Control over the Vertical Growth of Single Calcitic Crystals in

Sep 16, 2011 - Proposed mechanism for fibrillar morphological development in the vertical direction by binding of the adsorbed poly(acrylic acid) to s...
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Control over the Vertical Growth of Single Calcitic Crystals in Biomineralized Structures Shichoon Lee, Seung Goo Lee, Myungsun Sim, Donghoon Kwak, Jong Hwan Park, and Kilwon Cho* Department of Chemical Engineering, Pohang University of Science and Technology, Pohang, 790-784, Korea

bS Supporting Information ABSTRACT: Acidic biomacromolecules frequently incorporate into biomineralized structures to control the morphology and extent of crystal growth. The study of such processes has been hindered by the scarcity of a model system that mimics the influence of acidic biomacromolecules on mineral crystal growth. A carbonic anhydrase-assisted system was developed to model CaCO3 deposition at an air/solution interface. Textured CaCO3 crystals were found to grow in a direction orthogonal (vertical) to the air/solution interface. The crystal growth anisotropy became more pronounced upon addition of an anionic polymer, and an amorphous morphology was found at sufficiently high polymer concentrations. X-ray diffraction and highresolution transmission electron microscopy studies showed that most calcite crystals grew along the (014) and (001) planes vertically, whereas the (012) and (110) planes were oriented in the lateral direction. The added acidic polymers adsorbed predominantly onto the (012) or (110) faces of the growing crystals, contributing to epitaxy and crystal growth anisotropy in the vertical direction by inhibiting crystal growth at specific lateral faces that interacted with the acidic polymer. This alignment is characteristic of crystal growth in biomineralized calcites. These observations suggest that the presence of the acidic biomacromolecules induce crystals to grow with specific longitudinal and lateral orientations.

’ INTRODUCTION Biomineralization is an organic macromolecule-mediated crystallization process. Biomacromolecules are incorporated during the biomineralization process and control crystallization in biomineralized structures.1 8 Certain soluble and insoluble proteins are involved in biomineralization.9,10 Insoluble biomacromolecules act as substrates or compartments onto which crystals nucleate and grow via heterogeneous nucleation.9,10 Soluble acidic macromolecules adsorb and bind to specific faces of the incipient crystals, for example, via molecular recognition,2 5 and control the direction of crystal growth. Soluble biomacromolecules work cooperatively with the substrates, but many functions of soluble macromolecules remain unknown. The role of soluble acidic macromolecules in biomineralization has been studied by in vitro biomineralization methods using acidic proteins extracted from biomineralized structures6 or synthetic anionic polymers, such as poly(acrylic acid) (PAA) or phosphorylated polymers bearing acidic protein functional groups involved in biomineralization.7 Vapor deposition methods, such as dissolving ammonia and CO2 vaporized into a solution containing calcium ions,7 or bubbling CO27 through solutions containing calcium ions, are commonly used to deposit CaCO3 onto substrates. It has been reported that biominerals grow in the direction of the crystallographic c-axis via heterogeneous nucleation.2 6 However, these approaches do not afford epitaxial growth in the direction of the crystallographic axis or nanofibrillar CaCO3 structures via heterogeneous nucleation. We devised a CaCO3 deposition system11 at the air/solution interface that facilitated heterogeneous r 2011 American Chemical Society

nucleation and growth of CaCO3 in the presence of carbonic anhydrase (CA). CA is a ubiquitous enzyme responsible for CO2 hydration and dehydration in organisms. Recently, some authors reported that the CA enzyme is involved in biomineralization.12 14 The CA-assisted CaCO3 deposition system was used here to examine the role of soluble anionic macromolecules in the process of biomineralization.

