Biomimetic Crystallization of Toplike Calcite Single Crystals with an

National Engineering Research Center for Biomaterials, Sichuan University, ... College of Materials Science and Engineering, Sichuan University, Cheng...
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DOI: 10.1021/cg100294p

Biomimetic Crystallization of Toplike Calcite Single Crystals with an Extensive (00.1) Face in the Presence of Sodium Hyaluronate

2010, Vol. 10 4722–4727

Zhenhua Chen,† Caihong Wang,† Huihui Zhou,‡ and Xudong Li*,† †

National Engineering Research Center for Biomaterials, Sichuan University, Chengdu 610064, People’s Republic of China, and ‡College of Materials Science and Engineering, Sichuan University, Chengdu 610064, People’s Republic of China Received March 5, 2010; Revised Manuscript Received September 18, 2010

ABSTRACT: In this paper, we report the controlled crystallization of calcite by using hyaluronan, a primary constituent of the extracellular substance. Unusual toplike asymmetric calcite crystals with a single extensive (00.1) exposed face were harvested, in contrast to the {10.4} rhombohedral calcite obtained without any additives. The size of the crystal together with peculiar cap structural modifications could be modulated easily by altering the Hya concentration, possibly due to three-dimensional Hya templating crystallization control. SEM, XRPD, FT-IR, thermogravimetric analyses, and staining experiments with charged dyes were adopted for characterizing the morphology, predominant crystallographic orientations, phase, and the (001) face of the crystal and describing the breaking of the morphological symmetry.

Introduction Biogenic calcification of calcium carbonate is abundant in nature, involving the modulation and regulation of timedependent crystallization processes by living organisms, and it yields biominerals with controlled polymorph, hierarchical structure, and complex shape for varied biofunctional purposes, such as structural supports, protections, and mineral stores.1 The elaborate control of biogenic calcite single crystal has long been intriguing to the scientific community. The macroscopic shape of a single crystal is generally defined by regular and planar, stepped or kinked faces, reflecting the arrangement and the symmetry of the lattice. However, biogenic calcite single crystals hardly bear a strict relationship to the underlying crystal symmetry.2 Exemplary objects include otoconia of mammals, individual calcite single crystal elements of coccoliths, and single crystals with complex threedimensional structures such as sea urchin skeletal elements which form within confined volumes.3 The role of organisms as growth modifiers or templates for the shape control of calcium carbonate in calcite modification has received extensive investigations.4 At room temperature and pressure, calcite is the most thermodynamically favorable phase of the three anhydrous crystalline polymorphs (vaterite, aragonite, and calcite) and crystallizes into morphologically prevailing {10.4} rhombohedra without any additives.5 Under mimic biological control, the shape modification studies of calcite rhombohedra into the otoconia-like crystals shed light on the formation of biogenic calcite, but its thorough mechanism of formation still remains to be explored. These modified calcite crystals were obtained by using double diffusion in gel matrices,4b in the presence of glycoproteins elegantly extracted from seaurchin spines4e and tartaric/malic4g and aspartic acid.4f In principle, the barrel-shaped habit with trigonal faceted ends bears an overall symmetry close to 3m of calcite (illustrated in Figure 1A and B).4b Deviations from this symmetry more or *Corresponding author. Telephone/Fax: (þ) 86-28-85412102. E-mail: [email protected]. pubs.acs.org/crystal

Published on Web 10/07/2010

Figure 1. Schematic structure and symmetry properties of (A) the calcite (10.4) rhombohedron; (B) otoconia-like calcite; (C) toplike calcite. The arrows indicate the z axis, and the red points indicate the centrosymmetric properties of the crystals. The colors represent different forms of calcite crystals.

