Modulating the Arrangement of Charged Nanotubes by Ionic Strength

Letter pubs.acs.org/JPCL

Modulating the Arrangement of Charged Nanotubes by Ionic Strength in Salty Water Jiaojiao Tao,†,+ Ningdong Huang,†,+ Junjun Li,†,§ Mingming Chen,† Chengsha Wei,‡ Liangbin Li,*,†,‡ and Ziyu Wu*,† †

National Synchrotron Radiation Lab, College of Nuclear Science and Technology and ‡Department of Polymer Science and Engineering, CAS Key Lab of Soft Matter Chemistry, University of Science and Technology of China, Hefei, China S Supporting Information *

ABSTRACT: Despite the important role and potential application of charged cylindrical polyelectrolytes, biomacromolecules, and self-assembles, salt-modulated organization of those 1D charged nanostructures remains a topic relatively unexplored with an obscure underlying mechanism. In this Letter, the aggregation of oriented nanotubes self-assembled by ionic aromatic oligoamide in aqueous solution of NaCl over a wide concentration range is probed via small-angle X-ray scattering and a transmission electron microscope. The arrangement of nanotubes undergoes order−disorder transition sequences from an ordered rectangular phase to hexagonal packing and then to a lamellar gel. The observed transitions are understood by ionic effects on the electrostatic interaction between charged nanotubes and osmotic pressure due to ion partitioning. Above the physiological condition, electrostatic interactions are largely screened by the salts, while osmotic effects start to regulate the aggregation behavior and concomitantly deform the nanotubes. The study demonstrates rich phase behaviors of ordered, charged 1D nanostructures by tuning the ionic strength and underlying key physical principles. SECTION: Glasses, Colloids, Polymers, and Soft Matter

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the hierachical structure of charged nanotubes assembled by P7(COONa)3 via small-angle X-ray scattering (SAXS) and transmission electron microscope (TEM). Our study reveals rich phase behavior of and key principles regulating the aggregation of charged 1D nanostructures around the physiological ionic strength in salty water, which was almost exclusively accessible by theory or simulations heretofore.10,18 Those interesting findings not only help to understand the aggregation behavior of rod-like biomacromolecules in the presence of monovalent salts but also help to prepare ordered 1D nanoscale materials in aqueous environments. Addition of different molar ratios of NaCl to a 1.5 wt % P7(COONa)3 solution gave rise to distinctive appearances after aging for 1 month in Figure 1. At a low molar ratio of NaCl to P7(COONa)3, the aqueous system appeared to be a suspension of white mucus similar to a pure P7(COONa)3 solution with microfibers (Figure S1a,b, SI), as described in ref 17. At an intermediate salt level between the mole ratio of NaCl to P7(COONa)3 at around 0.75:1 and 25:1, the sample gradually turns transparent and more viscous. The translucent phenomenon of photographs is the expected consequence of the observed shorter microfibers (Figure S1c,d, SI) dissolved below a certain critical length, just like salt-in of protein due to the Hofmeister effect.19 Meanwhile, the increased viscosity of

nderstanding structure-directing factors such as ionic strength is very important in many areas, ranging from protein aggregation processes in human health1−3 to rational design of supramolecular assemblies.4−7 A formidable challenge is to gain fundamental understanding of rich aggregation behaviors of colloidal systems by tuning the interaction with salts, for example, short-range attraction, electrostatic repulsion, and osmotic pressure.8−10 A variety of ion-induced phenomena, including “like-charge” attraction and gel formation of polyelectrolytes, have been explored both experimentally and theoretically.11−13 However, salt-modulated organization of 1D nanostructures such as cylindrical polyelectrolytes or supramolecular assemblies remains a topic relatively unexplored, with obscure underlying mechanisms mostly due to the scarcity of experimental systems. The undiscovered mechanisms might be essential for understanding phenomena in biology14 and colloidal systems as well as for a myriad of potential applications of ordered, oriented 1D nanostructures.15,16 We have previously reported that nanotubes self-assembled by ionic aromatic oligoamide (BTA molecule denoted as P7(COONa)3 shown in Scheme S1 in the Supporting Information (SI)) can spontaneously arrange into a 2D rectangular array in aqueous solutions.17 Those ordered supramolecular nanotube bundles provide a novel model system to investigate the effects of ionic strength on arrangements and stabilities of organized 1D nanostructures for both fundamental purpose and applicable implication. In this work, we focus on the effects of salts (NaCl and NaBr) on © 2014 American Chemical Society

Received: February 13, 2014 Accepted: March 18, 2014 Published: March 18, 2014 1187

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Figure 1. Photographs of a 1.5 wt % P7(COONa)3 aqueous solution with different molar ratios of NaCl (or NaCl concentrations) after aging for 1 month. All of the ratios in this Letter denote molar ratios of NaCl to P7(COONa)3.

