Template-Guided Assembly of Silk Fibroin on Cellulose Nanofibers for

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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 ACS Nano, Just Accepted Manuscript • DOI: 10.1021/acsnano.7b04235 • Publication Date (Web): 13 Nov 2017 Downloaded from http://pubs.acs.org on November 14, 2017

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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, GA 303320245, USA §Department of Materials Science and Engineering, North Carolina State University, Raleigh, NC 27695-7907, USA

*Corresponding authors: [email protected]; [email protected]

Abstract The construction of multi-length scaled hierarchical nanostructures from diverse natural components is critical in the progress towards 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 supported 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−1m−2bar−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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The multi-length 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, CNF and amyloids from one side, and carbon fibers and nanotubes (1D components) and clay nanoplatelets and graphene (2D components) from other side.4-8 These nanocomposites demonstrated outstanding elasticity, strength and toughness as well as additive functionalities such as electrical conductivity, tunable transparency, or controlled permeability. However, attempts to integrate natural polymers with other bioderived reinforcing components rarely resulted in high-performance biomaterials due to a lack of multi-scale 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 β-sheet nanocrystals, these artificial silk materials still far low than the expectation. On the other hand, cellulose nanofiber (CNF) exists in the cell wall of plants, possessing 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 on the CNFs surface to facilitate their colloidal stabilization.11 The uniform 1D chiral geometry and abundant surface groups make CNF promising nanotemplates for fabricating advanced functional materials, including inorganic hollow nanotube,12 chiral metal nanocatalysts13 and flexible magnetic foams.14 Here, we report an all-natural bionanocomposites with exceptional mechanical performance by an unusual template-driven assembly, where silk fibroin self-assembles directly on straight segments of cellulose nanofibers 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 ACS Paragon Plus Environment

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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.

RESULTS AND DISCUSSION SF was extracted from the cocoons of Bombyx mori, which folded into domains of around 2 nm (Figure 1a and 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 and d, Figures S1b, S23, S24). The nanofibers are composed of continuous 280±115 nm long straight crystalline segments that separated by sharp kinks or misfit orientation, corresponding to the amorphous

Scheme 1. The assembly silk fibroin into shish kebab nanostructures on cellulose nanofibers.

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


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ATR-FTIR measurements, which are surface sensitive, and showed the absence of the characteristics bands beyond 1% sensitivity level (see Experimental and discussion in SI, Figure S23). Surprisingly, combining both components in solution results in a spontaneous formation of organized periodic nanostructures never observed for silk materials (Figure 1).

Figure 1. Morphologies of cellulose nanofibers, silks, and their assembly. AFM images: ACSSF-30 Paragon Plus Environment (a) SF, (c) CNF and (e) assembled 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).

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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 (Figure

Figure 2. Insight of the template-directed assembly of silk backbones on CNF: (a) Highresolution 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.

1e and f, 2, and Figures S1c, S2).


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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 single silk molecular chain as estimated by comparing the measured geometric dimensions of silk domain from high resolution AFM images considering tip dilation and theoretical value of silk backbone volume assuming dense packing (Fig. 2a). 16 The TEM image of the assembled SF-CNF materials also demonstrated that the individual nanofibers are coated by silk to form coreshell structures and bundles (inset in Figures 2a; Figure S3; see the Supporting Information). However, excessive CNF aggregation after drop casting on 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 silk fibroin 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 in-between (single sheet with 0.4 nm thickness) (Figure 2b). This model not only explains all these observed morphological features, also consistent with molecular dimensions of different SF secondary structures.17 We propose that the linearly heterogeneous/amphiphilic nature of CNF surface plays a critical role in this periodic self-organization of silk domains. 18, 19, The 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 interaction between silk protein chains with the cellulose nanofiber 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 water environment, the initial uniform silk structure adapted different organization with backbones assembled into aggregated disordered silk domains and extended and more flattened single-molecular ACS Paragon Plus Environment

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β−sheets structures (last structure in Figure 3a and Figure 3b). 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, weak van der Waals and electrostatic interactions can stabilize ordered structures and make ordered sheets more

Figure 3. All-atom MD simulations of the self-assembly of silk fibroin on cellulose nanofiber. (a) Representative all-atom simulation snapshots of initial SF-CNF 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 last 10 ns simulation and its standard deviation. A gray dotted line is the density profile for the initial SF-CNF distribution.

extended along the nanofiber surface (Figure S4). In fact, ordered structure of bio-molecules such as silk fibroins20 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 silk fibroin 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 oxygen-rich or hydrophilic region can facilitate significant structural changes by a decrease in the interfacial hydrogen bonding between silk and CNFsurface (Figure S5). Overall, the heterogeneous nature of CNF surface can induce different non-bonded ACS Paragon Plus Environment

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interactions with silk proteins which heavily influence the secondary structure of silk domains with formation of largely separated domains of different type 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 with -38 mV cannot be a major driving force in silk-nanofiber assembly.

