Article pubs.acs.org/Biomac
Continuous Paranematic Ordering of Rigid and Semiflexible Amyloid-Fe3O4 Hybrid Fibrils in an External Magnetic Field Jianguo Zhao,† Sreenath Bolisetty,† Stéphane Isabettini,‡ Joachim Kohlbrecher,§ Jozef Adamcik,† Peter Fischer,‡ and Raffaele Mezzenga*,† †
Laboratory of Food and Soft Materials, Department of Health Sciences and Technology, ETH Zurich, 8092 Zurich, Switzerland Laboratory of Food Process Engineering, Department of Health Sciences and Technology, ETH Zurich, 8092 Zurich, Switzerland § Laboratory of Neutron Scattering and Imaging, Paul Scherrer Institute, 5232 Villigen, Switzerland ‡
S Supporting Information *
ABSTRACT: External magnetic field is a powerful approach to induce orientational order in originally disordered suspensions of magneto-responsive anisotropic particles. By small angle neutron scattering and optical birefringence measurement technology, we investigated the effect of magnetic field on the spatial ordering of hybrid amyloid fibrils with different aspect ratios (length-to-diameter) and flexibilities decorated by spherical Fe3O4 nanoparticles. A continuous paranematic ordering from an initially isotropic suspension was observed upon increasing magnetic field strength, with spatial orientation increasing with colloidal volume fraction. At constant dimensionless concentration, stiff hybrid fibrils with varying aspect ratios and volume fractions, fall on the same master curve, with equivalent degrees of ordering at identical magnetic fields. However, the semiflexible hybrid fibrils with contour length close to persistence length exhibit a lower degree of alignment. This is consistent with Khokhlov−Semenov theoretical predictions. These findings sharpen the experimental toolbox to design colloidal systems with controllable degree of orientational ordering.
1. INTRODUCTION
c = B2iso
Orientational ordering may occur in suspensions of rod-like species by increasing the volume fraction, leading the particles to undergo a first-order isotropic (I) to nematic (N) liquid crystalline phase transition.1−5 On the basis of excluded volume interaction, Onsager introduced a seminal theoretical explanation for such thermodynamic phase behavior: at low volume fraction, the particles randomly disperse in an I state, where the orientational entropy dominates the free energy; above a critical value, the suspension undergoes a phase transition into N phase, characterized by an increase of the free volume entropy and a decrease of the orientational entropy.6 A convenient variable to formulate the theory is the dimensionless concentration c, which, once reaching a critical value, allows identifying the so-called bifurcation point, i.e., the critical concentration at which a N phase starts to nucleate from an I phase:6−8 © 2016 American Chemical Society
N π N L = L2D = Φ V 4 V D
(1)
where Biso 2 is the second viral coefficient, and equals the excluded volume (π/4)L2D, N is the number density, V is the total volume of suspension, L is the contour length, D is the diameter, and Φ is the volume fraction of rod-like particles. For rigid particles, Kayser and Ravechè theoretically evaluated that when c = 4, the disordered I phase starts to transform into N phase.9 However, many rod-like particles in real systems have some degree of flexibility, resulting in remarkably different phase transitions from rigid counterparts. Motivated by this fact, Khokhlov and Semenov included flexibility into Onsager’s theory, and predicted that flexibility would enhance the stability of I phase, and that the equivalent concentration at the critical Received: April 14, 2016 Revised: June 3, 2016 Published: June 15, 2016 2555
DOI: 10.1021/acs.biomac.6b00539 Biomacromolecules 2016, 17, 2555−2561
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Figure 1. Schematic representation for the fabrication of amyloid-Fe3O4 hybrid fibrils. (A) β-Lactoglobulin protein. (B) Amyloid fibrils. (C) Fe3O4 nanoparticles. (D) Diluted hybrid fibrils randomly dispersed in the I state. (E) Hybrid fibrils exposed to a magnetic field (0.5 T) exhibit birefringence under cross-polarized light. TEM images of amyloid fibrils SI (F), Fe3O4 nanoparticles (G), and hybrid fibrils (H).