’ RESULTS AND DISCUSSION CaCO3 deposition was induced at the air/solution interface by a reaction between calcium ions in solution and carbonate ions derived from CO2 in ambient air at room temperature in the presence of CA and basic buffer polyethylenimine (PEI). In a previous study,11 we showed that the CA induced CaCO3 deposition at the air/solution interface. In the absence of CA, no noticeable deposition was observed at the interface even in the presence of PEI, but most CaCO3 was precipitated at the bottom. A basic buffer transformed the hydrated CO2 into carbonate ions, which readily reacted with calcium ions to form CaCO3. In the absence of PEI, there was no noticeable precipitation at the bottom and deposition at the air/solution interface. The morphological evolution of the deposited crystals was observed as a function of the PAA concentration at a fixed concentration of CA and PEI. Received: June 19, 2011 Revised: September 16, 2011 Published: September 16, 2011 4920

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Figure 1. Morphological changes of the CaCO3 deposited at the air/solution interface for various PAA concentrations in the presence of 10 μg/mL CA and 10 mg/mL PEI in 10 mM CaCl2. (a) 10 μg/mL, (b) 30 μg/mL, (c) 50 μg/mL, (d) 100 μg/mL, (e) 150 μg/mL, (f) 150 μg/mL, (g) 200 μg/mL, (h) a schematic illustration of morphological changes at increasing PAA concentrations.

As the concentration of PAA increased, the deposition slowed. Figure 1 shows the morphological changes of the deposited CaCO3 grown at various PAA concentrations in solutions containing PEI and CA. At low PAA concentrations, CaCO3 crystals grew parallel to the interface to form a spherulite film, as shown in Figure 1a. As the PAA concentration increased, cone-like structures formed that were orientated orthogonal to the interface. At 30 μg/mL PAA, PAA cones were splayed out with an outer rim composed of many angular rods inside cones (Figures 1b and inset). At 50 μg/mL PAA, the PAA angular rods inside the cones grew almost vertically relative to the air/solution surface and resembled geological stacks piled with several small rectangular plates (Figure 1c). The faces were angular, and growth at the front ends was very smooth. These properties were consistent with the growth of CaCO3 structures via nonspecific inhibition by anionic components at the calcite surfaces.2 As the PAA concentration increased to 100 and 150 μg/mL, aggregated cone morphology was observed in which the cones were composed of many coaligned nanofibers (Figure 1d,e). As the PAA concentration increased, fibers grew vertically, and the lateral faces were round rather than angular. The ends of nanofibers are smooth, which resulted from similar growth rates at the growth fronts.15 17 Cones grew almost vertically relative to the interface and were linked together to form superstructured morphologies. At 150 μg/mL concentration, sheet structures appeared. The overall morphology, however, remained cone-like, and each sheet-like structure was layered and did not display an outer rim (Figure 1f). As shown in the lower right of Figure 1f, disorganized fibers about 80 nm in diameter were arranged at the feet of cones, and the 80 nm thickness was comparable to that of the sheet-like structures (upper right of Figure 1f). The domain boundaries between fibers on the sheet surfaces became less pronounced, indicating that flanking nanofibers assembled together and grew into sheet structures with a thickness corresponding to that of the

unassembled fibers. These observations suggested that the sheetlike structures formed from nanofibers that assembled and transformed on the mesoscale, reminiscent of the multistep growth process in biomineralization.18,19 Nanofiber formation with a high anisotropy and epitaxy was prominent at 100 150 μg/mL PAA. However, at 200 μg/mL PAA, most fibers neither organized into bundles nor grew vertically with respect to the interface. Instead, they were arranged on the surface, suggesting the almost amorphous deposition of the structures (Figure 1g). Figure 1h showed a schematic illustration of morphological changes at increasing PAA concentrations. The observations listed above suggested that the PAA was incorporated into the deposited CaCO3 and played a crucial role in the epitaxial growth of CaCO3 at the air/solution interface. This type of CaCO3 anisotropy and epitaxy has not been observed in other systems designed to biomimetically model CaCO3 synthesis because prior systems lacked the capacity for heterogeneous nucleation and epitaxial growth on surfaces. The concentration of PAA incorporated into the deposited CaCO3 was estimated by thermogravimetric analysis (TGA) of the powders harvested from the air/solution interface. A solution containing CA and PEI but no PAA exhibited trace amounts of weight loss up to 600 °C. Weight loss at 100 °C was ascribed to the loss of hydrated water, whereas losses in the range 200 400 °C were due to decomposition of the incorporated polymers.20 Increasing the PAA concentration to 200 μg/mL yielded a larger weight loss (Supplementary Figure 1, Supporting Information). Although the cationic PEI and water could also be incorporated into the powder, and the amounts incorporated were influenced by the PAA concentration in solution, a large proportion of the loss at 200 400 °C was likely due to incorporated PAA. This indicated that PAA occluded or adsorbed onto the deposited CaCO3. 4921

