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A Low Energy Route to DNA-wrapped Carbon Nanotubes via Replacement of Bile Salt Surfactants Jason K Streit, Jeffrey A Fagan, and Ming Zheng Anal. Chem., Just Accepted Manuscript • DOI: 10.1021/acs.analchem.7b02637 • Publication Date (Web): 31 Aug 2017 Downloaded from http://pubs.acs.org on September 1, 2017

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Analytical Chemistry

A Low Energy Route to DNA-wrapped Carbon Nanotubes via Replacement of Bile Salt Surfactants Jason K. Streit, Jeffrey A. Fagan, and Ming Zheng* Materials Science and Engineering Division, National Institute of Standards and Technology, 100 Bureau Drive, Gaithersburg, MD 20899-8542 *Corresponding author: [email protected]

ACS Paragon Plus Environment

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ABSTRACT DNA-wrapped carbon nanotubes are a class of bio-nano hybrid molecules that have enabled carbon nanotube sorting, controlled assembly, and biosensing and bioimaging applications. The current method of synthesizing these hybrids via direct sonication of DNA/nanotube mixtures is time consuming and not suitable for high throughput synthesis and combinatorial sequence screening. Additionally, the direct sonication method does not make use of nanotubes presorted by extensively developed surfactant-based methods, is not effective for large diameter ( > 1 nm) tubes, and can not maintain secondary and tertiary structural and functional domains present in certain DNA sequences. Here, we report a simple, quick, and robust process to produce DNA-wrapped carbon nanotube hybrids with nanotubes of broad diameter range and DNA of arbitrary sequence. This is accomplished by exchanging strong binding bile salt surfactant coating with DNA in methanol/water mixed solvent, and subsequent precipitation with isopropyl alcohol. The exchange process can be completed within 10 min and converts over 90% nanotubes into the DNA wrapped form. Applying the exchange process to nanotubes pre-sorted by surfactant-based methods, we show that the resulting DNA-wrapped carbon nanotubes can be further sorted to produce nanotubes with defined handedness, helicity, and endohedral filling. The exchange method greatly expands the structural and functional variety of DNA-wrapped carbon nanotubes, and opens possibilities for DNA-directed assembly of structurally-sorted nanotubes, and high throughput screening of properties that are controlled by the wrapping DNA sequences.


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INTRODUCTION Single-wall carbon nanotubes (SWCNTs) are a family of macromolecules with a simple chemical composition, but rich variation in structure and exceptional properties. To make use of their properties for applications, however, it is often necessary to individualize and process the nanotubes using a dispersant molecule that will coat the nanotube surface and form a hybrid assembly. DNA is a simple sequence-controlled polymer (SCP) that sets living cells apart from non-living molecular assemblies. Stable hybrid structures of DNA-wrapped SWCNTs (DNASWCNTs) were first synthesized fifteen years ago1 and have been studied extensively since.2-7 These hybrids provide a simple model system to study how SCPs can be utilized to control the physical and chemical interactions with other molecules, and how specific sequences that confer specific properties can be found in a vast sequence space via a limited number of trials. The extended nature of the non-covalent bonding between DNA and SWCNT and how it affects the physical and chemical properties of the hybrid are still waiting to be fully elucidated. From a practical point of view, DNA-SWCNTs have enabled development of a comprehensive solution to the structure-based sorting of SWCNTs.2,3 Promising applications of DNA-SWCNTs in biosensing and bioimaging are also being actively pursued.8,9 Future use of DNA coating to control the outcome of covalent chemical modifications of SWCNTs10 can also be envisioned. Several limitations in the preparation of DNA-SWCNTs hinder further development of these hybrids.

