Template-Guided Assembly of Silk Fibroin on Cellulose Nanofibers

Template-Guided Assembly of Silk Fibroin on Cellulose Nanofibers for Robust Nanostructures with Ultrafast Water Transport Rui Xiong,†,‡ Ho Shin Kim,§ Shuaidi Zhang,‡ Sunghan Kim,‡ Volodymyr F. Korolovych,‡ Ruilong Ma,‡ Yaroslava G. Yingling,§ Canhui Lu,*,† and Vladimir V. Tsukruk*,‡ †

State Key Laboratory of Polymer Materials Engineering, Polymer Research Institute of Sichuan University, Chengdu 610065, China School of Materials Science and Engineering, Georgia Institute of Technology, Atlanta, Georgia 30332-0245, United States § Department of Materials Science and Engineering, North Carolina State University, Raleigh, North Carolina 27695-7907, United States ‡

S Supporting Information *

ABSTRACT: The construction of multilength scaled hierarchical nanostructures from diverse natural components is critical in the progress toward all-natural nanocomposites with structural robustness and versatile added functionalities. Here, we report a spontaneous formation of peculiar “shish kebab” nanostructures with the periodic arrangement of silk fibroin domains along straight segments of cellulose nanofibers. We suggest that the formation of these shish kebab nanostructures is facilitated by the preferential organization of heterogeneous (β-sheets and amorphous silk) domains along the cellulose nanofiber driven by modulated axial distribution of crystalline planes, hydrogen bonding, and hydrophobic interactions as suggested by all-atom molecular dynamic simulations. Such shish kebab nanostructures enable the ultrathin membrane to possess open, transparent, mechanically robust interlocked networks with high mechanical performance with up to 30 GPa in stiffness and 260 MPa in strength. These nanoporous robust membranes allow for the extremely high water flux, up to 3.5 × 104 L h−1 m−2 bar−1 combined with high rejection rate for various organic molecules, capability of capturing heavy metal ions and their further reduction into metal nanoparticles for added SERS detection capability and catalytic functionalities. KEYWORDS: silk fibroin, cellulose nanofiber, ultrathin membrane, flexible nanocomposites, ultrafast permeation

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permeability. However, attempts to integrate natural polymers with other bioderived reinforcing components rarely resulted in high-performance biomaterials due to a lack of multiscale hierarchical organizations.9 Silk fibroin (SF) is one of the most common natural proteins produced by spiders and silkworms. Although natural spider silk fibers demonstrate amazing mechanical properties owing to the highly ordered assembly of soft silk random coil and hard βsheet nanocrystals, these artificial silk materials are still far lower than the expectation. On the other hand, CNF exists in the cell wall of plants, possessing an elastic modulus up to 200 GPa.10 CNFs are typically exfoliated from macroscopic cellulose fibers by 2,2,6,6-tetramethylpiperidine-1-oxyl (TEMPO) oxidation and mechanical treatment, thus leaving anionic carboxyl groups

he multilength scaled hierarchical nanostructures from diverse natural polymers are highly desired for developing all-natural nanocomposites with structural robustness and added functionalities such as controllable permeability, wetting ability, and structural color.1,2 To achieve this goal, natural materials smartly combine protein and polysaccharide nanofibers together to construct highly ordered nanofibril or layered nanostructures as observed in bone, teeth, wood, arthropod cuticles, crustacean exoskeletons, and mollusk shells.3 Inspired by these natural structure, a number of impressive works have been reported on the fabrication of advanced flexible nanocomposites by using a combination of biological and synthetic components such as silks, cellulose nanofiber (CNF), and amyloids from one side and carbon fibers and nanotubes (1D components) and clay nanoplatelets and graphene (2D components) from another side.4−8 These nanocomposites demonstrated outstanding elasticity, strength, and toughness as well as additive functionalities such as electrical conductivity, tunable transparency, or controlled © 2017 American Chemical Society

Received: June 17, 2017 Accepted: November 13, 2017 Published: November 13, 2017 12008

DOI: 10.1021/acsnano.7b04235 ACS Nano 2017, 11, 12008−12019

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ACS Nano Scheme 1. Assembly Silk Fibroin into Shish Kebab Nanostructures on Cellulose Nanofibers

on the CNFs surface to facilitate their colloidal stabilization.11 The uniform 1D chiral geometry and abundant surface groups make CNFs promising nanotemplates for fabricating advanced functional materials, including inorganic hollow nanotube,12 chiral metal nanocatalysts,13 and flexible magnetic foams.14 Here, we report an all-natural bionanocomposite with exceptional mechanical performance by an unusual templatedriven assembly, where SF self-assembles directly on straight segments of CNFs to form peculiar “shish kebab” hierarchical nanostructures with highly periodic organization of hydrophobic and hydrophilic silk domains (Scheme 1). We suggest that the strong and selective interfacial interactions between heterogeneous hydrophobic and hydrophilic domains of SF protein and the heterogeneous polysaccharide nanofibers facilitate this periodic assembly. The robust network of interlocked shish kebab nanostructures with stiff nanofiber cores possesses high mechanical strength and a highly open porous morphology. Notably, this structure demonstrates an added functionality in ultrafast water permeation and excellent nanofiltration efficiency far exceeding current examples.15 Besides, the porous structure and abundant surface groups enable the efficient absorption for heavy metal ions and their recovery.

