Article pubs.acs.org/Langmuir
Self-Assembly of Rodlike Virus to Superlattices Tao Li,† Xingjie Zan,‡ Yong Sun,§ Xiaobing Zuo,† Xiaodong Li,§ Andrew Senesi,† Randall E. Winans,† Qian Wang,*,‡ and Byeongdu Lee*,† †
X-ray Science Division, Advanced Photon Source, Argonne National Laboratory, 9700 South Cass Avenue, Argonne, Illinois 60439, United States ‡ Department of Chemistry and Biochemistry, University of South Carolina, 631 Sumter Street, Columbia, South Carolina 29208, United States § Department of Mechanical Engineering, University of South Carolina, 300 Main Street, Columbia, South Carolina 29208, United States S Supporting Information *
ABSTRACT: Rodlike tobacco mosaic virus (TMV) has been found to assemble into superlattices in aqueous solution using the polymer methylcellulose to induce depletion and free volume entropy-based attractive forces. Both transmission electron microscopy and small-angle X-ray scattering show that the superlattices form in both semidilute and concentrated regimes of polymer, where the free volume entropy and the depletion interaction are the dominant driving force, respectively. The superlattices are NaCl and temperature responsive. The rigidity of the rodlike nanoparticles also plays an important role for the formation of superlattices through the free volume entropy mechanism. Compared to the rigid TMV particle, flexible bacteriophage M13 particles are only responsive to the depletion force and thus only assemble in highly concentrated polymer solution, where depletion interaction is dominant.
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INTRODUCTION Crystalline assemblies, or superlattices, assembled from anisotropic nanoparticles have potential applications for the development of novel materials and devices with unique plasmonic,1,2 electrical,3,4 and magnetic properties.5 Among anisotropic particles, nanorods are one of the most studied.6−9 A variety of methods, utilizing enthalpic or entropic interactions such as solvent evaporation,10,11 DNA base pairing,12 and electrostatic-based assembly,13 have been developed to fabricate superlattices as well as other strategies based on external magnetic14,15 and electric fields.16,17 Recently, the use of the depletion force to promote superlattice formation has attracted much attention due to its simplicity and low cost.9,18,19 However, some competing mechanisms (such as the free volume entropy20) have clouded researchers understanding of the assembly process; thus, it remains unclear how parameters such as temperature, solvent ionic strength, and particle rigidity affect the complex balance of repulsive and attractive forces. Herein, we address these issues using rodlike viral particles as the building blocks and the polysaccharide methylcellulose as the depletant. Importantly, we show how the assembly process of these rodlike virus particles is affected by mechanisms from both free volume entropy and depletion. The depletion interaction between nanoparticles in a solution is invoked with the addition of polymers or micelles. These depletants exert an osmotic pressure on the particles and force them close to each other as a result of the additional gain in volume the depletants can explore. This osmotic pressure © 2013 American Chemical Society
results in an effective interparticle attractive force, which is often balanced by a repulsive electrostatic interaction originating from the surface charge of the particles.9,21−23 Biological nanoparticles, such as viruses and virus-like assemblies, are ideal systems for the study of nanoparticle assembly since they are monodisperse in size and shape. Among them, tobacco mosaic virus (TMV) has emerged as a promising building block in materials development25−29 with potential applications in catalysis,30,31 nanoelectronics,32−34 energy harvesting devices,35 and biomedical applications.36 TMV is composed of 2130 identical coat proteins assembled helically around a single-stranded RNA molecule (Figure 1a) forming a rigid-rod-like structure ∼18 nm in diameter and ∼300 nm in length, with a ∼4 nm central cavity (Figure 1b). TMV therefore provides an ideal model system to examine the self-assembly of rigid-rod-like particles. Recently, we reported the formation of TMV superlattices triggered by rigid polysaccharides such as methylcellulose (MC) (Figure 1c).20 The assembly process of MC/TMV superlattices was tuned with temperature, through its sol−gel transition, as shown in Figure 1d.20,37 Previously, we suggested that two mechanisms contribute synergistically to the assembly process: the free volume entropy mechanism and the depletion interaction. When rodlike TMV Received: July 31, 2013 Revised: September 11, 2013 Published: September 18, 2013 12777
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Figure 2. Schematic illustration of the assembly of TMV particles (a) before and (b) after assembly. On left, the depletion layer around TMV particles is designated with blue dotted lines and the nonaccessible volume due to rod orientation is shaded (green color). Once TMV particles assemble, polymers will gain the free volume shaded in left and additional depletion volume shaded (red color) in right.