The current protocol for producing DNA-SWCNTs calls for sonication of

DNA/SWCNT mixtures, essentially following the original recipe reported fifteen years ago.1 While the strong physical and chemical effects of sonication do lead to SWCNT debundling and DNA wrapping, collateral damage in the form of SWCNT defect generation, cutting of SWCNTs, and DNA modification is also inevitable.11 Furthermore, disruption of secondary and


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tertiary structures of DNA by sonication may also limit the use of DNA for analyte binding in the case of sensing, and hybridization in the case of controlled assembly of SWCNTs. In addition, the sonication procedure is typically followed by a mandatory time-consuming highspeed centrifugation step to remove undispersed and bundled SWCNTs. The whole process of wrapping one DNA sequence around SWCNTs thus takes a few hours to finish, incompatible with high throughput screening of the vast DNA library for desired outcomes conferred only by specific sequences. A low energy and fast route for generating arbitrary DNA-SWCNT hybrids is thus highly desirable. An obvious method would be to disperse, purify and sort SWCNTs using techniques developed with small-molecule surfactants and to only replace the surfactant by DNA at the very end to exploit the unique properties of DNA-SWCNTs. This idea has been explored using sodium dodecyl sulfate (SDS) -dispersed and sorted SWCNTs.12 However, the reported technique has a few limitations including a low yield (70% or less) for SWCNT recovery, a high DNA to SWCNT mass ratio (10:1), and a long processing time (a few hours). For a number of reasons, we aim at developing a more efficient replacement method that works for much stronger surfactants, i.e. the bile salts sodium cholate (SC) and sodium deoxycholate (SDC). Wenseleers et al. first reported the exceptional dispersion capability of bile salts for SWCNTs.13 Indeed, stable SWCNT dispersions can be formed with SDC concentrations as low as 0.1 % (mass basis). Such a stable coating is essential for a number of separation processes. It has been shown that ultracentrifugation methods can remove defective tubes and separate empty and solventfilled tubes that are coated by SDC.14,15 Length sorting of bile salt dispersed SWCNTs can also be accomplished by either a size-exclusion chromatography15 or polymer precipitation based method.16 Employing weaker surfactant SDS to modulate bile salt binding further enables


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atomic- and electronic-structure based sorting of SWCNTs, as has been demonstrated by the pioneering work of Arnold et al. using the density gradient centrifugation method17, and later by us and others using aqueous two-phase (ATP)18-23 extraction and gel chromatography24 respectively. This broad compatibility of bile salt dispersed SWCNTs with different sorting methods thus makes them extremely attractive as starting material for down-stream applications. The generation of DNA-SWCNTs through the replacement of a stronger surfactant coating may appear to be a more challenging route, but to our surprise, we find in this work that the DNA/surfactant exchange reaction in methanol/water is rapid and gives higher SWCNT recovery (on average over 90 %), and enables production of arbitrary DNA-SWCNTs from bile salt surfactant dispersed and processed SWCNTs. In this contribution, we focus on the description of the exchange procedure and its controlling factors, the demonstration of DNA-based separation of highly pre-processed SWCNT populations after exchange, and the generation of previously non-producible DNA-SWCNT populations.

MATERIALS AND METHODS Materials Cobalt-molybdenum-catalyst (CoMoCAT, SG65i grade, lot no. SG65i-L46, and EG150X grade, lot no. L4), plasma torch, and arc-discharge P2-SWCNT powders were acquired from Southwest Nanotechnologies, Raymor Industries, and Carbon Solutions, Inc. respectively. Sodium deoxycholate (SDC) (BioXtra, > 98%, Sigma-Aldrich), sodium dodecyl sulfate (SDS) (Sigma-Aldrich), iodixanol (sold as OptiPrep Density Gradient Media, Sigma-Aldrich), poly(ethylene glycol) (PEG) (6 kDa, Alfa Aesar), dextran 70 (DX) (≈70 kDa, TCI), polyacrylamide (PAM) (10 kDa, Sigma-Aldrich), poly(sodium 4-styrenesulfonate) (PSS) (70 kDa, Sigma-Aldrich), poly(vinylpyrrolidone) (PVP) (10 kDa, Sigma-Aldrich), baker’s yeast


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RNA ( Sigma-Aldrich), methanol (MeOH) (Fisher Scientific), ethanol (EtOH) (Fisher Scientific), and isopropyl alcohol (IPA) (Fisher Scientific) were acquired from the manufacturer without modification.