beyond 1% sensitivity level (see experimental and discussion in SI and Figure S23). Surprisingly, combining both components in solution results in a spontaneous formation of organized periodic nanostructures never observed for silk materials (Figure 1e). In these nanostructures, SF domains are arranged highly periodically along the straight CNF segments effectively with average spacing of 17 ± 4 nm and height variation of 0.7 ± 0.2 nm, doubling the CNF diameter to around 4−5 nm and the overall effective size increase (Figures 1e,f and 2, Figures S1c and S2). The effective thickness of silk domains that wrap on straight nanofiber segments can be estimated to be around 1 nm or the equivalent of about two silk backbone diameters. Additionally, the individual silk domain was determined to contain only a single silk molecular chain as estimated by comparing the measured geometric dimensions of silk domain from highresolution AFM images considering tip dilation and theoretical value of silk backbone volume assuming dense packing (Figure 2a).16 The TEM image of the assembled SF-CNF materials also demonstrated that the individual nanofibers are coated by silk to form core−shell structures and bundles (inset in Figure 2a, Figure S3). However, excessive CNF aggregation after drop casting on a carbon TEM support and the dried silk under high vacuum conditions compromise spatial resolution and observation of fine details. Based upon these geometrical parameters of the discovered nanostructure, we present a molecular model for the shish kebab morphology based upon AFM data (Figure 2b). In this model, we suggest that the periodical modulations observed along the SF-CNF nanofibers are caused by the preferential organization of the hydrophobic and hydrophilic SF domains along the CNF morphology. The diameter modulation observed here is created by alternately packing interconnected squashed hydrophilic random coil-silk domains in thicker regions (around 1 nm thickness) and of β-sheet monolayers inbetween (single sheet with 0.4 nm thickness) (Figure 2b). This model explains all of the observed morphological features also consistent with molecular dimensions of different SF secondary structures.17 We propose that the linearly heterogeneous/ amphiphilic nature of the CNF surface plays a critical role in this periodic self-organization of silk domains.18,19 The

RESULTS AND DISCUSSION SF was extracted from the cocoons of Bombyx mori, which folded into domains of around 2 nm (Figure 1a,b, Figure S1a). CNFs were exfoliated from natural wood and demonstrate only 2.7 ± 0.4 nm in diameter and above 1000 nm in length (Figure 1c,d, Figures S1b, S23, and S24). The nanofibers are composed of continuous 280 ± 115 nm long straight crystalline segments that are separated by sharp kinks or misfit orientation, corresponding to the amorphous region (Figure 1c). Within these straight segments, the nanofiber surface is molecularly smooth with linear microroughness along their axis around 0.16 nm, indicating near-perfect longitudinal packing of cellulose backbones with minimal surface defects and irregularities from traces of the branched hemicellulose components (Figure S24). This conclusion was further supported by ATR-FTIR measurements, which are surface sensitive, and showed the absence of the characteristic bands 12009


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Figure 1. Morphologies of SF, CNF and SF-CNF assembly. AFM images: (a) SF, (c) CNF, and (e) assembled SF-30 wt % CNF materials (the insets in a, c, and e are the AFM cross-section profiles, Z-scale: 10 nm) with corresponding schematics and DLS size distributions (insets).

hydroxyl and carboxyl moieties exist in hydrophilic planes, while the axial C−H functionalities form the hydrophobic (200) plane, the well-known features of CNF morphology. To further confirm the proposed organization, we carried out the all-atom molecular dynamics (MD) simulations of the interaction between silk protein chains with the CNF surfaces (Figure 3). These simulations introduce symmetric silk structures surrounding the nanofibers as the initial structure (see two

projections in Figure 3a). After MD simulations in a water environment, the initial uniform silk structure adapted different organizations with backbones assembled into aggregated disordered silk domains and extended and flattened singlemolecular β-sheets structures (last structure in Figure 3a,b). We found that strong nonbonded interfacial interactions, especially van der Waals contributions between silk backbones and CNF surface, play a pivotal role in inducing the structural changes and preferential aggregations along the nanofiber axis; whereas, 12010


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Figure 2. Insight of the template-directed assembly of silk backbones on CNF: (a) High-resolution AFM and TEM of SF-CNF nanostructure. Z-scale: 10 nm. (b) The model of periodically assembled silk backbones on CNF surface. (c) FTIR spectra and (d) peaks for amide I and amide II of CNF, SF, SF-30 wt % CNF structures as well as methanol treated SF-30 wt % CNF structures.

