Columnar Liquid Crystals Self-Assembled by Minimalistic Peptides for

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Columnar Liquid Crystals Self-Assembled by Minimalistic Peptides for Chiral Sensing and Synthesis of Ordered Mesoporous Silica Yuefei Wang, Wei Qi, Jiahui Wang, Qing Li, Xuejiao Yang, Jiaxing Zhang, Xingwei Liu, Renliang Huang, Mengfan Wang, Rongxin Su, and Zhimin He Chem. Mater., Just Accepted Manuscript • DOI: 10.1021/acs.chemmater.8b03496 • Publication Date (Web): 15 Oct 2018 Downloaded from http://pubs.acs.org on October 15, 2018

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Chemistry of Materials

Columnar Liquid Crystals Self-Assembled by Minimalistic Peptides for Chiral Sensing and Synthesis of Ordered Mesoporous Silica Yuefei Wang,†,ǁ Wei Qi,†,§,ǁ,* Jiahui Wang,† Qing Li,† Xuejiao Yang,† Jiaxing Zhang,† Xingwei Liu,† Renliang Huang,‡ Mengfan Wang, †,ǁ Rongxin Su,†,§,ǁ Zhimin He† †

State Key Laboratory of Chemical Engineering, School of Chemical Engineering and Technology, Tianjin University, Tianjin 300072, P. R. China. ‡ School of Environmental Science and Engineering, Tianjin University, Tianjin 300072, P. R. China. § Collaborative Innovation Center of Chemical Science and Engineering (Tianjin), Tianjin 300072, P. R. China. ǁ Tianjin Key Laboratory of Membrane Science and Desalination Technology, Tianjin 300072, P. R. China. ABSTRACT: We report the spontaneous formation of lyotropic liquid crystals from the self-assembly of a series of minimalistic peptides. The highly charged peptides could self-assemble into rigid helical nanofilaments in water and spontaneously order into hexagonal or “prehexagonal” liquid-crystalline phases with interfilament separations of up to 240 Å. The formation of liquid crystals from the self-assembly of such simple peptides is not only dictated by the concentration and pH, but also by the amino acid sequence of the peptides. Peptides containing the rigid Phe-Phe (FF) segment showed much higher propensity to form a liquid crystalline phase with a long-range order. Moreover, owing to the intrinsic chirality of the peptides, the self-assembled birefringent liquid crystals could serve as sensing elements for the visual discrimination of chiral species and as templates for the biomimetic synthesis of mesoporous silica with ordered cavities. The results offer new opportunities for the design of peptide liquid crystals which are potentially applicable in sensing, biomedicine, and material science.

n

INTRODUCTION

Liquid crystals are unique materials with self-healing, adaptive, and stimuli responsiveness, that have great potential for a wide range of applications.1,2 In biology, the liquid-crystalline phase of biopolymers (e.g., DNA, actins, and microtubules) play crucial roles in sustaining a wide range of important biological processes such as cell division, protein transport, and DNA package. Inspired by this, liquid crystals from synthetic biopolymers has been an active area of research in the field of chemistry and materials science.3-5 Polypeptides with helical conformation or global amphiphilicity could assemble into rigid 1D nanostructures in solution, leading to the formation of various liquid crystalline phase,6-15 as a result of the excluded volume interactions (Onsager theory).16 For example, Hamley et al reported the lytropic liquid crystalline behavior of a series of amyloid peptide derivatives17-19 and demonstrated that the poly(ethylene glycol)-peptide conjugates could form nematic and columnar phases in water.20-22 Mezzenga et al reported the discovery of cholesteric phases in amyloids, using βlactoglobulin fibrils shorten by shear stresses, which exhibit unprecedented structural complexity.23 Abbott and Gellman et al demonstrated the liquid crystalline formation from a series of well-designed β-polypeptides, and the phase behavior could be tailored by changing the peptide sequence and modifications.10-12 These peptide liquid crystals are appealing due to their biocompatibility and structural diversity, which could be used to guide the alignment of cells,14 or serve as templates for the fabrication of highly ordered materials.24-26 However, owing to the complex evolution of noncovalent forces, the liquid crystalline formation and their phase behaviors from selfassembly of much simpler peptides remain largely unexplored.

