Preparation of Ultrathin, Robust Nanohybrid Capsules through a

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Preparation of Ultrathin, Robust Nanohybrid Capsules through A “Beyond Biomineralization” Method Shaohua Zhang, Zhongyi Jiang, Weilun Qian, Jiafu Shi, Xiaoli Wang, Lei Tang, Hongjian Zou, and Hua Liu ACS Appl. Mater. Interfaces, Just Accepted Manuscript • DOI: 10.1021/acsami.7b00308 • Publication Date (Web): 21 Mar 2017 Downloaded from http://pubs.acs.org on March 26, 2017

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ACS Applied Materials & Interfaces

Preparation of Ultrathin, Robust Nanohybrid Capsules through A “Beyond Biomineralization” Method Shaohua Zhanga,c, Zhongyi Jianga,c, Weilun Qiana,c, Jiafu Shi*,b, Xiaoli Wangd, Lei Tanga,c, Hongjian Zoua,c, Hua Liua,c a

Key Laboratory for Green Chemical Technology of Ministry of Education, School of Chemical

Engineering and Technology, Tianjin University, Tianjin 300072, China; b

c

School of Environmental Science and Engineering, Tianjin University, Tianjin 300072, China; Collaborative Innovation Center of Chemical Science and Engineering (Tianjin), Tianjin

300072, China; d

Tianjin key Laboratory of Biomaterial Research, Institute of Biomedical Engineering, Chinese

Academy of Medical Science, Tianjin 300192, China. ABSTRACT: Herein, a facile and generic method is developed to prepare ultrathin, robust nanohybrid capsules by manipulating the dynamic structure of supramolecular nanocoatings on CaCO3 sacrificial templates through incorporating multivalent-anion substitution process into biomineralization. Above biomineralization level, multivalent anions, e.g., phosphate, sulfate or citrate, are employed to initiate the assembly of polyamine into continuous (non-segregated) polyamine-anion supramolecular nanocoatings on CaCO3 sacrificial templates. When contacting with the sodium silicate solution, the multivalent anions in the supramolecular nanocoatings are substituted by silicate because of the difference in dissociation behaviour, facilitating the structure-reconstruction of supramolecular nanocoatings. At biomineralization level, the substituted silicate can not only bind to polyamine through electrostatic and hydrogen bonding interactions, but also undergo silicification to generate interpenetrating silica framework. After

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dissolution of CaCO3, polyamine-silica nanohybrid capsules bearing an ultrathin wall of ~10-17 nm in thickness are formed, which exhibit super-high mechanical strength of ~2337 MPa in elasticity modulus. The capsules are then utilized for bioreactor construction through encapsulating glucose oxidase (GOD). The ultrathin capsule wall facilitates the diffusion of substrates/products and elevates the conversion efficiency, whereas the high mechanical strength ensures the structural integrity of capsules during multiple-cycle reactions. This method can also be applied for the preparation of ultrathin films on planar substrates, which would open a feasible way to prepare nanohybrid materials with different compositions and shapes. KEYWORDS: biomineralization, multivalent-anion substitution, supramolecular nanocoating, ultrathin nanohybrid capsules, bioreactor 1. INTRODUCTION As one kind of emerging materials, organic-inorganic hybrid materials have elicited ripples of excitement in many research communities due to their tunable topological structures and integrated properties from organic and inorganic moieties.1,2 Hybrid capsules, a typical freestanding thin film, are one representative branch of hybrid materials and broadly utilized in separation, catalysis, drug delivery, etc., of which merits of high mechanical strength, nanoscale thickness, and defect-free structure are highly pursued.3-5 Metal ions and inorganic nanoparticles (NPs) are two kinds of inorganic building blocks for the preparation of hybrid capsules.5 Usually, metal ions are employed to form hybrid capsules through coordination with organic moieties bearing metal-chelating groups.3,6,7 In general, the coordination bonding energy (200-400 kJ mol-1) is stronger than electrostatic force (50-200 kJ mol-1) and hydrogen bonding energy (5-30 kJ mol-1). However, most of coordination bonds are only stable in a narrow pH range (7-9), which severely restricts their applications in pH-fluctuant