Figure 3. All-atom MD simulations of the self-assembly of silk fibroin on CNF. (a) Representative all-atom simulation snapshots of initial SFCNF structure (five silk biomolecules) and the same after relaxation (last structure). A blue and orange color represents CNF and silk proteins, respectively. (b) Density profile of silk and CNF atoms along the axis parallel to the CNF. A black line corresponds to the average density profile of the last 10 ns simulation and its standard deviation. A gray dotted line is the density profile for the initial SF-CNF distribution. 12011


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Figure 4. Micromechanical properties of silk-CNF membranes. AFM images of ultrathin (a) SF-30 wt % CNF (inset is the thickness of the corresponding membrane) and (b) CNF membranes, z-scale is 10 nm. (c) SEM of the cross-section of thick SF-CNF membrane. (d) Young’s modulus and (e) ultimate strength of SF-CNF membranes with different CNF content. (f) Comparison of Young’s modulus and strength of SF-CNF membranes with other reported nanocomposites films containing CNF or SF materials; yellow region mainly contains SF based materials and blue region mainly contains CNF materials.

weak van der Waals and electrostatic interactions can stabilize ordered structures and make ordered sheets more extended along the nanofiber surface (Figure S4). In fact, the ordered structure of biomolecules such as SFs20 and DNAs21 can be disrupted by strong and localized van der Waals interactions, while it can be maintained or restored by balanced van der Waals, hydrogen bonding, and electrostatic interfacial interactions. Indeed, the our simulation result demonstrated that heterogeneous axial distribution can be initiated by uneven contributions of different types of hydrogen bonding: β-sheet monolayers of SF are maintained on hydrophobic or hydrogen atom-rich regions of CNF by forming hydrogen bonds between silk as hydrogen acceptors and CNF as hydrogen donors, while an oxygen-rich or hydrophilic region can facilitate significant structural changes by a decrease in the interfacial hydrogen bonding between silk and CNF surface (Figure S5). Overall, the heterogeneous nature of CNF surface can induce different nonbonded interactions with silk proteins which heavily influence the secondary structure of silk domains with formation of largely separated domains of different types which can facilitate the periodic ordering along the nanofiber axis. In terms of intermolecular interactions, hydrogen bonding and Coulombic should be further considered in view of overall surface potential of the components. First, the Coulombiccaused repulsion produced by the modest negative charged SF (−13 mV) and CNF (−38 mV) cannot be a major driving force

in silk-nanofiber assembly. However, these repulsive interactions are instructive in stabilizing and preventing larger-scale aggregation of individual SF-CNF nanostructures with an overall surface potential of −20 mV, and then, hydrogen bonding between silk backbones and CNF surfaces can be instrumental in driving local assembly. Indeed, FTIR spectrum of CNF shows a typical broad peak of −OH group stretching vibration at 3350 cm−1, which shifted to a lower frequency at 3300 cm−1 after assembling with SF due to increased intercomponent bonding (Figure 2c).22 Most importantly, the absorption peak at 1725 cm−1 assigned to the stretching vibration of carboxylic groups of CNF disappeared after the silk assembly on CNFs (Figure 2d).23 The pH of CNF, SF, and the mixture of SF-CNF solution in the self-assembly process is 6.8, 7.4, and 7.1, respectively, basically maintaining the same pH condition. This result indicates that the disappearance of the carboxylic group peak is not likely induced by the switch of counterion of the carboxylic group from Na+ to a proton. We suggest that this peak shifted to lower frequency and overlapped with the broad amid I peak (1657 cm−1) because of the interactions between carboxylic groups on CNF surfaces and amid groups of the silk components. Although the fraction of β-sheets in the fresh-prepared SF does not exceed 4% (Figure S6a), the methanol treatment largely promotes β-sheet presence to 25%, as confirmed by the strong peak centered at 1629 cm−1 and the further lower frequency shift of −OH and amid II, respectively (Figure S6b).24 Correspondingly, these changes in secondary structure 12012


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Figure 5. Transport performance of ultrathin membranes. (a) Comparison of pure water flux of SF-CNF membranes with other reported ultrathin membranes. (b) Plot from Hagen−Poiseuille relationship of flux × thickness and thickness for different membranes. (c) UV−vis curves, photos (left inset), and rejection rate (right inset) of methylene blue aqueous solution after filtrated with SF-CNF membranes with different thicknesses. (d) As-prepared 200 nm membrane supported on PC filter before and after filtrating R6G. (e) Rejection rate of 200 nmthick assembled SF-CNF membranes for different subjects. (f) Comparison of 5 nm gold NPs rejection rate of SF-CNF membranes with other reported ultrathin membranes. Abbreviations: CNF, carbonaceous nanofibers; SNF, silk nanofibril; SPEK-C, sulfonated polyetherketone; WS2, chemically exfoliated tungsten disulfide nanosheets; MoS2, molybdenum disulfide; NSC-GO, nanostrand channeled graphene oxide; PP2B, (5,5′-bis(1-ethynyl-7 polyethylene glycol-N,N′-bis(ethylpropyl) perylene-3,4,9,10-tetracarboxylic diimide)-2,2′-bipyridine.