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Figure 2. X-ray diffractometry of CaCO3 deposited at the air/solution interface at different PAA concentrations. (a) X-ray diffractogram for a θ/2θ scan, (b) diffraction intensity of {014} plane, (c) the calculated fwhm for the different planes, (d) coherence lengths estimated by applying Scherrer’s relation on the basis of the fwhm calculated at the different planes.

X-ray diffraction studies provide information about the epitaxy and anisotropy of crystal growth. Figure 2 shows X-ray diffractograms (XRD) as a function of PAA concentration. The peaks at 2θ = 29.4, due to the {014} calcite plane, were pivotal in these experiments. At 100 μg/mL PAA, several peaks due to the {012}, {110}, {113}, {022}, {024}, and {116} planes were noticeable. The widths of the peaks gradually broadened (Figure 2a) with increasing PAA concentration until a concentration of 200 μg/ mL. At this concentration, all peaks except for the 2θ = 29.4 peak nearly disappeared, indicating that an amorphous morphology was dominant. Peak broadening was examined on the major planes of calcite fiber crystal growth, both in the longitudinal and lateral directions. Broadening was observed in the diffractograms as a function of PAA concentration as shown in Figure 2b. Broadening is defined as a peak’s full width at half-maximum (fwhm) and is related to the coherence length (the average grain size of the perfectly ordered crystal domains) according to the Scherrer equation.1,2,5,6 The fwhm and the coherence lengths on each plane were calculated, as shown in Figure 2c. Note that the peaks due to all planes except for {014} were weak below 30 μg/mL or above 150 μg/mL PAA, indicating that crystal growth in those planes was not extensive. These values were excluded from the fwhm analysis. The fwhm gradually increased with increasing PAA, indicating a decrease in the coherence length, as shown in Figure 2d. The fwhm corresponding to each plane did not differ significantly at a given concentration, and the coherence lengths reach a minimum of 80 nm at 150 μg/mL PAA (Figure 2d). These results agreed with the reports3 6 that the coherence length of calcite crystals grown in solutions containing proteins extracted from sea urchin spines was smaller than that of calcite crystals grown without the extracted proteins. The smaller

Figure 3. 2D-XRD patterns obtained from the CaCO3 deposited at the air/solution interface in the presence of various PAA concentrations. (a) 10 μg/mL, (b) 50 μg/mL, (c) 150 μg/mL, (d) 200 μg/mL.

coherence length was accompanied by a higher degree of crystal nucleation. Nucleation events in several planes were more numerous at higher PAA concentrations. However, crystal growth was subsequently hindered, possibly in the {012} or {110} planes, by the enhanced growth of adjacent crystals, leading to growth in the vertical {014} or {001} directions. The reduced coherence length and enhanced nucleation rate during crystal growth did not fully explain the nanofiber formation and epitaxial growth at higher PAA concentrations. 4922

