Dissociation Transition of

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Effect of Nonionic Surfactant on Association/Dissociation Transition of DNA-Functionalized Colloids Minseok Song, Yajun Ding, Mark A. Snyder,* and Jeetain Mittal* Department of Chemical and Biomolecular Engineering, Lehigh University, Bethlehem, Pennsylvania 18015, United States S Supporting Information *

ABSTRACT: We report the effect of nonionic surfactants (Pluronics F127 and F88) on the melting transition of micron-sized colloids confined in two dimensions, mediated by complementary single-stranded DNA as a function of the surfactant concentration. Micron-sized silica particles were functionalized with single-stranded DNA using cyanuric chloride chemistry. The existence of covalently linked DNA on particles was confirmed by fluorescence spectroscopy. The nonionic surfactant not only plays a significant role in stabilization of particles, with minimization of nonspecific binding, but also impacts the melting temperature, which increases as a function of the nonionic surfactant concentration. These results suggest that the melting transition for DNA-mediated assembly is sensitive to commonly used additives in laboratory buffers, and that these common solution components may be exploited as a facile and independent handle for tuning the melting temperature and, thus, the assembly and possibly crystallization within these systems.

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INTRODUCTION Development of structural DNA nanotechnology over the last three decades has been spurred by significant scientific interest due to its potential impact on applications spanning molecular recognition to self-assembly of hierarchical material architectures.1,2 The highly specific and reversible nature of DNA hybridization provides a novel means for programming complexity of self-assembling materials across nanometer to micrometer scales. One promising route to structured materials has exploited the fine-tunability of interactions among particles functionalized with complementary single-stranded DNA, a strategy established in initial reports by Alivisatos et al.3 and Mirkin et al.4 A wide variety of experiments5−13 and simulations14−18 have since aimed to more fully elucidate DNA-mediated colloidal assembly. The first successful experiments for the formation of three-dimensional colloidal crystal structures composed of nanoparticles were performed by both Nykypanchuck et al.11 and Park et al.,12 while microparticle assembly was reported by Crocker et al.5,7 Recently, Macfarlane et al.9 developed a set of basic design rules governing structural diversity in colloidal crystals achievable with DNA-mediated assembly, and demonstrated these rules with DNA-functionalized gold nanoparticles. Continuing efforts to more fully elucidate DNA-mediated programmable assembly across scales, structures, and compositions are driven by potential applications in areas spanning sensing,19−21 photonics,22 and catalysis,23 among others. The fundamental design handle exploited in these systems is the ability to engineer and leverage DNA-mediated interactionsmore specifically, controlled hybridization and dehybridization (i.e., melting) between complementary DNA © 2016 American Chemical Society

strands tethered to separate particlesin order to tune the order and organization within particle assemblies.24,25 It is wellknown that temperature, among other factors, controls DNAmediated interactions.26,27 This makes a priori determination of the melting temperature and detailed insight into the nature (e.g., shape, extent, and concomitant particle dynamics) of the melting transition for particle-tethered DNA critical for tuning DNA-mediated particle assembly and, ultimately, colloidal crystallization. Specifically, Nykypanchuck et al.11 and Park et al.12 demonstrated the interplay between entropic and enthalpic contributions in deriving close-packed versus non-close-packed, thermodynamically stable particle structures upon cycling the system temperature through the DNA melting transition or several degrees below it.18,27 The shape of the melting transition sharpens upon tethering DNA to particles28,29 and as a function of increasing particle size, owing to the concomitant increase in the number of interparticle DNA hybridizations.30 Intrinsically sharp melting transitions require long incubation times, specialized DNA coupling chemistries enabling particle rotational freedom,7,31,32 or surface-mobile DNA linkers33 to widen the association/dissociation transition window to achieve crystallization. Additional factors such as DNA sequence,34 length,18,35 and surface density on particles27,36 as well as modulation of salt concentration in solution can also impact DNA-mediated interactions and associated melting behavior.36,37 Jin et al.35 investigated melting of DNA-coated gold nanoparticles using Received: June 3, 2016 Revised: August 19, 2016 Published: September 5, 2016 10017

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Figure 1. Schemes of (a) attachment of amino-modified oligonucleotides (H2N-DNA) to silica particles via intermediate silanization and cyanuric chloride chemistry, leading to (b) hybridization between complementary αDNA and βDNA sequences tethered to separate silica particles surfaces, and thus DNA-mediated particle binding.