But these repulsive

interactions are instructive in stabilizing and preventing larger-scale aggregation of individual SF-CNF nanostructures with overall surface potential of -20 mV. Then, hydrogen bonding between silk backbones and CNF surface 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 inter-component 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 cellulose nanofibers (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 to be 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 of carboxylic groups on CNF surfaces and amid groups of the silk components. Next, 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 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 (Figure S1d and S7b). Notably, it has been widely reported that the silk micelles also can self-assemble into nanofibrils at carefully controlled environment without adding of any CNF. 25,26 This assembly ACS Paragon Plus Environment

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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 if stable periodic domain morphology. In fact, the shish-kebab morphology remains the same (sizes, spacing, thickness) at different assembly times ranging from 12 hrs to 72 hrs 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, 0.1 wt% SF aqueous solution containing 7 vol% ethanol were incubated at pH 9.5 and room temperature for two 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, the as-prepare SF

nanofibrils show an random network of curved and folded nanobundles with octopus-like shapes in contrast to the straight and uniform SF-CNF nanofibers fabricated here (Figure S10 a and b). Although both samples show similar domain morphologies, the diameter and length of the silk nanobundles is 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 overall morphology of SF nanobundles is dynamic and changes dramatically with assembly time, the SF-CNF shish-kebab nanostructures are extremely stable. Next, we consider the role of these shish-kebab morphology in the mechanical performance of SF-CNF materials. The as-prepared spin-cast 50 nm ultrathin membranes show highly uniform porous morphology with 1 µm ×1 µm surface roughness (Rq) of 2.1 nm, similar with bare SF and CNF membranes (Figure 4a and 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 silk-decorated nanofibers (Figure S12, S13).


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Additionally, the bulging test generated reliable 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 release and transfer process that involves high stresses during drying and mechanical deformation,29 even suspend on a 300 µm circular aperture without any cracks or wrinkles (Figure S15). SF-CNF membranes with 30 wt% CNF possessing the highest mechanical performance with Young’s modulus of 30 ± 3 GPa and ultimate stress of 260 ± 36 MPa (Figure 4d and 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 SF-CNF 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 nanofiber along the axial direction.38 For instance, PVA-cellulose fibers composites showed very high strength (ultimate stress of around 800 MPa) and high elastic modulus of 30 GPa.39,40 The combination of cellulose nanofibers with spider silk also resulted in the ultrarobust microfibers with the elastic modulus of 55 GPa, 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 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 than 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 nitrogen absorption experiment (Figure S17).

Then, the water transport performance of the SF-CNF membranes with


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interlocked shish-kebab nanostructures was studied under the pressure of 1 bar for membranes with thickness from 50 nm to 1000 nm. Surprisingly, a 50 nm thick SF-CNF membrane demonstrates an extremely high flux, , up to 3.5 x 104 L h−1m−2bar−1, hundreds times higher than commercial filtration membranes and dramatically better than reported ultrathin membranes of 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−1m−2bar−1) is still much higher than that of most commercial filtration membranes.51

Figure 4. Micromechanical properties of silk-CNF membranes. AFM images of ultrathin (a) SF, (b) SF-30 wt%CNF and (c) CNF membranes, z-scale is10 nm. Inset is the edge of this membrane after transfer. (d) Ultimate strength and (e) Young’s modulus of SF-CNF membranes with different CNF content. (f) Comparison of Young’s modulus and strength of SF-CNF membranes with other reported nanocomposites containing various combinations of CNF or SF materials.