Figure 2. (a) The evolution of the arrangement of charged nanotubes under different mole ratios of NaCl to P7(COONa)3 was investigated by SAXS. The sample-to-detector distance was 2125 mm in order to show high order peaks. (b) Fitting SAXS experimental data of 0.75:1 by four Gaussian fittings. The obtained ratio of q values is close to 1:√3:2:√7, characteristic of the hexagonal phase. (c) An attempt to identify the structure at 60:1 by superimposing a new structure (dashed curve) on top of a hexagonal structure similar to that at 0.75:1 (short dotted curve). The dashed curve generates q values equal to 1:2:3, assumed as a lamellar structure.

samples possibly stems from the physical entangled microfibers. At high salt concentration, hydrogel formation is confirmed by an upside-down test (Figure 1) and rheological measurements (Figure S2, SI). The above interesting findings indicate changes of the supramolecular organization of nanotubes in the presence of NaCl, which will be explored by synchrotron radiation SAXS. The SAXS 1D curves are summarized in Figure 2a, denoted with proposed structural assignments. At 0.5:1 (or a concentration of NaCl of about 7.6 mM), the SAXS data indicate a rectangular lattice similar to that for the salt-free solution elucidated in ref 17; however, the Bragg scattering peaks shift to a smaller q value, corresponding to lattice expansion. With increasing NaCl concentration, the rectangular scattering peaks disappear, and three broad peaks emerge at 0.75:1 (11.4 mM NaCl). In Figure 2b, the scattering curve of 0.75:1 can be fitted well by four Gaussian peaks, with a q ratio of 0.523:0.918:1.001:1.453, very close to 1:√3:2:√7, characteristic of the hexagonal phase. As more salts are added (Figure 2a), a rather sharp feature at around 0.45 nm−1 accompanied by high order peaks appears at around 30:1 (0.45 M NaCl), which exists in a broad range of NaCl concentration up to 60:1 (0.9 M NaCl). The 60:1 experimental data can be reproduced remarkably well by superposition of the lamellar structure with a q ratio of 1:2:3, depicted by the dashed curve in Figure 2c (further confirmed by the FESEM image in Figure S3 in the SI) and the hexagonal phase (short dotted curve) similar to that of 0.75:1 in Figure 2b, indicating concurrence of two phases, as discussed in the following paragraph (the details of the Gaussian fitting are given in Figure S4 in the SI). However, all above scattering peaks disappear at 80:1 (1.2 M NaCl). The SAXS data suggest that by increasing the ionic strength, the arrangement of charged nanotubes evolves from a 2D rectangular phase to 2D hexagonal packing, then to a 1D lamellar array, and finally to a disordered structure. No specific anion effect is observed for NaBr, which also exhibits similar evolution sequences in Figure S5 (SI). The physiological concentration of NaCl of around 150 mM corresponding to a mole ratio of 10:1 in this study is most interesting for biological phenomena and biomedical application, which shows a subtle structural transformation procedure and merits more careful analysis. Higher resolution SAXS around this concentration between mole ratios of 1:1 and 60:1 in Figure 3 can better perceive the transformation from hexagonal packing to a lamellar array. With increasing salt concentration, the broad peak corresponding to the (10) peak of the hexagonal phase at low concentration of NaCl is squeezed and then splits into two discernible peaks larger than

