Superlattice of Rodlike Virus Particles Formed in Aqueous Solution

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Superlattice of Rodlike Virus Particles Formed in Aqueous Solution through Like-Charge Attraction Tao Li, Randall E. Winans, and Byeongdu Lee* X-ray Science Division, Advanced Photon Source, Argonne National Laboratory, 9700 S. Cass Avenue, Argonne, Illinois 60439, United States ABSTRACT: Rodlike tobacco mosaic virus (TMV) has been found to assemble into a 2D superlattice in aqueous solution with hexagonally packed structures in the presence of Ba2+ through like-charge attraction whereas lower-Z divalent ions such as Zn2+, Cd2+, Mg2+, and Ca2+ induce only liquidlike ordering. The molar ratio between Ba2+ and TMV is a crucial parameter in the formation of the superlattice. There is a critical molar ratio of Ba2+ to TMV at which TMV exhibits a transition from a nonordered colloidal state to an ordered crystalline state. It is also found that the superlattice is formed regardless of the pH and TMV concentration within the range studied.

’ INTRODUCTION The fabrication of highly ordered structures from 1D nanomaterials into a superlattice is of great interest because of their potential applications in the fields of electronic devices, sensing and imaging, and nanomedicine, which arise from their unique anisotropic structural features and specific shape-dependent properties.1 3 Spherical particles could form a superlattice either through a delicate balance between repulsive and attractive interactions for a dilute solution or by minimizing the inaccessible space between them in order to maximize the entropy for a concentrated system.4 6 For anisotropic particles, the entropy effect largely depends on the particle shape. If the shape of monodisperse particles is identical to the Wigner Seitz cell of a certain lattice, then they will pack into the lattice with 100% efficiency. For example, 1D cylinders will pack into a 2D hexagonal lattice, rhombic dodecahedra will pack into facecentered cubic structures, and truncated octahedra will pack into body-centered cubic structures.7 Among all anisotropic particles, nanorods are one of the most studied and from solvent evaporation will pack into a 2D hexagonal superlattice, which is the densest packing structure for nanorods.8 13 To induce self-assembly in solution with a relatively dilute concentration of nanorods, an attractive interaction between rods is required. A depletion interaction, which is an entropic interaction induced by adding smaller particles, can lead to larger inorganic nanorods mixed with smaller particles to form a 2D superlattice in solution.14,15 Additionally, it also has been demonstrated that exposure to X-ray radiation will trigger superlattice formation in a dilute solution, where the repulsive force between peptide nanorods created by X-ray forces them to orient with respect to each other and pack into a 2D hexagonal superlattice.16 Moreover, an enthalpic attraction can induce the r 2011 American Chemical Society

formation of a nanorod superlattice as well. For instance, when the ligands at the tips of the rods are selectively exchanged for hydrophilic ligands containing a carboxyl group while keeping the rest of the ligands on the sides of nanorods hydrophobic, a 2D hexagonal assembly is facilitated and stabilized through the formation of hydrogen bonding between neighboring rods.17 Like-charge attraction has also been proposed for the liquidlike ordering of biomolecular nanorods such as DNA, F-actin, the M13 or fd virus, and microtubules that have both positive and negative charges on their surfaces.18 23 In these systems, multivalent ions condense onto nanorods and neutralize most of their charges, leading to much reduced repulsion between each other. The multivalent ion not only reduces the repulsion but also increases the attraction between the nanorods.24,25 Compared to inorganic rods, the crystalline ordering of these biomolecular nanorods has not been reported yet in a dilute solution where the packing entropy is not the major contribution to self-assembly, if any. Here, for the first time as far as we recognize, it is shown that a rodlike tobacco mosaic virus (TMV) can form a superlattice in a dilute solution by like-charge attraction. TMV (∼18 nm in diameter and ∼300 nm in length) (Figure 1a), which is a naturally occurring protein cage arranged in the shape of a hollow cylinder carrying a 4 nm cavity, is the most studied model of biomolecular rodlike particles. TMV is composed of 2130 identical coat proteins assembled helically around a single-stranded RNA. It has been utilized as an ideal rigid nanorod to understand the self-assembly of rodlike particles and has emerged as a promising building block in material Received: June 6, 2011 Revised: July 19, 2011 Published: July 25, 2011 10929

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Figure 1. (a) Transmission electron microscopy (TEM) image of TMV without Ba2+. (b d) Field emission electron microscopy (FESEM) images of the TMV/Ba2+ superlattice. The scale bar in a is 150 nm.