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situations, such as separation and catalysis.8,9 In contrast, inorganic NPs can bind to organic moieties through multiple specific or non-specific interactions. The diversity of interactions and architectural control ensures the capsules against different external stimuli, and renders them excellent mechanical stability.10-12 In the past decades, researchers primarily focus on the introduction of pre-synthesized inorganic NPs into organic matrix to form hybrid capsules.13,14 The aggregation of inorganic NPs is inevitable and difficult to eliminate. As a result, ultrathin and defect-free hybrid capsules are often difficult to be acquired.15 Since 2000, biomineralization, a nano-engineering process by which living organisms produce hybrid materials using biomacromolecule as inducer and inorganic substance as precursor, has gained floods of attentions due to the facile, controllable and versatile features.16 The multi-scale hierarchical structure confers biominerals with ultrahigh mechanical strength.2 Simultaneously, the biomineralized biomacromolecules become more robust and efficient in comparison with the native ones.17-19 Interestingly, the hybridization process involves pre-assembly and segregation of macromolecule inducers with multivalent anions to form macromolecule-anion complex, termed as molecule-hybrid matrix,20,21 which helps to reduce free energy and kinetic barrier for nucleation and facilitate in situ deposition of inorganic precursors.22-24 For instance, silaffins, a well-known macromolecular inducer for biosilicification in diatom that composed of polyamine moieties covalently bonded with phosphate groups, could self-assemble and segregate into patterned molecule-hybrid matrix on diatom surface.25-28 The molecule-hybrid matrix then acted as a stable template and catalyst to facilitate the adsorption and condensation of silicate, leading to the formation of patterned biosilica as the diatom wall.21 Inspired by biomineralization, the templating and catalytic functions of molecule-hybrid matrix have been extensively explored to synthesize a series of delicate bulky and solid particulate structures.29-31 However, achievements


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relevant to ultrathin and defect-free capsules were rarely reported due to the strong segregation behavior of macromolecular inducers. The segregation phenomenon would cause the deposited molecule-hybrid matrix on substrates in a stable but discontinuous manner. Further mineralization along the scaffold of molecule-hybrid matrix would generate defects on the final ultrathin capsules. To ensure the integrity and continuity of the ultrathin capsules, multiple-cycle deposition and mineralization were often required through the incorporation of other techniques (commonly as layer-by-layer (LbL) assembly).11 Suppressing the segregation behavior of macromolecular inducers and manipulating the dynamic structure of molecule-hybrid matrix may offer a feasible way to form ultrathin and defect-free capsules, which, to the best of our knowledge, have not yet been covered till now.3,32 In this study, we reported a facile and universal method to prepare ultrathin, robust nanohybrid capsules. Above biomineralization level, the assembly process of poly(allylamine hydrochloride) (PAH, macromolecular inducer) and multivalent anions (phosphate, sulfate or citrate) was manipulated to suppress the segregation phenomenon. The resultant molecule-hybrid matrix, such as supramolecular nanocoatings of PAH-phosphate, PAH-sulfate or PAH-citrate, was then engineered through the substitution of multivalent anions by silicate. At biomineralization level, the substituted silicate further went through condensation to form interpenetrating silica framework. The multivalent-anion substitution and the subsequent condensation process enabled the formation of ultrathin and defect-free nanohybrid capsules. The chemical/topological structures and mechanical strength of the capsules were extensively characterized. The formation mechanism of the capsules, including the function of multivalent anions and the substitution process, was elucidated in detail. To our knowledge, this is the first attempt of introducing multivalent-anion substitution for the preparation of ultrathin nanohybrid capsules. Exploration


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of the as-synthesized capsule to encapsulate enzymes for constructing bioreactors was further carried out, which revealed the great potential of the nanohybrid capsules in bioconversion and biosensing, etc. 2. EXPERIMENTAL SECTION 2.1. Materials Poly(allylamine hydrochloride) (PAH, Mw ~15000), glucose oxidase from Aspergillus niger (GOD, 100-250 kU g-1, E.C.1.1.3.4) and 3,3',5,5'-tetramethylbenzidine dihydrochloride hydrate (TMB) were purchased from Sigma-Aldrich. Sodium silicate (Na2SiO3), dibasic sodium phosphate (Na2HPO4·12H2O), sodium dihydrogen phosphate (NaH2PO4·2H2O), sodium sulfate (Na2SO4),

sodium

citrate

dihydrate

(Na3C6H5O7·2H2O),

calcium

chloride

dihydrate

(CaCl2·2H2O), sodium carbonate (Na2CO3) and ethylenediaminetetraacetic acid (EDTA) were purchased from Tianjin Guangfu Fine Chemical Research Institute. Peroxidase (horseradish) (HRP, ≥300000 U g-1, E.C. 1.11.1.7) was obtained from Shanghai Yuanye Biotechnology Company Limited. The other chemicals without special illustration were of analytical grade. Water utilized in the experiments was obtained from the water purification system provided by Millipore. 2.2. Preparation of Polyamine-Silica (PS) Ultrathin Nanohybrid Capsules CaCO3 spheres with a diameter of ~5-6 µm were selected as the sacrificial templates and prepared by co-precipitation method as reported previously.23 The obtained CaCO3 spheres were dispersed into the freshly prepared PBS buffer (5 mM, pH 7.0) containing 0.2 mg mL-1 PAH. After shaking for 10 min, the suspension was centrifuged and washed with deionized water for three times. Then, the obtained spheres were dispersed into the freshly prepared solution of Na2SiO3 (30 mM, pH 7.0-8.0) and shaking for 10 min. The spheres were collected by