Diphenylalanine peptide (L-Phe-L-Phe, FF), which is extracted from the Alzheimer’s β-amyloid polypeptide, has attracted considerable attention because of its biological significance, chemical simplicity, and excellent capacity to form a wide range of functional nanostructures.27-31 Intriguingly, Han et al. reported that self-assembled FF nanowires could spontaneously form colloidal liquid crystalline phases in carbon disulfide.32 Moreover, recent work by Adams et al. showed that FF derivatives such as naphthalene-FF could form liquid crystalline worm-like micelles in water, which further formed rigid hydrogels upon the addition of salt or upon heat and cooling treatment.33-35 These results indicate that the FF peptide might serve as a versatile motif for the design of highly ordered peptide liquid crystals with new functions, owing to the strong π-π stacking between the side chain of FF and the capability of the peptide to form rigid, elongated structures that are essential for the formation of a liquid crystal.16,27,36,37 In this work, we studied the lyotropic liquid crystalline behavior of a series of minimalistic peptides using small-angle X-ray scattering and molecular dynamic simulations. The results suggest that the amino acid sequence not only determines the short-range interactions between the peptides, but also dictates the spontaneous crystallization in networks of the selfassembled nanofilaments. A colloidal liquid crystalline phase was observed for all the peptides consisting of a rigid FF segment as well as a repulsive terminus. The long-range order and optical anisotropy of the liquid crystalline peptides could transform chemical binding events into amplified optical signals that could be easily observed, even with naked eye. This allowed us to develop a feasible method for visually discriminating chiral diamines based on stereoselective bundling of the self-assembled nanofilaments. Moreover, the liquid crystalline peptide nanofilaments could also serve as templates for the

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Scheme 1. (a) Molecular structure of the peptide amphiphiles. (b) Schematic illustration of the hierarchical chiral selfassembly of the peptides into highly charged nanofilaments that spontaneously form a hexagonal liquid-crystalline phase with a large d-spacing. biomimetic synthesis of well-defined mesoporous silica with ordered cavities.

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RESULTS AND DISCUSSION

Self-assembly of highly charged nanofilaments that spontaneously order into liquid crystals We first studied the liquid-crystalline behavior of a wellknown archetypical dipeptide, Fmoc-diphenylalanine (FmocFF), which has been shown to be an excellent hydrogelator.3840 The Fmoc-FF peptide was dissolved in a 50 mM Tris-HCl buffer solution, to obtain transparent viscous solutions that were birefringent at or above 2 mM and pH > 7.55 (Figure S1, S2, S3). Using a polarized optical microscope (POM), we observed the schlieren texture of the peptide solutions (20 mM Fmoc-FF, 50 mM Tris-HCl, pH 8.8, 20 °C), which is the characteristic of a nematic liquid-crystalline phase (Figure S1b). Intriguingly, banded textures easily formed after gentle shearing of the liquids (Figure S1c). Such banded textures with lines perpendicular to the direction of the shear force are typically observed for liquid-crystalline polymers. Thus, the Fmoc-FF peptides probably formed lyotropic polymeric assemblies in Tris-HCl buffer solutions at high concentrations.41 Similar optical behaviors were also observed for other FF derivatives such as Fmoc-Phe-Phe-Ser (Fmoc-FFS), Fmoc-PhePhe-Asp (Fmoc-FFD), and Fmoc-Phe-Phe-Glu (Fmoc-FFE) peptide solutions (Figure S4, S5). Transmission electron microscopy (TEM), wide-angle X-ray diffraction (WAXD), and circular dichroism (CD) spectroscopy were used to probe the structures formed in the peptide solutions. As shown in Figure 1 a–d, the peptides self-assembled into high-aspect-ratio nano-