where χ∥ and χ⊥ are the components of the magnetic susceptibility tensor parallel and perpendicular to long molecular axis, respectively.20 The sign of Δχ determines how the director would be oriented in the presence of the magnetic field, where the positive sign leads to parallel orientation, and negative sign to perpendicular orientation. Due to the small anisotropy of the diamagnetic susceptibility of biological materials,21,22 a high magnetic field of at least several Tesla (T) was always required to induce the preferred orientation with the easy axis, e.g., nucleic acids,23 Pf1 bacteriophage,13 fd and m13 virus.14 In order to overcome this shortcoming, the idea of incorporating particles with high magnetic anisotropy into liquid crystals was first theoretically proposed by Brochard and de Gennes,24 and it was then experimentally determined that the new materials could be aligned in a magnetic field strength at least several hundred times smaller than those without dopants.25−27 For instance, due to the very high paramagnetic susceptibility of Fe3O4 nanoparticles, several materials with enhanced magneto-response performance were fabricated through their decoration, such as aligned selfassembled peptide nanotubes,28 red blood cells micromotors,29 and drug delivery nanodevices.30 Amyloid fibrils are an ideal liquid crystalline model system to study the orientation of semiflexible polymers in a magnetic field, especially due to their high aspect ratio.31−35 Upon heat treatment under certain conditions, amyloid fibrils could be formed in vitro through self-assembly of monomeric βlactoglobulin, the major component of whey protein found in bovine milk.36 Briefly, the globular protein at high incubation temperature and at low pH is unfolded and hydrolyzed into short peptides which self-assemble into rod-like protofilaments first and lead, with time to the formation of multistranded amyloid fibrils with varying periodicities.37−39 In our previous study, we synthesized Fe3O4 nanoparticle-modified β-lactoglobulin amyloid fibrils in situ and studied the orientational ordering of long semiflexible fibrils at different magnetic field strengths.40 Here, we prepared magneto-responsive hybrid fibrils by electrostatic complexation of β-lactoglobulin amyloid
point would shift to higher value.7,10 This is consistent with Vroege and Lekkerkerker’s theoretical calculation, who found the value of dimensionless concentration shifted to 6 at the critical point, where L is replaced by the persistence length Lp. Thus, the phase transition of semiflexible objects with LP ≤ L occurs at significantly higher volume fraction than that of stiff rods having the same aspect ratio (length-to-diameter).8 External magnetic fields applied to suspensions of magnetoresponsive rod-like particles may change the critical value of the dimensionless concentration at which the I−N transition is observed. Because of the anisotropic magnetic susceptibility tensor, the induced moment of particles in an external magnetic field leads to the alignment of a specific particle axis, inducing orientational ordering in originally disordered suspensions.11 Magnetic field induced spatial alignment was extensively examined in various systems, e.g., rod-like virus,12−14 goethite (α-FeOOH) nanorods,15−17 and anisotropic polymer chain aggregates of polystyrene.18 By incorporating a directional external field into the Onsager formalism, Khokhlov and Semenov described the liquid crystalline ordering of suspensions of rod-like and semiflexible particles as a function of external field strength.19 From the theoretical phase diagram, they deduced that increasing field strength could make the firstorder phase transition of rod-like particles occurring at progressively lower critical values of the dimensionless concentration. Furthermore, at the same field strength, suspensions of semiflexible persistent particles undergo the phase transition at much higher critical values of dimensionless concentration than that of rigid ones. Despite these important predictions, a systematic and comprehensive experimental benchmark of the expected theoretical behavior of rigid and semiflexible particles in the presence of an external field has yet to be conducted. In the investigation of the magnetic field induced orientation, one key parameter is the anisotropy of magnetic susceptibility Δχ, defined as Δχ = χ − χ⊥
(2) 2556
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Biomacromolecules fibrils of different lengths with Fe3O4 nanoparticles. This has allowed the design of different aspect ratios of the magnetoresponsive colloids, ranging from fully rigid to semiflexible fibrils, and we then studied the effects of concentration, flexibility, and aspect ratio on the liquid crystalline ordering in the presence of an external magnetic field, enabling a direct experimental benchmark of theoretical predictions.