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centrifugation and then added to the aqueous solution of EDTA (50 mM, pH 6.0) to remove CaCO3 component. Finally, PS ultrathin nanohybrid capsules were obtained after water washing and centrifugation for three times (6000 rpm, 1 min). PS ultrathin nanohybrid films were also formed on planar substrates (silicon wafer and Au QCM-D sensors) based on the same procedure as mentioned above. 2.3. Preparation of Ultrathin Nanohybrid Capsules Induced by Substitution of Sulfate and Citrate CaCO3 spheres, as the sacrificial templates, were added into the freshly prepared sodium sulfate or sodium citrate solution (5 mM, pH 7.0) containing 0.2 mg mL-1 PAH, which was shaking for 10 min. Similar to the preparation of PS ultrathin nanohybrid capsules, the obtained spheres were then added into the freshly prepared solution of Na2SiO3 (30 mM, pH 7.0-8.0) for 10 min. After removing CaCO3 spheres through EDTA treatment, ultrathin nanohybrid capsules were obtained. Similarly, Au QCM-D sensors were also selected as the planar substrates, on which the procedure of preparing ultrathin nanohybrid films was similar to that on CaCO3 spheres. 2.4. Preparation of GOD@capsule Systems GOD was first encapsulated into CaCO3 spheres during co-precipitation process. The GODencapsulated CaCO3 spheres were utilized as the templates to prepare PS ultrathin nanohybrid capsules. After removing the templates, GOD-encapsulated PS ultrathin nanohybrid capsules (GOD@capsule systems) were prepared. 2.5. Activity Assay of GOD@capsule Systems The activity of GOD@capsule systems was determined by monitoring H2O2 with TMB substrate through a second reaction catalyzed by HRP. Specifically, β-D-glucose would first


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diffuse into the ultrathin nanohybrid capsules and react with oxygen, generating gluconic acid and H2O2 catalyzed by the encapsulated GOD. The generated H2O2 was utilized to oxidize TMB into oxTMB catalyzed by HRP. The concentration of H2O2 could be calculated by monitoring the absorption intensity at 652 nm through UV-vis spectrometer (Hitachi U-3010). 2.6. Recycling Stability of GOD@capsule Systems Herein, GOD@capsule systems were collected by centrifugation after each reaction and reused for the next reaction after water washing. 2.7. Characterization SEM images were recorded by using a field-emission scanning electron microscope (FESEM, Nanosem 430). TEM image was measured through a field-emission transmission electron microscope (Tecnai G2 F20). Elemental analysis was determined by energy dispersive spectroscope (EDS) attached to TEM. Fourier transform infrared spectroscope (FTIR) spectrum was obtained on a Nicolet-6700 spectrometer. 32 scans were accumulated with a resolution of 4 cm-1 for the spectrum. The surface elemental composition was analyzed by X-ray photoelectron spectroscope (XPS) in a Perkin-Elmer PHI 1600 ESCA system with a monochromatic Mg Kα source and a charge neutralizer. Atomic force microscope (AFM) images of the ultrathin nanohybrid capsules were recorded through BRUKER Dimension Icon in tapping mode. AFM measurement of the supramolecular nanocoatings before and after silica deposition was performed under tapping mode in a closed fluid cell filled with deionized water using BRUKER Dimension Icon. Quartz crystal microbalance with dissipation (QCM-D) experiments were conducted using a Q-Sense instrument (QE401-F1304) equipped with a flow module. A QSX301 4.95 MHz gold sensor was employed. 3. RESULTS AND DISCUSSION


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3.1. Preparation and Formation Mechanism of Ultrathin Nanohybrid Capsules

Scheme 1. Schematic preparation process of Polyamine-Silica (PS) ultrathin nanohybrid capsules through the substitution of phosphate.

Capsules are one typical thin film bearing the self-enclosed, free-standing feature, which can be utilized in various applications, including catalysis, adsorption, drug delivery, etc. Our method was firstly presented through preparing Polyamine-Silica (PS) ultrathin nanohybrid capsules (Scheme 1). CaCO3 spheres prepared by co-precipitation were selected as the sacrificial templates and added into the freshly prepared PBS buffer (5 mM, pH 7.0) containing 0.2 mg mL1

PAH. PAH-Phosphate (PPA) supramolecular nanocoatings were then assembled on CaCO3

spheres through electrostatic and hydrogen bonding interactions between PAH and phosphate. The atomic ratio of N and P in PPA supramolecular nanocoatings was 2.4 (Figure S1, Supporting Information), which was consistent with previous literature.32 This result suggested that each phosphate group was surrounded by more than two amine groups in PPA supramolecular nanocoatings. Next, PPA-coated CaCO3 spheres were added into the freshly prepared sodium silicate solution. After the substitution of phosphate by silicate and further


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PAH-induced silicification, ultrathin PS nanohybrid films were formed on CaCO3 spheres. Finally, PS ultrathin nanohybrid capsules were obtained after removing CaCO3 component through EDTA treatment.