binding due to van der Waals interactions. The association/ dissociation profiles in the presence of various copolymers that were used as stabilizers showed that the melting temperature increased with decreasing stabilizer molecular weight, owing to a concomitant reduction in the steric hindrance effect. This sensitivity of the melting transition to additives in the form of copolymeric stabilizers is particularly interesting given the common use of additives like surfactants to stabilize colloidal particles against nonspecific aggregation in solution. Obvious questions thus emerge as to whether these required surfactants similarly impact the observed melting properties of DNAcoated particles, and if so, how changes in melting properties are sensitive to surfactant concentration. In this paper, we present the thermal behavior of micronsized DNA-functionalized silica particles with varying concentrations of Pluronic F127 (PEO100-PPO65-PEO100) or Pluronic F88 (PEO103.5-PPO39.2-PEO103.5).41,42 Such surfactants are frequently used to promote colloidal stability, avoid nonspecific aggregation, and, in the case of two-dimensional assembly of settled particles subject to Brownian motion, protect against surface adhesion. Single-stranded DNA molecules are covalently attached to the particle surface in a two-step functionalization reaction. We observe temperature induced association and dissociation of DNA-functionalized silica particles, which depends sensitively on the concentration of the nonionic surfactants. Our results suggest that commonly used additives in laboratory buffers such as Pluronic F127 and F88 can ultimately be used to modulate the melting transition of DNA-functionalized particles, in addition to other factors reported in the literature.

UV−vis spectroscopy. They reported how factors such as particle size, DNA surface density, salt concentration, and nonhybridizing linker length, manifested as interparticle distance, control the melting transition and its width. Dreyfus et al.27,28 established how an increase in DNA surface density leads to an increase in melting temperature and slight narrowing of the melting transition even for micron-sized particles. They determined this by optical microscopy of the melting transition for these quasi-two-dimensional systems (i.e., particles settled due to density difference with the solvent) defined on the basis of the fraction of nonaggregated (i.e., melted) particles or the “singlet fraction”. In addition to DNA-specific controls, multimodality of DNAfunctionalized particles has also been explored to tune the melting temperature and nature of the melting transition, and to ultimately exploit it for expanding structural complexity of DNA-mediated assemblies. Michele et al.38 reported that two well-defined melting temperatures can be used to sequentially trigger selective interactions in a two-component system. This allows for two-step gelation and core−shell gelation for mesoporous materials. Macfarlane et al.39 used a third nanoparticle component to achieve temperature-dependent topotactic interconversion between a binary and a ternary superlattice. They were able to generate five distinct ternary nanoparticle superlattices by insertion of smaller particles into a pre-established binary crystal structure, by activating DNAmediated attraction sequentially as a function of temperature. Without employing multimodal assembly, addition of solution phase moieties can also be employed for modulating the melting transition. Beyond tuning salt concentration, Valignat et al.40 reported that reversible self-assembly of DNA-coated particles can be achieved by introduction of a polymer that can adsorb on the surface of particles, presumably promoting interparticle steric repulsion. They showed that careful balancing of attractive interactions, owing to interparticle DNA hybridization, and steric and/or electrostatic repulsive interaction is needed for assembly of micron-sized particles, unlike nanoparticles, in order to overcome irreversible

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MATERIALS AND METHODS

Intermediate Silica Particle Functionalization. Silica particles (1 μm, micromod Partikeltechnologie GmbH, Germany) were functionalized with single-stranded 5′-primary amine-modified DNA, ssDNA (Integrated DNA Technologies, Inc.), via intermediate cyanuric chloride tethers as schematized in Figure 1a.43 The cyanuric chloride tethers were achieved by first functionalizing the native silica particles with (3-aminopropyl) triethoxysilane (APTES, Acros 10018