10:1 (150 mM NaCl) with a major one at around 0.55 nm−1 (denoted as Hex1) and a weak shoulder at around 0.50 nm−1 (denoted as Lam1). Peak Hex1 gradually diminishes and becomes unperceivable at 60:1, as indicated by the short dotted arrow. On the contrary, the weak shoulder Lam1 continuously shifts to smaller q and intensifies at elevated NaCl concentration, eventually dominating at 30:1 and overwhelming at 60:1, illustrated by the dashed arrow. The quantitative fitting parameters, that is, the first peak position of the two phases (qHex1 and qLam1) together with the ratio between the areas of the two Gaussian peaks, are plotted in Figure 3b. In conclusion, the phase diagram of NaCl−P7(COONa)3 mixtures display (I) rectangular expansion (0:1−0.5:1), (II) denser hexagonal packing (0.75:1−15:1), (III) coexistence of hexagonal and lamellar phases (15:1−60:1), and (IV) disordered gel (over 60:1). Besides measuring the microscopic structure in reciprocal space by SAXS, TEM was carried out to further investigate the morphology in real space. Figure 4a displays long and large bundles of parallel nanotubes with the lateral width centered at about 13.3 nm in a salt-free solution. With the addition of salts, the amount of parallel-aligned nanotubes reduces without other significant changes (Figure 4b,c). At 25:1 (Figure 4d), the nanotubes are obviously shortened. At 60:1 (Figure 4e, more TEM images in Figure S7, SI), the shortening effect is inferred by the overwhelming cross sections of nanotubes in close packing, where only a few short nanotubes can be spotted in the plane (Figure 4f). The shortening of nanotubes can be explained by changing the rate of nucleation related to propagation with additional NaCl.20 The introduced salt also modifies their shapes,21 which results in a much broader distribution of lateral width compared to that without NaCl, as described in Figure S8 (SI). This is due to the fact that the nanotubes are supramolecularly assembled by weak interactions vulnerable to subtle changes in aqueous environment. The deformation eventually breaks down the nanotubes at around 80:1, demonstrated by the nanofibrils networks (Figure 4g) with the elastic modulus increasing rapidly in Figure S2b (SI). The observed order−disorder transition sequences tuned by ionic strength are unique for this colloidal system possibly as a 1188

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those nanotubes may organize into small equilibrium clusters.24,25 Such a phenomenon also originates from a decrease of short-range attraction, which serves as a driving force for aggregation.26 Above 0.75:1, with a concentration of NaCl higher than 11.4 mM, the denser packing of the hexagonal bundles can be attributed to screening of the electrostatic repulsion between charged nanotubes as well as osmotic effects as results of ion partitioning between aggregates and the aqueous environment.27 Although the two mechanisms might be concurrent at a wide range of salt concentrations, their significance varies with NaCl concentration, as reflected by the contrast between a slow increase of qHex1 below 10:1 and rocketing of qHex1 above 15:1 in Figure 3b. For a mole ratio larger than 1:1, the osmotic pressure of the solution approximates proportional to cNaCl, the concentration of NaCl. The slope of the linear relationship between the osmotic pressure, equivalent to log(cNaCl) in our case, and the internanotubes distance of hexagonal packing a provides information on the decay length of repulsion between nanotubes (Figure S6, Supporting Information).28 The obtained decay length of the repulsion differs by magnitude below and above the mole ratio of 10:1, suggesting a distinctive driving force for denser packing of the hexagonal phase. In addition, with increasing salt concentration, the Debye screening length λD decreases, indicating a shorter effective distance of electrostatic interactions.29 At a molar ratio of 10:1, λD equals 7.95 Å, smaller than the surface−surface distance of about 1 nm between nearest nanotubes obtained from SAXS and TEM (see Table S1 in the SI). Therefore, the repulsion between charged nanotubes is mostly screened at 10:1, and at a higher salt concentration, the osmotic pressure becomes the dominant factor to compress the hexagonal bundles. Coincident with the onset of osmotic effects, the lamellar structure emerges, accompanied by the distortion of nanotubes. Under the influence of osmotic pressure, nanotubes are squeezed with the cross section turned elliptical. The deformed nanotubes then tend to align shoulder to shoulder parallel to the long axis, which is further elongated with increasing salt

Figure 3. (a) The evolution from the hexagonal phase to a lamellar array measured by high-resolution SAXS with a sample-to-detector distance of about 5235 mm at intermediate and high molar ratios of NaCl, with Lam1 denoting the first peak of lamellar and Hex1 that the of hexagonal structure, as discussed in the text. (b) Evolution of q values of Hex1 (up) and Lam1 (middle) and the peak area ratio of Lam1 to Hex1 obtained by Gaussian multipeak fitting on 2m SAXS in Figure 2a. The phase diagram of the NaCl−P7(COONa)3 mixtures is summarized in the text.