the as-prepared SF nanofibrils show a random network of curved and folded nanobundles with octopus-like shapes in contrast to the straight and uniform SF-CNF nanofibers fabricated here (Figure S10a,b). Although both samples show similar domain morphologies, the diameter and length of the silk nanobundles are around 6 nm and 300−500 nm, respectively (Figure S10c), much larger but shorter than that of very uniform SF-CNF nanofibers of 4 nm in diameter and up to 1 μm in length (Figure S10d). Moreover, if the overall morphology of SF nanobundles is dynamic and changes dramatically with assembly time, then the SF-CNF shish kebab nanostructures are extremely stable. Next, we consider the role of the shish kebab morphology in the mechanical performance of SF-CNF materials. The asprepared spin-cast 50 nm ultrathin membranes show highly uniform porous morphology with 1 μm × 1 μm surface microroughness (Rq) of 2.1 nm, similar to bare SF and CNF membranes (Figure 4a,b, Figure S11). Besides, ordered laminated morphology can be observed in the thicker membranes (Figure 4c). To analyze the mechanical properties, we used a quantitative nanomechanical mapping (QNM) scanning probe technique and bulging test.27 The corresponding QNM mapping demonstrates a uniform nanomechanical response of shish kebab nanostructure due to the higher stiffness of CNF and increased overall adhesion of silkdecorated nanofibers (Figures S12 and S13). Additionally, the

make the shish kebab nanostructures better defined with the thickness of the silk domain increasing to 0.9 ± 0.4 nm, while the average periodic spacing decreases to 14 ± 3 nm, thus resulting in more compacted nanoscale morphology of the same type (Figures S1d and S7b). Notably, it has been widely reported that the silk micelles also can self-assemble into nanofibrils in a carefully controlled environment without the addition of any CNF.25,26 This assembly is a slow process (at least 2 days) requiring strict hybrid solvent selection, pH, and temperature control. In contrast, the assembly of silk on the CNF in our case is a fastassembly process resulting due to stable periodic domain morphology. In fact, the shish kebab morphology remains the same (sizes, spacing, thickness) at different assembly times ranging from 12 to 72 h of exposure (Figure S8). Additionally, to understand the difference between the SF nanobundles and our SF-CNF nanostructure, we prepared the SF nanofibrils according to a recent study.25 Briefly, a 0.1 wt % SF aqueous solution containing 7 vol % ethanol was incubated at pH 9.5 and room temperature for 2 days. The obtained SF nanofibril dispersion shows turbid bluish tinge, indicating the presence of relatively large nanocolloidal structures and some aggregation (Figure S9). In contrast, the SF-CNF dispersion prepared in this study is clear and transparent, meaning that the size of SF-CNF is well below colloidal level (hundreds of a nanometer) and without any large-scale aggregation. Moreover, 12013


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Figure 6. Absorption performance for metal ions and turning them into functional metal NPs. (a) Absorption efficiency of SF-CNF for various metal ions. AFM images and photos (insets) of recycled gold NPs (b) and silver NPs (c) immobilized on SF-CNF membranes by hydrothermal technique. (d) Catalytic performance of recycled gold NPs for reducing 4-NP, insets are the scheme and photos before and after reduction. (e) SERS performance of recycled silver NPs for detecting R6G.

strength at break of 1 GPa, and toughness of 55 MJ m−3, owing to the strong binding ability of biocomponents and the high orientation factor of 0.86.41 Recently, the reinforcing epoxy films with CNF network demonstrated a 3-fold increase in Young’s modulus to 5.9 GPa and strength to 109 MPa.42 Although this enhancement factor is significant, the resulting mechanical performance is still far below that observed for the SF-CNF nanocomposites in this study. Such an outstanding mechanical performance combined with open porous morphology are highly desired for the ultrathin nanofiltration membranes with enhanced mechanical robustness (Figure 5).43,44 In fact, a narrow pore size distribution with an average pore size of 1.8 ± 0.5 nm was detected for 200 nm membrane by using a nitrogen absorption experiment (Figure S17). Then, the water transport performance of the SF-CNF membranes with interlocked shish kebab nanostructures was studied under the pressure of 1 bar for membranes with thickness from 50 to 1000 nm. Surprisingly, a 50 nm-thick SF-CNF membrane demonstrates an extremely high flux, F, up to 3.5 × 104 L h−1 m−2 bar−1, hundreds times higher than commercial filtration membranes and dramatically better than reported ultrathin membranes of a different nature (Figure 5a).43−50 Flux strongly depends upon membrane thickness, but even for the thicker membranes (>200 nm), the flux value (within 102 −103 L h−1 m−2 bar−1) is still much higher than that of most commercial filtration membranes.51 As known, the Hagen−Poiseuille equation predicts that the combination F × t, where t is the membrane thickness, should be constant under unchanged conditions (morphology, pressure, velocity, and viscosity).49,52 Indeed, the summary of