As known, Hagen–Poiseuille equation predicts that combination F×t where t is the membrane thickness should be constant under unchanged conditions (morphology, pressure, velocity,


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and viscosity).49,52 Indeed, the summary of 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 extremely high value for the thinnest possible membranes (50 nm) (Figure 5a). Correspondingly, the same F×t - t plot shows constant value only for intermediate SF-CNF thicknesses within 300 nm - 1000 nm. Thus, these thicker membranes follow the well-known and widely spread behavior predicted by Hagen–Poiseuille equation. However, for ultrathin membranes with thicknesses below 200 nm, F×t increases four-fold in the comparison with steady value of 4.5 x 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 enforce predominantly planar random orientation of nanofibers during wet fabrication that allows for effective opening size increase due to uneven contact of the shishkebab nanostructures. For further evaluation of transport properties, different dyes and labeled nanoparticles 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 (Figures 5e, 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 nanoparticles (Au NPs) (Table S1, Figure S20). Overall, both the flux rate and rejection rate of SF-CNF membranes fabricated in this study were several times 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


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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. On the other hand, strong π−π and hydrophobic-hydrophobic interactions between dye cores and tyrosine units of silk surfaces also contribute to high separation performance.


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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) the 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) The as-prepared 200 nm membrane supported on PC filter before and after filtrating R6G, (e) rejection rate of 200 nm thick assembled SF-CNF membranes for different subjects, (f) comparison of 5 nm gold nanoparticles 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) perylene3,4,9,10-tetracarboxylic diimide)-2,2’-bipyridine.

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 nanoparticles by these membranes via a bio-mineralization process as reported for silks (Figure 6b,c). 56 These reduced metal nanoparticles 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 (4-NP) to 4- aminophenol (4-AP) (Figure 6d).57


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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 detect R6G.

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 found to complete very fast, within 6 min.

Moreover, we

demonstrated the surface enhanced Raman scattering (SERS) ability of these membranes with reduced silver nanoparticles in detection of the trace amount of Rhodamine 6G down to very low concentration of 0.1 nM, on par with the best porous SERS substrates (Figure 6e).58

CONCLUSIONS In summary, we observed a peculiar shish kebab nanostructures formed by CNF-directed assembly of silk fibroin domains. In these nanostructures, highly periodic silk domains selfassembled along the straight segments of cellulose nanofibers up to 1 µm in length due to ACS Paragon Plus Environment

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modulated interfacial interactions along heterogeneous surfaces of amphiphilic cellulose nanofibers.

These well-ordered and very 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 that are unachievable for individual protein and polysaccharide components such as silk bundles, sulk fibers, and cellulose fibrous nanomaterials. The extremely high water permeability shown by the ultrathin membranes are two to three 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 nanoparticles facilitates added functionality for catalytic-related and SERS applications.

EXPERIMENTAL 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. 59 Then high speed centrifugation (10000 rpm, 20 min, 5°C) was used twice to purify the silk fibroin 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.60 Briefly, TEMPO (0.016 g, 0.1 mmol) and sodium bromide (0.1 g, 1 mmol) were added into wood pulp suspension (100 mL,1 wt.%). Then the desired amount of the NaClO solution (12%, 10 mmol NaClO per gram of cellulose) were added into 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


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17

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 cellulose nanofibers. High speed centrifugation (10000 rpm, 20 min, 5 °C) was conducted to separate the un-exfoliated cellulose fibers from the obtained cellulose nanofiber suspension. The resulting ultrafine cellulose nanofiber 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 conductometric titration, which is close to previous report60 (see the Supporting Information). During the TEMPO treatment and the purified process of the CNF, virtually all of the lignin and hemicellulose components have been 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 silk fibroin. The trace of hemicellulose is below 1 wt% as estimated from ATR-FTIR (for detail see the Supporting information, Figure S23). 11 Template directed-assembly of SF-CNF nanostructures Typically, 5 mL CNF suspension (0.1 wt%, pH 6.8) was added into a silk fibroin solution (10 mL, 0.1 wt%, pH 7.4) very slowly to avoid aggregation of silk fibroin. 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 oC for preventing 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 the low temperature and neutral condition.59,61 To characterize the morphology of the SF-CNF nanostructures by AFM, we prepared the samples by spinning coating the as-prepared mixture on the 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 high-resolution AFM images with 1024x1024 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 the silicon wafer from 2 wt% solution by spinning coating at 3000 rpm prior formation of SF-CNF film.62 To ensure efficient deposition, the concentration of mixture was around 0.5 wt%. After the thickness of membranes reaches 5060 nm, they were then rinsed with methanol to further crystallization. ACS Paragon Plus Environment

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nanomembranes were released by dissolving the sacrificial layer in acetone and transferred to copper grids with 300 µm aperture to test micromechanical performance (see below). Separation performance measurements For the separation test, all the SF-CNF (7:3 w/w) membranes were fabricated by vacuumassisted 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: =

(1)

where is the volume of the filtered water (L), is the effective membrane filtration area (m2), is the filtration time (h), and 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 around of 0.962 cm2.