result of a subtle balance between comprehensive interactions, including short-range attraction and long-range repulsion as well as osmotic pressure. Short-range attraction between charged nanotubes plays a vital role in their organization into the rectangular phase.10 At low molar ratio, additional salts will expand the rectangular lattice (Figure 2a), indicating weakened attraction. One probable interpretation is that the introduced salt inhibits dissociation of ionic terminals of P7(COONa)3, resulting in reduced charged density of nanotubes.22 The expansion will in turn reduce the attraction, which is usually regarded as short-range and decays rapidly with distance for like-charged rods.23 The consequence is that diminished attraction leads to vanishing of the rectangular structure and the nanotubes adopt a hexagonal configuration at a 0.75:1 molar ratio when repulsion dominates. The transition is accompanied by a reduction of domain size or correlation length (confirmed by the width of peaks in Figure 2a), where

Figure 4. TEM images of samples with molar ratios of NaCl to P7(COONa)3 at (a) 0:1, (b) 0.75:1, (c) 10:1, (d) 25:1, (e,f) 60:1, and (g) 80:1. All of the scale bars represent 50 nm. The samples were stained by 2% neutral phosphotungstic acid for 5 min. 1189

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concentration and gives rise to a lamellar feature with q ≈ 2π/d shifting to smaller value. Interestingly, all of these phenomena appear above a molar ratio of 10:1 NaCl, close to “physiological” solutions in vivo, where the stability of the hexagonal arrangement and robust nanotubes deliver a message for potential application in drug delivery, tissue engineering, and template systems.30−33 In conclusion, a variety of arrangements of charged supramolecular nanotubes are discovered by tuning the ionic strength in water. At low ionic strength, the like-charged attraction is depressed, resulting in expansion and eventual disappearance of highly ordered rectangular structure. At intermediate ionic strength, the nanotubes align predominately into hexagonal bundles, which are compressed due to screening of electrostatic repulsion from the like charges. Near the physiological condition, osmotic effects due to ion partitioning take over and gradually convert the hexagonal structure into lamellar arrays. Gels are formed when the lamellar component dominates, which eventually turn into a disordered network. Our study demonstrates the sensitivity of the aggregation forms of and interactions between ordered, charged 1D nanostructures to the ionic strength in aqueous environments. Furthermore, long-range ordered and oriented 1D charged nanotubes provide ideal candidates for ion conductivity materials32 as well as template materials.33

Present Address §

J.L.: Hangzhou Water Treatment Technology Development Center, National Engineering Research Center for Liquid Separation Membrane, Zhejiang, China. Author Contributions +

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work is supported by the National Natural Science Foundation of China (U1232129, 20904050, 11275205), the 973 program of MOST (2010CB934504), a Special financial grant from the Fundamental Research Funds for the Central Universities (WK2310000025), a Special financial grant from the China Postdoctoral Science Foundation 2013T60625, and the experimental fund of the Shanghai Synchrotron Radiation Facility (SSRF) and the National Synchrotron Radiation Lab (NSRL).

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EXPERIMENTAL METHODS SAXS measurements were carried out at beamline 16B1 in the Shanghai Synchrotron Radiation Facility. The X-ray wavelength was 0.124 nm, and a Mar165 CCD detector (2048 × 2048 pixels with a pixel size of 80 μm) was employed to collect twodimensional (2D) SAXS patterns. The sample-to-detector distances were 5235 and 2125 mm, respectively, to achieve high resolution or higher-order peaks located at larger q values. Fit2D software from the European Synchrotron Radiation Facility was used to analyze SAXS patterns in terms of the scattering vector q = 4π sin θ/λ, with 2θ as the scattering angle and λ as the X-ray wavelength. TEM images were measured on a JEM-2100F (JEOL, Japan) with an acceleration voltage of 200 kV. Before measurement, all the samples were stained by 2 wt % neutral phosphotungstic acid for 5 min. ASSOCIATED CONTENT

S Supporting Information *

Chemical structure of P7(COONa)3, optical morphology, frequency sweep rheology, SEM image of 60:1 sample, the details of Gaussian fitting, 1D SAXS curves of the effects of NaBr, mechanism of the transition tuned by ionic strength, and the statistic width of nanotubes from TEM images. This material is available free of charge via the Internet at http:// pubs.acs.org.