bulging test generated stress−strain curves from the freely suspended membranes to determine mechanical characterizations of ultrathin membranes (Figure S14a).22,28 It is important to notice that these membranes are strong enough to sustain a release and transfer process that involves high stresses during drying and mechanical deformation,29 even suspended on a 300 μm circular aperture without any cracks or wrinkles (Figure S15). SF-CNF membranes with 30 wt % CNF possessed the highest mechanical performance with Young’s modulus of 30 ± 3 GPa and ultimate stress of 260 ± 36 MPa (Figure 4d,e). These values are three times higher than that of neat silk membranes (Young’s modulus of 8 GPa and ultimate stress of 86 MPa) as well as significantly higher than that of neat CNF membranes (15 GPa in Young’s modulus and 190 MPa in ultimate stress) (Figure 4d,e). The toughness of SF-CNF membranes (1.5 MJ/m3) is also largely enhanced (Figure S14b). Besides, the exceptional mechanical performance of the SFCNF membranes extends beyond the property space reported for most SF or CNF-based nanocomposites (Figure 4f, Figure S16, detailed mechanism see the Supporting Information).9,25,30−37 It is important to note that CNF-based microfibers show superior mechanical performance during unidirectional tensile testing because of the uniform high alignment of individual polymer backbones and nanofibers along the axial direction.38 For instance, PVA-cellulose fiber composites showed very high strength (ultimate stress of around 800 MPa) and high elastic modulus of 30 GPa.39,40 The combination of CNFs with spider silk also resulted in the ultrarobust microfibers with an elastic modulus of 55 GPa, 12014


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ACS Nano available data for numerous reported membranes in terms of F × t vs t shows the general validity of this theory within modest variation of 10% for a wide range of thicknesses (within an order of magnitude) (Figure 5b). In contrast to reported membranes, the F value in our case increases much faster for thinner membranes, reaching an extremely high value for the thinnest possible membranes (50 nm) (Figure 5a). Correspondingly, the same F × t−t plot shows a constant value only for intermediate SF-CNF thicknesses within 300−1000 nm. Thus, these thicker membranes follow the well-known and widely spread behavior predicted by the Hagen−Poiseuille equation. However, for ultrathin membranes with thicknesses below 200 nm, F × t increases 4-fold in comparison with a steady value of 4.5 × 105 L m−2 h−1 nm for thicker membranes (Figure 5b). This scale-related change might be caused by the reorganization of morphology of SF-CNF membranes from 3D random network to 2D morphology under confined conditions of ultrathin films with thickness below the length of stiff and straight CNF segments (280 nm in this study). Thickness below 300 nm severely constrains the vertical orientation of stiff nanofiber segments and enforces predominantly planar random orientation of nanofibers during wet fabrication that allows for an effective opening size increase due to uneven contact of the shish kebab nanostructures. For further evaluation of transport properties, different dyes and labeled nanoparticles (NPs) were used to evaluate separation performance of CNF-SF membranes, which can be visually detected due to their high transparency (Figure 5c−e, Table S1, Figure S18). As we observed, the rejection rate for methylene blue (MB), which was calculated from the characteristic peak intensity of MB at 668 nm, can reach nearly 100% for 1 μm-thick membranes (Figure 5c). The separation performance of 200 nm-thick membranes for various components is shown in Figure 1e and Figure S19. These ultrathin membranes also demonstrated rejection rates of 77% for Rhodamine 6G (R6G, molecular dimensions of 1.8 × 1.4 nm, here and below), 80% for malachite green (MG, 1.5 × 1.2 nm), 85% for MB (dimensions: 1.5 × 0.6 nm), 94% for brilliant blue (BB, 2.3 × 1.8 nm), and 100% for 5 nm gold NPs (Table S1, Figure S20). Overall, both the flux rate and rejection rate of SF-CNF membranes fabricated in this study were higher than that reported for most inorganic and polymer membranes (Figure 5f).43,44,49,50,53−55 We suggest that the rejection rate and molecular-sieving mechanism in these membranes are controlled by the effective small pore dimensions combined with heterogeneous interactions of silk and cellulose surfaces.53 Apparently, the effective pore size of 1.8 nm facilitates geometrically controlled higher rejection rates for larger species such as BB and AuNPs. On the other hand, the net-negative surface potential of the SF-CNF nanostructures assists high retention of positively charged molecules (MB, R6G, and MG) with smaller molecular size. Strong π−π and hydrophobic−hydrophobic interactions between dye cores and tyrosine units of silk surfaces also contribute to high separation performance. Finally, these SF-CNF membranes are capable of capturing various heavy metal ions with high efficiency ranging from gold to nickel (Figure 6a). Then, these captured metal ions can be reduced into metal NPs by these membranes via a biomineralization process as reported for silks (Figure 6b,c).56 A combination of protein fibrils with other carbon components

