A Leaf out of Nature's Book: Hairy Nanocelluloses for Bioinspired

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A leaf out of Nature’s book: hairy nanocelluloses for bioinspired mineralization Amir Sheikhi, Ashok Kakkar, and Theo G.M. van de Ven Cryst. Growth Des., Just Accepted Manuscript • DOI: 10.1021/acs.cgd.6b00713 • Publication Date (Web): 22 Jun 2016 Downloaded from http://pubs.acs.org on June 26, 2016

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Crystal Growth & Design

A leaf out of Nature’s book: hairy nanocelluloses for bioinspired mineralization Amir Sheikhi,†,‡,†† Ashok Kakkar,†,‡ and Theo G.M. van de Ven*,†,‡,†† †

Department of Chemistry, ‡Centre for Self-Assembled Chemical Structures, and

††

Pulp and

Paper Research Centre, McGill University, Montreal, 3420 University Street, QC, H3A 2A7, Canada. *Email: [email protected]

KEYWORDS: nanocellulose, hairy nanocrystalline cellulose, bioinspired mineralization, amorphous calcium carbonate, vaterite

ABSTRACT: The quest for designing new materials to unravel and mimic the biogenic mechanisms behind the formation of superior natural structures through biomineralization has stimulated interest in a broad range of disciplines. Here, we show that cellulose, the basic structural material of trees, and the most abundant yet inactive biopolymer in the world, can be chemically engineered to yield a new class of nanocelluloses with a ppm-level biomimetic effect. We introduce hairy nanocelluloses, namely electrosterically stabilized nanocrystalline cellulose (ENCC) and dicarboxylated cellulose (DCC) as first polysaccharide-based materials to address

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key biomimetic material design concerns, involving (i) an all-natural backbone, (ii) no anthropogenic effects such as eutrophication due to the N-, P-, and/or S- bearing groups, (iii) capability for macroscale mineralization, (iv) no extreme and/or controlled reaction condition requirements, (v) a high efficiency at extremely low concentrations, and (vi) a strong polymorph selectivity. In a model system under ambient conditions, the bioinspired mineralization of calcium carbonate with ENCC/DCC resulted in macro-scale nacre-like sheets of vaterite, the least thermodynamically stable polymorph of CaCO3, which was then decorated with stabilized micro-scale lenticular vaterite to unveil the biomimetic mineralization mechanism. The emergence of these advanced sustainable nanomaterials may open new horizons in the field of bioinspired nano-engineering, for designing inorganic nanostructures and hybrid inorganicorganic nanocomposites.

INTRODUCTION Nature often adopts simple, yet elegant solutions to address the biological needs of species and protects them by conquering life-threatening challenges. Within the past few decades, uncovering the intelligence behind the nanobio-development of highly customized natural materials and mimicking them to design superior structures, or to prevent the formation of pathological species have gained tremendous scientific attention.1–6 More than half of approximately five dozens of biogenic minerals discovered to date contain Ca2+,7 a key cation in cell signaling and regulation,8 which forms the most abundant biomineral, i.e., calcium carbonate.9 Extraordinary morphology, spacing, size, and order of this mineral, are all results of the synergy between multi-functional cell-regulated organic nanomaterials (e.g., glycoproteins)


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and calcium ions while utilizing carbonates, mostly in invertebrates for improved protection, photosynthesis, mobility, and even vision through combined macro- and micro-scale features.10– 13

Among CaCO3 polymorphs, vaterite has made a crucial contribution to biology, and a fundamental impact on our lives. Some interesting biological examples include, but not limited to (i) statoliths in fresh water mysid shrimps to sense gravity, balance, and stabilize visual field,14 (ii) asteriscus, a mm-sized semicircle in one of the otoliths (teleost fish inner ear bone) responsible for hearing and sensing,15 (iii) Herdmania momus sea squirt vaterite spicules,16 and (iv) nacre-like hierarchical brick-and-mortar packing in freshwater lackluster pearls.17 Some important applications of synthetic vaterite include smart drug delivery vehicles,18 bioactive coatings,19 and micromanipulation.20 Other calcium carbonate polymorphs, e.g., amorphous calcium carbonate (ACC), aragonite, and calcite may also take part in biological functions.12 The co-occurrence of stable ACC and anhydrous crystalline CaCO3, e.g., prisms or nacres,21 is extremely rare, and indirect methods, such as protein extraction/re-addition,22,23 have provided some insights into the amorphous-to-crystalline (A-C) transition mechanism. Theoretical studies have suggested that the classical nucleation theory is unable to explain the A-C transition,24 and only recently, the A-C transition dynamics have been directly observed using sophisticated microscopy techniques such as in situ (liquid cell) transmission electron microscopy.25