Figure 1. Topological and chemical structure of PS ultrathin nanohybrid capsules. (a, b) SEM images, (c) AFM height image, (d) EDS, (e) FTIR and (f) XPS spectrum of PS ultrathin nanohybrid capsules. Insets in (b) and (c) were, respectively, the high-resolution TEM image and height profile of PS ultrathin nanohybrid capsules. Note that the small peak at around 1 keV in (d) was ascribed to the Cu element from the copper mesh.

Figure 1 exhibited a collapsed structure of PS ultrathin nanohybrid capsules with a diameter of ~5-6 µm, which should be owing to the ultrathin capsule wall and water evaporation during sample preparation. Non-defective and amorphous structures were observed when amplifying the capsule wall (Figure 1b). To determine the capsule wall thickness, atomic force microscope (AFM), a general equipment to measure the thickness of thin films and capsules, was used.33,34


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As shown in Figure 1c, a non-uniform height profile was obtained, which should be attributed to the ridge generated by the collapsed structure of PS ultrathin nanohybrid capsules. Wall thickness of PS nanohybrid capsules was calculated to be 17.3±0.9 nm by making half of the smallest height difference in the height profiles of three different capsules, demonstrating the ultrathin structure of PS nanohybrid capsules. The Si element detected in energy dispersive spectroscope (EDS) spectrum confirmed the involvement of silicate/silica in PPA supramolecular nanocoatings (Figure 1d). Besides, C and N elements were also detected, which were totally from PAH. No peak of P element was observed, indicating the complete removal of phosphate during silicate substitution and silicification. Accordingly, the detected O element should totally come from the introduced silicate/silica. To further validate the absence of phosphate in PS ultrathin nanohybrid capsules, Fourier transform infrared spectroscope (FTIR) and X-ray photoelectron spectroscopy (XPS) spectrum of the capsules was also conducted (Figure 1e and f). Consistently, no characteristic band for phosphate and peak for P element were observed. As was reported,35 two main species of Si(OH)3O- and Si(OH)4 should exist in fresh dilute sodium silicate solution (30 mM, pH 7.0~8.0). P element in phosphate showed stronger oxidizing ability than Si element in silicate, which reduced the electron density around O element. This contributed to the bigger dissociation constant of H3PO4 and H2PO4- than Si(OH)4 (Table S1, supporting information). Thus, Si(OH)3O- could bind -NH3+ in polyamines more strongly than H2PO4- and HPO42-, which facilitated the substitution of phosphate by Si(OH)3O-. Besides the substitution of phosphate by silicate, silicification induced by PAH also occurred, which was demonstrated by absorption band of Si-O-Si groups at around 796 and 1100 cm-1 in FTIR spectrum (Figure 1e). The calculated atomic ratio of Si and O of 1:2.47 from the EDS spectrum (Figure 1d), combined with Si-OH groups detected in FTIR and Si 2p XPS


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spectrum (Figure S2, supporting information), further confirmed the partial condensation of silicate during the formation of PS ultrathin nanohybrid capsules.

Figure 2. Formation of interpenetrating silica framework induced by PPA supramolecular nanocoatings. (a) AFM phase image of a partially coated silicon wafer by PPA supramolecular nanocoatings (z-scale: 29.2o) with visible boundary. The partially coated silicon wafer was immersed in freshly prepared sodium silicate to induce silica deposition by PPA supramolecular nanocoatings, forming PS ultrathin nanohybrid films. (d) AFM phase image near the boundary of PS ultrathin nanohybrid films coated silicon wafer (z-scale: 47.2o). (b, e) Height profile along the black line in (a) and (d), respectively. (c, f) High-resolution 3D AFM phase image of PPA supramolecular nanocoatings (z-scale: 14.4o) and PS ultrathin nanohybrid films (z-scale: 28o). Note: to keep the original topology of the films, the above-mentioned AFM experiments were conducted under deionized water in tapping mode.


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To demonstrate the formation mechanism of PS ultrathin nanohybrid capsules, a partially coated silicon wafer, a planar substrate, by PPA supramolecular nanocoatings was used to induce silica deposition. AFM was used to examine the morphology, roughness and thickness of PPA supramolecular nanocoatings before and after silica deposition. As shown in Figure 2a and c, PPA supramolecular nanocoatings exhibited a dense and smooth appearance with a root mean square (RMS) roughness of 29.0 nm. After silica deposition, a rougher surface with an RMS roughness of 41.9 nm was obtained (Figure 2f). The reason should be that the generated silica nanoaggregates induced by PAH roughened the surface of PS ultrathin nanohybrid films. Interestingly, the thickness of PPA supramolecular nanocoatings decreased from 26.3 to 11.0 nm after silica deposition (Figure 2b and e). The sharp decrease of the thickness should be ascribed to the partial disassembly of PPA supramolecular nanocoatings during the substitution of phosphate by silicate. Some nanoaggregates loosely packed on the periphery of PS ultrathin nanohybrid films were also observed as pointed by the blue arrows (Figure 2d). These nanoaggregates were probably formed by silicification induced by the released PAH, further indicating the partial disassembly of PPA supramolecular nanocoatings during silica deposition.