was demonstrated to be promising for the recovery of valuable heavy metal ions from the wasted water.37,57 In recent study, Mezzenga et al.57 reported the high efficiency removal of heavy metal ions from water by using amyloid-activated carbon nanocomposites films followed by reduction into metal NPs for the catalysis and electrical conductivity. These reduced metal NPs of 5−20 nm can be considered for further applications due to their rich functionalities. In fact, the catalytic activity of the recycled gold NPs was evaluated by reducing 4-nitrophenol (4NP) to 4- aminophenol (4-AP) (Figure 6d).58 The characteristic peak of 4-NP decreases gradually, and the color changes from light yellow to clear during the catalysis reaction, while the characteristic peak of 4-AP at 300 nm emerges. This reaction was completed very fast, within 6 min. Moreover, we demonstrated the surface enhanced Raman scattering (SERS) ability of these membranes with reduced silver NPs in detection of the trace amount of Rhodamine 6G down to a very low concentration of 0.1 nM, on par with the best porous SERS substrates (Figure 6e).59

CONCLUSIONS In summary, we observed peculiar shish kebab nanostructures formed by CNF-directed assembly of SF domains. In these nanostructures, highly periodic silk domains self-assembled along the CNFs with length up to 1 μm due to modulated interfacial interactions along heterogeneous surfaces of amphiphilic CNFs. These well-ordered and stable periodic SF-CNF nanostructures with nanoscale periodicity enable the fabrication of open 2D network ultrathin membranes with excellent mechanical robustness and ultrafast water transport. The extremely high water permeability shown by the ultrathin membranes are 2−3 orders faster than those of commercial ultrafiltration membranes. Moreover, these interlocked nanostructures with high mechanical performance, solvent insolubility, and high transparency demonstrate outstanding pollutant removal performance with high flux and selectivity. Moreover, their ability of capturing metal ions followed by the “on-spot” reduction to metal NPs facilitates added functionality for catalytic-related and SERS applications. EXPERIMENTAL SECTION Preparation of Silk Fibroin Solution. Silk fibroin aqueous solution was prepared from Bombyx mori silkworm cocoons by a standard procedure, including splitting, degumming, dissolving, and dialysis.60 Then high-speed centrifugation (10,000 rpm, 20 min, 5 °C) was used twice to purify the SF solution. The as-prepared final solution (around 4 wt %) was diluted to the desired concentrations immediately and stored at 4 °C for use within a month. Preparation of Cellulose Nanofibers Dispersion. Cellulose nanofibers were isolated from the never-dried wood pulp through TEMPO oxidation, ultrasonic treatment, and purification using a known method.61 Briefly, TEMPO (0.016 g, 0.1 mmol) and sodium bromide (0.1 g, 1 mmol) were added into a wood pulp suspension (100 mL,1 wt %). Then, the desired amount of the NaClO solution (12%, 10 mmol NaClO per gram of cellulose) was added to the above mixture at room temperature while stirring at 500 rpm. The pH was maintained at 10 using 1 M NaOH until no pH change was observed. The TEMPO-oxidized cellulose was thoroughly washed with DI water by centrifugation. A slurry of the TEMPO-oxidized cellulose 0.2 wt % was further treated using an ultrasonic tip for 2 h to produce the CNFs. High-speed centrifugation (10,000 rpm, 20 min, 5 °C) was conducted to separate the unexfoliated cellulose fibers from the obtained CNF suspension. The resulting ultrafine CNF suspension was diluted to the desired concentrations. The amount of the carbonyl groups introduced on the CNF was determined to be 1.3 mmol/g by 12015