filaments with a diameter of ~3.3 nm for Fmoc-FF and ~4.2 nm for Fmoc-FFS, Fmoc-FFD, and Fmoc-FFE. In situ WAXS analysis revealed that the peptide solutions yield scattering peaks at 4.7 Å for Fmoc-FF and 4.6 Å for Fmoc-FFE (Figure 1e and f), which could be attributed to the periodic spacing between the peptide segments within the β-sheet secondary structure.42-44 A weak diffraction peak at 3.6 Å for Fmoc-FF and at 3.8 Å for Fmoc-FFE, respectively, were also observed. Despite slight variations at ~3.7 Å, these reflections could be attributed the π-π stacking distances between the aromatic side chains and the Fmoc protecting groups.42 The CD spectra of the diluted peptide solutions show signature positive bands at 193-195 nm and negative bands at 206-215 nm in the peptide region (Figure 1g), which might be attributed to the β-sheet secondary structures.45 The Cotton effects corresponding to the aromatic (255, 270 and 278 nm) and fluorenyl adsorption (302 nm) suggest the chiral organization of the peptides via π-π stacking interactions within the self-assembled nanofilaments.46 It should be noted that, to eliminate the interference of linear dichroism on CD signal (Figure S6), the peptide solutions for CD analysis was diluted to 2 mM for Fmoc-FF and 3 mM for Fmoc-FFS, Fmoc-FFD and FmocFFE, respectively. Fourier-transform infrared spectra (FTIR) of the peptide solutions show a major peak at 1636 cm−1 for Fmoc-FF and 1632 cm−1 for Fmoc-FFS, Fmoc-FFD, and Fmoc-FFE (Figure 1h). Despite slight deviations in the peak positions, the adsorption peaks in this range could be attributed to β-sheets,47 which is consistent with the results of WAXS and CD. Moreover, the weaker peaks at ~1690 cm−1 might have arisen from the adsorption of the stacked carbamate group in Fmoc-peptides as reported by Ulijn et al.47


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Figure 2. Dynamic simulation models representing the chiral selfassembly of the negatively charged Fmoc-FF (a–b) and FmocFFE (c–d) peptides at 100 ns. The initial packing model was constructed based on the single-crystal structure reported by Adams et al.42

Figure 1. (a–d) Representative TEM images of the self-assembled peptide nanofilaments derived from Fmoc-FF, Fmoc-FFS, FmocFFD, and Fmoc-FFE, respectively. (e) Synchrotron WAXS pattern of a 2.46 wt% Fmoc-FF peptide solution (50 mM Tris-HCl, pH 8.8) at 20 °C. The red arrows denote the alignment direction. (f) In situ WAXS data showing the scattered intensity versus the scattering vector q (log−log plot) for the Fmoc-FF and Fmoc-FFE peptide solutions. (g–h) CD and FTIR spectra of the peptide solutions.

Possible molecular packing during the fibrilization of Fmoc-FF has been deduced in the pioneering work by Ulijn et al.; they showed that the peptides are arranged in anti-parallel interlocked β-sheets.40 However, in Tris buffer solutions, peptides such as Fmoc-FF and Fmoc-FFE should carry strong negative charges owing to the higher pKa of the Tris counterions. The strong electrostatic repulsions could alter the selfassembling behavior of the peptides, which should in principle self-assemble in a manner similar to that of a peptide amphiphile.48 Therefore, possible packing models considering electrostatic interactions are proposed for the individual selfassembly of Fmoc-FF and Fmoc-FFE. On the basis of the

single-crystal structure reported by Adams et al.42 and our results of WAXS, CD and FTIR analyses (Figure 1f-h), we built two initial packing models, as shown in Figure S7. Both the models are composed of four parallel β-sheets, in which the Fmoc groups are packed on the inside of the cylinder and serve as the hydrophobic core and four strands of hydrophilic negatively charged carboxylate groups run along the outside of the cylinder. The initial crystalline architectures were not stable owing to the strong repulsive electrostatic interactions between the peptides. MD simulations were used to optimize the geometry. As shown in Figure 2, the cylinders spontaneously twisted anti-clockwise after 100 ns of calculations, yielding stable right-handed filaments with diameters of 3.3 nm and 4.2 nm for Fmoc-FF and Fmoc-FFE, respectively. The diameters of the optimized structures shown in Figure 2b and d are consistent with the size determined by TEM (Figure 1a and d). Although the single crystal structure might be different from the structures formed in solutions, the optimized structure of the chiral nanofilaments agree well with the results of WAXS, TEM, CD and FTIR analyses, thus representing possible models for the self-assembly of highly charged peptides. Small angle X-ray scattering of the peptide solutions and the corresponding phase diagram. We used solution-based small-angle X-ray scattering (SAXS) measurements to explore the liquid-like ordering in the peptide solutions. As shown in Figure 3a, the 2D SAXS pattern of a 0.5 wt% peptide solution produces an elliptical diffusive signal with a large axial ratio, indicating the orientational order of the peptide solution. Intriguingly, with