S3D = −
∫0
π /2
I(Θ)(3 cos 2 Θ − 1) sin Θ dΘ
∫0
π /2
I(Θ) sin Θ dΘ
(3)
where I(θ) is the intensity of neutron scattering, θ is the azimuthal angle. 2.6. Birefringence Measurement. The optical birefringence measurement on the basis of phase modulation technique was performed following the procedure in ref 42. In Brief, a sample cuvette was placed in the middle of superconducting magnet (Cryogenic, UK) with adjustable field strength from 0 to 5.5 T, in a direction perpendicular to the laser beam. The light from a diode laser (Newport, Irvine, CA) was directed with nonpolarizing mirrors (Newport, Irvine, CA) through a first polarizer (Newport, Irvine, CA) and a photoelastic modulator (Hinds instruments, USA) before going through the sample. It then went through a second polarizer orientated 90° relative to the first one before being detected by a photo detector (Hinds instruments, USA). Two lock-in amplifiers (SRS, Sunnyvale, USA) were used to detect the harmonic I1ω and I2ω of the ac signal. The birefringence Δn was calculated by
2. EXPERIMENTAL SECTION 2.1. Materials. β-Lactoglobulin protein was purchased from TU Munich. Anionic Fe3O4 nanoparticles were purchased from Ferrotec Corporation (EMG-707). Hydrochloric acid (35 wt % solution in D2O, 99 atom % D) and sodium deuteroxide (30 wt % solution in D2O, 99+ atom % D) were purchased from Sigma-Aldrich. 2.2. Sample Preparation. β-Lactoglobulin protein was purified according to the protocol in ref 31. Briefly, βlactoglobulin solution was centrifuged and dialyzed against Milli-Q water, and then freeze-dried for storage. The mature amyloid fibrils (referred in what follows as SI) were obtained after heat treatment of β-lactoglobulin D 2O solution. Consequently, fibrils were diluted and mixed with desired content of Fe3O4 nanoparticles at pD 3, followed by incubation at 60 °C for 15 min and equilibration at 4 °C overnight. The detailed procedures are shown in section 3 (Figure 1). To prepare hybrid fibrils with a series of varying aspect ratio, ranging from fully rigid (L ≪ Lp) to semiflexible (L ∼ Lp), mature fibrils SI were homogenized using a benchtop homogenizer (Kinematica GmbH, Switzerland) at various shearing strengths and time duration, prior to the mixing procedure with Fe3O4 nanoparticles. 2.3. Atomic Force Microscopy (AFM). Fibril solutions were diluted into a final concentration of 0.1 wt % by pD 2 D2O and then 20 μL of solution were deposited onto freshly cleaved mica, incubated for 2 min, rinsed with Milli-Q water and dried with compressed air flow. AFM experiments were performed by using a MultiMode VIII Scanning Probe Microscope (Bruker, USA) covered with an acoustic hood to minimize noise. AFM images were acquired in tapping mode under ambient conditions. The contour length of amyloid fibrils and their quantitative length and height distribution were obtained by using Fiber App, an open source tracking and analysis software written in MATLAB.41 2.4. Transmission Electron Microscopy (TEM). 4 μL of diluted sample were placed on a carbon-coated copper grid (Quantifoil, Germany), and then rinsed 2 times by Milli-Q water after 60 s adsorption. Following each step, the excess solution was removed by a filter paper. Then, the dried grid was examined using TEM (FEI, model Morgagni, NL) operated at 100 kV. 2.5. Small Angle Neutron Scattering (SANS). In order to quantify the spatial ordering of hybrid fibrils, SANS was carried out at SANS-I beamline at the Paul Scherrer Institute (PSI, Villigen, Switzerland), equipped with a superconductive magnet with a horizontal field mounted perpendicular or parallel to the neutron beam. Magnetic fields ranged from 0 to 5 T. The neutron wavelength was 0.8 Å, and detection distance was 6, 11, and 18 m, corresponding to a q range covering from 0.005 to 0.3 Å−1. The samples were equilibrated for 20 min in the presence of a magnetic field before measurements. The scattered intensity versus azimuthal angle spectra was used to calculate the 3D order parameter S3D:40
Δn = −
δλ 2πd
(4)
where λ is the wavelength of laser (635 nm), d is the sample thickness (0.2 cm), and δ is dimensionless parameter given by ⎛ I1ωJ (A 0) ⎞ 2 ⎟⎟ δ = arctan⎜⎜ I ω J ⎝ 2 1 (A 0 ) ⎠
(5)
where A0 is the amplitude of photoelastic modulator (2.405 rad), and J1(A0) and J2(A0) are Bessel functions, with J1(2.405) = 0.5191 and J2(2.405) = 0.4307, respectively.