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Figure 3. Dynamic formation process of PS ultrathin nanohybrid films. (a). Change in frequency and dissipation during the formation of PS ultrathin nanohybrid films. The PPA supramolecular nanocoatings were first coated on Au QCM-D sensor with PBS buffer (5 mM, pH 7.0) containing 0.2 mg mL-1 PAH. Then, PPA supramolecular nanocoatings were used to induce silica deposition with freshly prepared sodium silicate solution (30 mM, pH 7.0~8.0). The flow rate was set as 100 µL min-1. (b) Schematic silica deposition process induced by PPA supramolecular nanocoatings.

To in-depth understand the mechanism of silica deposition, the growth kinetics of PS ultrathin nanohybrid films was monitored by quartz crystal microbalance with dissipation (QCM-D). First, PPA supramolecular nanocoatings were coated on Au QCM-D sensor, another planar substrate. At this stage, the frequency dropped linearly for ~60 min (Figure 3a), suggesting the


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continuous growth of PPA supramolecular nanocoatings. The deposition rate of PPA supramolecular nanocoatings was calculated to be 404 ng cm-2 min-1 according to Sauerbrey equation. When fresh sodium silicate solution (30 mM, pH 7.0~8.0) was added, the frequency initially went through a decrease of about 120 Hz (Figure S3, supporting information). Since the frequency shift was about 4 Hz (data not shown) for bare Au QCM-D sensor when replacing water with fresh sodium silicate solution (30 mM, pH 7.0~8.0), the big frequency shift of 120 Hz should correspond to the quick absorption of silicate. Subsequently, the frequency maintained a relative stable value for ~2 min, which should be due to the equilibrium between the release of phosphate and absorption of silicate. After a short equilibrium, the frequency got sharply increased. This should be due to the partial disassembly of PPA supramolecular nanocoatings induced by anions substitution and condensation of silicate, which was in line with the decreased thickness assessed by AFM. Finally, the frequency reached a plateau indicating the accomplishment of silicification. Taken together, the silica deposition process induced by PPA supramolecular nanocoatings could be divided into three steps (Figure 3b). (i) First, the silicate was absorbed by PPA supramolecular nanocoatings and bonded with the partially protonated primary amine groups of PAH. Due to the smaller dissociation constant of Si(OH)4 than H3PO4 and H2PO4-, phosphate in PPA supramolecular nanocoatings would be released. However, at the initial stage, the release rate of phosphate was smaller than the absorption rate of silicate, causing the mass increase of the films. (ii) Along with the absorption of silicate, the release rate of phosphate increased, leading to the partial disassembly of PPA supramolecular nanocoatings. Simultaneously, the absorbed silicate went through condensation, forming interpenetrating silica framework. (iii) Finally, all phosphate was released from the films and silicification was accomplished.


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The proposed silica deposition mechanism showed somewhat similarity to biosilicification induced by silaffins in diatoms (Figure S4, supporting information). Due to the zwitterionic structure, bearing phosphate groups and polyamines, silaffins would assemble into aggregates through the electronic and hydrogen bonding interactions.21 Silicic acid was then dissolved in the aggregates and underwent condensation, thus forming silica NPs. Since the phosphate groups were covalently bonded to silaffins, the assembly of silaffins was difficult to regulate, and the substitution of phosphate groups during silicification would not occur. In our study, to suppress the segregation behavior of PAH-phosphate assembles, we first manipulated the interaction between phosphate and PAH to form continuous PPA supramolecular nanocoatings. Silicate then substituted phosphate in PPA supramolecular nanocoatings and went through condensation, forming PS ultrathin nanohybrid films. The formation of PPA supramolecular nanocoatings and subsequent substitution of phosphate by silicate were actually above the level of conventional biosilicification. It should be noted that PAH adsorbed on substrates in the absence of phosphate could also induce silicification (Figure S4, supporting information). However, to obtain continuous and defect-free nanohybrid films, multiple cycles of absorption and silicification were required, which was labor-intensive and time-consuming.11 3.2. Extension of "Beyond Biomineralizaiton" Method to Prepare Ultrathin Hybrid Films and Capsules through Substitution of Other Multivalent Anions by Silicate


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Figure 4. AFM height images of ultrathin nanohybrid capsules prepared through the substitution of (a) sulfate and (b) citrate by silicate.