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Figure 3. (a) 2D SAXS pattern of the peptide solutions at various concentrations (100 mM Tris-HCl, pH 8.8, 20 °C). (b) In situ SAXS data showing the background-subtracted scattered intensity versus the scattering vector q (log−log plot). The data sets are offset vertically for clarity. (c) Center-to-center spacing between the nanofilaments as a function of the peptide concentration. The insets show the phase transition of the peptide nanofilaments from a nematic liquid-crystalline phase to a highly ordered hexagonal one.

increasing peptide concentration, the corresponding 2D patterns show typical diffuse arcs, which are ascribed to the Bragg reflections. Figure 3b shows the processed SAXS data as a function of the scattering vector q. The scattered intensity profile of a 0.5 wt% peptide solution has a slope of −1 in the low q region (Figure S8), indicating the presence of cylinderlike nanostructures. The scattering profile of the Fmoc-FF nanofibers can be fitted with the form factor model calculated for a core-shell cylinder, yielding an core diameter of 1.6 nm and an outer diameter of ~3.8 nm (Figure S8, Table S1). This value is slightly higher than the diameter of 3.3 nm estimated by molecular modeling, which might be due to the condensation of the Tris counterions on the surface of the nanofilaments.49 It should be noted that the scattered intensity profile of the 0.5 wt% aqueous solution of Fmoc-FF showed no obvious diffraction peaks, indicating the sole orientational order of the self-assembled nanofilaments. However, with an increase in the peptide concentration, sharp reflection peaks were observed in the low q range, which could be attributed to the (100) reflections between the nanofilaments within the liquidcrystalline phase. This result indicates that increasing the peptide concentration results in the crystallization of the nanofilaments. The scattered profile of a 2.46 wt% peptide solution (46 mM) contained sharp diffraction peaks in the q range of 0.2–1.2 nm−1. The positions of the peaks follow q/q* ratios of 1 : 3 : 4 : 7 : 9 : 12 (where q* is the principal peak position), which is characteristic of a columnar hexagonal lattice (space group p6mm). The center-to-center spacing, d between the nanofilaments can be deduced from the first peak, q100 using the equation, d = (2π/ q100) × (2/ 3), yielding an exceptionally large spacing of 24.2 nm, which is ~8 fold higher than the diameter of the nanofilaments. We plotted the center-to-center spacing between the peptide nanofilaments and the corresponding liquid-like ordered structures as a function of the peptide concentration. The sole orientational order of

the nanofilaments is achieved at peptide concentrations ranging from 0.1 to 0.5 wt% (Figure 3c, nematic phase, Figure S3). With an increase in peptide concentration (1.0–2.0 wt%), the order of the peptide nanofilaments increased with a centerto-center spacing ranging from 35.2 nm to 27.9 nm, depending on the peptide concentration. At relatively high concentrations (> 2.0 wt%), the peptide nanofilaments spontaneously ordered into a columnar hexagonal lattice with a center-to-center spacing of ~24.2 nm (Figure 3c, hexagonal phase, Figure S3). These results are consistent with those of the previous work by Stupp et al., according to whom, the hexagonal stacking of repulsive filaments at higher concentrations occurs spontaneously.15,50 Thus, we have demonstrated the formation of a columnar liquid crystalline phase from the self-assembly of Fmoc-FF. To the best of our knowledge, there is no known example of the formation of a columnar liquid crystalline phase by the self-assembly of such a simple dipeptide. To gain further insights into the mechanism of the formation of the liquid crystalline phase, we investigated the phase behavior of peptide amphiphiles bearing various peptide sequences using POM, TEM, and in situ SAXS analysis. The results are summarized in Table 1. We included a negatively charged amino acid residue such as Glu (E) or Asp (D) at the terminus of Fmoc-FF to increase the charge repulsion at the termini of the peptides. As shown in Figure 4a, the Fmoc-FFE peptide, bearing two negatively charged carboxylate groups self-assembled into longrange ordered nanofilaments with a diameter of ~4.2 nm in water at pH 6.75 (Figure 4d, g, Figure S5). The 1D SAXS pattern of a 3 wt% Fmoc-FFE peptide solution (pH 6.75, 46 mM, 100 mM Tris-HCl) showed a diffuse arc at q = ~0.28 nm−1 (Figure S9a), which could be attributed to the (100) reflections between the nanofilaments in the liquid-crystalline phase. With a further increase in the peptide solution, the scattered profile of a 4 wt% Fmoc-FFE peptide solution showed a