Specific ssDNA sequences were purchased from Integrated DNA

Technologies. Nanotube Sample Preparation Raw SWCNT powder was dispersed in aqueous solutions of 10 g/L SDC using 1 h of tip sonication at a nominal power of 1 W/mL. The suspension was then centrifuged for 1 h at 1885 rad/s (Beckman J-2 centrifuge, JA-20 rotor) to remove large aggregates and impurities. The supernatant was collected for further processing. Details of additional variations to the production of specific nanotube populations, such as the endohedral filling with alkanes25, rate-zonal ultracentrifugation separation, and surfactant gradient ATP separation are given in the SI.

These populations were dialyzed using pressurized stirred

ultrafiltration cells (Millipore) prior to the exchange procedure to remove polymers and/or iodixanol to less than 1 µg/mL concentrations, while setting the surfactant concentration to 10 g/L SDC. The yield of this step is nearly 100%. SWCNT Characterization UV-vis-NIR absorption measurements were obtained with a Varian Cary 5000 spectrophotometer over a wavelength range of (200 to 1400) nm or (200 to 2400) nm. All spectra were acquired using a 10 mm or 1 mm path length quartz cuvette. Baseline corrections were applied by subtracting a separately measured spectrum of a blank solution. Prior to measurements, DNA-SWCNT samples purified by the ATP method were concentrated and removed from the polymer system by the PEG precipitation method.26 Circular dichroism (CD) spectra were acquired using an OLIS DSM 1000 CD spectrophotometer, covering a spectral range of 300 to 900 nm. All CD spectra were measured using a circular quartz cell with an optical path length of 2 mm.


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NIR ﬂuorescence was measured using a Horiba-Yvon Nanolog-3 spectroﬂuorometer equipped with a liquid-nitrogen-cooled 512-element InGaAs array detector. Excitation was specified by a 450 W xenon lamp and dual 1200 × 500 gratings. Nanotube fluorescence was collected at 90° and dispersed onto the detector array using a 100 × 800 grating. Instrumental resolution was set at 6 nm for excitation and 8 nm for emission. The integration time was 40s per spectra. All emission spectra were corrected for detector efficiency and lamp excitation. Exchange procedure The exchange procedure for producing the samples used in this contribution is described below. The total volume of the exchange process can be scaled up or down as long as the relative DNA, nanotube, PAM, and alcohol concentrations remain consistent. The exchange procedure (for 150 µL of SWCNTs at ≈ 1 mg/mL concentration dispersed in 10 g/L SDC) is as follows: 1. Addition of 25 µL of 25 % (m/v) PAM and mixing. 2. Addition of 30 µL of 10 mg/mL DNA and mixing. At this point, the mixture has ~ 3 % PAM, and a DNA to SWCNT mass ratio = 2. 3. Addition of 90 µL of methanol and mixing, this step is repeated a total of three times so that final volume of methanol added is 270 µL. At this point the DNA has replaced the SDC on the SWCNT surface. 4. To remove the SDC, 600 µL of IPA is added to the mixture. 5. Briefly centrifuge (≈1 s at 17000g) to form a loose pellet of DNA-SWCNT, PAM, and DNA (pellet 1). 6. Remove and further centrifuge the supernatant from step 5 at 17000g for 2 min to precipitate out any remaining PAM and DNA (pellet 2).