less occurred in those studies, dependent upon kinetic variations and additive-mediated surface energy alterations of specific crystallographic forms.2b Morphological symmetry reducing/breaking is always one of the frontier themes in the crystal engineering field. As concerns calcite single crystals, to the best of our knowledge, the published results referred to breaking of the morphological symmetry are very limited. Most of them only refer to chiral single crystals and mirror breaking of the morphological symmetry.4f ,g,6 The barrelshaped calcite crystal with its intrinsic centrosymmetry missing (Figure 1C) has not ever been documented, according to the best of our knowledge. In the present work, asymmetric, toplike calcite crystals were obtained by using an extracellular substance, sodium hyaluronate (Hya), as the nucleation and growth template. As a major constituent of the extracellular matrices, Hya plays an important role in matrix assembly, cell proliferation, cell migration, and embryonic/tissue development.7 Hya is a high negatively charged glycosaminoglycan composed of repeating units with abundant carboxyl groups (Scheme S1, Supporting Information), and it has been widely investigated in the cosmetic and pharmaceutical industries, as drug carriers, in tissue regeneration, in fabrication of noble metal nanoparticles, in surface functionalization, and in templating synthesis of inorganic nanoparticles.7,8 Herein, we report the r 2010 American Chemical Society

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Table 1. Sample Preparation and Designation of Synthetic CaCO3 Crystals in the Absence and Presence of Hya sample

Hya (mg)

CaCl2 (mg)

morphology

polymorph calcite (%)

type of nucleation of calcite

HC0 HC1 HC2 HC3

0 2.0 4.0 6.0

111 111 111 111

rhombohedron toplike toplike toplike

100 100 100 100

random along [001] along [001] along [001]

synthesis of toplike calcite crystals and their peculiar morphology evolution with varying Hya concentrations. Experimental Section Calcium chloride (A. R., Chengdu Kelong Chemical Reagent Ltd., China) and ammonium carbonate (A. R., Guangdong Xilong Chemical Ltd., China) were used to form calcium carbonate. Sodium hyaluronate (Hya for biomedical purposes, 1180 kDa) was purchased by Jiangyin Runhe Bioengineering Co. Ltd., China. Deionized water (18.3 MΩ cm) was used to make all aqueous solutions. The crystallization method was based on the diffusion of carbon dioxide (CO2) into calcium chloride solution.4d All solutions used had a calcium chloride concentration of 0.1 M. A series of calcium chloride/Hya solutions were prepared, and the concentration of Hya was varied from 0.2 to 0.6 mg mL-1. In a typical procedure, a solution of calcium chloride (10 mL, 0.1 M) was added into a conical flask (25 mL), where 2 mg of Hya was further added. The mixtures were stirred using vortex mixing (IKA, Vortex, Genius 3) to obtain homogeneous solutions. Then, the resultant calcium/Hya solution was stored overnight at 4 °C to avoid any air bubbles. Then, the solution was reverted to ambient temperature and the flask was covered with aluminum foil punctured with a needle. A glass Petridish was filled with crushed ammonium carbonate and was also covered with a punctured piece of aluminum foil. Subsequently, the flask and the Petri-dish were both placed in a closed desiccator at room temperature for 2 days. The vessel was left still in a fume cupboard prior to harvesting the crystals. Finally, the collected crystals were rinsed with deionized water several times and air-dried for further analyses. All experiments were repeated at least twice. Before use, all glassware used was ultrasonicated in ethanol, rinsed with deionized water, soaked in a H2O-HNO3-H2O2 solution (removing any organisms on the glassware to the utmost extent), rinsed with deionized water, and finally dried with acetone. Control experiments were also carried out in the absence of Hya. The feed composition and designation of the synthetic CaCO3 crystals in the absence or presence of Hya are listed in Table 1. The synthetic CaCO3 crystals were characterized by using scanning electron microscopy, staining experiments with charged dyes, X-ray diffraction, Fourier transform infrared spectroscopy, and thermogravimetric analysis. X-ray diffraction patterns (XRDP) were collected on a DX-1000 X-ray diffractometer with Cu KR radiation to confirm the phase and crystallographic orientations of the formed crystals. The accelerating voltage and the applied current were 40 kV and 25 mA, respectively, and the data were recorded at a scanning rate of 0.06° s-1 in 2θ ranging from 10° to 70°. The morphology was examined on a field emission scanning electron microscope (FESEM, S-4800 HITACHI). The molecular species of hyaluronate sodium and the formed calcite crystals were identified by using Fouriertransform infrared spectroscopy (FTIR) with the KBr pellets method. The FTIR spectra of the samples were recorded on a PerkinElmer spectrum one B system between the wavenumbers 4000 and 400 cm-1 with a resolution of 4.00 cm-1. Thermogravimetric analysis was performed on a Netzsch thermal analyzer TG (STA 449C), and the samples were examined under a nitrogen atmosphere at a constant rate of 10 °C min-1, with scanning from room temperature to 600 °C. To validate that the complex of sodium hyaluronate (Hya) and calcium ions exists, the viscosity experiment of Hya at various concentrations in the absence and presence of 0.1 M CaCl2 was performed. The added amount of Hya was varied from 0.012 to 0.15 g. Every specimen for a viscosity experiment has a volume of 30 mL. The viscosities for the Hya and Hya-Ca systems were measured with a suspended level Ubbelohde viscometer which had a flow time of about 200 s for water at 298.15 K. Flow time measurements were performed with a Schott AVS 310 photoelectric