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Figure 4. (a–c) Molecular structure of the peptide amphiphiles. (d–f) Schematic illustration of the liquid-like ordering of the peptide assemblies in solutions. (g–i) TEM images of the assemblies formed by Fmoc-FFE, Fmoc-FEW and Fmoc-FWH, respectively. (j–l) 2D SAXS pattern of the Fmoc-FFE, Fmoc-FEW, and Fmoc-FWH peptide solutions. (m–o) In situ SAXS data of the peptide solutions of Fmoc-FFE, Fmoc-FEW, and Fmoc-FWH, respectively, showing the background-subtracted scattered intensity versus the scattering vector q (log−log plot).

diffuse arc at q1 = ~0.36 nm−1, and a very weak arc at q2 = ~0.72 (Figure 4j, m, Figure S9a). Compared to the diffraction patterns of Fmoc-FF solutions, the loss of higher order reflection peaks in the higher q range indicates that the crystallinity of the self-assembled Fmoc-FFE nanofilaments is relatively poorer than that of the Fmoc-FF and is probably in a “pre-hexagonal” phase with a center-to-center spacing of ~25.9 nm at 3 wt% and ~20.0 nm at 4 wt%. The Fmoc-FFD peptide solutions showed similar liquid crystalline behavior to that of the Fmoc-FFE (Figure S9b). Instead, upon the incorporation of a relatively hydrophobic amino acid residue, such as His (H), the negatively charged Fmoc-FFH self-assembled into flat nanoribbons at pH 10, forming a nematic liquid crystalline phase (Figure S10). The processed SAXS curve of the Fmoc-FFH assemblies in water has a slope of −2 (Figure S10b), indicating the presence of layered nanostructures. The scattering profile can be fitted with the form factor model calculated for layers, yielding an average thickness of 9.19 nm. High-magnification TEM images revealed that the nanoribbons are composed of stacked nanofilament bundles (Figure S10d). This indicated that the Fmoc-FFH probably selfassembled firstly into nanofilaments in a mannar similarly to that of the Fmoc-FFE, which further stacked with each other into flat nanoribbons (Figure S10b, 3D model). Furthermore, upon the inclusion of a positively charged amino acid residue such as Arg (R) at the terminus of Fmoc-FF, the zwitterionic Fmoc-FFR molecules could also self-assembled into 1D nanofilaments in water (Figure S11a). However, due to the lack of electrostatic repulsions, the nanofilaments further twist with each other into helical bundles (Figure S11b-c), that were entangled with each other without any liquid crystalline ordering (Figure S11d). These results indicate that the formation of