As described above, the anion substitution during silica deposition was due to the smaller dissociation constant of Si(OH)4 than H2PO4-. To verify this hypothesis, two other multivalent anions, sulfate (SO42-) and citrate (Cit3-), were selected to prepare supramolecular nanocoatings and subsequently induce silica deposition. The dissociation constant for HSO4- and HCit2- was 1.0×10-2 and 4.0×10-7, respectively, which was bigger than Si(OH)4 (Table S1, supporting information). Correspondingly, SO42- and Cit3- in the supramolecular nanocoatings should also be substituted by Si(OH)3O- during silica deposition. As shown in Figure S5 and S6, the frequency got sharply decreased after pumping Na2SO4 and Na3Cit solution (5 mM, pH 7.0) containing 0.2 mg mL-1 PAH, respectively, suggesting the successful deposition of PAH-Sulfate (PSA) and PAH-Citrate (PCA) supramolecular nanocoatings on Au QCM-D sensor. After adding fresh sodium silicate solution, the frequency for PSA and PCA supramolecular nanocoatings first decreased, then increased and finally reached a plateau, which presented similar tendency with PPA supramolecular nanocoatings. The increase of frequency should be due to the partial disassembly of PSA and PCA supramolecular nanocoatings. This indicated that SO42- and Cit3- in the supramolecular nanocoatings were also substituted by silicate during silica deposition, which


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was consistent with the results predicted by dissociation constant. Although bearing similar frequency variation after adding fresh sodium silicate solution, different films went through different time intervals to reach a plateau. For PSA supramolecular nanocoatings, a shorter time interval was required in comparison with PPA supramolecular nanocoatings (1.2 vs 6.5 min), suggesting the stronger interaction between HPO42- and -NH3+ than SO42- (Figure S5b and S3, supporting information). The stronger interaction could also be speculated from the higher deposition rate of the PPA supramolecular nanocoatings than PSA supramolecular nanocoatings (404 vs 261 ng cm-2 min-1). This was in line with the smaller dissociation constant of H2PO4(6.3×10-8 vs 1.0×10-2 for H2PO4- and HSO4-), which again evidenced our hypothesis. Interestingly, when Cit3- was adopted, a higher deposition rate of 1136 ng cm-2 min-1 was observed, and longer time intervals (72.8 min) was required for the frequency to reach a plateau after the addition of fresh sodium silicate solution (Figure S6b, supporting information). This seemed to be inconsistent with the bigger dissociation constant of HCit2- (4.0×10-7 vs. 6.3×10-8 for HCit2- and H2PO4-). Given the higher charge number of Cit3- than HPO42-, it can be deduced that, except for the dissociation constant, charge number of the multivalent anions may also have an impact on the formation of supramolecular nanocoatings and silica deposition. Once CaCO3 spheres instead of planar substrates were adopted as the sacrificial templates, capsules could also be acquired through the substitution of sulfate and citrate (Figure 4). The as-prepared capsules exhibited intact structure (Figure S7, supporting information) and ultrathin capsule wall bearing the thickness of 10.4±1.8 and 14.0±3.4 nm for sulfate and citrate, respectively. 3.3. Structure Manipulation and Mechanical Stability of PS Ultrathin Nanohybrid Capsules


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Figure 5. (a-c) AFM height images of PS ultrathin nanohybrid capsules prepared by adding CaCO3 spheres into freshly prepared PBS buffer (5 mM, pH 7.0) containing different concentration of PAH (a) 0.1, (b) 0.2 and (c) 0.4 mg mL-1, which was denoted as P(0.1)S, P(0.2)S and P(0.4)S ultrathin nanohybrid capsules. (d) Thickness and roughness of PS ultrathin nanohybrid capsules calculated from the corresponding AFM height images (a-c). The error bars were obtained by measuring three different capsules. (e) Percentage of deformed P(0.2)S ultrathin nanohybrid capsules as a function of poly(sodium-p-styrenesulfonate) concentration.

According to the proposed formation process and mechanism, PS ultrathin nanohybrid capsules should show structural evolution when changing the preparation conditions, e.g., PAH concentration. At low PAH concentration of 0.1 mg mL-1, PS ultrathin nanohybrid capsules exhibited the thinnest capsule wall with a thickness of 10.8±0.5 nm (Figure 5a and d), whereas part of the nanohybrid capsules got broken (Figure S8, supporting information). When the PAH


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concentration was increased to 0.2 mg mL-1, intact nanohybrid capsules with thicker capsule wall of 17.3±0.9 nm were obtained (Figure 5b and d). Further increasing the PAH concentration to 0.4 mg mL-1, the wall thickness did not increase anymore (17.2±0.6 nm, Figure 5c and d). However, large aggregates were observed among nanohybrid capsules (Figure S8c, supporting information), which should be PAH-Silica aggregates. At this concentration, PPA would be formed at a relatively fast rate. Hence, some of PPA may grow within the gap of CaCO3 spheres rather than at CaCO3 surface, which further induced the formation of PAH-Silica aggregates. When the PAH-Silica aggregates among nanohybrid capsules were amplified, an appearance of fused NPs was observed (Figure S9, supporting information). Partial PAH should be included in the aggregates, which did not help to increase the thickness of PPA supramolecular nanocoatings and PS ultrathin nanohybrid capsule wall. Once the PAH concentration reached 0.8 mg mL-1, only large aggregates without capsules could be observed (Figure S8d, supporting information). Notably, with the increase of PAH concentration from 0.1 to 0.4 mg mL-1, the roughness of PS ultrathin nanohybrid capsules did not alter a lot (Figure 5d), showing a similar surface structure (Figure 5a-c). Besides the thickness and roughness, the mechanical strength of PS ultrathin nanohybrid capsules was also evaluated using a previously reported compression method.33 Poly(sodium-p-styrenesulfonate) (Mw ~70000) solution was used to create the osmotic pressure to compress the nanohybrid capsules through different poly(sodium-p-styrenesulfonate) concentration between bulk solution and interior of the capsules. As shown in Figure 5e, with the increase of poly(sodium-p-styrenesulfonate) concentration, more and more PS ultrathin nanohybrid capsules got deformed. The elasticity modulus of PS ultrathin nanohybrid capsules was determined to be 2337 MPa through a theoretical model based on continuum mechanics,37 which was much higher than elasticity modulus of PAH/poly(sodium-p-styrenesulfonate)