Figure 2. (a) One-dimensional scattering curve of TMV/Ba2+ superlattice resulting from averaging the 2D image (shown in the inset). (b) Schematic representation of the Ba2+-triggered organization of TMVs. White precipitates, which are superlattices of hexagonally packed TMVs, are formed from a transparent aqueous TMV solution after the addition of Ba2+ solution.

development.26 31 The isoelectric point of TMV is 3.4, and the surface of TMV is negatively charged at neutral pH.

Furthermore, the surface of TMV can be readily modified via bioconjugation or genetic modification.32 34 Also, TMV-based 10930

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Figure 3. X-ray measurements performed at various positions on a 2-mm-diameter capillary containing an aqueous solution of Ba2+ and TMVs, where the molar ratio of Ba2+ to TMV is 18.4  104. (a) Schematic drawing of the capillary. SAXS and X-ray transmittances are measured at positions a g. (b) SAXS data and (c) X-ray transmittances and integrated intensities. The box highlights the interfacial region between water and the precipitation phases.

nanomaterials have shown great potential in the applications of catalysis, nanoelectronics, and energy-harvesting devices.35 44 In a search of the literature, no reports on the formation of the crystalline superlattice of TMVs in a dilute solution have been found; however, their liquid-crystalline ordering at concentrations higher than 5 vol % is well known. In this article, it is shown that Ba2+ can trigger the formation of TMV superlattice in a dilute solution. In doing so, there is a critical molar ratio of Ba2+ to TMV (Mc) at which TMVs transition from a colloidal state to a crystalline state. Below Mc, TMVs form a colloidal suspension that is phase-separated from a transparent aqueous solution, and above Mc, TMVs are crystallized into a hexagonally packed structure and precipitate out. Other metal ions such as Zn2+, Cd2+, Mg2+, and Ca2+ are studied as well, but the results show that the formation of a superlattice occurs with Ba2+ selectively.

’ EXPERIMENTAL SECTION Materials. TMV is purified according to a procedure in the literature.13 BaCl2 (>98.0%), ZnCl2 (>99.99%), CdCl2 (>99.0%), MgCl2

(>98.0%), and CaCl2 (>96.0%) have been purchased from SigmaAldrich and used as received. Water (18.2 MΩ) was obtained from a Milli-Q system (Millipore). Sample Preparation. A BaCl2 aqueous solution (e.g., 2.2 mg in 30 μL of water for the sample shown in Figure 2) is added to a solution of TMV (0.9 mg in 30 μL of pure water), followed by a vortex mixing for 15 s, and the mixed solution is transferred to a 2-mm-diameter quartz capillary tube that is sealed and kept at room temperature for 24 h. For all mixed solutions, the TMV concentration is 15 mg/mL (thus the volume fraction of TMV is 1.7%), unless otherwise noted. A similar protocol was used to prepare the TMV/metal complex with different metals. Measurement. To prepare the sample for TEM measurement, a 0.02 mg mL 1 TMV solution (10 uL) was deposited onto a carboncoated copper grid, dried for 20 min, and characterized with a JEOL 100CXII electron microscope. Field electron scanning electron microscopy (FESEM) was performed with a Hitachi S4700 SEM. Both TEM and FESEM characterization were run in the Electron Microscopy Center of Argonne National Laboratory. Small-angle X-ray scattering (SAXS) measurements were performed at the 12-ID-C station at the Advanced Photon Source (Argonne National Laboratory, Argonne, IL). The X-ray energy was 12 keV, which corresponds to a wavelength of 10931

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Figure 4. SAXS data for two TMV/Ba2+ samples with different molar ratios of Ba2+ to TMV: mBa2+/mTMV = 9.2  104 (top) and 6.9  104 (bottom). 1.0332 Å. The sample-to-detector distance was about 2 m. A 2D CCD detector was used to acquire images with typical exposure times in the range of 0.01 1 s.