A desire to mimic naturally occurring minerals with superior structures and/or properties, has given rise to the development of a spectrum of ion-templating organic materials based on synthetic macromolecules or natural biopolymers. Carbohydrate-based polymers (e.g.,


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deprotected β-D-(pyranosyloxy)ethyl methacrylate)26 were shown to yield a mixed polymorph (calcite, aragonite, and vaterite) precipitate; chitosan-polyacrylic acid membranes produced sheets of mixed aragonite-vaterite or pure aragonite polymorphs;27 pure calcite was grown on cellulose powder;28 carboxymethyl chitosan was able to change the morphology of calcite with no influence on the crystal packing;29 anionic dextran resulted in polydispersed microparticles of vaterite and calcite;30 polyacrylamide-grafted α-cellulose and polyacrylic acid-grafted α-cellulose produced calcite and mixed calcite-vaterite particles at room temperature, respectively;31 top-like calcite was achieved using sodium hyaluronate in the presence of ammonium;32 xanthan and gellan precipitated stack-like calcite and pectin, κ-carrageenan, and sodium alginate produced rosette-like calcite;33 and polyanionic DNA formed thin calcite films.34

An analysis of current biomimetic mineralization agents suggests that they suffer at least from one of the following shortcomings: (i) synthetic macromolecular backbone;35 (ii) anthropogenic effects due to functionalization with N-, P-, and/or S-36 bearing groups35 such as amines, phosphates, phosphonates, and sulfonates, which are considered as nutrition and acidifiers when disposed, leading to environmental eutrophication and acidification;37–39 (iii) inability in macroscale mineralization;40 (iv) extreme and/or controlled reaction condition requirements;41,42 (v) inefficiency at low concentrations;43 and (vi) lack of polymorph selectivity.13 We endeavored to address these issues by engineering the most abundant yet chemically inactive biopolymer (cellulose) to introduce threshold nanocellulose-based biomineralization motifs. Our ultimate goals are to template ions for the selective synthesis of the least stable polymorphs under ambient conditions, and to decelerate the mineralization process for the facile investigation of polymorph transition mechanism using conventional electron microscopy tools.


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We aimed to design cellulose-based nanomaterials for biomimetic mineralization by understanding the structure-property relationship of nanobuilding blocks of wood, i.e., nanocrystalline and nanofibrillated celluloses in a supersaturated model system involving calcium and carbonate ions. This is followed by the chemical modification of cellulose fibers to yield a new class of biomimetic motifs, called hairy nanocelluloses, overcoming the structural limitations of conventional nanocelluloses.

EXPERIMENTAL Conventional nanocelluloses including nanocrystalline cellulose (NCC) and nanofibrillated cellulose (NFC) were provided by FPInnovations, Pointe-Claire, Canada and USDA’s Forest Products Laboratory, Madison, WI, U.S.A., respectively. Hairy nanocellulose (HNC)44 were synthesized as cationic (cationic nanocrystalline cellulose, CNCC),45 neutral (sterically stabilized nanocrystalline cellulose, SNCC),46 and anionic (electrosterically stabilized nanocrystalline cellulose, ENCC)47 nanoparticles and anionic cellulose chains (dicarboxylated cellulose, DCC) according to our previous recipes.44,48 Briefly, cellulose fibers were oxidized by periodate treatment to yield intact dialdehyde modified cellulose (DAMC), which was used as an active intermediate to prepare the family of HNC. CNCC, SNCC, and ENCC (DCC) were prepared by a Schiff-base reaction with Girard’s reagent T, heating at 80°C for 6 h, and chlorite oxidation, respectively, with intermittent co-solvent addition and centrifugation. ENCC was reacted with HCl for 15 h at 45 °C to obtain hydrolyzed ENCC (HENCC) with a significantly reduced charge content. The mineralization experiments were conducted by mixing 15 mL of CaCl2 (20 mM) with the same amount of NaHCO3 including a desired amount of a nanocellulose at room