electrostatic repulsion, we studied the effects of polymer concentration, ionic strength, temperature, and the rigidity of the virus particles by employing transmission electron microscopy (TEM) and small-angle X-ray scattering (SAXS). The assembly/disassembly process of TMV particles into bundled superlattices can be controlled by varying the ionic strength and temperature. Compared to rigid TMV particle, flexible M13 viral particles were not assembled through the free volume entropy mechanism. As a result, the range of variable d spacing for the M13 was limited.
Figure 1. (a) Transmission electron microscopy (TEM) image of TMV particle. The scale bar is 100 nm. (b) PyMol rendering of TMV structure using coordinates from PDB Databank. (c) Chemical structure of methylcellulose (MC). (d) Schematic representation of formation of MC/TMV superlattice hydrogel. MC/TMV superlattice sol is formed by addition of MC into the TMV water solution at room temperature. MC/TMV superlattice sol becomes MC/TMV hydrogel as the temperature increases. At elevated temperature, the hydrogen bonding through which MC store water molecules breaks and hydrophobic groups of MC interacts with each other due to hydrophobic interaction, which cause the formation of hydrogel.24 A fraction of the released water from MC moves to the TMV superlattices, resulting in the increase of the inter-TMV in superlattices spacing. MC/TMV superlattice hydrogel becomes sol when cooled down.
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EXPERIMENTAL SECTION
Materials. Methylcellulose (Mw 210 000 Da) was purchased from Sigma-Aldrich and used as received. TMV and M13 were isolated as reported previously.27,41 Water (18.2 MΩ) was obtained from a MilliQ system (Millipore). Preparation of MC/TMV Superlattice. To prepare the MC/ TMV mixture containing 15 mg/mL of TMV and 4 wt % MC, a solution of TMV (15 mg/mL, 500 μL) was added to MC in aqueous solution (84 mg/mL, 500 μL) with stirring. The other samples were prepared in the same manner by varying the amounts of polymer and TMVs. Nanomechanical Measurement of TMV and M13. Deformation behavior of TMV as well as M13 virus was studied by in-situ indentation under AFM (Dimension 3100, Vecco). A detailed procedure can be found in previous work.42 Solutions containing the samples were dropped onto Si wafers and dried under ambient conditions (∼30% RH). Tapping mode scanning was used to locate the individual virus, followed by indentation at a constant loading rate. Si3N4 tips with lower spring constant (kc) were used for both imaging and indentation to achieve better force resolution. As a key factor during the calculation of AFM tip force and elastic modulus, kc of an AFM cantilever was calibrated using nanoindentation method.43 The as-calibrated value of kc was approximately 0.73 N/m. The radius of AFM tip used in the study was calibrated with standard AFM tip characterizer (Veeco) prior to indentation tests. Using data from the linear elastic regime of the samples, the elastic properties of the samples were interpreted. Measurements. In a typical TEM measurement, a 10 μL TMV solution (0.02 mg mL−1) was deposited onto a carbon-coated copper grid, dried, and characterized with a JEOL 100CXII electron microscope. The SAXS experiments were performed at 12-ID-B station with X-ray energy of 12 keV. The sample-to-detector distance was about 2 m. A Pilatus 2M detector (Dectris Ltd.) was used to acquire scattering data with typical exposure times in a range of 0.1− 1.0 s. For the heating/cooling experiment, the samples were prepared in aluminum pans, sealed, and placed on a LTS 420 heating stage
particles are mixed with a rigid polymer, there can be two types of nonaccessible regions for the polymer chains. First, the depletion layer around the TMV due to the electrostatic repulsion and size of polymers effectively makes the size of TMV larger.18,38 Second, the volumes between these rigid-rodlike polymers, TMVs, and rigid sections of polymer chains, which are shaded in Figure 2a, are not accessible to either polymers or TMV particles. In the free volume entropy mechanism, which is well-known for liquid crystals,39,40 the latter nonaccessible volume is minimized by aligning rigid-rodlike objects to each other including both TMV to TMV alignment and TMV alignment to the polymer’s rigid segments. The depletion interaction arises when the polymer concentration is relatively high. The interaction forces TMV particles close to each other to reduce the total depletion volume by increasing the overlapped depletion region surrounding each individual particle (shaded in Figure 2b). Eventually, TMV particles will form superlattices balanced by the electrostatic repulsion and entropic attractive interactions. In this work, in order to confirm that the assembly is mainly due to the balance of the entropic attractions and the 12778
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(Linkam Scientific Instruments). Temperature was varied with a rate of 1 °C/min from 25 to 55 °C and dwell time of 5 min at each end.
