwell times of the amino acids, as well as the large range of dwell times for each amino acid. As the amino acid ions travel through the SWNT, they have numerous opportunities to interact with and adsorb onto the inner SWNT wall, possibly through hydrophobic interactions or through a cation−π interaction.91 If adsorption on the wall were frequent, the transit time would be dominated by adsorption/desorption kinetics, and Yeh and Hummer used just such a model to explain their simulation of translocation of RNA segments through an SWNT segment.92 In their model, the average time for an ion to transit through an SWNT has contributions from the drift velocity from the electric field and adsorption/desorption rates, as expressed in the equation

k ⎞ L⎛ ⟨t ⟩ = ⎜1 + ads ⎟ v⎝ kdes ⎠

64.7 41.7 44.4 21.1 63.3

av velocity (m/s)

Histograms of dwell times for the amino acids all exhibited a steadily decreasing tail at long dwell times, as shown for 0.1 M glycine in Figure 7 and for the rest of the amino acids in the

Figure 7. Dwell-time (ms) distributions for 0.1 M glycine hydrochloride. The short dwell times correspond to direct transport; the blue line is a fit to guide the eye, and the dark line is an exponential fit to the tail of the data. The long dwell times correspond to moleculeions that trapped and desorbed before exiting the SWNT. The fit to the long dwell times was used with eq 2 to find kdes.

Supporting Information (Figures S7−S9). Therefore, we applied the adsorption model of Yeh and Hummer to the amino acid dwell times, and full details of the analysis are given in the Supporting Information. Table 2 summarizes the dwell times and kads and kdes values for the four amino acids studied. As expected, the adsorption rate constants for glycine at 0.1 and 1.0 M were quite similar. Interestingly, the desorption rate constant was greater for the higher concentration (1.0 M) than Table 2. Average Dwell Times and Adsorption and Desorption Rate Constants for the Four Amino Acids Investigated in This Research

(1)

amino acid

where L is the length of the SWNT, v is the drift velocity, and kads and kdes are the rate constants for adsorption and desorption, respectively. If the electric-field-induced drift velocity is fast compared to diffusion, then the flow can be characterized by a contribution from drift flow and a tail of molecules that have adsorbed and

glycine (0.1 M) glycine (1.0 M) valine (1.0 M) β-alanine (0.1 M) glutamic acid (0.1 M) G

av dwell time (ms) 82.5 61.8 35.9 68.8 78.0

± ± ± ± ±

64.7 41.7 21.1 6.9 63.3

kads (s−1) 18.2 20.0 20.0 46.0 30.8

± ± ± ± ±

5.3 5.4 18.5 9.6 4.3

kdes (s−1) 12.7 21.2 38.4 46.2 24.8

± ± ± ± ±

7.6 5.7 36.0 9.7 3.4


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oxide have been reported,94 but that is not a suitable comparison system for the same reason. An additional factor to consider is the shape of the amino acid molecules. Previously studied ions were monatomic and therefore spherical. The amino acid ions considered here are approximately prolate tops. Transport through the tube will thus depend on whether the molecule’s long axis is parallel or perpendicular to the nanotube’s axis, as the two configurations will entail significantly different numbers of collisions with water molecules and different transit times. Additionally, nonspherical molecules can undergo spinning and tumbling motions that will certainly affect the dwell times. It is possible that multiple collisions of such ions with water molecules and with the SWNT walls would make the time required to transit the tube essentially constant, especially if such collisions are effective at converting translational energy into rotational energy. A search of the literature did not locate any simulations of small molecules in SWNT nanopores, especially a description of collisions and the motion of these ions. Molecular dynamics simulations have proven quite effective at elucidating details of molecular and ionic motion through SWNT nanopores,47,51,72−78 and we hope that our results inspire a theoretical study of the role of molecular shape in transport through SWNTs. Finally, the use of nanopores for the sensing and identification of biopolymers such as proteins, RNA, and DNA has been explored by many scientists. Experiments have demonstrated that SiN and SiC nanopores have the ability to detect DNA,4,95−97 distinguish between different homopolymers,98 identify specific domains along a strand,99 and differentiate single-stranded from double-stranded homopolymers.100 Single-stranded DNA oligomers have also been shown to travel through both SWNT24,62 and MWNT63 nanopores, in agreement with theoretical predictions.101 Despite these advances, sequencing of these biomolecules has yet to be achieved. Such a step will require an accurately measurable property or properties that allow unambiguous identification of each subunit of the entire molecule. Therefore, we examined our data to determine whether the conductance changes and/or mobilities could distinguish the different amino acids from each other. The data in Table 1 show that although the average conductance changes for the various amino acids are different, the ranges in measured values generally overlap. For the mobilities, the average values are fairly close to each other and also exhibit significant overlap in the range of observed values. However, the combination of these properties does show some differences. In Figure 8, panel a shows the linear scale, and panel b shows the log−log scale of conductance changes and ion mobilities. On the basis of these data, conductance change and mobility would not be able to distinguish glutamic acid from β-alanine. On the other hand, the data from glycine show almost no overlap from those of glutamic acid and β-alanine, showing that measurements of these properties could distinguish between glycine and either glutamic acid or β-alanine. These measurements of the SWNT nanopore transport properties of individual amino acids illustrate some potential difficulties in using an SWNT nanopore to sequence a biopolymer. As our results show, not all of the monomers would result in distinct conductance changes and mobilities. The studies here involved individual molecule-ions, and the problem would likely be more challenging for a chain of linked