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7. Redisperse pellet 2 with 150 µL of H2O and use this solution to redisperse pellet 1. Light bath sonication (30 s to 60 s) is typically applied to aid in the redispersion process. We estimate that the exchange procedure eliminates > 90% SDC. Repeat steps 4 to 7 at least once; this reduces the SDC content sufficiently to enable DNA-based SWCNT separation to occur in an ATP system. 8. Lastly, add a small volume of a stock 5 mol/L NaCl solution to the DNA-SWCNT dispersion to reach a final NaCl concentration of 0.1 mol/L. Here, NaCl is added to the same concentration typically used for DNA-SWCNT dispersions produced from direct sonication.

ATP separation procedure The separation of DNA-SWCNTs in an ATP system follows previously established procedure.3,27 In brief, SWCNT separation was carried out using an ATP system comprised of 7.75% PEG and 15.0% PAM. The volume of each separation varied between 0.5 and 1.5 mL. Final nanotube concentration in the ATP system was 0.3 times the stock solution. Depending on the partitioning behavior of the DNA-SWCNT dispersions, either the top phase (1-T) or bottom phase (1-B) was removed for further purification. For multi-stage separations, modulating agents such as PVP or DX were added to systematically partition the SWCNTs into the top or bottom phase, respectively. All separations were performed at ~20 oC. More details pertaining to each separation can be found in the SI.

RESULTS AND DISCUSSION Surfactant exchange process Even though SDC is a strong surfactant for SWCNT dispersion in water, its dispersant activity is expected to drop in less polar solvents as individual SDC molecules become better solubilized.


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Indeed, by titrating methanol into SDC-SWCNT, one can easily observe SWCNT aggregation when the methanol content reaches above 50 %. In contrast, DNA-SWCNTs remain stable in the presence of 50 % methanol. In general, the stability of DNA-SWCNTs in methanol/water mixture is sequence-dependent, and some dispersions can withstand as high as 90 % methanol (Figure S1 in SI). We also observe that many DNA sequences are capable of dispersing SWCNTs in 50 % methanol under mild bath sonication, suggesting that the methanol/water mixture is a better solvent for DNA-SWCNT hybrids than water alone. Ethanol and IPA on the other hand are found to be bad solvents for DNA-SWCNTs. While the physical basis of solvent quality of different alcohols for DNA-SWCNTs may be rationalized by future studies, the phenomenon itself can nonetheless be exploited, as shown in this work. Scheme 1 illustrates the exchange procedure described in the Materials and Methods section. To enable the exchange process, methanol is added gradually up to ~ 60% to the SDC-SWCNT dispersion in the presence of DNA (DNA to SWCNT mass ratio = 2) and ~3 %

PAM.

Experimentally, we observe that the addition of a suitable water-soluble polymer to the exchange mixture increases the overall recovery of both nanotube and DNA (see discussion below). We propose that the added polymer can act like a matrix to hinder SWCNT movement while ensuring DNA and surfactant diffusion. Once DNA-SWCNTs are formed in methanol/water mixed solvent, they can be easily precipitated by adding a salt, or IPA, or both. Addition of IPA also collapses the polymer matrix, leading to the precipitation of both DNA-SWCNTs and the unbound DNA, leaving majority of SDC well solubilized in the mixed solvent. The incorporation of polymer and IPA precipitation makes the overall exchange process quick and robust. The whole process takes a few minutes to finish (as compared to a few hours for the earlier method of Giraldo et al.12), and yields SWCNT recovery of > 90% by mass.


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Scheme 1 DNA/SDC exchange process

Figure 1 provides detailed optical characterization of a CoMoCAT SG65i SWCNT population before and after a SDC to (GT)20 exchange. The wavelength of the SWCNT intrinsic optical features are affected by the local dielectric environment surrounding the SWCNTs as set by different dispersants, providing a direct route for evaluation of the interfacial layer by absorbance and fluorescence spectroscopy. Figure 1A shows that after the exchange process the intrinsic optical absorption features of the SWCNTs in the population redshift and broaden to positions identical to those achieved from direct DNA dispersion. This indicates that the SDC has been successfully displaced

by DNA. Additional confirmation comes from fluorescence

measurements (Figure 1B,C) which show an expected redshift and intensity decrease after DNA exchange. The most stringent test, however, is the successful separation of the resulting DNASWCNTs using the ATP methodology. This result will be presented in detail later. To demonstrate the importance of the water-soluble polymer used in the exchange process, we measured SWCNT recovery (calculated by comparing the initial and final concentrations of individually dispersed SWCNTs based on the integrated absorption of the E11 region) for an SDC