a highly ordered liquid crystalline phase from the selfassembly of simple peptides is rather a complex process, which is not only determined by the pH and peptide concentration, but is also closely related to the amino acid sequence of the peptide. Both the type of charge on the side chain and the hydrophobicity of the amino acid residues played crucial roles in the formation of peptide liquid crystals. Remarkably, when the Phe-Phe (FF) segment was replaced by the Phe-Trp (FW) segment, all the peptides including Fmoc-FWD, Fmoc-FWE, Fmoc-FWH, Fmoc-FWK, and Fmoc-FWR simply yielded isotropic solutions in water with very weak or no birefringence (Figure S12, S13). As shown in Figure 4b, e and h, the Fmoc-FWE tripeptide, in which the phenylalanine residue of Fmoc-FFE is replaced by tryptophan, self-assembled into a mixture of nanofilaments and nanospheres at pH 6.75. The 2D and 1D SAXS pattern of the 4 wt% Fmoc-FWE peptide solution in 100 mM Tris-HCl buffer revealed much lower anisotropy (Figure 4 k and n) than that of the Fmoc-FFE (Figure 4j, m), indicative of a much disordered arrangement of the peptide assemblies in solutions (Figure 4e). Furthermore, the Fmoc-FWH tripeptide (Figure 4c), which bears a relatively hydrophobic amino acid residue at the Cterminal, self-assembled into flat nanoribbons with a width in the range of 8.7–22 nm in water at pH 10 without any longrange ordering (Figure 4f and i). 2D SAXS pattern reveals that the Fmoc-FWH solution (46 mM) was completely isotropic (Figure 4l). The processed SAXS curve of the FmocFWH supramolecular assembly in water has a slope of −1.91 (Figure 4o), slightly lower than −2 in the low q region, which could be attributed to the heterogeneity of the peptide assemblies. These results indicate that peptides containing the PhePhe segment show much higher propensity to form long-range



ordered nanofilaments compared to the peptides containing the Phe-Trp segment under the same conditions (Table 1, Table S2 and Figure S12). A possible explanation is that the FF moiety contributed to the formation of more rigid and elongated nanofilaments than those of the FW segment, thereby possibly facilitating the formation of peptide liquid crystals. Table 1. Liquid crystalline behavior of the peptides bearing different amino acid sequences. Peptidesa

Crystalline phase

fiber diameterb [nm]

Hexagonal

3.3

24.2

Fmoc-FFS

Nematic

4.2

--

Fmoc-FFD

“Pre-hexagonal”

4.2

25.0

“Pre-hexagonal”

4.2

25.9

Nematic

8-35

--

Fmoc-FFH

e

Fmoc-FFR

Isotropic

4.2-50

--

d

Isotropic

--

--

Fmoc-FWEd

Isotropic

--

--

e

Isotropic

8.7-22

--

Fmoc-FWK

Isotropic

20-50

--

Fmoc-FWR

Isotropic

4.2-50

--

Fmoc-FWD

Fmoc-FWH

a

These thick ribbons preferred to stack with each other into larger aggregates (Figure 5c). Moreover, the stereoselective condensation of the long-range ordered nanofilaments changed the phase behavior of the solutions in entirely different ways. As shown in Figure 5f and g, the peptide solutions remained transparent for several days and showed strong birefringence after the incorporation of (1S,2S)-(-)-1,2-diaminocyclohexane (Figure 5f). However, in the presence of (1R,2R)-(-)-1,2diaminocyclohexane, a large amount of flocs formed in the

d-spacingc [nm]

Fmoc-FF

Fmoc-FFE

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The concentration of the peptide solutions is 46 mM.

b

The diameter or width of the self-assembled nanostructures are determined on the basis of the high-magnification TEM images. c

The d-spacing is determined by the first peak q100 using the equation d = (2π/ q100) × (2/ ). d

Fmoc-FWD and Fmoc-FWE self-assemble into a mixture of nanospheres and nanofilaments at pH 6.75. e

The imidazole side chain in histidine (H) has a pKa of ~6.04. Thus, the Fmoc-FFH or Fmoc-FWH mainly bears negative charges at pH 10.