’ RESULTS AND DISCUSSION At the bottom of a container (either a 2-mm-thick quartz capillary or a 1 mL plastic tube), we observed white precipitation that occurred slowly and took at least 24 h to complete. Field emission scanning electron microscopy (FESEM) images of the precipitate indicate that TMVs form bundled structures that are several tens of micrometers long and several micrometers in diameter (Figure 1b d). Further characterization of their

nanoscale structure has been performed using SAXS, which is reported in this article. SAXS has been demonstrated to be a powerful technique in characterizing the nanostructure in the solution.5,7,16,45 Figure 2a shows the azimuthally averaged 1D SAXS profile, where 10 sharp diffraction peaks are discernible. The positions of 10 peaks with respect to the principal peak, q/q*, are 1, (3)1/2, (4)1/2, (7)1/2, (9)1/2, (12)1/2, (13)1/2, (14)1/2, (21)1/2, and (25)1/2 (where q* is the principal peak position), suggesting that the precipitate is a 2D hexagonal superlattice of TMVs as modeled in Figure 2b and its domain size is at least 300 nm as calculated on the basis of the peak width. The inset of Figure 2a is the 2D scattering image of the TMV/Ba2+ samples, revealing that the 2D superlattice is randomly oriented. 10932

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Figure 6. SAXS data from the precipitation phases of TMV/Ba2+ solutions with various mBa2+/mTMV molar ratios. From bottom to top are data with increased molar ratios. Data are arbitrarily scaled for clarity.

Figure 5. (Top) SAXS data from the water (O) and precipitation (0) phases and their GNOM fitting (thin red line) of TMV/Ba2+ samples, where mBa2+/mTMV = 6.9  104. Data have been arbitrarily scaled for clarity. (Bottom) Pair distance distribution functions (PDDF) from GNOM fittings in a for the water (O) and precipitation (red 0) phases.

Compared to other flexible DNA, F-actin, and M13 virus species, TMV is more rigid, which may cause superlattice formation in solution. In the literature, they form only bundled structures with liquidlike ordering.18 20 The center-to-center distance between TMVs, d, in the superlattice is calculated using q* = 4π/(3)1/2d. For instance, when the molar ratio between Ba2+ and TMV, mBa2+mTMV, is 18.4  104, q* is around 0.03356 Å 1, which gives d = 21.6 nm. To characterize the structure of the TMV assembly and the distribution of Ba2+ and TMV in each phase of the phaseseparated solution, SAXS (Figure 3b) and X-ray transmittance (Figure 3c) measurements were made at various locations in the solution in the sealed capillary (Figure 3a). The relative populations of TMV in the precipitation (bottom) and water (top) phases in the capillary can be estimated from the SAXS data. For example, Figure 3b shows that there is no form factor scattering of TMV in the water phase (g) but weak, broad diffraction peaks whose intensities are at least an order of magnitude lower than those in the interfacial or precipitation region as shown in Figure 3c. This indicates that most of the TMVs in the water phase are precipitated out and even remaining TMVs are not dispersed as they are in a pure aqueous solution without Ba2+ but form small bundles. Interestingly, positions of diffraction peaks that are directly related to the inter-TMV distance were constant