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polyelectrolyte capsules of 750 MPa.38 Detailed calculation process could be found in the supplementary information (Figure S10, supporting information). The enhanced mechanical stability of PS ultrathin nanohybrid capsules should be ascribed to the interpenetrating framework of silica as well as electrostatic and hydrogen bonding interaction between silica and polyamine. 3.4. Enzymatic Application of PS Ultrathin Nanohybrid Capsules

Figure 6. (a) Confocal fluorescence microscope image of FITC-labeled BSA-encapsulated P(0.2)S ultrathin nanohybrid capsules. (b) The conversion of β-D-glucose as a function of reaction time catalyzed by GOD@capsule systems enabled by P(0.1)S, P(0.2)S and P(0.4)S ultrathin nanohybrid capsules, and (PAH/Silica)2 nanohybrid capsules prepared by combining bioinspired mineralization and LbL assembly. (c) Recycling stability of GOD@capsule systems.

Capsules in close resemblance to cell hold great promise for the construction of the enzyme@capsule system. The enzyme could be encapsulated in the lumen of the capsules and substrate/product could diffuse in/out of the capsules through the semipermeable capsule wall. Commonly, the capsule wall in the enzyme@capsule system would cause additional diffusion resistance and reduce catalytic activity compared with free enzyme. Thinning the capsule wall could reduce the diffusion resistance and elevate the activity of the enzyme@capsule system. In


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our work, PS ultrathin nanohybrid capsules with a thickness of ~10-17 nm were prepared under mild conditions that were amenable for retaining enzyme structure.

Table 1. Kinetic parameter of free GOD and GOD@capsule system Enzymes

Km [mM]

Vmax [mM min-1]

kcat [s-1]

Free GOD

15.3

0.628

418.667

GOD@capsule system

15.6

0.412

14.268

Glucose oxidase (GOD), a widely used enzyme in bioconversion, biomedical and food industry, was chosen as the model enzyme to construct GOD@capsule system. GOD was first entrapped into CaCO3 spheres, which was then used as the template to prepare PS ultrathin nanohybrid capsules. The immobilization efficiency was determined to be 64.9, 77.0 and 77.4% for P(0.1)S, P(0.2)S and P(0.4)S ultrathin nanohybrid capsules. The low immobilization efficiency for P(0.1)S ultrathin nanohybrid capsules should be due to the partially broken capsule wall. With the increase of PAH concentration, intact nanohybrid capsules with thicker capsule wall were obtained, which elevated the immobilization efficiency. P(0.2)S ultrathin nanohybrid capsules exhibited BET surface area of 76.2 m2 g-1, pore volume of 0.411 cm3 g-1 and pore diameter of 5.7 nm, which could successfully inhibit the leaching of GOD (8.6 nm in diameter) from the capsule lumen (Figure S11, supporting information). To further demonstrate the successful encapsulation and determine the distribution of the enzyme in PS ultrathin nanohybrid capsules, FITC-labeled BSA, a protein with similar isoelectronic point but lower molecular weight compared to GOD, was encapsulated in P(0.2)S ultrathin nanohybrid capsules. As shown in Figure 6a, the green fluorescence was mainly emitted near the boundary of the capsule wall, which demonstrated that proteins were successfully encapsulated in PS ultrathin nanohybrid capsules. The partial enrichment of proteins around the capsule wall should be attributed to the