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Langmuir Organics),43,44 the amine groups of which were subsequently reacted with cyanuric chloride (CCl, Sigma-Aldrich). Specifically, 0.9 mL of a 50 mg/mL silica particle solution was washed three times by sequential centrifugation (4000 rpm/1 min; MTX-150, TOMY SEIKO Co., Ltd.) and replacement of the supernatant with fresh ethanol (190 proof). The resulting ∼3 wt % ethanol−silica solution was sonicated for 20 min to redisperse particles. APTES was added to the resulting solution to achieve an APTES:(surface silanol) molar ratio of 1.2:1, with silica surface silanol functionality estimated assuming monodisperse spherical particles of 1 μm diameter, silica density of 2 g/cm3, and surface silanol density of ∼6 SiOH/nm2.45 The mixture was allowed to react in a sealed centrifuge tube for ∼12 h at room temperature under moderate rotation. The resulting NH2-functionalized silica particles were washed six times by centrifugation and redispersion in ethanol. The composition of unreacted APTES in the supernatant from each washing step was assessed via reaction of its amine functionality with ninhydrin44,46 reagent, resulting in Ruhemann’s purple, concomitant visible purple coloration of the solution, and development of signature UV−vis bands at 407 and 570 nm as measured on a UV−vis spectrophotometer (Ultrospec 3300 pro, Biochrom Ltd.). The ninhydrin reaction was carried out through addition of 250 μL of 20 mM ninhydrin in ethanol to 1 mL of the test solution, in this case the supernatant, with subsequent heating at 65 °C for 30 min. Washing cycles, involving centrifugation and redispersion, were continued on the functionalized particles until the ninhydrin-treated supernatant became colorless and the UV−vis signature nearly disappeared. Three washings beyond the number where colorless supernatants were achieved (typically 3) were consistently performed to ensure removal of all unreacted APTES. Subsequent ninhydrin indicator reactions were carried out as described above on the 1 wt % NH2-functionalized silica particles in ethanol to investigate the existence of amine groups on the silica particles. Amine functionality was estimated at a density of ∼3.6 NH2/nm2. The NH2-functionalized silica particles were transferred from ethanol to acetonitrile (Alfa Aesar, 99.7%) by three centrifugation and solvent exchange steps, yielding a final solids content of ∼5 wt %. To this solution N,N-diisopropylethylamine (DIEA, Sigma-Aldrich) was added, followed by 30 min sonication to redisperse the particles, and final addition of cyanuric chloride (CCl, Sigma-Aldrich) to achieve a DIEA:CCl:(surface silanol) molar ratio of ∼17.5:69:1, where surface silanol density was estimated as described previously. After reacting at room temperature for 2 h, the mixture was washed 6 times by sequential centrifugation and solvent exchange with fresh acetonitrile, and sonication steps. Aliquots of the resulting mixture were solvent exchanged with ethanol and used for carrying out ninhydrin indicator reactions as described above to assess the success of nucleophilic substitution of the CCl chlorine by amines on the surface of silica particles. Figure 2a compares the UV−vis absorption spectra for ninhydrin-treated NH2-functionalized and CCl-functionalized silica particles, with existence and absence, respectively, of absorption bands near 407 and 570 nm indicating the NH2 functionalization of the base silica particles and nearly complete reaction of CCl with that functionality. ssDNA Functionalization of Silica Particles. Covalent attachment of DNA oligomers to the surface of CCl-functionalized silica particles was carried out following the procedure outlined by Steinberg and co-workers43 using complementary DNA oligomers proposed previously by Crocker and co-workers26 (Integrated DNA Technologies) (Figure 1b): 5′-NH2-(CH2)6-(T)50-TAATGCCTGTCTACC-3′ (αDNA) and 5′-NH2-(CH2)6-(T)50-TGAGTTGCGGTAGAC-3′ (βDNA). CCl-functionalized silica particles in acetonitrile were first cleaned with, and redispersed at, a concentration of ca. 3.2 wt % in a borate buffer (pH 8.5) consisting of 200 mM boric acid and 50 mM sodium tetraborate. 100 μL of this CCl-functionalized silica solution was added to an oligo-NaCl solution prepared by mixing 324 μL of borate buffer including 848 mM NaCl and 6 μL of 300 μM DNA in an aqueous solution. The mixture was allowed to react in a sealed Eppendorf tube for ca. 12 h at room temperature under gentle rotation. The DNA-functionalized silica particles were then washed more than 6 times by centrifugation and redispersion in TE buffer (pH