3. RESULTS AND DISCUSSION We fabricated magneto-responsive hybrid amyloid fibrils as illustrated in Figure 1. In order to have a good contrast for SANS measurements, 2 wt % solution was prepared by dissolving the β-lactoglobulin protein powder in D2O and adjusted to pD 2 with 1 M DCl solution (Figure 1A). Positively charged, semiflexible amyloid fibrils were obtained after 5 h incubation at 90 °C (Figure 1B). Then, we diluted the fibrils suspensions below I-N boundary (Figure S1), and changed into pD 3 prior to mixing with negatively charged Fe3O4 spherical nanoparticles (Figure 1C). Finally, hybrid fibrils were fabricated after incubation at 60 °C for 15 min and equilibration at 4 °C overnight as a result of electrostatic complexation. When monitored between cross-polarizers, a dark I phase was observed (Figure 1D). As soon as a magnetic field was applied, the magneto-responsive Fe3O4 nanoparticles drove the orientational ordering of the hybrid fibrils. Consequently, the suspension turned into birefringent (Figure 1E), becoming what is sometimes referred as a “paranematic” (pN) phase.11,16,43 Figure 1F−H shows TEM images of long semiflexible amyloid fibrils, and Fe3O4 nanoparticles before and after mixing, respectively. These hybrid fibrils are a unique model for studying the liquid crystalline behavior in a magnetic field, due to their combination of flexibility, high aspect ratio, and outstanding magneto-responsiveness. AFM images and the statistic size distribution of the amyloid fibrils before and after the shearing process needed to decrease their contour length (and aspect ratio) are presented in Figure 2557
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Figure 2. AFM images of amyloid fibrils having different dimensions prepared at various shearing strengths and duration. Mean contour lengths ⟨L⟩ and heights ⟨D⟩ (in nm) of SI−SIV are provided as insets.
2 and S2. The persistence length of amyloid fibrils in D2O is approximately 1.5 μm, according to Adamcik et al.44. Original long fibrils SI display indeed semiflexible behavior because their contour length is close to the persistence length. After the shearing treatment, fibrils undergo a significant decrease in contour length, and thus a decrease in flexibility (fibrils SII− SIV). Thus, SI fibrils are classified as semiflexible, while fibrils SII−SIV as rigid. Moreover, the length distribution of fibrils got significantly narrowed after the shearing procedure (Figure S2A). We also observed a slight reduction in average height distribution (Figure S2B) after homogenization, which may be due to the decrease of multistranded versus single stranded fibrils as a consequence of shearing.44 In the hybrid suspension, most of the neutron scattering intensity is attributed to amyloid fibrils, because the nuclear scattering length of Fe3O4 is comparable to that of the solvent D2O (Table S1 and Figure S3).45 The hybrid fibrils containing 0.333 wt % amyloid fibrils SIII and 0.220 wt % Fe3O4 particles showed no sign of ordering before exposure to a magnetic field, as evidenced by the isotropic neutron scattering pattern in Figure 3A. As soon as a 0.1 T magnetic field (data not shown) was applied perpendicular to the neutron beam, a remarkable anisotropic scattering pattern was observed, which indicated that the hybrid fibrils started to be oriented in a direction parallel to the magnetic field. Anisotropy was further increased before reaching saturation in alignment at the field strength of 0.5 T. Apparently, the large magnetic susceptibility of Fe3O4 nanoparticles present in the hybrid allows for an asymptotic saturated orientation at magnetic field strengths tens of times smaller than what would be required to align rod-like biological particles.14,46 The suspension relaxed back to the original I state after magnetic field was off, confirming the reversible nature of the process, in agreement with analogous systems in low magnetic fields.16 These observations were confirmed by plotting the scattered intensity as a function of the azimuthal angle in Figure 3B, in which the evolution of anisotropy at
Figure 3. (A) 2D SANS profiles for hybrid fibrils (0.333 wt % amyloid fibrils SIII, 0.220 wt % Fe3O4 nanoparticles) in the presence of a magnetic field perpendicular to the neutron beam, and (B) the intensity as a function of the azimuthal angle at varied magnetic field strengths, radially integrated in a q range from 0.005 to 0.025 Å−1. For the sake of clarity, intensity values have been shifted; the two series at 0 T indicate the initial and final state of the systems, prior to and after exposure to the magnetic field. (C) Scattering intensities measured in a magnetic field parallel to the neutron beam. The inset is the 2D SANS profile acquired at 5 T.