for the lower concentration (0.1 M). This suggests that the desorption process could involve hydrogen ions, which are present in much greater amounts in the 1.0 M solution. For example, collisions of hydrogen ions with adsorbed glycine ions could induce desorption, leading to a larger observed rate constant. The rate constant data in Table 2 help to explain the observed trends in dwell times. First, although the dwell times for 0.1 M glycine and 1.0 M glycine are the same within the error bars, the average dwell time for the higher concentration is lower, indicating faster transit through the SWNT at higher concentration. For the two concentrations, the kads values are essentially the same, but the kdes value is higher for the 1.0 M concentration. This means that molecules in the 1.0 M solution desorb at a much higher rate. Consequently, at the higher concentration, molecules spend less time adsorbed to the inner wall and travel through the SWNT more rapidly. Likewise, valine was found to have the shortest dwell time of all of the amino acids studied. Notably, it has a kads value similar to that of glycine, but its kdes value is much higher. These rate constant data suggest that valine also spends little time adsorbed, allowing it to travel through the SWNT quickly. Qualitatively, the trend seems to be that kads increases with increasing molecular size. For these amino acids, the hydrophobic portion increases in size relative to the charged portion, suggesting that the adsorption process involves a hydrophobic interaction between that part of the amino acid and the SWNT wall. If the attractive force for adsorption were instead a cation−π interaction, it would be approximately the same for all of the amino acids, because all have similar pKa values and are protonated to the same degree in our experiments. That would lead to similar kads values. However, our observation indicates different kads values, suggesting that another force, such as hydrophobic interactions, is responsible for the adsorption. Little comparable work has been done on the comparison of the adsorption and desorption kinetics of amino acids. Yeh and Hummer determined rate constants for RNA hexamers (adenine, A6, or uracil, U6) that are about 8 orders of magnitude greater than those we found here. However, they used much higher electric fields (∼5 × 108 V/m versus ∼5 × 103 V/m) and noted that the rate constants depend exponentially on the applied field. An additional complication in comparing their rate constants to those obtained in this study is that the RNA hexamers they investigated are much larger than the single amino acid molecule-ions of this study. Those larger molecules offer greater possible interaction areas with the SWNT. Significant work has been performed to investigate the adsorption of monatomic ions, primarily divalent transitionmetal cations, to oxidized SWNTs and MWNTs.93 However, the adsorption mechanism for that process is believed to involve an interaction between the cation and carboxylic acid groups on the outside of the nanotubes, which are a product of the oxidation of the nanotubes. Our SWNTs have smooth, unfunctionalized interiors, so the adsorption mechanism for the amino acids is likely to be different. Indeed, the adsorption of most metal cations follows second-order or pseudo-secondorder kinetics, whereas the dwell times of the amino acids exhibit an exponential decrease, indicative of first-order (or pseudo-first-order) kinetics. Therefore, adsorption of monatomic ions to oxidized SWNTs and MWNTs is not an appropriate comparison system for our results. Similarly, numerous studies of the adsorption of metal ions to graphene H



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AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. ORCID

Mark D. Ellison: 0000-0003-3201-8478 Michael S. Strano: 0000-0003-2944-808X Present Address ‡

Students at Agnes Irwin High School, Rosemont, Pennsylvania 19010, United States. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work was supported by National Science Foundation Awards CHE-1306349 and CHE-1306529. This work used the Extreme Science and Engineering Discovery Environment (XSEDE), which is supported by National Science Foundation Gant OCI-1053575. Specifically, Gaussian calculations were performed on the Bridges system, which is supported by NSF Award ACI-1445606, at the Pittsburgh Supercomputing Center (PSC). The authors thank Erica Ellison and Sam Faucher for critical proofreading of the manuscript.

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Figure 8. Conductance change and mobility distributions displayed on (a) linear and (b) log−log scales.

amino acids, because individual events would not likely be observed.

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CONCLUSIONS In conclusion, we have demonstrated the motion of amino acid molecular ions through an SWNT nanopore. The dwell times of the amino acids are independent of the applied voltage because of trapping/desorption of the ions with the internal wall of the SWNT as they pass through the tube. The blocking of current through the SWNT is found to be related to the molecular volume of the blocker. Using measurements of conductance-change and mobility measurements has the potential for identification of a particular amino acid, but challenges remain for using SWNT nanopores to sequence biomolecules.

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ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.jpcc.7b08727. Details of device fabrication, SEM image of the device, glycine current data, space-filling models of amino acids inside an SWNT, dwell-time distribution data, and calculation of adsorption and desorption rate constants (PDF) I


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Transport of Amino Acid Cations through a 2.25-nm-Diameter Carbon

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