Figure 2. SEM images of calcite crystals obtained in HC0 ([Ca2þ] = 11.1 mg mL-1) and HC1([Ca2þ] = 11.1 mg mL-1, [Hya] = 0.2 mg mL-1): (A) A full view of typical calcite rhombohedron crystals obtained in the absence of sodium hyaluronate (HC0); (B) A full view of toplike calcite crystals obtained in the presence of 2.0 mg of sodium hyaluronate (HC1); (C) Typical calcite rhombohedron single crystal; (D) Typical toplike calcite single crystal. time unit (Schott, Germany) with a resolution of 0.01 s. At least three time recordings reproducible to 0.02 s were obtained, and the average value was used in the calculations. The viscosity of the solution, η, is given by the following equation:9 η=F ¼ Bt - C=t

ð1Þ

where F is the solution density, which was determined with an Anton Paar DMA 60/602 vibrating-tube digital densimeter, t is the flow time, and B and C are the viscometer constants, which were obtained by the measurements on water at 298.15 and 308.15 K. The densimeter and viscometer were thermostated using Schott thermostat units, which have a thermal stability of (0.01 K. To further confirm the interactions between Hya and Ca2þ, the conductivity experiment of hyaluronan at various concentrations in the absence and presence of 0.1 M CaCl2 was performed. The added amount of Hya was varied from 0.02 to 0.5 g. Every specimen for the conductivity experiment has a volume of 50 mL. The conductivities for the Hya and Hya-Ca systems were measured with a Mettler Toledo conductometer (Sevenmulti, Mettler Toledo, Switzerland) at 298.15 K. The conductance cell was equipped with a water circulating jacket, and the temperature was controlled within (0.03 K with a DC-2006 low temperature thermostat (Shanghai, Hengping Instrument Factory). The cell was calibrated with aqueous KCl solutions at different concentrations, and a cell constant of 0.784618 cm-1 was determined.

Results and Discussion The slow-diffusion protocol was used to crystallize calcite. Figure 2 shows the SEM images of calcite obtained in the absence (HC0) and presence of a low Hya concentration (0.2 mg mL-1, HC1, Table 1), along with the abrupt morphology change of calcite from classical rhombohedra (HC0) to the unusual toplike morphology (HC1). High magnification SEM images

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Figure 4. Optical and fluorescence micrographs of toplike crystal after staining with negatively charged (coomassie brilliant blue) and positively charged dye (fast dark blue): (A) optical micrograph and (B) fluorescence micrograph of HC-1 calcite toplike crystal stained by coomassie brilliant blue; (C) optical micrograph and (D) fluorescence micrograph of HC-2 calcite toplike crystal stained by fast dark blue. Figure 3. SEM images of (A) toplike calcite obtained in HC2; (B) typical toplike calcite obtained in HC-3; and (C) the specific tectonic structure on the top of the crystal in part B. The [Ca2þ] are both 11.1 mg mL-1 in HC2 and HC3, and the [Hya] are 0.4 mg mL-1 and 0.6 mg mL-1 in HC2 and HC3, respectively.