different magnetic fields can be easily followed. When the magnetic field was applied parallel to the beam, the intensity increased and a broad peak emerged at q = 0.04 Å−1, as expected for a paramagnetic alignment with director parallel to the magnetic (and neutron beam) direction, and with a characteristic interfibril distance of 157 Å (Figure 3C), similar to what is observed in concentrated suspensions of DNA in zero-field,47 and dilute cobalt nanorods in a liquid crystalline polysiloxanes matrix in the presence of a magnetic field.27 The effect of concentration on spatial alignment of hybrid fibrils SIII at a series of increasing magnetic field strengths is shown in Figure 4. At low field strengths, both the 3D order parameter and optical birefringence signal of the concentrated hybrid fibrils SIII showed a high sensitivity to the external magnetic field. The birefringence at the saturated regime rose with increasing concentration, as intuitively expected. Similarly, 2558
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dimensionless concentration,7,10 in agreement with simulation48,49 and experimental results.50,51 It is worth stressing further here that we have taken in all cases the contour length to calculate the aspect ratio, as this is comparable (fibrils SI) or lower (fibrils SII−SIV) than the persistence length of the fibrils, dividing the system in two main classes: semiflexible and rigid fibrils. We examined the phase behavior of the hybrid fibril colloidal suspensions at fixed dimensionless concentration ΦL/D (Table S2 and S3). When the magnetic field strength was increased, both the 3D order parameter and the birefringence signal of all the rigid hybrid fibrils SII−IV were enhanced, as shown in Figure 6A and B. What’s more, and in both cases, the curves for
Figure 4. Evolution of the 3D order parameter (A) and optical birefringence (B) for hybrid fibrils SIII as a function of magnetic field strength.
the spatial orientation induced by the magnetic field was highly concentration-dependent. The structural aspect ratio is the other key parameter for ordering of rod-like colloidal objects. The aspect ratio of hybrid fibrils SI is more than twice that of SIII (Figure 2). However, the 3D order parameter as well as the optical birefringence signal of the latter at the saturated regime was higher than that of SI at identical hybrid fibril concentration and magnetic field strength (Figure 5). These results could be explained in terms of the semiflexible nature of SI compared to the rigid form of SIII. Khokhlov and Semenov theoretically explained that in the limit of zero-field, a system of “persistent”, that is, semiflexible chains reaches the N phase at much larger critical values of the
Figure 6. (A) 3D order parameter of stiff hybrid fibrils as a function of magnetic field at constant dimensionless concentration (0.886). The exponential curve fitting (dark red color) was calculated according to S3D = A(1 − e−B/B0), where A is the asymptotic order at infinite field, B is the magnetic field, and B0 is a characteristic relaxation constant. Birefringence signal of stiff (B) and semiflexible (C) hybrid fibrils at constant dimensionless concentration (0.643).