concentration, TMV particles did not form aggregates, in agreement with the previous SAXS result (Figure 3a).20 As the MC concentration was above the semidilute concentration, TMVs began to form bundled structures several tens of micrometers long (Figure 3b), which display highly ordered hexagonal symmetry along the short axis, as determined by SAXS. In contrast to the fd particle assembly, we found no evidence of ordering along the long axis direction for TMV particles. The structure instead resembled a bundle of TMV particles arranged like a nematic liquid crystal, where each particle is displaced randomly along the long axis of the bundle. Interestingly, although no lamellar stacking was found, each TMV particle forms a head-to-tail alignment with adjacent particles, with gap distances smaller than could be observed by TEM, which has also been observed in the literature.45 This observation indicates that the repulsive interaction between the ends of two TMV particles is negligible compared to the attractive force that minimizes the packing volume. We hypothesize that this type of head-to-tail association may also be in part responsible for the nematic-type structure by preventing the separation of TMV particles into lamellar stacks. As the concentration of MC is concentrated, all TMV particles formed long bundles (Figure 3c), which are again composed of long fiberlike TMV particles as can be seen in the enlarged TEM image (Figure 3d). Effect of Ionic Strength. The internal structure of the bundle was studied with SAXS. As mentioned above, TMV particles display a hexagonal ordering in the plane of the bundle with well-defined spacing. Previously, we showed through modeling that the gap spacing is likely determined by the balance between the attractive interaction caused by the polymer and the electrostatic repulsion from the surface charge of TMV particles.20 If this were true, one should be able to tune the Debye length and therefore repulsive electrostatic force that exists between the negatively charged TMV particles, resulting in a tunable interparticle distance (d spacing) by manipulating the ionic strength of the solution.40 Since MC is a neutral polymer, varying the solution ionic strength, for example with NaCl, will not change the surface charge of the polymer. However, NaCl has a strong interaction with water due to the ions’ stronger hydration ability, which may disrupt the hydrogen bonding between MC and water molecules, thereby decreasing MC solubility.46 The solubility decrease may eventually reduce the radius of gyration (Rg) of MC and
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RESULTS AND DISCUSSION TEM Analysis of MC/TMV Superlattices. Previous studies on the depletion-based assembly of the filamentous fd virus suggested that virus particles can form stacked lamella structures, similar to smectic liquid crystals.44 While we previously reported that TMV particles formed a bundled structure with a hexagonal ordering along the TMV short direction, it was not clear whether they may also present a certain degree of ordering along the TMV long axis like its fd counterparts. Because of limitations in X-ray resolution, the superlattice morphology was examined by TEM at various polymer concentrations. Figure 3 shows TEM images for TMV
Figure 3. TEM images of MC/TMV samples at different MC concentrations such as (a) 0.1 wt %, (b) 1 wt %, and (c, d) 4 wt %. TMV concentration is 2 mg/mL. Scale bars are 500 nm. The boundaries between dilute regime and semidilute regime and between semidilute regime and concentration regime are denoted the overlap (c*) and entanglement concentration (c**), respectively. In the case of MC, the c* and c** are 0.42 and 4.5 wt %, respectively.
assemblies at three representative MC concentrations: (1) dilute concentration, (2) semidilute concentration, and (3) concentrated concentration. For MC concentrations of dilute
Figure 4. (a) Zeta potential of TMV as a function of NaCl concentration in water. The concentration of TMV is 2 mg/mL. (b) SAXS data of MC/ TMV samples at different NaCl concentrations in water. Inset is the calculated d spacing at a variety of NaCl concentrations. MC is 2 wt %, and TMV concentration is 2 mg/mL. 12779
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Figure 5. (a) SAXS curves of MC/TMV superlattice at different temperatures during heating process. Data are arbitrarily scaled for clarity. (b) Calculated d spacing of TMV/MC superlattice at different temperatures. MC is 4 wt %, and TMV concentration is 15 mg/mL.