(Figure 2) reveal the relationship and differences in morphology between rhombohedral (R) and toplike (T) calcite. Typical R calcite (Figure 2C) is centrosymmetric and formed by six smooth {10.4} faces with a size of about 10 μm. The z axis of the R crystals (see arrows in Figure 1A) runs along the body diagonal of the rhombohedron. Typical T calcite obtained in 0.2 mg mL-1 Hya (HC1), as shown in Figure 2D, displays a pseudocylindrical trunk of 80 μm in length, a cap formed by three (10.4) facets, and a flat round base more or less parallel to the 00.1 plane. The cap of the T calcite crystal (HC1) is similar to that typical of R calcite. The obvious difference between the R and T calcite is that the latter one is dominated by its pseudocylindrical trunk. The obtained unusual toplike calcite single crystals suggest that Hya has a strong influence on the crystallization of calcite. To understand the underlying mechanism, further investigations into Hya concentration-dependent calcite crystallization were carried out, and the Ca concentration was fixed at 11.1 mg mL-1 for all the experiments. Figure 3A shows the typical toplike calcite obtained in the presence of 0.4 mg mL-1 Hya (HC2), with the typical cylindrical trunk length being 40 μm. This is one-half of the HC1 crystals and confirms the enhanced influence of the higher Hya-concentration on the nucleation frequency and on the mean size of calcite. Meanwhile, together with the reduction of the trunk length of HC2 crystals, significant morphology modifications also occurred at the cap. At variance with the case of the HC1 crystals, the cap of the HC2 crystals gave a terrace structure. With increasing the concentration of Hya to 0.6 mg mL-1, the pseudocylindrical trunk of the HC3 crystals evolves toward the shape of a steep rhombohedron (probably, the (10.1) form) (Figure 3B). High magnification SEM images (Figure 3C) show that the peculiar shape of HC3 toplike calcite is due to a combination of unidentified rhombohedra truncated by small (00.1) microfacets. Staining experiments with charged dyes were adopted for validation of the (00.1) facet.10a,b The results shown in Figure 4 and Figure S1 reveal that the round-bottom of the T calcite is stained with positively charged dye (fast dark blue). But, the

Figure 5. (A) XRPD patterns of calcite obtained in (a) HC-1, (b) HC-2, or (c) HC-3. (d) Standard calcite XRPD pattern JCPDS card No. 050586. (B) FTIR spectra of (a) Hya, (b) HC-0, (c) HC-1, (d) HC-2, and (e) HC-3.

negatively charged dye (coomassie-brilliant blue) selectively stains the top of the T calcite crystal ((10.4) facets, Figure 4B). These staining results are well consistent with the literature.10a,b In addition, it is worthy to note that the trunk portion of the HC1 crystal (not shown) and the whole HC2 and HC3 crystals are also stained by fast dark blue (Figure 4D, Figure S1F). It seems that, besides (00.1), fast dark blue could also stain the (hk.0) and other non-(10.4) calcite facets (the unassigned top facets emerged on HC2 crystal). This might be due to the interactions between dyes and Hya molecules absorbed in the crystals, even if the underlying mechanism is not clear yet. The structural features of these toplike crystals were validated by XRPD patterns (Figure 5A). The toplike calcite crystals, nucleated and grown in the presence of increasing Hya-concentrations, reveal a distribution of the XRPD

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Figure 6. TG analyses of calcite obtained in HC-0 to HC-3.

Scheme 1. Schematic Process of Nucleation and Growth of Toplike Calcite Single Crystal