Figure 2. (a) UV−vis absorption spectra of ninhydrin-treated supernatants of NH2- and cyanuric chloride (CCl)-functionalized silica particles, as specified, with characteristic absorption bands at 407 and 570 nm labeled. (b) Fluorescence spectra of solutions of CClfunctionalized silica particles before (“CCl”) and after (“F-DNA”) reaction with fluorescently labeled (Cy5-modifed) DNA. 8.0) consisting of 10 mM tris-HCl (pH 8.0), 1 mM ethylenediaminetetraacetic acid (EDTA), and 100 mM NaCl. The existence of unreacted DNA was assessed by UV−vis measurements for each supernatant. Typically, more than 4 washes were required to remove most of the nontethered DNA. In order to quantify the density of DNA oligomers on the silica particle surface, DNA oligomer functionalization of NH2-functionalized particles, analogous to that described above, was carried out using fluorescently labeled DNA (5′-NH2-(CH2)6-TTTTTTATGTATCAAGGT-Cy5−3′, F-DNA, Integrated DNA Technologies).34 Fluorescence measurements (λex = 648 nm, λem = 668 nm) on a TECAN infinite M2000 PRO (Figure 2b) comparing fluorescence spectra collected for solutions of the CCl-functionalized silica particles and silica particles subsequently functionalized with Cy5-modified DNA reveal distinctly marked absorption over signature Cy5 wavelengths (680 nm-740 nm) only in the case of functionalization with the Cy5-modifed DNA. Based on calibrated absorption at 696 nm correlated with F-DNA concentration (without silica particles), a DNA surface density of approximately 120 000 DNA/particle was estimated. Since the F-DNA bears a different sequence and lower number of base pairs (18 bps) compared to the nominal DNA employed in this study (65 bps), we anticipate that this estimated density may serve as an upper bound for the actual density of the 65-bp DNA on the silica surface. Microscopy Setup for Temperature Studies. A POCmini-2 Tissue Culture Chamber System (PeCon GmbH), hereafter referred to as a “heating chamber”, was utilized for systematic heating and cooling of solutions of DNA-functionalized particles. Particle solutions were held by a silicone O-ring (ID = 20 mm, OD = 30 mm) 10019

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Langmuir sandwiched between two round borosilicate coverslips (diameter = 30 mm, thickness = 0.17 mm, Hemogenix) mounted within the heating chamber. In cases where plasma-based passivation of the glass coverslip surfaces was carried out, ethanol-washed and nitrogendried coverslips were treated for 90 s in a March Plasma Systems Model PX-250 at 350 mTorr of oxygen and 100 W forward power. The local temperature within the heating chamber was measured with a thermocouple (K-type, thickness = 0.25 mm, OMEGA Engineering, INC.) inserted at the chamber center. The chamber itself was placed on a Nikon Eclipse TE2000U inverted optical microscope equipped with 40× air immersion objective with 1.5× amplifier. A temperature controller (Tempcontrol 37−2 digital, PeCon GmbH) and a chambercompatible heating insert (Heating Insert P, PeCon GmbH) were used to scan and hold temperatures of the system during image collection. Full sedimentation of the DNA-functionalized silica particles occurred within ∼1 h, owing to the silica density (ca. 2 g/cm3), enabling twodimensional (2D) optical imaging on the inverted microscope at a focal depth of ca. 1 μm to sufficiently capture 2D particle dynamics, aggregation, and assembly within the system.28,47,48 Optical analysis was employed to quantify particle dynamics and association during sequential temperature ramping/equilibration (i.e., heating and cooling cycles), with a minimum of five optical images from different regions across the sample chamber collected at each equilibrated temperature step. Subsequent image analysis was carried out using ImageJ software, employing particle identification and area percentage calculations in order to quantify the spatially and temporally averaged fraction of individually dispersed particles, or so-called “singlet fraction”, relative to particles incorporated within aggregates. Cooling and Heating Elucidation of Melting Curve. Melting curves for mixtures of particles functionalized with complementary strands of DNA were quantified on the basis of the degree of particle dispersion and assembly/aggregation by the singlet fraction at a specific equilibrated temperature. For each melting study, a solution of equal amounts of prescribed types of DNA-functionalized particles (e.g., αDNA-βDNA as well as αDNA-αDNA and βDNA-βDNA controls) was prepared in salty (100 mM NaCl) TE buffer with a total particle volume fraction of 0.0005 wt %, amounting to a nominal surface density of sedimented particles within the heating chamber of approximately 0.01 particle/μm2. To this mixture, a controlled amount of Pluronic nonionic surfactant F127 (0.1, 1.0, 2.0 wt %) or F88 (0.1, 1.0, 2.0, 4.0 wt %) was added (Figure S1). Bath-sonication was carried out for 10 min followed by brief vortex mixing in order to ensure homogeneous particle dispersion. Melting behavior was assessed through cooling and subsequent heating experiments. Solutions were initially heated at 60 °C for 1 h in an oil bath. Simultaneously, the heating chamber was preheated to a temperature exceeding the characteristic αDNA-βDNA melting temperature, here at least 40 °C. After injecting 650 μL of the heated solution into the coverslip/O-ring reservoir in the preheated chamber, cooling studies were carried out by gradual, stepwise reduction of the set point temperature, and intermediate temperature equilibration via ambient cooling. Cooling cycles were terminated once temperatures (here, ca. 25 °C) well below the nominal DNA melting temperature were reached and the singlet fraction reduced to approximately 10% or less. Subsequent heating cycles were performed by stepwise increase in the equilibrated set point temperature of the system.