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to (GT)20 exchange in the presence of different polymers. We find that certain polymers work better than others, with PAM and DX giving the best results with over 90 % SWCNT recovery after exchange. Contrastingly, exchanges that utilize polymers such as PSS and PEG give recoveries that are lower than the 76 % obtained in a control exchange with no polymer. The exact role of the aqueous polymer is still yet to be understood and future experiments will further explore this area. We note that for applications where polymer additives are undesirable, one can use salt plus IPA to precipitate and collect DNA-SWCNTs formed through exchange. Another important aspect of the exchange procedure is the minimization of material waste through IPA precipitation. Figure 1D shows that near complete precipitation of DNA occurs when higher polarity alcohols are used as the precipitating agent. This results in a constant DNA to SWCNT mass ratio throughout the exchange procedure and allows for the exchange procedure to be repeated multiple times without the need of additional DNA. As a practical matter, we observed that the exchange efficiency is also somewhat DNA sequence dependent. For example, shorter sequences were typically more difficult to exchange than longer ones, and C/T sequences often give better exchange efficiency than A/T sequences. However, these variations were typically small, and could be compensated for by simply increasing the DNA to SWCNT mass ratio to higher than 2:1.


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Figure 1 Characterization of the DNA exchange procedure. Absorption spectra (A) and photoluminescence 2D excitation-emission plots (B) of SWCNTs in 1% SDC and after exchange with (GT)20. (C) Magnified regions of (B) highlighting the (6,5) emssion peak. A clear spectral red shift and decrease in emission intensity indicates a successful coating exchange from SDC to (GT)20. Red vertical lines in mark spectral positions of the (6,5) emission peaks. (D) Absorbance spectra of (GT)20 (0.3 mg/ml) before and after precipitation with MeOH, EtOH, and IPA. All precipitation experiments were performed in the presence of ~3% (m/v) PAM. A greater amount of DNA precipitation and recovery is obtained when using lower polarity alcohols.

Finally, we have also investigated the role of surfactant composition and concentration in the exchange process. Among SWCNT dispersions stabilized by SDS, SC and SDC, we found that SDC dispersion yields the highest exchange efficiency. Furthermore, at DNA to SWCNT ratio of


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2, we found that SWCNTs dispersed in 1% SDC gives higher yield than that in 0.1 % SDC. These suggest, counter-intuitively, that stronger surfactant binding favors DNA exchange. We reason that during the exchange process a transition state forms where the SWCNT surface is partially exposed. If the kinetics of surfactant desorption off the SWCNT surface is much faster than DNA adsorption, the transition state may lead to irreversible nanotube bundling. We hypothesize that SDC may have a slower desorption rate than that of SDS and better matches the adsorption rate of DNA leading to a slower rate of bundling. Regardless of physical mechanisms behind our observations, for SWCNT dispersions made with surfactants other than SDC, we recommend adding SDC to the final concentration of 1 % to the dispersions for efficient DNA exchange process.

Chirality sorting after DNA/surfactant exchange DNA coating enables structure-based sorting of SWCNTs. We have shown previously that when specific DNA sequences are used to make SWCNT dispersions via the direct sonication process, specific (n,m) species can be extracted via the ATP method.3,27 This sorting method is based on hydration energy difference among analytes to be separated and is extreme sensitive to minute structure changes. Thus, ATP separation can be viewed as a stringent test of DNASWCNT structures assembled via the low energy exchange process. We demonstrate that the exchange process passes this test by utilizing previously identified DNA recognition sequences to separately replace SDC from a common SWCNT dispersion. Among 7 tested recognition sequences, all but one, CT(C)3TC selective for the (7,6) SWCNT, enabled purification of the corresponding (n,m) species. Figure 2 shows the optical spectra of three successful examples. These results suggest that for most DNA sequences the DNA-SWCNT structures produced by the low energy exchange process are similar to those made by the direct sonication process. It is


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conceivable that upon exchange, certain sequences such as CT(C)3TC may adopt configurations different from those obtained via high energy direction sonication process. This possibility is further discussed later.