regardless of the measured locations. X-ray transmittance values show the opposite trend in SAXS intensity; it is higher in the water phase (spot g) than in the precipitation phase (spots a d), indicating that there is more Ba2+ in the precipitation phase than in the water phase. This result suggests that Ba2+ ions are predominantly located in the precipitation phase and are relevant to the formation of the TMV superlattice. The effect of the molar ratio of Ba2+ to TMV on superlattice formation has been studied; SAXS data were obtained on seven different molar ratio samples. All samples except [Ba2+] = 0 show phase separation. Figure 4 compares the SAXS patterns from two representative samples, where the sample for Figure 4 (top) represents samples with low Ba2+/TMV ratios and that for Figure 4 (bottom) represents those with high Ba2+/TMV ratios. Samples with a molar ratio of Ba2+/TMV = 9.2  104 show diffraction peaks for the precipitation phase and no TMV signal for the water phase whereas for samples with mBa2+/mTMV = 6.9 104 no diffraction peaks are observed at any position on the capillary. Only the form factor scattering of TMV is observed for the top part of the capillary whereas a more diffuse scattering pattern whose form factor minima are smeared out is observed for the bottom part of the capillary. In fact, the precipitation phase was not white-powder-like but was more or less colloidallike. In Figure 5, the pair distance distribution function (PDDF) has been calculated using GNOM.46 GNOM fits and PDDFs are shown in Figure 5 (top and bottom, respectively) for both the water and precipitation phases of the low Ba2+/TMV ratio samples. The largest dimension along the cross section (D) obtained for TMV in the water phase is around 18 nm, which is in good agreement with the value reported in the literature.47 In the case of TMVs in the precipitation phase, it is clear that the maximum pair distance is further stretched out, suggesting that there are Ba2+ ions located at the surfaces of TMVs. Figure 6 summaries all SAXS curves from the bottom of capillaries. When the molar ratio of Ba2+ to TMV is below 9.2  104, only a colloidal suspension is formed. When it is above this value, TMVs are arranged into a crystalline lattice. Thus, 10933

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Langmuir Ba2+/TMV = 9.2 104 will henceforth be defined as the critical molar ratio, Mc, of Ba2+ to TMV. As discussed previously, TMVs in the colloidal suspension do not form an assembly but bind Ba2+ onto their surfaces. It is likely that the repulsion between these TMVs and Ba2+ overwhelms any attractive interaction

Figure 7. SAXS data from the precipitation phases of TMV/Ba2+ solutions with two different volume fractions of TMV: (bottom) 0.1 vol % (1 mg/mL) and (top) 3.4 vol % (30 mg/mL). Data are scaled for clarity.

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between TMVs. When Ba2+/TMV is greater than Mc, this assembly behavior changes rather quickly. TMVs form a highly ordered superlattice by increasing the concentration of Ba2+ by 30%. This assembly behavior as a function of Ba2+/TMV in the precipitation phase is consistent with that in the water phase. When SAXS curves in the water phases of both samples are compared (Figure 4), we found that because Ba2+/TMV is less than Mc there are far more free TMVs or TMVs do not form any amorphous clusters or a superlattice. Later in this article, the approximate numbers of free TMVs and assembled TMVs in the water and precipitation phases are calculated. Furthermore, SAXS data have been obtained (Figure 7) for solutions with two different TMV volume fractions, 0.1 and 3.4%, with a fixed Ba2+/TMV. It took longer (several hours) for TMVs in 0.1% solution to form the initial precipitate than those at a higher volume fraction of 3.4% (several minutes). However, both samples show sharp diffraction peaks although a weaker intensity in the 0.1% solution because of the smaller number of TMVs. The fact that the TMV superlattice forms regardless of the volume fraction of TMV in solution suggests that superlattice formation is not due to the entropy effect and that there is an attractive interaction between TMVs. Figure 8a,b shows I(0) values of SAXS curves in the water phase and the volume fraction of the precipitation phase, respectively. In this study, I(0) is proportional to the number of TMVs, thus I(0) in Figure 8a represents the relative number of TMVs in the water phase. Above Mc, there was practically no TMVs left in the water phase, suggesting that almost all TMVs precipitated. Considering that the same number of TMVs is used for each sample, if all TMVs in solution are crystallized into

Figure 8. Results from scattering experiments for solutions with various mBa2+/mTMV molar ratios: (a) SAXS intensities at q = 0, or I(0), from the water phase, (b) volume fractions of the precipitation phases, (c) X-ray transmittances with respect to that of water and data fitting using an exponential function (red line), and (d) d spacings calculated from the first-order peaks of the data shown in Figure 6. 10934

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Figure 9. SAXS curves from the precipitation phase of the TMV/Ba solution obtained for various pH values, where the Ba2+/TMV molar ratio is fixed at 18.4  104. Data are scaled for clarity.