Figure 6. The d/d0 ratio of MC/TMV superlattice at various temperatures for different MC and TMV concentrations. d0 is the spacing of the MC/ TMV superlattice with a fixed MC and TMV concentration at 25 °C. The concentration of MC in each plot is (a) 0.5, (b) 1, (c) 2, and (d) 4 wt %. The TMV concentration is varied from 1 (black square), 2 (red circle), 4 (blue up triangle), 15 (pink down triangle), and 30 mg/mL (green diamond).
subsequently the osmotic pressure that the MC would invoke.20 If this were the case, one would expect an increase the interparticle distance with increasing NaCl concentration. To determine which of these two mechanisms plays a greater role in the assembly of TMV, the ionic strength was varied by the addition of NaCl in the range of 0−1000 mM. This addition subsequently screened the surface charge of TMV, as confirmed by zeta potential measurements (Figure 4a). As the NaCl concentration was increased from 0 to 100 mM, the zeta potential values changed from −55 to −20 mV, and the sample still formed superlattices, as shown in Figure 4b. The d spacing decreases by 2.9 nm, from 24.8 to 21.9 nm (inset of Figure 4b). In other words, the gap between two adjacent TMV particles decreased from 6.8 to 3.9 nm. This result suggests that the decrease in the repulsive electrostatic force arising from TMV surface charge screening has a greater effect than the possible decrease in attractive depletion force resulting from a saltinduced decrease in MC solubility. 18,46 As the NaCl concentration was further increased, the diffraction peaks
became broader, demonstrating that the superlattice size decreases and becomes less well-ordered. At 0.5 M of NaCl, only a single broad diffraction peak is observed, indicating that TMV particles formed nonordered aggregates instead of the highly ordered superlattice, as one may expect if both the attractive and repulsive interactions get significantly weaker.10,18,47 Effect of Temperature. The d spacing is not only dependent on the ionic strength but also temperatureresponsive. As the temperature increases, MC has a sol−gel transition through a hydration−dehydration process. It was previously demonstrated that the TMV superlattice diffraction peaks became broader as the temperature was increased from 25 to 55 °C, suggesting that the structure changed from a crystalline state to a noncrystalline state.20 To better understand the effect of temperature on the d spacing, SAXS data were recorded on at at different temperatures of 25, 35, 45, and 55 °C (Figure 5a). The d spacing decreased from 22.8 to 21.6 12780
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Figure 7. (a) SAXS data of M13 in water and its GNOM fitting (red thin line) of M13 particle. (b) Pair distance distribution functions (PDDF) obtained from program GNOM by fitting the SAXS data of M13(c) AFM images of M13 particle.
Figure 8. (a, b) Experiment data obtained from MC/TMV and MC/M13 samples, respectively. Solid and open squares represent the ordered superlattice and nonordered assemblies, which are obtained from SAXS data. The samples with two or more peaks are considered as the ordered superlattice while these with less than two peaks are called nonordered assemblies. The dotted curves in (a) and (b) are the boundary that divide regimes of ordered superlattice (gray area) and nonordered assemblies (white area).
nm, ∼1.2 nm, as the temperature changes from 25 to 45 °C, as shown in Figure 5b. Next, we systemically studied the effect of temperature on the d spacing at a wide range of TMV and MC concentrations. As the temperature increased, the d spacing decreased and the variation of the d spacing was in the range of 5% compared to that at 25 °C (Figure 6a−d). Again at 55 °C, where MC became a gel, the ordered superlattices changed to nonordered aggregates. When MC was in its sol state at 25 °C, MC held water molecules through H-bonding, which started to break with the increase of temperature and the expanded conformation MC chains collapsed.24 The released water hydrated the TMV superlattice and increased the gap between TMV, resulting in the increase of d spacing. As the gap reached a threshold, where the collapsed conformation cannot invoke enough attractive interaction through either the free volume entropy or depletion mechanisms, the ordered structures of TMV assembly turned into nonordered aggregates.