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Crystal Growth & Design Two-dimensional X-ray diffractometry (2D-XRD) patterns were examined as a function of PAA concentration, as shown in Figure 3a d. At 10 μg/mL PAA, a circular pattern due to the {014} plane was apparent on the beam center, and a large broad band in the center of the diffractogram was attributed to an amorphous morphology (Figure 3a). At 50 μg/mL PAA, several thick large bands due to the {014} and {012} planes gradually appeared (Figure 3b). At 100 150 μg/mL PAA, several discrete bands appeared like the selected area diffraction pattern (SAED) of a single crystal identified by high-resolution transition electron microscopy (HR-TEM). These bands were assigned to the {014}, {110}, {006}, and {012} planes (Figure 3c). These results indicated that crystals in the cones orientated in the specific plane at the concentrations of the added PAA as much as single crystals. The center of a large discrete band oriented orthogonal to the beam axis was assigned to (014), indicating that most crystals grew vertically in this plane. The (006) plane was oriented 45° with respect to the (014) plane. Bands at the side of the diffractogram were assigned to the {110} and {012} planes. The bands were obliquely oriented, 55° and 70°, respectively, with respect to the vertical (014) plane. These were assigned to the {012} planes and indicated the presence of aggregated orthogonally oriented single crystalline cones. A (110) plane observed in the diffraction pattern of single crystalline calcite should be orthogonal to the (006) plane. Therefore, the {110} band on the diffractogram might arise from other cones with different crystal growth orientations. The band assigned to the (006) plane was weak but discernible in the diffractogram, indicating that some fibers grew along the crystallographic c-axis. The growth of calcite in biomineralized structures has been shown to occur along the crystallographic caxis.2,3,6,9 Although this system did not perfectly mimic the formation of biomineralized structures, it modeled fiber growth along the c-axis that was PAA concentration-dependent. The appearance of discrete bands corresponding to certain angles at specific PAA concentrations suggested that PAA may interact with specific crystal planes in a concentration-dependent manner, thereby controlling crystal growth in those planes. Anionic groups, such as the carboxylic acid groups of PAA, interact with the cationic metal ions of metal carbonates and control the growth direction of metal carbonate crystals via these interactions. The carboxylic groups of proteins extracted in the biomineralized structures have been reported to interact principally with the {110} planes of growing crystals.2,3,6,9 The groups in the experiment using synthetic polymer interact principally with the {012} plane.23 Therefore, it is reasonable that crystal growth and inhibition in the lateral directions occurred in the {012} or {110} planes in this work. A thick band in the {014} ring appeared on the horizontal surface. This feature was attributed to the presence of cones that had fallen over during the dipping process in which the deposited layer was placed on a silicon wafer. Such cones most likely lay on the surface at an angle of 15°. At 200 μg/mL PAA, the only discrete bands observed were those of the {014} plane (Figure 3d). Instead, a large broad band was present, indicating the almost amorphous deposition of CaCO3. These observations agreed with XRD and scanning electron microscopy (SEM) analysis, which suggested that the nanofibers were neither organized nor grew in a specific direction, such that no crystals developed along the {012}, {110}, and {006} planes. These results indicated that excessive concentrations of acidic components delayed the crystal growth and

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Figure 4. HR-TEM analysis of a low-magnification image, SAED and lattice spacings at various PAA concentrations. At the zone axis [100], (a) 30 μg/mL, (b) 150 μg/mL. At the zone axis [110], (c) 100 μg/mL. Indices are based on JCPDS 88-1812 for calcite with lattice parameters: a = 4.978, c = 17.462.

Figure 5. Schematic drawing of the protruding carboxylic acid groups of the PAA, and the potential binding of these groups to specific calcite faces developed using the Mercury software. View along the b axis. The calcium (dark circles) and the carbonate groups (open circles) are depicted. (Left) (012) plane, (right) (110) plane.

promoted an amorphous state, thereby preventing the anisotropic and epitaxial growth of the nanofibers. High-resolution transmission electron microscopy (HR-TEM) analysis confirmed that most fibers grew in the (014) plane in the longitudinal direction and in the (012) plane in the lateral direction over all PAA concentrations (Figure 4a,b, Supplementary Figure 3). This result was consistent with the results of 2DXRD analysis. At higher concentrations, 100 150 μg/mL PAA, some fibers grew along the (003) plane in the longitudinal direction and in the (110) plane in the lateral direction, indicating that a proportion of fibers grew along the crystallographic caxis (Figure 4c). This observation suggested that fiber growth 4923