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REFERENCES

(1) Wong, G. C. L.; Pollack, L. Electrostatics of Strongly Charged Biological Polymers: Ion-Mediated Interactions and Self-Organization in Nucleic Acids and Proteins. Annu. Rev. Phys. Chem. 2010, 61, 171− 189. (2) Kornyshev, A.; Lee, D.; Leikin, S.; Wynveen, A. Structure and Interactions of Biological Helices. Rev. Mod. Phys. 2007, 79, 943−996. (3) Javid, N.; Vogtt, K.; Roy, S.; Hirst, A. R.; Hoell, A.; Hamley, I. W.; Ulijn, R. V.; Sefcik, J. Supramolecular Structures of Enzyme Clusters. J. Phys. Chem. Lett. 2011, 2, 1395−1399. (4) Schatz, G. C. Using Theory and Computation to Model Nanoscale Properties. Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 6885− 6892. (5) Ungar, G.; Liu, Y.; Zeng, X.; Percec, V.; Cho, W. D. Giant Supramolecular Liquid Crystal Lattice. Science 2003, 299, 1208−1211. (6) Wang, D. L.; Huang, Y. J.; Li, J. J.; Xu, L.; Chen, M. M.; Tao, J. J.; Li, L. B. Lyotropic Supramolecular Helical Columnar Phases Formed by C3-Symmetric and Unsymmetric Rigid Molecules. Chem.Eur. J. 2013, 19, 685−690. (7) Gorp, J. J. V.; Vekemans, J. A.; Meijer, E. W. C3-Symmetrical Supramolecular Architectures: Fibers and Organic Gels from Discotic Trisamides and Trisureas. J. Am. Chem. Soc. 2002, 124, 14759−14769. (8) Sanders, L. K.; Xian, W.; Guaqueta, C.; Strohman, M. J.; Vrasich, C. R.; Luijten, E.; Wong, G. C. L. Control of Electrostatic Interactions between F-actin and Genetically Modified Lysozyme in Aqueous Media. Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 15994−15999. (9) Young, K. L.; Jones, M. R.; Zhang, J.; Macfarlane, R. J.; EsquivelSirvent, R.; Nape, R. J.; Wu, J. S.; Schatz, G. C.; Lee, B.; Mirkin, C. A. Assembly of Reconfigurable One-Dimensional Colloidal Superlattices due to a Synergy of Fundamental Nanoscale Forces. Proc. Natl. Acad. Sci. U.S.A. 2012, 109, 2240−2245. (10) Harreis, H. M.; Kornyshev, A. A.; Likos, C. N.; Löwen, H.; Sutmann, G. Phase Behavior of Columnar DNA Assemblies. Phys. Rev. Lett. 2002, 89, 018303. (11) Sinha, P.; Szilagyi, I.; Montes Ruiz-Cabello, F. J.; Maroni, P.; Borkovec, M. Attractive Forces between Charged Colloidal Particles Induced by Multivalent Ions Revealed by Confronting Aggregation and Direct Force Measurements. J. Phys. Chem. Lett. 2013, 4, 648− 652. (12) Ha, B. Y.; Liu, A. J. Counterion-Mediated Attraction between Two Like-Charged Rods. Phys. Rev. Lett. 1997, 79, 1289−1292. (13) Kuang, Y.; Gao, Y.; Shi, J.; Lin, H. C.; Xu, B. Supramolecular Hydrogels Based on the Epitope of Potassium Ion Channels. Chem. Commun. 2011, 47, 8772−8774. (14) Härd, T. Amyloid Fibrils: Formation, Polymorphism, and Inhibition. J. Phys. Chem. Lett. 2014, 5, 607−614.

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J.T. and N.H. contributed equally to this work.

Notes

AUTHOR INFORMATION

Corresponding Authors

*E-mail: [email protected]. Tel: 0086-0551-63602081. Fax: 0086-0551-65141078 (L.L.). *E-mail: [email protected]. Tel: 0086-0551-63602077. Fax: 0086-0551-65141078 (Z.W.). 1190