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temperature, followed by 1 min mixing and incubation without further agitation for a desired time. To quench the mineralization reaction, the supernatant was decanted, and the precipitate was rinsed with deionized water, followed by drying at 50 °C for at least 24 h. Secondary nucleation, to decorate the vaterite macro-sheets, was achieved by incubating the precipitate with ~ 50 µL of nanocellulose-containing supersaturated solution in the oven (50 °C for at least 24 h). Scanning electron microscopy (SEM) showed the morphology of precipitated phase, focused ion beam (FIB) milling enabled us to prepare a cross section of lenticular micro-features on vaterite flakes to be examined by transmission electron microscopy (TEM, morphology), selected area electron diffraction (SAED, crystal structure), and energy dispersion spectroscopy (EDS, chemical composition). Furthermore, X-ray diffraction (XRD) was conducted on an electrochemically-coated gold electrode with calcium carbonate in the presence of nanocelluloses to confirm the polymorph structure. To investigate the hairy nanocellulosecalcium carbonate complexation, surface potential of ENCC while undergoing the bioinspired mineralization was measured using electrophoretic light scattering (ELS). Detailed Materials and Methods are presented in the Supporting Information.

RESULTS AND DISCUSSION Conventional nanocrystalline cellulose (NCC) with a fairly low surface charge density (< 0.5 mmol g-1 sulfonate, introduced during a sulfuric acid-mediated synthesis), are stable in a highly carbonated solution (20 mM); however, upon introducing Ca2+ to initiate mineralization, they immediately aggregate and form a soft, white layer at the bottom of a vial (Figure S1a, Supporting Information), in which CaCO3 nucleation and growth takes place. In the carbonate solution, NCC benefits from electrostatic stability (ζ-potential ~ -40 mV at pH ~ 9 and ionic


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strength ~ 20 mM),49 which is then affected by the divalent cations, resulting in diffuse double layer shrinkage and Ca2+-mediated bridging aggregation. NCC aggregates show affinity toward CaCO3 crystals and adsorb on them, as evidenced in Figures 1a-d. However, they are ineffective in directing the mineralization pathway, leading to the most thermodynamically stable CaCO3 crystal morphology (rhombohedral) and packing (calcite, PXRD and EDS spectra in Figures S1c-e, Supporting Information). We have previously shown that NCC is considerably sensitive to ionic strength, and aggregates at ~ 50 mM of NaCl.49 On the one hand supersaturation is required to initiate the mineralization process, while on the other, NCC suffers from colloidal instability. Thus, increasing NCC content in the pre-nucleation solution (to increase the available negatively charged functional groups) does not help manipulate the nucleation and growth of CaCO3. This suggests that the first requirement for successful bioinspired mineralization is colloidal stability.

We focused on the carboxylated biomacromolecules to simultaneously overcome the environmental concerns associated with the so-called nutrition and acidifier groups (N, P, and S). Nanofibrillated cellulose (NFC) bearing ~ 0.64 mmol g-1 carboxylic acid groups, located on the glucose carbon #6 (C6) from TEMPO-mediated oxidation of fibers, was incubated in the same precipitating system as for NCCs. Interestingly, regardless of the additive concentration, similar results as for NCC were obtained: colloidal aggregation (Figures S1-b, Supporting Information) and the formation of stable calcite crystals (Figure 1e). Increasing the COOH content higher than ~ 3 mmol g-1 (degree of substitution DS ~ 0.5) while maintaining the crystal structure of NCC or NFC intact is infeasible,50 because the higher the carboxyl content, the more soluble the crystalline cellulose layers, and the higher the possibility of the system falling apart.


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Note that typical DS of COOH in oxidized conventional nanocelluloses is ~ 0.1, equivalent to all accessible hydroxyl groups.51 At such a low functional group density, no cellulose-based material can effectively direct the mineralization process. Thus, a new building block is required to push the structural boundaries of conventional nanocelluloses.

Hairy cellulose nanocrystalloids, bearing both crystalline and amorphous cellulosic regions with DS ~ 1 benefit from extremely high colloidal stability (electrosterically or sterically).48 Sterically-stabilized nanocrystalline cellulose (SNCC) bears aldehyde groups,46 therefore, it is not affected by the salt concentration. Cationic hairy nanocrystalline cellulose (CNCC) has quaternary amines, thus it is always positively charged,45 and anionic electrosterically-stabilized nanocrystalline cellulose (ENCC) and dicarboxylated cellulose (DCC)47 are both stable up to at least 200 mM of a divalent cation.52 Given their colloidal stability, this family of nanocelluloses and biopolymers may help establish the effect of pendant functional groups on mineralization.