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Figure 6. Proposed mechanism for fibrillar morphological development in the vertical direction by binding of the adsorbed PAA to specific faces (crosssectional view).

in the lateral direction would be inhibited in the (012) or (110) planes by PAA specifically adsorbed on the face, leading to the overgrowth of nanofibers at the (014) or (001) planes. Some authors2,3,6,21,22 have reported that the acidic proteins extracted from biomineralized structures or a designed peptide interacted preferentially with the (110) faces of calcite because the calcite ester groups are oriented perpendicular to the faces and provide stereochemical recognition by the carboxylic groups. Others23 have reported that the carboxylic groups on acidic polydiacetylene films rearrange and fit onto the (012) face, and calcite crystals can nucleate from that face. These reports agree with the results of this work in that the surfaces of most fibers examined by 2D-XRD and HR-TEM presented a (012) plane (lattice image shown in Figure 4a,b), and at higher PAA concentrations, some fibers face the (110) plane (lattice image shown in Figure 4c). Although rearrangements of PAA were not observed, it is reasonable that the carboxylic groups would interact specifically with the crystal faces. The diagram shown in Figure 5 indicates that the carboxylic acid groups of PAA may interact with the calcium atoms at the (012) or (110) faces by substituting the ester groups of carbonates, thereby inhibiting the corresponding planes in the lateral direction. The crystals may overgrow at the (014) or (001) planes due to epitaxy. Growth in the [014] and [012] directions was prevalent at all PAA concentrations, but at higher PAA concentration, growth in the (110) and (001) was also noticeable. Access of the carboxylic groups to the (012) face was good at all PAA concentrations, but interactions with the (110) face required specific concentrations of the acidic polymer. Suitable concentrations of acidic polymer may be used to control inhibition of crystal growth via adsorption of the anionic components to specific faces to promote crystal growth and nanofiber formation orthogonal to the surface. CaCO3 biomineralization involves the initial formation of amorphous CaCO3 (ACC),18 followed by transformation into oriented single crystalline forms. In this system, the formation of ACC became more favorable at higher PAA concentrations. Crystal nucleation at surfaces with adsorbed PAA resulted in crystallization in the [012] direction, which then continued across the domain. During crystallization, some incorporated PAA may be expelled from the growing crystalline domains, whereas other PAA may become trapped at the crystal domain boundaries like soluble biomacromolecules in the biomineralized structures. The calculated coherence length reached 80 nm in the (012) plane, a size comparable to the diameters of the overgrown nanofibers formed

at 150 μg/mL PAA (Figures 1f and 4b). This result suggested that the nanofibers formed a single domain in the lateral direction. In contrast, hundreds of domains were stacked in the vertical direction, resulting in vertical growth and anisotropic nanofiber formation. The adsorbed PAA may initially trigger crystal nucleation, but in the final stages of the process, PAA would be expected to inhibit crystal growth in a specific direction. PAA did not adsorb significantly onto the (014) face, but rather preferred the (012) face. Crystal growth, nucleation, or deposition, therefore, proceeded preferentially at the (014) plane. These processes led to crystal overgrowth in the vertical [014] direction, resulting in epitaxial growth and nanofiber formation. In the lateral direction, crystal growth was inhibited by the adsorbed PAA. However, mineral bridge formation or the presence of defects in the crystal domain boundaries caused secondary nucleation and crystal domain formation on the lateral face, resulting in cone morphology, as shown in the schematic diagram shown in Figure 6. The model is similar to that proposed by Oaki et al.24 They reported the growth of nanocrystals, which formed oriented architectures through several growing stages. The stages included achieving a certain nanocrystal size, inhibiting growth of the nanocrystals by the specific adsorption of acidic polymers, the resumption of growth by forming mineral bridges, and the subsequent addition of another nanocrystal to the preformed nanocrystals. In this system, the mineral bridge was not observed, but the formed fibers were anisotropic and grew epitaxially. The preferential adsorption of acidic polymers is expected to promote anisotropic growth, favoring formation of nanofibers oriented orthogonal to the surface.