reflections different from that reported in the standard of pure calcite (JCPDS 050586). Going into detail, the percentages of the intensity deviations (calculated by means of relation 2 of the Supporting Information) increase with Hya concentration and the intensities of the lattice equidistances d208 and d214 are particularly affected (Tables S1 and Figure S3). Their expanding patterns are given in the inset in Figure 5A and further indicate that the center of gravity of the reflection (d214) is slightly displaced from pattern to pattern. These features indicate that Hya-molecules not only are adsorbed on the growing surfaces of the calcite (so modifying the crystal shape) but can also be absorbed in the calcite lattice in well-defined growth sectors (so changing the profile shapes of the corresponding XRPD peaks, in both 2θ position and intensity). A similar phenomenon was also demonstrated in the growth of CaCO3/Li2CO3 anomalous mixed crystals,10c even if, in this last case, the carbonate groups are common to both the Li and Ca carbonate structures. The different FTIR spectra of the obtained toplike calcite, pure calcite, and pure Hya (Figure 5B) reveal that, with increasing amount of added Hya, the characteristic absorption bands of Hya become more evident in the spectra of the obtained T calcite crystals (indicated by arrows in Figure 5B). These results suggest that Hya might have been gradually incorporated into the T calcite crystals. The amount of Hya hybridized in the fabricated T calcite crystals is about 0.5 wt % for HC1, 1.6 wt % for HC2, and 3.1 wt % for HC3, according to the thermogravimetric (TG) analyses (Figure 6). From the above results, it is evident that Hya plays a pivotal role in the

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Figure 7. Viscosity of Hya at various concentrations in the absence and presence of 0.1 M Ca2þ.

shape development of calcite from rhombohedra to the toplike and in the simultaneous modification of toplike crystals, i.e. the trunk length reducing and the cap morphological modifications. Compared with those cylindrically shaped and/or the otoconia-like crystals,4 the present toplike calcite crystals only have one cap. This leads to the interesting question of how one set of symmetrically equivalent faces comes to be missing and why this asymmetric toplike calcite is stable enough to form macroscopic single crystals. We tentatively put forth the possible mechanism (in Scheme 1) to interpret the crystallization of unusual toplike calcite crystals and the breaking of the morphological symmetry of calcite rhombohedron. First, we speculate that the Hya matrix (Scheme 1A) with part fluid acts as a three-dimensional growth template which contains the entrapped Ca2þ, hydration water molecules, and Naþ. The stable complexation of Ca-Hya was validated by using viscosity and conductivity measurements equivalent to our previous work.8 The viscosities for the Hya and Hya-Ca systems (Figure 7) show that the added Ca2þ notably reduces the Hya viscosity. This reduction is due to the complexing of Ca2þ and Hya, which alleviates the interactions among adjacent Hya molecules as well as interactions between Hya and water molecules. Meanwhile, this complexation remarkably confines the free migration of Ca2þ. The conductivities for the Hya and Hya-Ca systems are shown in Figure 8. ΛHya-Ca-ΛHya indicates that the increase of added hyaluronan significantly decreased the conductivity of Ca2þ (0.1 M), reflecting that Hya has a strong capability to constraint the free ion migration of Ca2þ. The ascertainment of Hya-Ca complexing based on viscosity and conductivity measurements is further supported by previously reported results obtained by using XRPD, circular dichroism spectroscopy, and nuclear magnetic resonance.11 Subsequently, when the system of Hya-Ca was placed under the diffusion of ammonium carbonate, the CO2 provides the carbonate source and ammonium buffers the pH of the solution (Scheme 1B), thus initiating the precipitation of calcite (Scheme 1C). The 00.1 form is known to be highly polar10 and does not frequently occur in laboratory crystals, even if it moderately occurs in a geological environment. Dominant {001} facets were reported in the controlled CaCO3 crystallization with a polyelectrolyte additive of polystyrene sulfonate (PSS).10a,b The selective adsorption of PSS onto one (00.1) face gave rise to asymmetric primary crystals which assembled into calcite mesocrystals (crystals assembled from nanoscopic building units in an almost perfect three-dimensional orientation) with a convex-concave structure driven by dipolar long-range interactions. Tabular calcite crystals with extensive hexagonal (001) faces were obtained in the