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Figure 2 Absorbance spectra of (A) parent SWCNT mixture dispersed in 1 % SDC, (B) (8,3) SWCNTs selected from the top phase of a PEG/PAM system after CTT(C)2TTC exchange, (C) (8,4) SWCNTs selected from the top phase of a PEG/PAM system after (GT)20 exchange, and (D) (6,5) SWCNTs selected from the top phase of a PEG/PAM system after TTA(TAT)2ATT exchange.

Orthogonal sorting enabled by DNA/surfactant exchange


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The DNA/surfactant exchange makes it possible to integrate DNA-based and surfactant-based SWCNT sorting to achieve a higher efficiency and resolution than that of the individual separation schemes. Figure 3 provides an example to illustrate this point. A large concentration of (6,5)-enriched SWCNTs can be easily obtained from a SDC-dispersed SWCNT raw material via the standard SDC dispersion and surfactant gradient ATP extraction process.21 The absorbance spectrum of such a sample, shown in Figure 3A, reveals however, that despite minimum metallic SWCNT contamination, there is noticeable semiconducting impurities from (6,4), (9,1), and (8,3). Additionally, circular dichroism (CD) measurement shows that the fraction is enriched in + (6,5) enantiomers (defined as having positive CD signal at the E22 optical transition), but the degree of enantiomeric excess is far from that of the pure sample (≈ 84 mdeg at E22).3 Replacing SDC by the (6,5) recognition sequence TTA TAT TAT ATT 3 allows us to carry out further separation, which dramatically reduces the content of other semiconducting species (Figure 3C). Moreover, the separation yields both enantiomers at nearly 100% enantiomeric excess level (Figure 3D), identical to those obtained from directly dispersed TTATATTATATT-SWCNT hybrids.3 An advantage conferred by the exchange route is that only the mass of DNA required to wrap (6,5) is necessary. Gross separation of the initial SDC parent dispersion, which contained over 25 (n, m) structures, vastly reduces DNA needed to disperse non-(6,5) species.


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Figure 3 Combining separation procedures for high purity enantiomer separation. (A) Absorption and corresponding CD (B) spectra of (6,5)-enriched SWCNTs in 1% SDC obtained from a multistage surfactant-based separation in a PEG/DX system (see Materials and Methods for details). (C) Absorption and corresponding CD (D) spectra of TTA(TAT)2ATT-(6,5) enantiomer hybrids selected from a multistage separation in a PEG/PAM system after DNA exchange of sample in (A,B). The (+) (6,5) and (-) (6,5) enantiomer hybrids are referred to by the sign of their E22 CD peaks. Both enantiomer hybrids exhibit near identical features and intensities but opposite signs. For comparison, CD intensity is normalized by E22 absorption intensity. A second example of the utility of DNA/surfactant exchange is the separation and purification of endohedrally-filled SWCNTs. Controlled endohedral filling, i.e. filling the nanotube core with a substance such as an alkane, represents a very attractive way of modulating the physical