’ CONCLUSIONS This study demonstrated that a devised CA-assisted system induced CaCO3 deposition at the interface between air and a solution containing calcium ions and an acidic polymer. As the concentration of the acidic polymer increased, cones composed of nanofibers grew orthogonal to the interface, and the coherence lengths of the crystals decreased. 2D-XRD and HR-TEM analysis indicated that the CaCO3 crystals were single crystalline and grew epitaxially within a range of PAA concentration. Crystal growth was inhibited mainly along the (012) direction and, to a certain extent, in the (110) plane in the lateral direction, possibly due to adsorption of the acidic polymer at the specific face. Crystals mainly overgrew in the (014) plane (and to a certain extent in the 4924

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Crystal Growth & Design (001) plane), leading to the vertical growth of nanofibers. In this in vitro biomineralization experiment, we showed that acidic polymers that mimicked the acidic biomacromolecules associated with in vivo biomineralization processes were incorporated into the deposited CaCO3 and controlled crystal growth by interacting with specific faces of the growing crystals. As a result, nanofibers formed and crystals grew vertically on the substrate.

’ EXPERIMENTAL SECTION CaCO3 deposition was achieved in a 10 cm Petri dish containing 50 mL of a 10 mM CaCl2 solution in the presence of carbonic anhydrase (CA; bovine erythrocytes, Sigma Aldrich) and poly(acrylic acid) (PAA; molecular weight 2000 g/mol). The dishes were covered with a plastic lid (perforated with several 2 mm diameter holes), and the solution was stirred at 300 rpm for 24 h then allowed to rest, covered with the perforated lid. Polyethylenimine (PEI; a water-soluble highly branched polymer with primary, secondary, and tertiary amine groups of molecular weight 400) was used as a basic buffer component. Each solution pH was monitored over 24 h and was found to vary over the range 11 9.5. All experiments were carried out with changing PAA concentration at the fixed concentrations of 10 μg/mL CA and 10 mg/mL PEI. Solutions were freshly prepared from Milli-Q water prior to use. The formed CaCO3 was collected on a silicon wafer that had been cleaned with piranha solution for further characterization. After the substrate was picked up, it was rinsed with water twice, and subsequently blown dry with N2. Before TGA the samples were dried in a vacuum oven for 2 days, and then the analysis was conducted under a nitrogen atmosphere flow up to 600 °C. Field-emission scanning electron microscopy (FE-SEM, Hitachi S-4800) was used to examine the precipitate morphology. Synchrotron X-ray diffraction (XRD, wavelength 1.54 Å) studies were performed, including θ/2θ scans in reflection mode on 10C1 and 2D-XRD scans on 4C2 beamline at the Pohang Accelerator Laboratory (PAL), Korea. The sample-to-detector distance for the 2D-XRD experiment was 147.46 mm, and the distance of each band from beam center was calculated by numbering pixels. The bands were assigned based on d-spacing and 2θ values by the relation, tan 2θ = the distance from beam center to band/ the sample to detector distance. The CaCO3 was transferred to a grid in ethanol and then annealed at 80 °C for 20 min to investigate the direction of CaCO3 crystal growth using HR-TEM (Tecnai F20).

’ ASSOCIATED CONTENT

bS

Supporting Information. (1) Figure of thermogravimetric analysis, (2) the changes for X-ray diffraction intensities at the centers of peaks, (3) another HR-TEM analysis. This material is available free of charge via the Internet at http://pubs.acs.org.

’ AUTHOR INFORMATION Corresponding Author

*Tel: 82-54-279-2270. Fax: 82-54-279-8298. E-mail: kwcho@ postech.ac.kr.

’ ACKNOWLEDGMENT The authors thank Jong Min Kim at the Korea Institute of Science and Technology for technical support with HR-TEM analysis. This work was supported by a grant from the Center for Nanostructural Materials Technology (2011K000176) under the 21st Century Frontier R&D Programs, and Green Science Program of the Research Institute of Science and Technology.

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