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obtained in amine acid, acidic protein, abalone nacre protein, and amylose.4 This is probably due to the plentiful functional groups of the Hya networks for coordinating Ca2þ. The previously reported studies revealed that much larger calcite was obtained with tetradentate additives than with unidentate additives.4h In contrast, the presence of a straight cylindrical trunk of the toplike calcite and with increasing Hya concentrations, reducing the length and concomitant appearance of newly stepped facets and cap structures, suggests a strong influence of Hya on both the nucleation and growth mechanisms of calcite, owing to complex adsorption/absorption phenomena. Figure 8. Conductivity of Hya at various concentrations in the absence (ΛHya) and presence of 0.1 M Ca2þ (ΛHya-Ca). ΛHyaCa-ΛHya indicates that the increase of added Hya significantly decreased the conductivity of Ca2þ (0.1 M).

presence of lithium, with their stabilization being due to the Liþ incorporation of into surface interstitial sites.10c,12a,12b Drawing an analogy, we can say that our (001) facets are stabilized in Hya modulating crystallization processes (Scheme 1C). In general, growth along the c axis is relatively fast so that the (001) face is not observed under usual crystallization conditions.12 However, the [001] development is the one of the most frequently observed phenomena in biogenic calcium carbonate, e.g. in the prismatic layers of nacre.12 Polysaccharide moieties of intracrystalline glycoproteins extracted from sea urchins and molluscs have been found to interact with growing calcite on the planes approximately parallel to the c axis.4d The present work reveals the presence of an apparent cylindrical portion and a gradual reduction in the trunk length of the toplike crystals with increasing Hya concentrations, suggesting the occurrence of molecular interactions along the [001] axis between Hya molecules and crystal (Scheme 1D). In the present study, macroscopic asymmetric toplike calcite crystals were obtained because Hya has salient properties compared with PSS or the other organic/inorganic additives used to modify/template the crystallization of calcite.4,10As a primary component of extracellular matrices, Hya is a watersoluble polyelectrolyte polysaccharide. It seems plausible that the calcite cluster with Hya associates with the positive side and that Naþ associates with the negative side. Note that, since Hya and Naþ differ in both size and charge, it is feasible to envision that the Na would be more readily displaced to allow free Ca2þ and carbonate to the negative side. Furthermore, the dissolved Hya long chains with a large number of carboxyl, hydroxyl, and amino groups form viscoelastic three-dimensional entangled molecular networks which occupy large volumes of water and have a capability to bind cations.7a Then, we hypothesize that the viscoelastic networks of ionized Hya under the ammonia carbonate diffusion method impose unique spatial confinements upon the colloidal aggregation of the primary clusters (Scheme 1D-F). The scenario secures asymmetric growth rates for these two opposite {001} facets, and hence, an asymmetric shape (Scheme 1D-F) is formed. Obviously, the incorporation of Hya into calcite, as revealed by XRPD, FTIR, and TG results, is important in obtaining the present asymmetric toplike crystals, but the underlying mechanism for the absorbed Hya remains to be interpreted. The macroscopic size of the toplike crystals (tens of micrometers) in the present work is much larger than those doublecapped cylindrical calcite crystals (several micrometers)

Conclusion We reported the controlled crystallization of calcite by using Hya, a primary constituent of the extracelluar substance. Unusual toplike calcite single crystals with asymmetric shape and one extensive round (00.1) facet were harvested, at variance with the usual {10.4} calcite obtained without any additives. The size of the T calcite together with delicate cap structural modifications could be modulated easily by changing the Hya concentration. Although the characterization and mechanism discussion of the obtained toplike calcite crystals are still on a descriptive level, the present interesting results might provide supplementary information for better understanding the fantastic biological control on crystallization, and we expect that the three-dimensional Hya template (as part of the fluid with bound Ca2þ ions for the crystallization control) would receive further in-depth investigations. Acknowledgment. This work is supported by the National Basic Research Program of China (No. 2005CB623903 and 2007CB936102), the National Natural Science Foundation of China (30970729), Sichuan Provincial STP (No. 05 SG022012), and the Doctoral Programs Foundation of Ministry of Education of China (No. 20090181110067). Supporting Information Available: Structure of Hya disaccharide unit, SEM/optical and fluorescence micrographs, and analytical data of the reflection intensity deviation of toplike calcite crystals. This material is available free of charge via the Internet at http:// pubs.acs.org.

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