all three hybrid fibrils showed comparable evolution over the saturated regime (>0.1 T), by falling on the same master curve. However, the optical birefringence signal of hybrid fibrils SI (Figure 6C) was almost 3-fold lower than that of SII−IV for equivalent dimensionless concentration (Figure 6B), consistent with the findings presented in Figure 5 and in line with expectations from the Khokhlov−Semenov theory.19 These results confirm, for the first time, the crucial role played by the flexibility of anisotropic colloidal particles in the ordering induced by an external magnetic field and provide an important benchmark for the theoretical predictions of Khokhlov and Semenov in the zero-field limit.7,10 The comparison with the
Figure 5. Comparison of the 3D order parameter (A) and optical birefringence (B) between hybrid fibrils SI and SIII at various magnetic field strengths and identical concentration. 2559
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Biomacromolecules nonzero field limit is much less straightforward. First, we observe that the exact dimensionless field used by Khokhlov and Semenov cannot be extracted here since the single particle orientation cannot be resolved and the results presented here are based on the collective orientation of the fibrils. Second, it is worth mentioning that the I−N transition in the case of Khokhlov-Semenov theory is of first-order, whereas here a continuous pN ordering is observed. The continuous transition from I to pN according to Khokhlov−Semenov theory is expected only above a critical value of the magnetic field, but in our system, it occurs at vanishingly small magnetic fields. Lastly, for rigid and semiflexible fibrils, no N phase should be observed according to Khokhlov and Semenov for dimensionless concentrations lower than 3 and 9, respectively, whereas in the present case a pN ordering can be observed at dimensionless concentrations below 1. In the present work, the saturated 3D order parameter of the pN phase of the hybrid fibrils suspension is significantly lower than that of N phases at the transition point in other anisotropic colloidal systems.51,52 We believe that this stems from the fact that, in our work, the concentration of fibrils is much lower than the critical value at which the pure N phase is observed (Figure S1), so that the orientation observed for the saturated pN phase under an external magnetic field remains substantially lower than other cases where both field and concentration effects sum up.53,54 Nonetheless, these results allow for the first time since the seminal work of Khokhlov and Semenov one to disentangle the effect of semiflexibility of the anisotropic particles from the other variables in the development of orientational order.
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AUTHOR INFORMATION
Corresponding Author
*E-mail: raff
[email protected]. Notes
The authors declare no competing financial interest.
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ACKNOWLEDGMENTS The authors acknowledge Dr. Jorge Gavilano (SANS I, PSI, Villigen, Switzerland) for assistance with the SANS experiments, and Electron Microscopy of ETH Zürich (EMEZ) for support of TEM. Jianguo Zhao would thank the China Scholarship Council for fellowship during his Ph.D. study.
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REFERENCES