Target molecules and gold nanoparticles 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:

= 1 − × 100% (2)

where and are the concentrations of compound in the feed and permeate respectively, determined by UV-vis spectroscopy. Hagen–Poiseuille equation52 relates flux and membrane thickness as: =

∆

(1) via the

pore radius rp, the pressure difference ∆p; the water viscosity, µ, and the total water travel distance, L. This theory predicts that considering the L linearly relates to the membrane thickness t under usual approximation, L= κ (2), the the product =

∆

(3) should be

constant under unchanged conditions (morphology, pressure, velocity, and viscosity).49 Characterization


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AFM images were captured by AFM (ICON, Bruker) with soft tapping mode at 0.7 Hz in usual manner. 63 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 TEM copper grid before the TEM characterization, and the SF-CNF on silicon wafer was sputtered 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−visible

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 were carried out by Micromeritics ASAP 2020. XPS spectra were obtained with a Thermal Scientific K-alpha XPS instrument. Absorption test SF solution (1 mL, 0.5 wt%) was carefully added into CNF dispersion (5 mL, 0.15 wt%) and keep them at 4oC for a day. Then, 10 ml various metal ion solutions (10 mM, HAuCl4, AgNO3, CuCl2 and NiCl2) were added in 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 13000 rpm for 10 min. The absorption performance of the SF-CNF hybrid were evaluated by the XPS. Additionally, filtration method was used to absorb and recycle these metal ions. Briefly, 10 ml 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 90oC. For the catalytic activity, gold NPs supported on membranes was added to a solution consisting of 48.6 mg NaBH4 in 10 mL (0.1 mM) 4-NP to catalyze the reduction of 4-NP.57 Reactions were performed in room temperature with continuous stirring. For the SERS activity, silver NPs supported on membranes was added ion to R6G solution with various concentration for 30 min, then the membranes were dried in room temperature for further Raman characterization. Bulging test


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For bulging tests, all samples were air-dried overnight and carried out at room temperature and 45% RH using a previous reported procedure.42,64 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 () and vertical deflection at the apex of the deformed nanomembrane ( ! ) were captured simultaneously and converted to stress " = # $ /4ℎ! (3) and strain ( = 2! $ ⁄3 # $ (4), where ℎ is the thickness of the nanomembrane and # is the radius of the aperture.

Molecular Dynamics Simulation Each silk macromolecules consist of 258 amino acids which represents a typical repetitive amino acid sequences of Bombyx Mori proteins (Figure S21). Identical silk fibroin 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 are 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 were 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).65 The simulations of silk – CNF complex were conducted for 200 ns using AMBER 16 package with ff14SB force field66 for silk structure and GLYCAM-06j force field67 for the CNF. The system was carefully minimized and equilibrated with our 11 stage protocol which has used in our previous studies for the surfaces20 and other bio-molecules.21 First, 10,000 steps of minimization was carried out for only solvent molecules while the silk fibroin and CNF were restraint with 200 kcal/mol.


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Then, with the same restraint on the silk fibroin–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 silk fibroin–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 silk fibroins and the CNF. The additional four minimization stages were performed for 1,000 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 1,000 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 method 68 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 1.9.3.69 Also, CPPTRAJ module 70 in AMBERTOOL 16 package is used for non-bonded interactions, secondary structure based on the dictionary of protein secondary structure (DSSP) method.71 ASSOCIATED CONTENT Supporting Information The Supporting Information is available free of charge on the ACS Publications website at DOI:\\.... Additional experimental details, Figures S1−S24, Scheme 1 and Table S1. Acknowledgment This work was supported by Natural Science Foundation of China (51473100), China Scholarship Council (201406240067), Air Force Office for Scientific Research FA9550-14-10269c and FA8650-D-16-5404, U.S. National Science Foundation CBET-1401720, Department of Energy Award No. DE-FG-02-09ER466004. 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. Conflict of interest The authors declare no conflict of interest.


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ACS Nano

Assembled SF-CNF 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

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Template-Guided Assembly of Silk Fibroin on Cellulose Nanofibers for

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