Mineralization of CaCO3 with SNCC (Figure 1f) and CNCC (Figures 1g and 1h) produced similar results as with NCC. None of them was able to change the crystal morphology and habit (rhombohedral calcite was obtained). Interestingly, as opposed to NCC and CNF, the inorganic crystals cannot be coated with either SNCC or CNCC, because of the poor interaction between aldehyde or amine groups with Ca2+. This furnishes the second requirement for an effective cellulose-based mineralization: a high grafting density of negatively charged functional groups may promote interactions with CaCO3 prenucleation clusters and nuclei. Note that while these criteria are necessary, they may not be enough to effectively mimic the biomineralization process, and parameters such as flexibility, conformation, and stereochemistry may play key


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roles. Noticeable examples are the inability of polyacrylic acid (PAA)53 and polysaccharidebased crystal modifiers (e.g., carboxymethyl cellulose, CMC)54 to achieve macro-scale pure vaterite at low [COO-]/[Ca2+].

ENCC, bearing a crystalline body similar to NCC sandwiched between protruding dicarboxylated cellulose chains, satisfies the two requirements discussed above. A high density of adjacently carboxylated natural polyanions induces attraction towards Ca2+ and calcium carbonate clusters:

The affinity of COO- towards CaCO3 crystals is well supported in literature.55 When the ENCC concentration is ~ 0.033 ppm, no significant influence on the CaCO3 mineralization is observed, and rhombohedral calcite is obtained (Figures 2a-d). Increasing the ENCC concentration to ~ 0.66 ppm (Figures 2e-h), a mixture of flake-like macro-structures (Figure 2e) and colloidal micro-structures (Figures 2f-h) of vaterite as well as rhombohedral calcite crystals (Figure 2e) are produced. Under these conditions, no deformed calcite is observed, suggesting that the stabilizing effect of ENCC is localized on the non-transformed species of vaterite with almost no influence on the most thermodynamically stable polymorph, calcite. Further increase in ENCC content beyond ~ 1.65 ppm totally eliminates the calcite formation, permitting the growth of vaterite flakes to several hundreds of micrometers (Figures 2i and 2j, also see the PXRD and


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EDS spectra in Figure S2, Supporting Information). These flakes adopt nacre-like structures, which may be of particular interest in designing mechanically reinforced hybrid materials (Figure S3, Supporting Information). To the best of our knowledge, this is the first report of such an efficient polysaccharide-based biomimetic mineralization additive.

The ζ-potential of ENCC in a CaCl2 solution attests to the complexation of calcium ions with COO- groups, reflected in a significant potential drop from ~ -70 mV to ~ 0 mV. The colloidalbased platform of ENCC may enable embedding any desired species, grafted on the backbone, into the inorganic structures for advanced inorganic-organic hybrid materials; however, when such applications are not aimed, cleaved DCC chains may act as biomimetic mineralization agents. Foregoing experiments with DCC, containing highly-charged solubilized cellulose chains bearing no crystalline regions, show a similar effect as ENCC at a 5 fold lower concentration, i.e., ~ 0.33 ppm. This provides some insights into the mechanism of ENCC-CaCO3 interactions: the main contributors in the adsorption of ENCC on calcium carbonate (prenucleation clusters, nuclei, ACC, and vaterite) are the protruding, flexible DCC chains, owing to their high charge density and conformational freedom. Accordingly, cellulose pulp is not the only possible raw material to synthesize this class of superefficient nanomaterials; any type of biomass, including sawdust,56 can be utilized for such a purpose. This opens up a promising opportunity to convert low-grade, cheap, and green raw materials with no environmental footprints to highly functional biomineralization motifs.

To shed light on the mechanism of vaterite formation, supersaturation driven secondary nucleation was induced by incubating the precipitated CaCO3 with ~ 50 µL of the supernatant at


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50 °C as detailed in the Experimental Section. In the presence of ENCC or DCC, the macro-scale vaterite flakes were decorated by lenticular micro-scale particles (~ 5 µm diameter) as shown in Figure 3. These micro-features attain a uniform shape when DCC was the organic additive (Figures 3d-g), which is attributed to the higher capacity of DCC in stabilizing the early stages of CaCO3 precipitates. In the presence of ENCC, the microparticles were mostly located at the edge of the macro-flakes and underwent a unidirectional growth along the edge (Figure 3b). Favorable growth at crystal edges compared to terraces is well established by the theory of nucleation and growth.57 An extremely similar patterned growth of vaterite is observed in the cold water salmon ear bone (Oncorhynchus keta asteriscus), shown in Figure 3c (SEM image provided by Prof. T. Kogure, the University of Tokyo).