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properties of SWCNTs. Previous studies have demonstrated filling of dye molecules to introduce additional excitation channels via energy transfer28, or to confer non-linear optical effects29, and the filling of simple alkanes to improve the optical properties of SWCNTs.25 Initial clean-up and sorting of such filled SWCNT materials is most conveniently done through the surfactant-based approaches to remove excess filling molecules and other non-SWCNT content in the synthetic mixture. We demonstrate here, for the first time, that DNA exchange allows for the extraction of single chirality species with controlled endohedral environment. Figure 4 compares the optical properties of C24H50@(8,4) and H2O@(8,4) SWCNTs selected from a PEG/PAM system after replacing SDC with (GT)20. (It should be noted that direct dispersion of the alkane filled SWCNTs by DNA followed by ATP sorting was attempted but not successful). As expected, we find the optical properties of the alkane-filled SWCNTs to be superior to those of the waterfilled. Absorption spectra (Figure 4A) indicate that the alkane-filled (8,4) nanotubes possess a 1.3 times larger peak-to-baseline ratio for the E11 absorption peak due to linewidth narrowing, while fluorescence measurements for the alkane-filled sample (Figure 4B) show that emission from the E11 optical transition has a 5 nm narrower line width and is 2 times stronger in intensity when compared to that of the water-filled (8,4) SWCNTs. We anticipate that single chirality, alkane-filled material will be beneficial for future applications such as bioimaging and sensing.


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Figure 4 Optical characterization of ATP-selected C24H50@(8,4) and H2O@(8,4) SWCNTs after (GT)20 exchange. (A) Comparison of absorption spectra for C24H50@(8,4) and H2O@(8,4) SWCNT fractions. Spectra are normalized at 800 nm for ease of comparison. Peak-to-baseline ratios are found to be ≈1.3 times larger for C24H50@(8,4) SWCNTs than for H2O@(8,4) SWCNTs. (B) Comparison of fluorescence spectra for C24H50@(8,4) and H2O@(8,4) SWCNT fractions. We observe the E11 fluorescence emission peak of the C24H50@(8,4) SWCNTs to be ≈2 times brighter and 5 nm more narrow (see inset of peak-normalized emission) than that of the H2O@(8,4) SWCNTs. Emission intensity is scaled by integrated E11 absorption for proper comparison. Excitation wavelength is 598 nm. Dispersion and separation of larger diameter SWCNTs Another substantial advance enabled by the SDC to DNA exchange procedure is the production of dispersed nanotube populations that were previously non-producible due to processing barriers. A first example is production of undamaged large diameter DNA-SWCNTs. Dispersion of SWCNTs by DNA via direct sonication is most effective for small diameter (d ≤ 1 nm) tubes. For larger diameter tubes, direct dispersion by DNA gives much lower yield in comparison with bile salt surfactants. Compounding the problem is sonication induced irreversible oxidation, which becomes more and more pronounced for larger diameter tubes unless antioxidants are added to the sonication mixture (Figure S3). In contrast, efficient


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dispersion as well as structure-based sorting of larger diameter SWCNTs (up to 2 nm) and DWCNTs by bile salts can be routinely performed.18,30 The new DNA/surfactant exchange process allows us to wrap large diameter SWCNTs by DNA with high efficiency and minimal oxidation, and to further separate them into fractions of narrower polydispersity. Figure 5A shows fractionation of empty plasma torch (Raymor) nanotubes (diameter 1.0 to 1.3 nm) that are coated by the sequence CTT(C)8TTC after replacing the initial SDC coating. Clear metallic (top blue trace) and semiconducting tube (bottom black trace) enrichment are observed. Near singlechirality structures in this diameter range can also be isolated after DNA exchange, such as (9, 9) species, shown in Figure 5B. More examples are presented in Figures S4 and S5. SWCNTs made by the arc-discharge method ( d = 1.3 to 1.6 nm) are a favorable choice for construction of field-effect transistors. In Figure 5C, we show that DNA coating can be introduced to semiconductor enriched, C30H62-filled arc-discharge P2-SWCNTs presorted by ATP using the SC/SDS redox sorting method, and further fractionated to narrow down the diameter distribution. It should be noted that while the sequence T4C3T4 used in the sorting experiment does not yield dramatic diameter or chirality sorting, a DNA-SWCNT population with such pristine optical transitions was not previously producible by any methodology. This advancement provides ideal parent nanotube dispersion for combinatorial screening of DNA sequences for diameter and chirality separation of large diameter tubes.