(1) Bawden, F. C.; Pirie, N. W.; Bernal, J. D.; Fankuchen, I. Nature 1936, 138, 1051−1052. (2) Rill, R. L.; Strzelecka, T. E.; Davidson, M. W.; Vanwinkle, D. H. Physica A 1991, 176, 87−116. (3) Tang, J. X.; Fraden, S. Liq. Cryst. 1995, 19, 459−467. (4) Buining, P. A.; Lekkerkerker, H. N. W. J. Phys. Chem. 1993, 97, 11510−11516. (5) Viamontes, J.; Oakes, P. W.; Tang, J. X. Phys. Rev. Lett. 2006, 97, 118103. (6) Onsager, L. Ann. N. Y. Acad. Sci. 1949, 51, 627−659. (7) Khokhlov, A. R.; Semenov, A. N. Physica A 1981, 108, 546−556. (8) Vroege, G. J.; Lekkerkerker, H. N. W. Rep. Prog. Phys. 1992, 55, 1241−1309. (9) Kayser, R. F.; Raveche, H. J. Phys. Rev. A: At., Mol., Opt. Phys. 1978, 17, 2067−2072. (10) Khokhlov, A. R.; Semenov, A. N. Physica A 1982, 112, 605−614. (11) Leferink Op Reinink, A. B. G. M.; van den Pol, E.; Petukhov, A. V.; Vroege, G. J.; Lekkerkerker, H. N. W. Eur. Phys. J.: Spec. Top. 2013, 222, 3053−3069. (12) Fraden, S.; Hurd, A. J.; Meyer, R. B.; Cahoon, M.; Caspar, D. L. D. J. Phys. (Paris) 1985, 46, 85−113. (13) Torbet, J.; Maret, G. J. Mol. Biol. 1979, 134, 843−845. (14) Tang, J. X.; Fraden, S. Phys. Rev. Lett. 1993, 71, 3509−3512. (15) Lemaire, B. J.; Davidson, P.; Ferre, J.; Jamet, J. P.; Panine, P.; Dozov, I.; Jolivet, J. P. Phys. Rev. Lett. 2002, 88, 125507. (16) Lemaire, B. J.; Davidson, P.; Ferre, J.; Jamet, J. P.; Petermann, D.; Panine, P.; Dozov, I.; Stoenescu, D.; Jolivet, J. P. Faraday Discuss. 2005, 128, 271−283. (17) Wensink, H. H.; Vroege, G. J. Phys. Rev. E 2005, 72, 031708. (18) Meeten, G. H. Polymer 1974, 15, 187−189. (19) Khokhlov, A. R.; Semenov, A. N. Macromolecules 1982, 15, 1272−1277. (20) Binnemans, K.; Gorller-Walrand, C. Chem. Rev. 2002, 102, 2303−2345. (21) Jackson, R. Ann. Sci. 2015, 72, 435−489. (22) Worcester, D. L. Proc. Natl. Acad. Sci. U. S. A. 1978, 75, 5475− 5477. (23) Maret, G.; Schickfus, M. V.; Mayer, A.; Dransfeld, K. Phys. Rev. Lett. 1975, 35, 397−400. (24) Brochard, F.; de Gennes, P. G. J. Phys. (Paris) 1970, 31, 691− 708. (25) Chen, S. H.; Amer, N. M. Phys. Rev. Lett. 1983, 51, 2298−2301. (26) Beck, P.; Liebi, M.; Kohlbrecher, J.; Ishikawa, T.; Ruegger, H.; Fischer, P.; Walde, P.; Windhab, E. Langmuir 2010, 26, 5382−5387.
4. CONCLUSIONS By loading Fe3O4 nanoparticles with amyloid fibrils, we fabricated hybrid fibrils having high orientational magnetoresponse, and systematically investigated the ordering induced by a dipole-type magnetic field at various field strengths, concentrations, and aspect ratios. The order observed in all cases was of pN type, with a continuous increase of order parameter and birefringence from zero to a saturation plateau level upon increasing the magnetic field strength. When varying the aspect ratio and volume fraction at constant dimensionless concentration and magnetic field strength, the stiff hybrid fibrils displayed identical degrees of orientation falling on a single master curve for both order and birefringence curves versus field intensity. On the other hand, semiflexible hybrid fibrils with the same dimensionless concentration reached lower orientation levels compared to the rigid counterparts as a consequence of their semiflexible nature. To the best of our knowledge, this is the first direct experimental proof of the Khokhlov−Semenov theory in the nonzero-field limit regime, which predicts that the ordered phase for anisotropic colloidal particles is highly restricted by the semiflexible nature. Due to the ubiquitous role of external fields, such as magnetic, electric and flow fields, in ordering liquid crystalline systems of anisotropic particles with and without semiflexible nature, we believe these results advance our understanding of field-induced order in fibrous systems and may pave the road to optimal design of functional materials with directional features.