agents. Here, we have studied the assembly of DNAfunctionalized silica microparticles in the presence of controlled amounts of Pluronics. We have specifically employed inverted optical microscopy to image two-dimensional assembly of gravity-settled microparticles undergoing Brownian motion on a glass coverslip. Optical microscopy snapshots in Figure S2 and movies in the Supporting Information (SI) of native nonfunctionalized silica particles (SI SiO2 control movie) and ones functionalized with only αDNA (SI Figure S2a movie, Figure S2b movie) in salty (100 mM NaCl) TE buffer solution demonstrate the role of surfactant in aiding particle dispersion. Specifically, in the absence of surfactant, while plasma-based passivation of the glass coverslip surface circumvents adhesion of gravity-settled particles, and thus allows for Brownian particle motion and particle contact, irreversible particle aggregation (i.e., resistance to dispersion into singlets with subtle changes in temperature) is observed. The lack of DNA complementarity between particles functionalized with only αDNA underscores the nonspecific nature of the aggregation, deriving simply from saltinduced colloidal destabilization. The addition of nonionic surfactant, here F127, results in dispersion of individual DNAfunctionalized and native silica particles or “singlets” due to surfactant-induced particle stabilization against nonspecific particle aggregation. This uniform singlet dispersion of particles functionalized with noncomplementary DNA was found to hold for system temperatures spanning at least 25−40 °C as long as surfactant was present. Only upon addition of particles functionalized by complementary DNA (βDNA) were particle aggregates observed in the presence of surfactant. Figure 3a shows aggregation of silica particles of two distinct sizes functionalized, respectively, with complementary αDNA (1 μm particles) and βDNA (1.5 μm particles) at room temperature in salty TE buffer containing nonionic surfactant F127. Here, the two different particle sizes enable differentiation of complementary αDNA and βDNA functionality and, thereby, binding between complementary particles. Direct binding between like-sized particles with noncomplementary DNA is not observed. Instead, as shown in the inset in Figure 3a, these particles are only part of an aggregate when they are bound together with an intervening unlike particle carrying complementary DNA strands. Taken together with the lack of aggregate formation in the presence of surfactant F127 for native silica particles bearing no DNA functionality (see SI SiO2 control movie), these data clearly evidence that particle clustering in the presence of surfactant results from interparticle interactions mediated by hybridization between complementary DNA as opposed to nonspecific particle aggregation under conditions suitable for self-assembly. With confirmation of DNA-mediated particle binding enabled by the ability to visually differentiate complementary particles based on differences in size, we turn our attention for the remainder of this paper to monomodal particle systems to avoid additional complexity arising from size asymmetry. We have also verified the thermal reversibility of the DNAmediated assembly process. Namely, the temperature-dependent dissociations and associations among a mixture of 1 μm particles, half of which have been functionalized with αDNA and half functionalized with βDNA, were studied in salty TE buffer with surfactant F127. Figure 3b−d and Figure S3 show representative optical microscopy snapshots of the temperature-dependent dissociation and association of DNA-functionalized silica particles. Whereas at room temperature most of the

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RESULTS AND DISCUSSION DNA-mediated particle assembly is often carried out in buffer solutions wherein hybridization between complementary particle-tethered DNA strands, herein referred to as αDNA and βDNA, is tuned by controlling solution salt content. In order to counterbalance salt-induced particle destabilization, Pluronics (Figure S1) nonionic surfactants composed of one centrally positioned hydrophobic poly(propylene oxide) (PPO) and two end-positioned hydrophilic poly(ethylene oxide) (PEO) regions (e.g., F127 − PEO100-PPO65-PEO100, F88 − PEO100-PPO39.2-PEO100) are commonly used as stabilizing 10020

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Figure 3. Optical microscope snapshots of (a) bimodal room temperature assemblies of silica particles functionalized separately with complementary αDNA (1 μm particles) and βDNA (1.5 μm particles) in salty TE buffer and 0.1 wt % Pluronic F127. Insets show magnifications of representative clusters indicating DNA-mediated interactions between particles of different sizes functionalized with complementary DNA. (b−d) Optical snapshots of 50/50 mixtures of 1 μm (monomodal) αDNA- and βDNA-functionalized silica particles under the same solution conditions, but equilibrated at specified temperatures spanning the melting transition (i.e., corresponding to points i−iii along melting curve in Figure 4a), show the corresponding transition from aggregates to high singlet fraction.