Stereoselective bundling of the liquid crystalline nanofilaments for the visual discrimination of chiral species. The long-range ordering of the self-assembled peptide nanofilaments could have practical ramifications in various fields. Since the pioneering work by Abbott and coworkers,51-53 the use of liquid crystals as sensing elements for the detection of biomolecules has attracted particular attention owing to the high resolution, sensitivity, and low cost. The orientational order and optical anisotropy of the liquid crystalline molecules could transform chemical binding events into amplified optical signals that can be easily observed, even with naked eye. Owing to the intrinsic chirality of the self-assembled peptide nanofilaments, here we demonstrate that the condensation of longrange ordered peptide nanofilaments by multivalent cations is highly stereoselective (Figure 5a). It allowed us to develop a facile method for visually discriminating chiral species. For example, when (1S,2S)-(-)-1,2-diaminocyclohexane is used as the divalent condensation agent, four individual Fmoc-FF peptide nanofilaments would stack into a structure with a square symmetry, leading to the formation of uniform fiber bundles with a diameter of ~6.7 nm (Figure 5b and d, Figure S14a and c). However, upon using (1R,2R)-(-)-1,2diaminocyclohexane, the peptide nanofilaments condensed into large nanoribbons with a thickness of 20-30 nm (Figure 5c) and width of 20-130 nm (Figure 5e, Figure S14b and d).

Figure 5. (a) Schematic illustration of the stereoselective condensation of the peptide nanofilaments using chiral diamines. (b–e) AFM and TEM images showing the structures within the peptide solutions after the incorporation of (1S,2S)-(+)-1,2diaminocyclohexane (b, d) and (1R,2R)-(-)-1,2diaminocyclohexane (c, e), respectively. The images were captured after 12 h of incubation at 20 °C. The cross-section height curve of a fiber and the arrows in (b) indicated that the fiber is composed of four nanofilaments stacked in a square symmetry. (f, g) POM images showing the distinct phase behavior of the peptide solutions (11.4 mM, pH 8.8) in the presence of 5.7 mM (1S,2S)-(-)-1,2-diaminocyclohexane and (1R,2R)-(+)-1,2diaminocyclohexane, respectively.


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Figure 6. (a) Schematic illustrations of the peptide-templated synthesis of mesoporous silica with ordered cavities. (b–e) SEM (b) and TEM (c–e) images of the mesoporous silica synthesized using Fmoc-FFE as the templates. (f, g) XRD and nitrogen adsorption-desorption isotherm of the mesoporous silica. The inset graph in (g) shows the pore size distribution of the silica calculated using the BJH method.

peptide solution. Using POM, we observed “spherulite” domains within the peptide solution (Figure 5g), which could be attributed to the further aggregation of the peptide nanofilament bundles (Figure S15). The results demonstrate that based on the liquid-crystalline ordering of the self-assembled peptide nanofilaments, it is possible to discriminate chiral species using a simple polarized optical microscope or even with naked eyes. Templated synthesis of mesoporous silica with ordered cavities The development of a peptide-based method for the fabrication of nanostructured inorganic materials has been an active area of research over the past few decades.24,54 Hartgerink et al. reported the formation of hollow silica nanotubes using peptide nanofiber templates self-assembled from ultrashort peptides.55 Lu et al. used ultrashort peptide I3K as template to synthesize long and uniform silica nanotubes under ambient conditions.56 However, owing to the lack of understanding on the liquid crystalline behavior of peptides, the use of ultrashort peptides for the fabrication of highly ordered mesoporous materials has been reported rarely.57 Here, we show that liquid-crystalline peptide nanofilaments could serve as tem-

plates for the biomimetic synthesis of well-ordered mesoporous silica nanofibers at room temperature and neutral pH (Figure 6a). To promote the condensation of the silica precursor on the peptide templates, we incorporated tetraethyl orthosilicate (TEOS) as the silica source in the peptide solutions and trimethoxysilylpropyl-N, N, N-trimethylammonium chloride (TMAPS) as the co-structure directing agent.58 The mixtures were stirred for 12 h at 25 °C, during which a large amount of flocs formed within the mixtures, and then incubated at 80 °C in an oven for an additional 12 h. The precipitates were collected by centrifugation and calcined at 600 °C in a muffle furnace. The silica structures formed by the templation of different peptides were observed by TEM. As shown in Figure S16, well-defined silica nanotubes could be obtained using the Fmoc-FF peptide as the template, whereas mesoporous silica nanofibers with highly ordered mesopores were formed upon using the Fmoc-FFE and Fmoc-FFD tripeptides, respectively. However, disordered silica nanospheres are formed when peptides that do not order into liquid-crystalline structures, such as Fmoc-FWD or Fmoc-FWE, are used as templates. These results indicate that the templated synthesis of highly ordered silica nanomaterials closely relies on the liquid crystalline behavior of the peptides. Figure 6b–c show