The cross section of two adjacent microparticles on a large flake, prepared by focused ion beam (FIB) milling (Figures 4a-c, also see Figure S4, Supporting Information), shows a distinct boundary between the micro-structures and the macro-scale substrate (Figures 4d-f), confirming the secondary nucleation process. Lenticular features comprise radially-oriented atoms (e.g., Figure 4e) along the hemisphere center, which suggests that the crystallization starts from the center and moves towards the periphery. Each semi-circular sector is made of ordered structures close to the center separated by disordered regions near the edge as seen in Figures 4g-i. Elemental analysis (EDS) suggested that the carbon content in the disordered region (C/Ca ~ 7 mol/mol) is always higher than that in the ordered parts (C/Ca ~ 3 mol/mol), which may reflect the fact that the DCC chains are stabilizing the disordered regions. Note that these ratios are obtained after eliminating impurities, such as copper (from the grid, ~ 2-5 % mol) and chlorine (~ 3 % mol). Selected area electron diffraction (SAED, insets of Figures 4g and 4h) confirm


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that the ordered regions are made of vaterite, and the disordered regions between each ordered sector in the lenticular microstructures is ACC (smeared rings in the diffraction pattern). The coexistence of ACC with vaterite after ~ 30 days attests to the strong stabilizing effect of DCC (ENCC) even at [COO-]/[Ca2+] ratios as low as ~ 0.001 mol/mol. According to these observations, the mechanism of nucleation and growth is suggested in Scheme 1.

As shown in Scheme 1, upon Ca2+ addition to the mixture of CO32-/ENCC (DCC), carboxyl groups become saturated with free Ca2+ and those in the CaCO3 nuclei (confirmed by a noticeable decrease in the ENCC ζ-potential), and provide new nucleation sites to attract CO32and form ACC, the least thermodynamically stable polymorph of calcium carbonate. In the meantime, because [Ca2+] >> [COO-], homogeneous nucleation from the reaction between Ca2+ and CO32- takes place simultaneously to form ACC, which is immediately stabilized by ENCC or DCC. This is consistent with the observed preferred interaction of COO- with CaCO3 over Ca2+.58 Note that the adsorption of DCC chains onto the early stages of CaCO3 clusters may dissolve them, and only nuclei which grow beyond a critical size57 are able to form a stable phase. Furthermore, to stabilize a CaCO3 cluster (including numerous Ca2+), probably a few DCC chains are sufficient to block the surface, and prevent phase transformation to calcite. This may explain such a high efficiency of ENCC/DCC. The DCC-stabilized ACC nanocomposites gradually undergo a phase transformation to the next thermodynamically stable polymorph, i.e., vaterite; however, this transition is governed by very slow kinetics, which may result in the ACC-vaterite coexistence (as proven in Figures 4g-i). Stable vaterite microstructures grow in an almost 2D fashion to form macro-scale flakes, which never transform to calcite, even after several months.


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To understand the effect of local charge density, the charge content of ENCC was decreased by the HCl-mediated hydrolysis of the β(14) linkage to result in hydrolyzed ENCC (HENCC). The same concentration of COO- as ENCC while distributed among a larger number of particles (lower charge content per particle) was used for mineralization. Interestingly, upon introducing Ca2+, HENCC (COO- content ~ 0.34 mmol g-1) aggregates and phase separates, resulting in similar outcome as conventional NCC and NFC. Thus, the first requirement for successful mineralization, i.e., colloidal stability, is not satisfied. The superior performance of ENCC and DCC is compared to other nanocelluloses and some highly efficient biomimetic additives in Table 1. While for example [COO-]/[Ca2+] ~ 600 mmol/mol is required to achieve vaterite using polyacrylic acid, ENCC and DCC fulfill this task at [COO-]/[Ca2+] < 1 mmol/mol.