particles are aggregated in fractal-like structures and the singlet fraction is quite low, aggregate dissociation is observed with increasing temperature to the point of high singlet fraction at the highest temperatures studied. Subsequent decrease in the sample temperature leads again to rapid (i.e., within minutes) particle association and recovery of fully aggregated structures, similar to the initial state, once room temperature is reached. Qualitative insight into the kinetics of the concomitant association (upon sequential cooling) and dissociation (upon sequential heating) was obtained through quantification of the temporal evolution of the singlet fraction at specific temperatures during the mapping of the melting curve. As shown in Figure S4, the singlet fraction appears to stabilize approximately 30 min after any step-change in temperature. As such, melting curves generated in this study have been prepared through 30 min equilibration at temperatures above and below the transition region, and 1 h equilibration in the transition region, to conservatively ensure establishment of equilibrium in this critical range. Ultimately, these data establish that the DNAfunctionalized silica microparticles studied herein undergo specific and reversible, temperature-dependent binding consistent with DNA hybridization and dehybridization between complementary particle-tethered DNA strands. To determine the effect of nonionic surfactant on DNAfunctionalized particle aggregation and its temperature dependence, we calculate the percentage of singlet particles as a function of temperature, quantified as “melting curves”, with increasing F127 concentration. Figure 4a−c shows melting curves obtained by sequential cooling and heating steps, which

Figure 4. Percentage of singlets as a function of cooling (closed symbols) and subsequent heating (open symbols) for a 50/50 mixture of αDNA- and βDNA-functionalized particles in salty TE buffer with specified wt % of Pluronic F127 ranging among (a) 0.1, (b) 1.0, and (c) 2.0 wt %. Vertical dashed lines indicate critical micelle temperatures (CMT) as specified for each F127 concentration from Alexandridis et al.41 Error bars represent standard deviations computed for singlet fractions quantified for a given equilibration temperature from at least five spatially and temporally separated optical snapshots. Optical microscope snapshots corresponding to the system with 0.1 wt % F127 (a) equilibrated (i) below (25.8 °C), (ii) within (28.9 °C), and (iii) above (31.5 °C) the melting transition are shown in Figure 3b−d.

are based on the image analysis of optical microscopy data collected after equilibration at each temperature. Representative snapshots for varying singlet percentages along the melting curve in Figure 4a(i−iii) are shown in Figure 3b−d, respectively. As expected, most particles are bound to each other at low temperatures (singlet percentage 80%). 10021

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Langmuir There is a relatively sharp transition, on the order of several degrees, between the singlet and aggregated extremes, which is consistent with previous estimates from experiment and theory.27 The temperature range over which the transition from an aggregated to unbound state happens is much narrower than the range of temperatures over which the hybridization between a pair of free DNA strands occurs in solution. This narrowing can be attributed to binding between a pair of particles, induced by hybridization between multiple pairs of DNA strands, and is often cited as a primary reason for the inability to design suitable annealing protocols to obtain highly ordered (crystalline) aggregates.49 One can also expect that the location of the transition region (i.e., specific temperature at the midpoint in the melting curve) will be an important factor in achieving such crystalline assemblies, owing to the influence of thermal motion on particle annealing believed to be important for establishing and extending particulate order and long-range periodicity. We find that as F127 concentration is increased from 0.1 wt % (Figure 4a) to 2 wt % (Figure 4c), the melting temperature changes from ca. 29 °C to ca. 33 °C. DNA-functionalized particles in salty TE buffer with 0.1 wt % F127 show similar melting profiles during cooling (solid melting curve) and subsequent heating (dotted melting curve), indicating a fully reversible transition between aggregated and isolated particles. Melting profiles in salty TE buffer with 1 wt % F127 and 2 wt % F127 are also relatively similar, especially below the melting temperature. For temperatures above the transition region, a lower percentage of singlet particles are observed during the subsequent heating steps, presumably a manifestation of much longer equilibration times needed for complete unbinding as reflected by the decreasing measured diffusivity with increasing surfactant concentration (Figure S5). These changes in the melting behavior induced by F127 may be related to the micelle formation in these triblock copolymers (Figure S1). Specifically, nonionic surfactants such as F127 dissolve in dilute aqueous solution (TE buffer in this case) as monomer units, but form micelles as the concentration or the temperature is raised above the critical micelle concentration (CMC) or critical micelle temperature (CMT), respectively. These micelles consist of a hydrophobic core of the PPO segment and a hydrophilic shell of the PEO segments.50,51 As a guide, we have used the phase behavior data that was previously reported by Alexandridis et al.41 for a variety of Pluronic PEOPPO-PEO copolymers in aqueous solutions. The CMTs are shown as vertical dashed lines in Figure 4 for 0.1, 1.0, and 2.0 wt % F127 concentrations. In the case of 0.1 wt % F127, the melting temperature is lower than the CMT, while the melting temperatures are higher than the corresponding CMTs for 1.0 and 2.0 wt % F127. This suggests that the formation of micelles at the temperatures of interest with increasing F127 concentration is likely responsible for the observed changes in the melting transition. To further test this inference, we replace Pluronic F127 with Pluronic F88, which has a much higher CMT at similar surfactant concentrations. For reference, the CMT of F88 in 0.1 wt % aqueous solution is about 50 °C as compared to 32 °C for F127. Figure 5 shows the effect of F88 concentration on the melting behavior of DNA-functionalized particles. The melting curves, namely, the melting transition temperatures, are quite similar for 0.1 and 1.0 wt % F88 (Figure 5a) in the salty TE buffer, with CMTs in both cases exceeding the transition temperatures. Further increasing the F88 concentration to 2.0