superlattices then the number of precipitated TMVs in Figure 8b should be identical for all samples unless the number of Ba2+ ions bound to TMVs is significantly different. Indeed, the volume of precipitates stays constant above Mc. Figure 8c shows the X-ray transmittance in the water and precipitation phases. A lower transmittance is due to a higher concentration of Ba2+. Thus, it is clear that there is higher concentration of Ba2+ in the precipitation phase than in the water phase, suggesting that Ba2+ condensation on the TMV surface is a driving force in superlattice formation. X-ray transmittance in the water phase decreases exponentially with increasing molar ratio, following Beer’s law. The X-ray transmittance of the precipitation phases also decreases, but its rate is far slower, indicating that above Mc most of the Ba2+ is present in excess and stays preferentially in the water phase but does not participate in superlattice formation. The inter-TMV distance did not vary significantly with the Ba2+/ TMV molar ratio as shown in Figure 8d. These constant X-ray transmittance and d-spacing values above Mc indicate that there is a critical number of Ba2+ ions that can be loaded onto the TMV surface. This critical number of Ba2+ ions on TMV was calculated by approximating the Ba2+ concentration in the water phase on the basis of the X-ray transmittance. Considering that the relative number of TMV molecules in the water phase is negligible (Figure 8a) and assuming that all Ba2+ ions in the precipitation phase surround the TMVs, there are 27 Ba2+ ions calculated to be around each subunit at Mc, which corresponding to about 3 Ba2+/nm2 on the TMV surface. The assumption that there is no unbound Ba2+ in the precipitation phase may be false because the precipitation phase is still in the aqueous solution that contains unbound Ba2+ions and thus the actual number of Ba2+ ions around TMV may be smaller than the number calculated. This value at Ba2+/TMV = 9.2  104 is at least doubled at Ba2+/TMV = 50  104 according to the decreased X-ray transmittance in Figure 8c; however, the d spacing in Figure 8d does not decrease further. This result suggests that the d spacing is not a strong function of the interaction energy between TMVs once the surface coverage of Ba2+ reaches a certain critical value.

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Figure 10. SAXS curves of TMV/metal ion solutions. The metal ions are Cd2+, Zn2+, Ca2+, and Mg2+ from top to bottom. The molar ratio of ions to TMV are 4.7  104, 8.5  104, 10.4  104, and 17.1  104 for the Cd2+, Zn2+, Ca2+, and Mg2+ samples. Data are scaled for clarity.

If the superlattice is formed as a result of the balance between repulsive and attractive interactions, then the d spacing will vary with pH because the surface charge density of TMV depends on the pH.48 To prove this hypothesis, the pH effect on the superlattice formation has been studied for two molar ratio samples; one is at 9.2  104, and the other is at 18.4  104. It turns out that for both conditions not only the d spacing but also the degree of ordering are unaffected, as shown in Figure 9. Additionally, the X-ray transmittance of precipitates is the same within error, suggesting that the amount of Ba2+ bound to TMV does not depend on the pH. All of these results suggest that the TMV crystallization in this system happens through Ba2+ bridging or like-charge attraction.24,49 51 In this work, the inter-TMV distance (2 nm) is rather large for a single Ba2+ to bridge two TMVs, indicating that the bridging is not the driving force in the formation of the superlattice. Therefore, the like-charge interaction induced by Ba2+ on the TMV surface is believed to be the main reason for TMV crystallization. Ba2+ condensed as a “Manning” layer induces the like-charge interaction that occurs after the molar ratio of Ba2+ to TMV reaches a certain critical value that is about 9.2  104, which is termed the critical molar ratio in this work. The strength of the like-charge attraction may not be enough to overcome the electrostatic repulsion at a lower Ba2+/TMV ratio condition than the critical molar ratio. The superlattice is formed as Ba2+/TMV reaches the critical value. The amount of Ba2+ on the TMV surface does not increase further with increasing Ba2+ concentration in solution. Lastly, experiments with different low-Z divalent ions such as Cd2+, Zn2+, Ca2+, and Mg2+ and with monovalent ions have been performed. As is well known, monovalent ions did not induce the superlattice whereas all four divalent ions applied in this work did cause the precipitation of TMVs. Figure 10 shows SAXS curves from the precipitation phases of the four samples. These scattering curves are very similar to each other, but they are very different from those of samples with Ba2+. For instance, the 10935