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electrostatic attraction between negatively charged protein and positive charged PAH in the ultrathin nanohybrid capsule wall. Then, the activity of the as-prepared GOD@capsule system was evaluated and an equal amount of enzyme was added for different capsules (Figure 6b). The GOD@capsule system enabled by P(0.2)S ultrathin nanohybrid capsules exhibited the highest activity. The initial activity in 10 min was calculated to be 41.1 µM min-1, which was higher than that of the systems enabled by P(0.1)S and P(0.4)S ultrathin nanohybrid capsules (27.5 and 22.5 µM min-1). Moreover, the equilibrium conversion for the GOD@capsule system enabled by P(0.2)S ultrathin nanohybrid capsules was 94.0%, which was much higher than that of the systems enabled by P(0.1)S and P(0.4)S ultrathin nanohybrid capsules (69 and 51.0%). For control, (PAH/Silica)2 hybrid capsules prepared through the conventional method of combining bioinspired mineralization and LbL assembly (Figure S12, supporting information) were also used to construct GOD@capsule system. (PAH/Silica)2 hybrid capsules exhibited comparable thickness with the P(0.2)S ultrathin nanohybrid capsules (17.7±2.0 vs 17.3±0.9 nm). The GOD@capsule system enabled by P(0.2)S ultrathin nanohybrid capsules exhibited higher initial activity than that enabled by (PAH/Silica)2 hybrid capsules (41.1 vs 21.6 µM min-1). This phenomenon might be acscribed to the slightly higher roughness of PS ultrathin nanohybrid capsules, which facilitated the diffusion of the substrates through the capsule wall. Moreover, our GOD@capsule system exhibited similar Km with free enzyme (15.6 vs 15.3 mM), demonstrating minor alternation of the substrate binding affinity after immobilization (Table 1). However, kcat decreased from 418.7 to 14.3 s-1 after immobilization, suggesting the increased diffusion resistance from the capsule wall. As compared with our previous work,39 kcat of immobilized GOD is increased by ~26 times (14.3 vs 0.539 s-1), which should be arisen from the ultrathin capsule wall. Finally, the recycling stability of GOD@capsule system was examined (Figure 6f),


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which showed elevation with the increase of PAH concentration. After recycling for 7 times, the residual relative activities were, respectively, 11.0, 28.0 and 40.0% for GOD@capsule systems enabled by P(0.1)S, P(0.2)S and P(0.4)S ultrathin nanohybrid capsules. Frankly speaking, the recycling stability was not so desirable, which may be ascribed to the loss of capsules during centrifugation. Further improvement could be realized through changing the recycling methods (such as filtration) or constructing monolithic reactors upon our enzyme@capsule systems. 4. CONCLUSIONS In summary, a "beyond biomineralization" method was exploited to prepare ultrathin, robust nanohybrid capsules. The assembly process of polyamine and multivalent anions ensured the deposition of supramolecular nanocoatings onto CaCO3 sacrificial templates in a non-segregated manner, while the substitution of multivalent anions by silicate and subsequent silicification opened a new way to acquire ultrathin nanohybrid capsules. The substitution process was dominated by the dissociation constant difference of multivalent anions, but also influenced by the charge number that the anions bear. The nanohybrid capsules could be formed through the substitution between different

multivalent-anion/silicate pairs (e.g., phosphate/silicate,

sulfate/silicate or citrate/silicate, etc.). The as-prepared capsules exhibited ultrahigh mechanical strength and amenable for constructing bioreactor. The robust nanohybrid capsules with semipermeable wall effectively inhibited the leakage of encapsulated GOD, whereas the ultrathin capsule wall facilitated the diffusion of the substrates/products. This method could also be utilized for the preparation of ultrathin films by using of various planar substrates (e.g., silicon wafer, Au QCM-D sensor, etc.). This study may deepen the insight of mineralization mechanism of organisms and widen the application of mineralization for nanohybrid material synthesis. ASSOCIATED CONTENT


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Supporting Information. Calculation method of immobilization efficiency and loading capability; EDS spectrum of PPA supramolecular nanocoatings coated CaCO3 spheres; Si 2p XPS spectrum of PS ultrathin nanohybrid capsules; change in frequency and dissipation after the addition of sodium silicate solution; schematic silica deposition process; change in frequency and dissipation during the formation of Polyamine-Sulfate/Silica (PSS) and Polyamine-Citrate/Silica (PCS) nanohybrid films; AFM images of ultrathin nanohybrid capsules prepared through the substitution of sulfate and citrate; SEM image of PS nanohybrid capsules; percentage of deformed PS ultrathin nanohybrid capsules as a function of poly(sodium-p-styrenesulfonate) concentration; N2 adsorption-desorption isotherm and the pore size distribution of PS ultrathin nanohybrid capsules; AFM height image of (PAH/Silica)2 hybrid capsules; Lineweaver-Burk plot of free GOD and GOD@capsule system and ionization equilibrium constant (Ka) and pKa of monosilicic acid, phosphoric acid, sulfuric acid and citric acid. This material is available free of charge via the Internet at http://pubs.acs.org. AUTHOR INFORMATION Corresponding Author *E-mail: [email protected]; Fax: +86-22-27890566; Tel: +86-22-27890566 (Jiafu Shi) Notes The authors declare no competing financial interests. ACKNOWLEDGMENT This work was supported by the National Natural Science Funds of China (21406163, 91534126, 21621004), Tianjin Research Program of Application Foundation and Advanced


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TOC graphic


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Preparation of Ultrathin, Robust Nanohybrid Capsules through a

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