Figure 5. Percentage of singlets as a function of cooling (closed symbols) and subsequent heating (open symbols) temperatures for 50/50 mixtures of αDNA- and βDNA-functionalized particles in salty TE buffer with Pluronic F88 at concentrations of (a) 0.1 wt % (circles) and 1 wt % (triangles) and (b) 2 wt % (squares) and 4 wt % (diamonds). Error bars represent standard deviations computed for singlet fractions quantified for a given equilibration temperature from at least five spatially and temporally separated optical snapshots. The vertical dotted lines indicate critical micelle temperature (CMT) at specified F88 concentrations in aqueous solution from Alexandridis et al.41

or 4.0 wt % (Figure 5b) brings the CMTs near to or below the transition temperature, respectively, and leads to a concomitant increase in the melting temperature, which is consistent with the F127 results. These results clearly suggest a link between the melting properties of DNA-functionalized particles and the CMT of nonionic surfactant added to the buffer solution. The melting transition is found to be relatively insensitive to the amount of surfactant if the CMT of the surfactant is much higher than the temperatures at which DNA-tethered particles dissociate into isolated particles, with the noted and as of yet unexplained difference in reversibility at the lowest surfactant concentrations (0.1 wt %) between Pluronics F127 (fully reversible, Figure 4a) and F88 (reversible below to slightly above the melting temperature, Figure 5a). On the other hand, if the melting transition temperature and the surfactant CMT are similar, the aggregation behavior of DNA-functionalized particles is dependent on the concentration of the nonionic surfactant. This insight may be useful in the following two ways when exploiting DNA-mediated interactions to assemble particles into ordered crystalline structures: (i) the selection of nonionic surfactant can be made based on preliminary investigations so 10022