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(15) Higgins, D. A.; Tran-Ba, K.-H.; Ito, T. Following Single Molecules to a Better Understanding of Self-Assembled OneDimensional Nanostructures. J. Phys. Chem. Lett. 2013, 4, 3095−3103. (16) Kohlstedt, K. L.; Olvera de la Cruz, M.; Schatz, G. C. Controlling Orientational Order in 1-D Assemblies of Multivalent Triangular Prisms. J. Phys. Chem. Lett. 2013, 4, 203−208. (17) Li, J. J.; Huang, N. D.; Wang, D. L.; Xu, L.; Huang, Y. J.; Chen, M. M.; Tao, J. J.; Pan, G. Q.; Wu, Z. Y.; Li, L. B. Highly Ordered, Ultra Long Nanofibrils via the Hierarchical Self-Assembly of Ionic Aromatic Oligoamides. Soft Matter 2013, 9, 4642−4647. (18) Zhang, F.; Skoda, M. W. A.; Jacobs, R. M. J.; Martin, R. A.; Martin, C. M.; Schreiber, F. Protein Interactions Studied by SAXS: Effect of Ionic Strength and Protein Concentration for BSA in Aqueous Solutions. J. Phys. Chem. B 2007, 111, 251−259. (19) Lo Nostro, P.; Ninham, B. W. Hofmeister Phenomena: An Update on Ion Specificity in Biology. Chem. Rev. 2012, 112, 2286− 2322. (20) Morgan, D. M.; Dong, J. J.; Jacob, J.; Lu, K.; Apkarian, R. P.; Thiyagarajan, P.; Lynn, D. G. Metal Switch for Amyloid Formation: Insight into the Structure of the Nucleus. J. Am. Chem. Soc. 2002, 124, 12644−12645. (21) Lu, K.; Guo, L.; Mehta, A. K.; Childers, W. S.; Dublin, S. N.; Skanthakumar, S.; Conticello, V. P.; Thiyagarajan, P.; Apkarian, R. P.; Lynn, D. G. Macroscale Assembly of Peptide Nanotubes. Chem. Commun. 2007, 26, 2729−2731. (22) Varghese, A.; Rajesh, R.; Vemparala, S. Aggregation of Rod-Like Polyelectrolyte Chains in the Presence of Monovalent Counterions. J. Chem. Phys. 2012, 137, 234901. (23) Jensen, N. G.; Mashl, R. J.; Bruinsma, R. F.; Gelbart, W. M. Counterion-Induced Attraction between Rigid Polyelectrolytes. Phys. Rev. Lett. 1997, 78, 2477−2480. (24) Groenewold, J.; Kegel, W. K. Anomalously Large Equilibrium Clusters of Colloids. J. Phys. Chem. B 2001, 105, 11702−11709. (25) Stradner, A. S.; Sedgwick, H.; Cardinaux, F.; Poon, W. C. K.; Egelhaaf, S. U.; Schurtenberger, P. Equilibrium Cluster Formation in Concentrated Protein Solutions and Colloids. Nature 2004, 432, 492− 495. (26) Sciortino, F.; Mossa, S.; Zaccarelli, E.; Tartaglia, P. Equilibrium Cluster Phases and Low-Density Arrested Disordered States: The Role of Short-Range Attraction and Long-Range Repulsion. Phys. Rev. Lett. 2004, 93, 055701. (27) Sanders, L. K.; Guaqueta, C.; Angelini, T. E.; Lee, J. W.; Slimmer, S. C.; Luijten, E.; Wong, G. C. L. Structure and Stability of Self-Assembled Actin−Lysozyme Complexes in Salty Water. Phys. Rev. Lett. 2005, 95, 108302. (28) Todd, B. A.; Parsegian, V. A.; Shirahata, A.; Thomas, T. J.; Rau, D. C. Attractive Forces between Cation Condensed DNA Double Helices. Biophys. J. 2008, 94, 4775−4782. (29) Strey, H. H.; Parsegian, V. A.; Podgornik, R. Equation of State for DNA Liquid Crystals: Fluctuation Enhanced Electrostatic Double Layer Repulsion. Phys. Rev. Lett. 1997, 78, 895−898. (30) Chaban, V. V.; Prezhdo, O. V. Water Boiling Inside Carbon Nanotubes: Toward Efficient Drug Release. ACS Nano 2011, 5, 5647− 5655. (31) Briggs, B. D.; Knecht, M. R. Nanotechnology Meets Biology: Peptide-Based Methods for the Fabrication of Functional Materials. J. Phys. Chem. Lett. 2012, 3, 405−418. (32) Huang, Y. J.; Cong, Y. H.; Li, J. J.; Wang, D. L.; Zhang, J. T.; Xu, L.; Li, W. L.; Li, L. B.; Pan, G. Q.; Yang, C. L. Anisotropic Ionic Conductivities in Lyotropic Supramolecular Liquid Crystals. Chem. Commun. 2009, 48, 7560−7562. (33) Sone, E. D.; Zubarev, E. R.; Stupp, S. I. Semiconductor Nanohelices Templated by Supramolecular Ribbons. Angew. Chem., Int. Ed. 2002, 41, 1706−1708.

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