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ACS Nano conductometric titration, which is close to previous reports61 (see the Supporting Information). During the TEMPO treatment and the purified process of the CNF, virtually all of the lignin and hemicellulose components were removed. Most importantly, the hemicellulose has similar chemical structure and functional groups with cellulose, mainly consisting of hydroxyl groups, thus not affecting significantly the surface chemical composition critical for adsorption and beading of SF. The trace of hemicellulose is below 1 wt % as estimated from ATR-FTIR (for details see the Supporting Information and Figure S23).11 Template-Directed Assembly of SF-CNF Nanostructures. Typically, 5 mL of CNF suspension (0.1 wt %, pH 6.8) was added into a SF solution (10 mL, 0.1 wt %, pH 7.4) very slowly to avoid aggregation of SF. The pH of the resulted mixture was determined to be around 7.1. The silk protein is highly sensitive to pH and temperature, so we stored the mixture in a refrigerator at 4 °C to prevent the formation of silk β sheets and silk nanofibrils. It is known that the fresh silk solution can maintain stable structure for 3−4 weeks in low temperature and neutral conditions.60,62 To characterize the morphology of the SF-CNF nanostructures by AFM, we prepared the samples by spin coating the as-prepared mixture on a piranha solution treated silicon wafer at 3000 rpm for 30 s. The ultrasharp AFM probes with a radius of around 2 nm (Bruker) were used to capture the highresolution AFM images with 1024 × 1024 pixel resolution in order to reveal nanoscale shish kebab nanostructures and correctly evaluate geometrical dimensions. Fabrication of SF-CNF Membranes. To test the mechanical properties of ultrathin SF-CNF membranes, a sacrificial cellulose acetate (CA) layer was deposited on a silicon wafer from a 2 wt % solution by spinning coating at 3000 rpm prior to formation of SFCNF film.63 To ensure efficient deposition, the concentration of mixture was around 0.5 wt %. After the thickness of membranes reached 50−60 nm, they were then rinsed with methanol to further crystallization. Freestanding nanomembranes were released by dissolving the sacrificial layer in acetone and transferred to copper grids with 300 μm aperture to test micromechanical performance (see Bulging Test). Separation Performance Measurements. For the separation test, all of the SF-CNF (7:3 w/w) membranes were fabricated by vacuum-assisted filtration of the SF-CNF dispersions with polycarbonate filtration membranes (pore size, 200 nm; diameter, 47 mm; VWR), followed by approximately 30 s of methanol treatment.44 The separation test was carried out on a vacuum VWR filtration device (membrane diameter of 47 mm, inner diameter of funnel top 35 mm) using reported procedures.44 Water flux (F, L m−2 h−1 bar−1) was measured by filtrating 200 mL water across the membrane and calculated using the following equation: F=

V AtP

TEM copper grid before the TEM characterization, and the SF-CNF on silicon wafer was sputtered with a 5 nm gold layer before the SEM characterization. The thickness increase of the nanomembrane was measured independently using a spectroscopic ellipsometer (M2000U, Woolam). Optical transmittance of nanomembranes and separation performance was determined using a Shimadzu 1601 UV−vis spectrometer. Attenuated total reflectance Fourier transform infrared spectroscopy (TR-FTIR) measurements were carried out on a Bruker FTIR spectrometer, Vertex 70, equipped with a narrowband mercury cadmium telluride detector. Dynamic light scattering (DLS) measurements were conducted using a Malvern Zetasizer Nano-S instrument. Nitrogen absorption experiment was carried out by Micromeritics ASAP 2020. XPS spectra were obtained with a Thermal Scientific Kalpha XPS instrument. Absorption Test. SF solution (1 mL, 0.5 wt %) was carefully added to the CNF dispersion (5 mL, 0.15 wt %) and kept at 4 °C for a day. Then, 10 mL of various metal ion solutions (10 mM, HAuCl4, AgNO3, CuCl2, and NiCl2) was added to the above dispersion, respectively. The positively charged metal ions will induce the gelation of SF-CNF dispersion immediately. Then, absorbed metal ions on the SF-CNF were separated from the unbonded ion solution by centrifuge at 13,000 rpm for 10 min. The absorption performance of the SF-CNF hybrid was evaluated by the XPS. Additionally, filtration method was used to absorb and recycle these metal ions. Briefly, 10 mL of various metal ion solutions were filtrated through the SF-CNF membranes, and then the Au3+ and Ag+ ions immobilized on membranes were reduced into NPs by baking in water for overnight at 90 °C. For the catalytic activity, gold NPs supported on membranes were added to a solution consisting of 48.6 mg of NaBH4 in 10 mL (0.1 mM) of 4-NP to catalyze the reduction of 4-NP.58 Reactions were performed in room temperature with continuous stirring. For the SERS activity, silver NPs supported on membranes were added to a R6G solution with various concentrations for 30 min, and then the membranes were dried in room temperature for further Raman characterization. Bulging Test. For bulging tests, all samples were air-dried overnight and carried out at room temperature and 45% RH using a previously reported procedure.42,65 Briefly, a copper grid with a 300 μm aperture was mounted on an airtight holder, which was connected to a linear pump that can supply negative hydraulic pressure to the suspended nanomembrane. The pressure applied on the deflected nanomembranes was recorded by a pressure gauge directly connected to the pressure application system. A homemade single wavelength interferometer equipped with a He−Ne laser was used to monitor the vertical deflection of the apex of the membrane as the membrane was bulged, as shown in Scheme S1. Therefore, the pressure (P) and vertical deflection at the apex of the deformed nanomembrane (d) were captured simultaneously and converted to stress σ = Pr 2/4hd

(1)

and strain

where V is the volume of the filtered water (L), A is the effective membrane filtration area (m2), t is the filtration time (h), and P is the suction pressure across the membrane (bar). The filtration area of the filter is determined to be around 9.62 cm2, but the porosity of the PC membrane is around 10%, resulting an effective membrane filtration area of around 0.962 cm2. Target molecules and gold NPs were used to evaluate the membrane performance by filtrating the feed (20 mL) across the membrane under around 90 kPa pressure. The rejection rate (R, %) is calculated by using the following equation:

R=1−

Cp Cf

× 100%

(3)

ε = 2d 2/3r 2

(4)

where h is the thickness of the nanomembrane and r is the radius of the aperture. Molecular Dynamics Simulation. Each silk macromolecule consists of 258 amino acids, which represents a typical repetitive amino acid sequence of Bombyx mori proteins (Figure S21). Identical SF structure was used in the previous combined experimental and computational study and successfully interpreted silk’s specific behavior on the surfaces.20 The CNF structure is composed of 32 polysaccharide chains, and each chain has 39 glucose units. The CNF model used in the simulation is approximately 3.38 nm in diameter and 20 nm in length. The CNF was initially covered by five silk chains, which were positioned within 4 Å of the surface of fiber and then solvated in explicit TIP3P water (Figure S20).66 The simulations of the silk-CNF complex were conducted for 200 ns using the AMBER 16 package with ff14SB force field67 for the silk structure and GLYCAM-06j force field68 for the CNF. The system was carefully minimized and

(2)

where Cp and Cf are the concentrations of compound in the feed and permeate, respectively, determined by UV−vis spectroscopy. Characterization. AFM images were captured by AFM (ICON, Bruker) with soft tapping mode at 0.7 Hz in a usual manner.64 The TEM was performed with FEI Tecnai Osiris at 120 kV, and SEM was conducted on FEI Inspect F SEM at 10 kV accelerating voltage. A small drop of SF-CNF dispersion was cast on a carbon supported 12016


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ACS Nano equilibrated with our 11 stage protocol which was used in our previous studies for the surfaces20 and other biomolecules.21 First, 10,000 steps of minimization were carried out for only solvent molecules, while the SF and CNF were restrainted with 200 kcal/mol. Then, with the same restraint on the SF-CNF complex, the temperature of the system was gradually increased to 300 K during 40 ps. NPT simulations for at least 200 ps were performed with the SF-surface complex restrained with 200 kcal/mol in order to obtain a correct packing of the water. Then another minimization with 10,000 steps and a second NPT 200 ps equilibration were performed with the restraint of 20 kcal/mol on both SFs and the CNF. The additional four minimization stages were performed for 1000 steps by gradually decreasing the restraint on the complex. As a final equilibration step, a minimization and reheating step without constraint were carried out for 1000 steps and 40 ps, respectively. After careful equilibration steps, production simulation was executed for 200 ns under the NPT-ensemble at 300 K with 2 fs time step. Particle mesh Ewald (PME) summation method69 was used to calculate the electrostatic potential under periodic boundary condition in all directions. The results illustrated in this study, including representative snapshots and density-profile analyses, were analyzed by VMD 1.9.3.70 The CPPTRAJ module71 in AMBERTOOL 16 package is used for nonbonded interactions, secondary structure based on the dictionary of protein secondary structure (DSSP) method.72

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ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acsnano.7b04235. Additional experimental details, Figures S1−S24, Scheme 1 and Table S1 (PDF)

AUTHOR INFORMATION Corresponding Authors

*E-mail: [email protected]. *E-mail: [email protected]. ORCID

Shuaidi Zhang: 0000-0001-9949-8301 Vladimir V. Tsukruk: 0000-0001-5489-0967 Notes

The authors declare no competing financial interest.

ACKNOWLEDGMENTS This work was supported by Natural Science Foundation of China (51473100), China Scholarship Council (201406240067), Air Force Office for Scientific Research FA9550-14-1-0269c and FA8650-D-16-5404, U.S. National Science Foundation CBET-1401720. We thank Department of Energy award No. DF-FG-02-09ER466004 for SERS Analysis. H.S.K. and Y.G.Y. contributions were supported by National Science Foundation CMMI-1150682 and the NSF’s Research Triangle MRSEC (DMR-1121107). We thank Lijuan Zhang, Michelle Krecker, and Amy Ng for technical assistance. REFERENCES (1) Wegst, U. G. K.; Bai, H.; Saiz, E.; Tomsia, A. P.; Ritchie, R. O. Bioinspired Structural Materials. Nat. Mater. 2015, 14, 23−36. (2) Sanchez, C.; Arribart, H.; Giraud Guille, M. M. Biomimetism and Bioinspiration as Tools for the Design of Innovative Materials and Systems. Nat. Mater. 2005, 4, 277−288. (3) Barthelat, F.; Yin, Z.; Buehler, M. J. Structure and Mechanics of Interfaces in Biological Materials. Nat. Rev. Mater. 2016, 1, 16007. (4) Li, C.; Adamcik, J.; Mezzenga, R. Biodegradable Nanocomposites of Amyloid Fibrils and Graphene with Shape-Memory and EnzymeSensing Properties. Nat. Nanotechnol. 2012, 7, 421−427. 12017


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