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Additional information includes amyloid fibrils SI−IV suspensions observed between cross-polarizers, size distribution of amyloid fibrils SI−IV, SANS intensity of Fe3O4 nanoparticles as a function of the azimuthal angle, comparison of scattering length density of D2O and Fe3O4, and details of hybrid fibrils investigated for SANS and birefringence measurements (PDF)
ASSOCIATED CONTENT
S Supporting Information *
The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.biomac.6b00539. 2560
DOI: 10.1021/acs.biomac.6b00539 Biomacromolecules 2016, 17, 2555−2561
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Biomacromolecules (27) Riou, O.; Lonetti, B.; Davidson, P.; Tan, R. P.; Cormary, B.; Mingotaud, A. F.; Di Cola, E.; Respaud, M.; Chaudret, B.; Soulantica, K.; Mauzac, M. J. Phys. Chem. B 2014, 118, 3218−3225. (28) Reches, M.; Gazit, E. Nat. Nanotechnol. 2006, 1, 195−200. (29) Wu, Z. G.; Li, T. L.; Li, J. X.; Gao, W.; Xu, T. L.; Christianson, C.; Gao, W. W.; Galarnyk, M.; He, Q.; Zhang, L. F.; Wang, J. ACS Nano 2014, 8, 12041−12048. (30) Hu, S. H.; Kuo, K. T.; Tung, W. L.; Liu, D. M.; Chen, S. Y. Adv. Funct. Mater. 2009, 19, 3396−3403. (31) Jung, J. M.; Mezzenga, R. Langmuir 2010, 26, 504−514. (32) Mezzenga, R.; Jung, J. M.; Adamcik, J. Langmuir 2010, 26, 10401−10405. (33) Jordens, S.; Isa, L.; Usov, I.; Mezzenga, R. Nat. Commun. 2013, 4, 1917. (34) Zhao, J. G.; Li, C. X.; Mezzenga, R. J. Phys.: Condens. Matter 2014, 26, 464112. (35) Zhao, J. G.; Bolisetty, S.; Adamcik, J.; Han, J.; Fernandez-Ronco, M. P.; Mezzenga, R. Langmuir 2016, 32, 2492−2499. (36) Jung, J. M.; Savin, G.; Pouzot, M.; Schmitt, C.; Mezzenga, R. Biomacromolecules 2008, 9, 2477−2486. (37) Bolisetty, S.; Adamcik, J.; Mezzenga, R. Soft Matter 2011, 7, 493−499. (38) Adamcik, J.; Mezzenga, R. Macromolecules 2012, 45, 1137− 1150. (39) Mezzenga, R.; Fischer, P. Rep. Prog. Phys. 2013, 76, 046601. (40) Bolisetty, S.; Vallooran, J. J.; Adamcik, J.; Mezzenga, R. ACS Nano 2013, 7, 6146−6155. (41) Usov, I.; Mezzenga, R. Macromolecules 2015, 48, 1269−1280. (42) Liebi, M.; Kohlbrecher, J.; Ishikawa, T.; Fischer, P.; Walde, P.; Windhab, E. J. Langmuir 2012, 28, 10905−10915. (43) van der Beek, D.; Davidson, P.; Wensink, H. H.; Vroege, G. J.; Lekkerkerker, H. N. W. Phys. Rev. E 2008, 77, 031708. (44) Adamcik, J.; Jung, J. M.; Flakowski, J.; De Los Rios, P.; Dietler, G.; Mezzenga, R. Nat. Nanotechnol. 2010, 5, 423−428. (45) Sears, V. F. Neutron News 1992, 3, 26−37. (46) Maret, G.; Dransfeld, K. Top. Appl. Phys. 1985, 57, 143−204. (47) Livolant, F.; Leforestier, A. Prog. Polym. Sci. 1996, 21, 1115− 1164. (48) Dijkstra, M.; Frenkel, D. Phys. Rev. E: Stat. Phys., Plasmas, Fluids, Relat. Interdiscip. Top. 1995, 51, 5891−5898. (49) Chen, Z. Y. Macromolecules 1993, 26, 3419−3423. (50) Odijk, T. Macromolecules 1986, 19, 2313−2329. (51) Purdy, K. R.; Fraden, S. Phys. Rev. E 2004, 70, 061703. (52) Belamie, E.; Davidson, P.; Giraud-Guille, M. M. J. Phys. Chem. B 2004, 108, 14991−15000. (53) Lemaire, B. J.; Davidson, P.; Ferre, J.; Jamet, J. P.; Panine, P.; Dozov, I.; Jolivet, J. P. Phys. Rev. Lett. 2002, 88, 125507. (54) van der Beek, D.; Petukhov, A. V.; Davidson, P.; Ferre, J.; Jamet, J. P.; Wensink, H. H.; Vroege, G. J.; Bras, W.; Lekkerkerker, H. N. W. Phys. Rev. E 2006, 73, 041402.
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DOI: 10.1021/acs.biomac.6b00539 Biomacromolecules 2016, 17, 2555−2561