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Absorbance (arb. units)


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Figure 5 Absorption spectra of ATP-separated larger diameter SWCNTs after DNA exchange. (A) Electronic bandgap-dependent fractionation of empty Raymor SWCNTs in a PEG/PAM system after CTT(C)8TTC exchange. (B) Empty (9,9) SWCNTs selected from the top phase of a PEG/PAM system after C5TC6 exchange. (C) Selected diameter-dependent fractions of semiconducting-enriched C30H62@P2 SWCNTs in a PEG/PAM system after T4C3T4 exchange. Noise spikes centered at 1950 nm results from water absorption. Room temperature DNA assembly in quasi-one dimensional space Although the power of the exchange technique to enable improved production of DNASWCNT hybrids is clear, not all of the parameters affecting the exchange process are elucidated. The exchange process described above proceeds at room temperature, which is advantageous in terms of maintaining secondary structures of DNA. On the other hand, such mild processing may


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lead to the trapping of metastable wrapping structures, as suggested by a few observations. First, we have observed that after DNA/surfactant exchange, some recognition sequences give higher separation yield than others. In the experiment described in Figure 3, the (6,5) recognition sequence TTA TAT TAT ATT can only extract ≈ 22% of the + (6,5) species present in the starting SDC-dispersed (6,5) enriched sample, suggesting that not all recognition DNA sequences are forming the ordered structure on the target SWCNTs necessary for ATP separation.

At the molecular level, exchange involves randomly stripping off a few SDC

molecules initially associated with a SWCNT to accommodate an incoming DNA strand. After all the bound SDC molecules have been removed, the DNA molecules adsorbed on the SWCNT may not be in the energy minimized conformation. Such a “glassy” state may require a large activation energy to relax to the ground state conformation due to limited relaxation pathways imposed by the quasi-1D nature of the SWCNT surface. The direct sonication dispersion process may also encounter this situation, but the high energy perturbations introduced during sonication could speed up such relaxation dramatically. To solve the slow relaxation problem in the exchange process, future work will focus on exploring temperature annealing treatments to drive the assembled DNA structures to the ground crystalline state. A second, more attractive, approach is to directly screen the DNA library for a new set of recognition sequences that fold quickly and correctly at room temperature. Lastly, it may be that a residual amount of surface adsorbed methanol on DNA-SWCNTs may also alter their hydration energy and ATP separation. More work is clearly needed to fully optimize the exchange process.

CONCLUSION


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We have developed a simple, robust and efficient process to form DNA-SWCNTs through replacement of SDC surfactant coatings. The room temperature, homogeneous solution phase process provides a new way of studying DNA/SWCNT interactions. By applying time-resolved spectroscopy measurements to the new reaction route, one may extract kinetic and thermodynamic parameters defining sequence- and chirality- dependent DNA/SWCNT interactions, in a manner similar to what has been shown by the study of DNA replacement by surfactants.31 The exchange method greatly expands the structural and functional variety of DNA-SWCNTs, and opens possibilities for DNA-directed assembly of structurally-sorted nanotubes.32 Elimination of the sonication process also makes it possible to apply welldeveloped aptamer technology33,34 to identify sequences that bind to specific SWCNT populations. More broadly, since the new synthesis method can be carried out in a high throughput manner, screening of many properties that are controlled by the coating of DNA sequences is now possible.

SUPPORTING INFORMATION AVAILABLE: The Supporting Information is available free of charge on the ACS Publications website. Included are Details pertaining to the alkane-filling procedure, ATP separation procedure, effect of sonication on large diameter dispersions, and DNA exchange and separation of larger diameter SWCNTs. Also included are Figures S1-5.


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A Low Energy Route to DNA-Wrapped Carbon ... - ACS Publications

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