CONCLUSIONS This work introduces the first class of highly efficient (threshold) and environmentally-friendly polysaccharide-based biomimetic mineralization materials called hairy nanocelluloses. Through facile chemical reactions, cellulose fibers are disintegrated from the amorphous regions to yield functional nanoparticles and biopolymers with significant potential for next generation biomimics. As a model system, the mineralization of calcium carbonate under ambient conditions was engineered using electrosterically stabilized nanocrystalline cellulose (ENCC) and dicarboxylated cellulose (DCC) at ppm levels, and stable macro-scale vaterite flakes were produced. Hinging on the high stabilization efficiency of these cellulosic nanomaterials, we were able to slow down the mineralization kinetics for several months. A secondary nucleation enabled us to decorate the vaterite flakes with near mono-dispersed lenticular CaCO3


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microparticles made of a patterned coexistence of vaterite and amorphous calcium carbonate, which unveiled the mineralization mechanism. ENCC and DCC may help provide cost-effective, green, and superefficient production of uncommon inorganics including vaterite, a polymorph with a wide spectrum of applications in drug delivery, reinforced nanocomposites, and smart coatings, and open new horizons for polysaccharide-based mineralization.


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FIGURES

Figure 1. Mineralization of calcium carbonate by mixing 15 mL of CaCl2 (20 mM) with 15 mL of a NaHCO3 (20 mM) solution including 1 mg of NCC (a-d), NFC (e), SNCC (f), or CNCC (g and h) after 24 h incubation at room temperature yields rhombohedral calcite. Both NCC and NFC undergo a fast aggregation upon contacting Ca2+ due to weak colloidal stability (see also Figure S1, Supporting Information), and coat the calcite surface (c, d, and e, with red arrows indicating the nanocellulose aggregates). SNCC (f) bears dialdehyde cellulose chains and CNCC (g and h) accommodates quaternary amine functionalized cellulose chains, both of which are impotent in interacting with CaCO3 and do not affect the mineralization. These yield two critical requirement for the nanocellulose-assisted engineering of calcium carbonate habit, i.e., colloidal


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stability and proper anionic functionalization. Note also that the PXRD spectra is presented in Figure S1, Supporting Information.

Figure 2. Biomimetic mineralization of CaCO3 using a similar mixing method as detailed in Figure 1, involving 1 µg (a-d), 20 µg (e-g), and 50 µg (i and j) of ENCC after ~ 1 month


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incubation. At low ENCC concentration (~ 0.033 ppm, a-d), calcite is formed. Increasing ENCC to ~ 0.66 ppm (e-h) results in a calcite (rhombohedral)-vaterite (macro-flakes and microparticles) mixture. Further increase of ENCC (~ 1.65 ppm, i-j) totally eliminates the calcite polymorph, yielding macro-scale sheets of vaterite (PXRD and EDS spectra in Figure S2, Supporting Information).

Figure 3. Inducing a secondary nucleation by incubating the precipitated phase of an ENCC (1.65 ppm, a and b) or DCC (0.33 ppm, d-g)-containing supersaturated calcium carbonate solution (similar to Figure 1) with ~ 50 µL of the supernatant results in the decoration of vaterite sheets with lenticular microparticles. These particles may undergo an unsymmetrical growth at the edge of the flakes (b), resembling well the biomineralization of CaCO3 in cold water fish ear


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(c, vaterite in the asteriscus of salmon, Oncorhynchus keta, SEM image from Kogure Lab., the University of Tokyo). The detailed structure of these microparticles is presented in Figure 4.

Figure 4. Two adjacent lenticular microparticles are selected (a, SEM image) and coated with a thin layer of Pt (b), followed by focused ion beam (FIB) milling (c) to achieve a cross-sectional view (see also Figure S3, Supporting Information) of the features sitting on a macro-scale CaCO3 sheet. The slab is examined with TEM (d), and an alternating radial vaterite-ACC hierarchical


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structure with the ACC located close to the microparticle periphery (marked in e and f, magnified in g-i) is observed. A close look at the ACC-vaterite boundaries (g-i) reveals that the atoms adopt different orientation in each crystalline region (e.g., in i, two crystalline regions with a 25° (bottom) and 75° (top) orientation slope are separated by an amorphous region), shaping the lenticular structures. Dislocation and stacking fault in the crystalline regions are also observed. This sheds light on the stabilization mechanism in the ENCC (DCC)-mediated biomimetic mineralization.