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Langmuir that its CMT is higher than the temperatures of interest, and/or (ii) one can select an appropriate nonionic surfactant to tune the melting transition temperature for practical convenience or to obtain desirable behavior. We also find that the width of the melting transition is slightly increased (Figures 4c and 5b). While this attribute can be of practical importance during the thermal annealing steps for structural rearrangement of particles into ordered assemblies, alternative strategies proposed by Rogers and Manoharan52 to tune this width arbitrarily offer more versatility in this regard. An obvious question that follows relates to how the presence of micelles serves to increase the melting transition temperature. One possibility is the existence of depletion attractions between DNA-functionalized particles in addition to the attractive interactions induced by DNA hybridization. Depletion attractions are known to exist between colloidal particles with the addition of components such as nanoparticles, micelles, or polymers, owing to the exclusion of nonadsorbed smaller particles/moieties from the region between larger particles.53 Previously, it was reported that micelles can be used to induce depletion attractions between spherical particles.54−58 There, Sober and co-workers,58 measuring the interaction free energy between colloidal polystyrene latex particles and a flat surface in the presence of charged cetyltrimethylammonium bromide (CTAB) micelles, did not observe any attractive interaction below the CMC of CTAB. An attractive minimum was, however, clearly seen with increasing surfactant concentration above the CMC. Moreover, Kumar et al. and Ray et al. recently reported that charged silica nanoparticles can be clustered due to depletion attraction in the presence of nonionic surfactant.54,56 To test for the existence of depletion attractions in the systems studied here, we performed control experiments using only αDNA-functionalized particles (i.e., to avoid particle clustering driven by αDNA-βDNA hybridization) at different F127 concentrations (0.1, 1.0, 2.0 wt %) and temperatures typical of the melting transitions (25−40 °C). In each case, upon equilibration, singlet percentages were quantified from optical microscopy images of the samples. Figure 6 shows that the average singlet fraction, namely, the average number of particles that are not physically clustered, across all conditions studied is effectively independent of the surfactant concentration. This absence of particle clustering for temperature and surfactant conditions below and above corresponding CMCs suggests that either depletion attractions are not present, or, if they are, they are too weak to cause particle aggregation in the absence of DNA hybridization. To rationalize the observed changes in particle aggregation as a function of surfactant concentration, we put forward the following hypothesis. The magnitude of repulsive interactions caused by electrostatics (between negatively charged DNA backbones) and steric hindrance among DNA strands confined between a pair of particles may be larger than the depletion attraction induced by micelles. In the case of mixtures of αDNA- and βDNA-functionalized particles, attraction between the particles may be primarily controlled by DNA hybridization, with the weaker attraction caused by depletion (unable by itself to cluster particles) possibly adding to the total attraction strength. Srivastava and co-workers59 recently demonstrated the concept of a supercompressible DNA nanoparticle lattice, which exhibits isotropic compression in the presence of different osmotic pressure, dependent on surfactant concentration. It is, thus, conceivable that a modest

Figure 6. Average of measured singlet percentages for αDNA-coated particles in TE buffer containing 100 mM NaCl and specified concentrations of Pluronic F127 (0.1, 1.0, 2.0 wt %) after holding the system at temperatures spanning the melting transitions (25−40 °C) for equilibration times of 30 and 60 min. Error bars reflect the standard deviation of the singlet percentage measured from optical microscopy images taken after 30 or 60 min equilibration across all temperature conditions measured for the specified surfactant concentrations.

decrease in interparticle distance due to secondary depletion effects could induce a higher number of interparticle DNA hybridizations, thereby increasing the melting temperature. The ability to harness the full potential of the apparent surfactantdriven tunability of DNA-mediated particle assembly in the future will require further elucidation of the role and magnitude of depletion forces through quantification of micelle size relative to the size of the assembling particles and analysis of sensitivities to ionic strength.

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CONCLUSIONS We have identified an influence of the concentration and physicochemical nature of Pluronic nonionic surfactants (Pluronic F127 and F88) on the association/dissociation transition of micron-sized silica colloids functionalized with complementary single-stranded DNA. From the cooling and the subsequent heating of mixtures of particles functionalized separately with complementary DNA strands, we have shown that the corresponding reversible melting transition between singlet and aggregated particles confined in two dimensions is affected by the concentration of the noninonic surfactant. This surfactant-induced tunability of the melting transition, in terms of both its temperature and, to a smaller extent, its width, appears to be facilitated, in part, by corresponding micelle formation. This may be due to a combined effect of primary interparticle attraction mediated by DNA hybridization and secondary depletion forces. Ultimately, the identification of this melting transition sensitivity to additives commonly employed to avoid nonspecific aggregation in DNA-mediated particle assembly suggests that careful consideration must be given to how additives in these systems are employed. Moreover, this finding reveals how such common additives may ultimately serve multiple purposes of stabilization against irreversible and nonspecific aggregation, modulation of surface-mediated 10023

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interactions for two-dimensional DNA-mediated assembly, and active tuning of the temperature window to conditions wherein highly crystalline particulate structures may be more easily achieved through DNA-mediated assembly.

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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.langmuir.6b02096. Pluronic F127 and F88 physicochemical data, supplementary optical images of Pluronic and DNA-mediated microparticle assembly, equilibration of singlet fractions, mean squared displacement measurements and estimated particle diffusivities (PDF) SiO2 control movie (MPG) Melting Curve movie (MPG) Figure S2a movie (MPG) Figure S2b movie (MPG)

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AUTHOR INFORMATION

Corresponding Authors

*E-mail: [email protected]. *E-mail: [email protected]. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work was supported by the U.S. Department of Energy, Office of Basic Energy Science, Division of Material Sciences and Engineering under Award (DE-SC0013979).

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REFERENCES

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