Effects of Rigidity of 1D Particles. The effect of the rigidity of 1D particle was studied by comparing the assembly of the rigid TMV virus with a flexible rodlike particle, bacteriophage M13. The filamentous M13 virus is approximately 6.5 nm in diameter and 880 nm in length and has been broadly used as a molecular building block for various applications in biotechnology.41,48−52 Based on the pair distance distribution function (PDDF) calculated from GNOM software package,53 the largest dimension along the cross section (D) obtained for M13 in water is around 6.8 nm (Figure 7a,b), which is in good agreement with AFM results (Figure 7c) and values reported in the literature.41,48−52 From the AFM images, M13 appears as a flexible, partially coiled chain and is clearly more flexible than TMV (compare AFM images from Figure 7c to the TEM images of TMV in Figure 1a). The persistence lengths of TMV and M13 are approximately 3000 mm and around 1265 nm, respectively,54,55 indicating that M13 is at least a factor of 1000 times more 12781
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Langmuir flexible in this sense. Furthermore, the elastic modulus, which may also reflect the rigidity of particles,56,57 was determined for both TMV and M13 by nanoindentation (see Supporting Information for more details). From these results, the elastic modulus of TMV was calculated to be 0.98 ± 0.2 GPa, which is in good agreement with the literature42 and approximately 60% greater than that of M13 (0.62 ± 0.1 GPa). The effect of particle rigidity on depletion- and free volumetype assembly was examined with SAXS by exploring the superlattice phase behavior at varying MC and particle concentrations, for both the rigid TMV and flexible M13 particles (Figure 8). Interestingly, the TMV particles formed superlattices over a wider MC and particle concentration range than their flexible M13 counterparts. While the MC/TMV system formed superlattices in both the semidilute regime (c < c**, ∼4.5 wt % MC) where the free volume mechanism dominates the assembly process and the concentrated regime (c > c**) where the particles assemble through depletion interactions, the MC/M13 system only formed superlattices close to the concentrated regime. Considering the free volume entropy mechanism, flexible 1D particle assumes a greater conformational freedom than their rigid counterparts, resulting in less free volume that the polymer could gain by confining the particles to a superlattice. In other words, for the polymer to gain additional free volume, the osmotic pressure applied to the particles by the polymer would not only have to push particles closer together but also would have to straighten them. This conformational change, from a coiled to straight rod, has been observed in the literature for flexible virus as the polymer concentration increases in order to increase the overlap volume between two rods.58 In this case the loss of the conformational entropy of the virus must be compensated by the gain from the depletion interaction, which is not required for the rigid rods. These results suggest that both mechanisms preferentially assemble rigid rods over flexible ones. In summary, rigid MC polymer plays two key roles in invoking rodlike particles to form superlattice: it induces the depletion attraction and the free volume entropy mechanism that is not expected for soft polymers.9,20,59 These two entropic attractions are balanced by the electrostatic repulsion which can be screened by the addition of salt into the system. TEM clearly shows that the assembled structure of TMV particles is a bundled structure. Interestingly, long fiber with head-to-tail assembly of TMV is observed. By changing the salt and temperature, the superlattice of TMV particles disassembled or disordered when both repulsive and attractive interactions became weaker.
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ACKNOWLEDGMENTS
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REFERENCES
We are thankful for the use of Advanced Photon Source, an Office of Science User Facility operated for the U.S. Department of Energy (DOE) Office of Science by Argonne National Laboratory, was supported by the U.S. DOE under Contract DE-AC02-06CH11357. Q. Wang is grateful for the financial support from the US NSF CHE-0748690 and US NSF DMR-0706431. Y. Sun and X. D. Li thank the financial support from the U.S. National Science Foundation (CMMI-1129979 and CMMI-0968843).
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ASSOCIATED CONTENT
S Supporting Information *
Mechanical properties of the M13 and TMV using the nanoindentation method. This material is available free of charge via the Internet at http://pubs.acs.org.
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AUTHOR INFORMATION
Corresponding Authors
*E-mail
[email protected] (Q.W.). *E-mail
[email protected] (B.L.). Notes
The authors declare no competing financial interest. 12782
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