SCHEMES

Scheme 1. Mechanism of anionic hairy nanocrystalline cellulose (ENCC)-mediated biomimetic mineralization of calcium carbonate. Dicarboxylated cellulose (DCC) chains, bearing an exceptionally high density of carboxylic acid (~ 6 mmol g-1), permit an effective complexation with CaCO3 nuclei, which serve as stabilizing amorphous calcium carbonate (ACC) growth sites. ACC is then transformed to the next thermodynamically stable polymorph, i.e., vaterite. The co-


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existence of ACC-vaterite as uniform lenticular microparticles can be simply achieved at an ambient condition, and macro-scale vaterite sheets O(1 mm) are finally produced. Note that the structure of ENCC is thoroughly explained elsewhere.48


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TABLES Table 1. Biomimetic mineralization of CaCO3 using conventional (blue shade) and hairy (ineffective: orange shade, and effective: green shade) nanocelluloses at an ambient condition. Some of the efficient macromolecules are also presented for comparison. Biomimetic mineralization agent

Colloidal stabilitya

Functional groups [FG]

FG density (mmol g-1)

Added amount (mg)

[FG]/[Ca2+] (mmol/mol)

Precipitated CaCO3 polymorph

Various acids59

amino

NA

NH3+& COO-

NA

NA

1000, and [Mg]/[Ca2+] =4

Mixed calcite and vaterite microparticles

Poly acrylic acid and (NH4)2CO3 53

NA

COO-& NH4+

NA

NA

>600 (Mw=1.2250 kDa) & 2000

Microsphere vaterite (~3 µm)

NCC

No

SO3-

> 1.7

Calcite

NFC

No

COO-

0.64

≥1

>> 2.1

Calcite

CNCC

Yes

NH4+

1.7

≥1

>> 5.8

Calcite

SNCC

Yes

COH

6

≥1

>> 20.4

Calcite

HENCCb

No

COO-

0.34

≥1

>> 1.2

Calcite

ENCC

Yes

COO-

5.5

0.05

0.9

Vateritec

DCC

NA

COO-

6

0.01

0.2

Vateritec

a

At [Ca2+] = [HCO3-] ~ 10 mM in 30 mL final supersaturated solution. bHENCC stands for hydrolyzed ENCC, obtained from reacting ENCC with HCl at 45 °C for 15 h according to the procedure outlined in the Experimental Section. cMacro-scale (clean) vaterite flakes or decorated with micro-scale lenticular features coexisting with ACC.


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ASSOCIATED CONTENT Supporting Information. Extended Materials and Methods and Figures S1-S4 (colloidal instability of conventional NCC and CNF, PXRD spectrum, EDS, and complimentary SEM and TEM images). The Supporting Information is available free of charge on the ACS Publications website. AUTHOR INFORMATION Corresponding Author *Email: [email protected] ACKNOWLEDGMENT Financial support from Natural Sciences and Engineering Research Council (Canada), Fonds de Recherche du Québec Nature et technologies (FRQNT, Quebec, Canada), and Centre for Self‐ Assembled Chemical Structures (CSACS) is gratefully acknowledged. The assistance of the Facility for Electron Microscopy Research (FEMR), McGill University, in particular Prof. H. Vali, Drs. D. Liu and K. Sears, and L. Mongeon is much appreciated. The SEM image of salmon (Oncorhynchus keta) asteriscus was kindly provided by Prof. T. Kogure, the University of Tokyo. We would like to thank Profs. T. Friščić and N. Tufenkji, McGill University for using their PXRD and Zetasizer instruments, respectively, and appreciate C. Nickels and L. Do for the training on the PXRD instrument. ABBREVIATIONS NCC, nanocrystalline cellulose; NFC, nanofibrillated cellulose; HNC, hairy nanocellulose; CNCC, cationic nanocrystalline cellulose; SNCC, sterically stabilized nanocrystalline cellulose;


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For Table of Contents Use Only

A leaf out of Nature’s book: hairy nanocelluloses for bioinspired mineralization Amir Sheikhi, Ashok Kakkar, and Theo G.M. van de Ven*

First class of cellulose-based nanomaterials with an exceptional performance in directing the mineralization toward the long-time stabilization of thermodynamically rare inorganic polymorphs is introduced. Electrosterically stabilized nanocrystalline cellulose (ENCC) and dicarboxylated cellulose (DCC) successfully mimic the biomineralization of CaCO3 at ppm levels, opening new horizons for sustainable polysaccharide-based bioinspired crystal design and engineering.


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A Leaf out of Nature's Book: Hairy Nanocelluloses for Bioinspired

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