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Langmuir diffraction peaks in Figure 10 are very broad compared to those in Figure 10, and typically only three peaks are discernible. The diffraction patterns were not improved by a higher ion concentration. It seems that only Ba2+ can induce superlattice formation. This is similar to the ion-specific binding phenomenon, which is commonly observed but not yet clearly understood in many other biological systems. For example, Mn2+ and Cd2+ could condense DNA while Ca2+ and Mg2+ show no condensation.18 Recently, it was reported that Ba2+, Ca2+, or Sr2+ induces the condensation of microtubules whereas other divalent ions such as Mg2+ do not.23

’ CONCLUSIONS It has been demonstrated that TMVs can assemble into a 2D superlattice with a length to several tens of micrometers in aqueous solution in the presence of Ba2+. In contrast, lower-Z divalent ions such as Cd2+, Zn2+, Ca2+, and Mg2+ can induce only liquidlike ordering. The investigation with SAXS suggests that surface-bound Ba2+ not only screens the electrostatic repulsion but also induces the attraction between TMVs when the molar ratio of Ba2+ to TMV reaches a critical value, which leads to the formation of a superlattice. Center-to-center distances of TMVs in the superlattice do not vary with the Ba2+/TMV ratio, TMV concentration, and pH as long as they are formed with a Ba2+/TMV molar ratio higher than the critical value. ’ AUTHOR INFORMATION Corresponding Author

*E-mail: [email protected].

’ ACKNOWLEDGMENT We are thankful for the use of the Advanced Photon Source, Electron Microscopy Center, an Office of Science user facility operated for the U.S. Department of Energy (DOE) Office of Science by Argonne National Laboratory, which was supported by the U.S. DOE under contract no. DE-AC02-06CH11357. ’ REFERENCES (1) Rueckes, T.; Kim, K.; Joselevich, E.; Tseng, G. Y.; Cheung, C. L.; Lieber, C. M. Science 2000, 289, 94–97. (2) Zhong, Z. H.; Wang, D. L.; Cui, Y.; Bockrath, M. W.; Lieber, C. M. Science 2003, 302, 1377–1379. (3) Murphy, C. J.; Sau, T. K.; Gole, A. M.; Orendorff, C. J.; Gao, J.; Gou, L.; Hunyadi, S. E.; Li, T. J. Phys. Chem. B 2005, 109, 13857–13870. (4) Cigler, P.; Lytton-Jean, A. K. R.; Anderson, D. G.; Finn, M. G.; Park, S. Y. Nat. Mater. 2010, 9, 918–922. (5) Park, S. Y.; Lytton-Jean, A. K.; Lee, B.; Weigand, S.; Schatz, G. C.; Mirkin, C. A. Nature 2008, 451, 553–556. (6) Pusey, P. N.; Vanmegen, W. Nature 1986, 320, 340–342. (7) Jones, M. R.; Macfarlane, R. J.; Lee, B.; Zhang, J.; Young, K. L.; Senesi, A. J.; Mirkin, C. A. Nat. Mater. 2010, 9, 913–917. (8) Park, S.; Lim, J. H.; Chung, S. W.; Mirkin, C. A. Science 2004, 303, 348–351. (9) Talapin, D. V.; Shevchenko, E. V.; Murray, C. B.; Kornowski, A.; Forster, S.; Weller, H. J. Am. Chem. Soc. 2004, 126, 12984–12988. (10) Ahmed, S.; Ryan, K. M. Nano Lett. 2007, 7, 2480–2485. (11) Ming, T.; Kou, X. S.; Chen, H. J.; Wang, T.; Tam, H. L.; Cheah, K. W.; Chen, J. Y.; Wang, J. F. Angew. Chem., Int. Ed. 2008, 47, 9685– 9690. (12) Guerrero-Martinez, A.; Perez-Juste, J.; Carbo-Argibay, E.; Tardajos, G.; Liz-Marzan, L. M. Angew. Chem., Int. Ed. 2009, 48, 9484–9488.

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dx.doi.org/10.1021/la202121s |Langmuir 2011, 27, 10929–10937