the TEM images of mesoporous silica nanofibers templated by Fmoc-FFE. The nanofibers have an average diameter of ~50 nm and lengths up to micrometers. The high-magnification TEM image (Figure 6c) reveals that the silica nanofibers are mesoporous with aligned channels running along the fiber axis. The mesoporous structure of the silica nanofibers was further confirmed by X-ray diffraction (Figure 6d) and nitrogen adsorption analysis (Figure 6e). The XRD pattern exhibited a diffraction peak at q1 = 1.47 nm−1, indicating that the mesoporous silica fibers have ordered mesoporous structures. The very weak diffraction peak at q2 = ~2.55 nm-1 indicates that the mesopores may have a two-dimensional hexagonal unit cell, although the occurrence of this crystalline feature was quite low. The nitrogen adsorption-desorption isotherm of the mesoporous silica nanowires showed a type IV curve (Figure 6e), which is characteristic of a typical uniform mesoporous architecture. The Brunauer-Emmett-Teller (BET) specific surface area of the silica was calculated to be 1510 m2/g, indicating the high porosity of the silica nanomaterials. Moreover, according to the Barrett-Joyner-Halenda (BJH) method, the pore diameter was estimated to be approximately 2.4 nm (Figure 6e, inset), which is nearly consistent with the results of TEM analysis (Figure 6c). These results demonstrate the great promise of the peptide liquid crystals for biomimetic templated synthesis of highly ordered inorganic materials.

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CONCLUSIONS

We demonstrated the spontaneous formation of liquid crystals from the self-assembly of minimalistic peptide amphiphiles. The negatively charged peptides could selfassemble into highly charged nanofilaments that spontaneously ordered into columnar liquid crystalline phase in water. By changing the amino acid sequences, we demonstrated that the formation of peptide liquid crystals is not only determined by the pH and peptide concentration but is also closely related to the amino acid sequence of the peptide, which determines the shape and surface charge of the peptide assemblies, and thus the long-range ordering in networks of the self-assembled nanostructures. The results provided new insights into the formation of peptide liquid crystals, which will enhance the relevance of peptide-based materials for a broad spectrum of applications, i.e., serving as probes for chemical sensing or templates for the fabrication of other functional nanomaterials.

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ASSOCIATED CONTENT

Supporting Information. Experimental procedures; POM images of the peptide solutions and TEM images of the Fmoc-FFS and Fmoc-FFE assemblies (Figure S1-S5); circular dichroism measurement (Figure S6); Initial packing model of Fmoc-FF and Fmoc-FFE (Figure S7); SAXS data fitting of the Fmoc-FF peptide solution (Figure S8, Table S1); SAXS data of Fmoc-FFE and Fmoc-FFD at various concentrations (Figure S9); POM, TEM, SEM and SAXS analysis of Fmoc-FFH and Fmoc-FFR peptide solutions (Figure S10-S11); POM and TEM images of peptides bearing various amino acid sequence (Figure S12-S13). Self-assembly conditions for the formation of liquid crystals from various peptides (Table S2); Additional TEM and SEM images showing the stereoselective bundling of the liquid crystalline nanofilaments (Figure S14-S15); TEM images of the silica nanostructures templated by various peptides (Figure S16). This material is available free of charge via the Internet at http://pubs.acs.org.

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AUTHOR INFORMATION

Corresponding Author

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* [email protected]

Notes The authors declare no competing financial interest.

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ACKNOWLEDGMENT

This work was supported by the National Natural Science Foundation of China (Nos. 21621004, 21476165, 21606166, 51773149, 21777112, 21676191), the Beiyang Young Scholar of Tianjin University (2012), and the State Key Laboratory of Chemical Engineering (No. SKL-ChE-08B01). The authors thank Prof. Zhonghua Wu and Dr. Guang Mo of BSRF for assistance with the X-ray scattering measurement.

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REFERENCES

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