Article pubs.acs.org/crystal
Variation in Mesoscopic Textures of Biogenic and Biomimetic Calcite Crystals Ryoichi Miyajima,† Yuya Oaki,† Toshihiro Kogure,‡ and Hiroaki Imai*,† †
Department of Applied Chemistry, Keio University, 3-14-1 Hiyoshi, Kohoku-ku, Yokohama 223-8522, Japan Department of Earth and Planetary Science, Graduate School of Science, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan
‡
S Supporting Information *
ABSTRACT: Mesoscale granular textures having a single-crystalline feature are widely observed on various biogenic and biomimetic calcite crystals, although the distribution of organic phases and the magnitude of lattice strain in the textured crystals vary with organism species or growth conditions of the biomimetic process. The prismatic layer of a fan mussel exhibits a relatively homogeneous, lowstrain texture consisting of nanoscale grains with discrete organic inclusions; the prism structures of a pearl oyster and an avian eggshell have a high-strain granular texture with localized organic phases. The high-strain granular textures were artificially produced through the mesoscopic dendritic growth of calcite by the physical impedance of a rigid gel matrix. Facet growth of the crystal involving nanoscale segregation of soluble polymers in a supersaturated solution would result in the formation of the lowstrain body having mesoscopic textures.
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INTRODUCTION In nature, the inorganic skeletons of organisms have complicated architectures that are made up of micrometric structures.1−5 One of the features of CaCO3 in the inorganic skeletons called biominerals is imperfection related to organic inclusions in the crystalline body. The intracrystalline organic phases and lattice strain of CaCO3 crystals have been investigated for various biominerals using several techniques.6−16 The lattice strain is commonly attributed to the presence of organic inclusions. One of the authors14 reported the distribution of the organic inclusion and lattice strain in three kinds of prismatic layers. The biogenic calcites in P. fucata and C. nippona have inhomogeneously distributed organic molecules and local large lattice strains, whereas homogeneous distribution of organic molecules with low strain was observed in A. pectinata. The strained structures of calcite were found to have high mechanical strength and toughness compared with simple single crystals.17 Therefore, the relationship between the lattice strain and the organic inclusions in the single crystals is important for the design of novel structural materials. In recent years, granular textures consisting of oriented nanocrystals less than 100 nm in size with the incorporation of biological macromolecules have been observed as common to various CaCO3-based biominerals.18−30 Our groups19,20 showed that the biogenic CaCO3 crystals are composed of bridged nanograins that are arranged in the same crystallographic direction. A nanocluster structure with well-aligned small crystal domains on spicules of a sponge was revealed by atomic force microscopic and transmission electron microscopic investigation.21 Cölfen et al.30 proposed the concept of mesocrystals consisting of nanoscale units as the micrometric © 2015 American Chemical Society
structure of biominerals. A mesocrystal is regarded as the oriented assembly of individual nanoparticle building units of 1−1000 nm in diameter. However, recent results using several characterization techniques suggested that the biominerals are composed of continuous crystalline bodies, not isolated units such as those in a mesocrystal.31 The distribution of impurities, lattice strain, or dislocation has been reported for calcite bodies of various biominerals.14,24 On the other hand, the relationship between the distribution of organic phases, impurities, or lattice strain and the granular textures has not been sufficiently clarified.32 In the current study, we investigated the granular textures of biogenic calcite in several CaCO3-based biominerals in parallel with the variation of biomolecule distribution and lattice strain. The formation of bridged nanocrystals and mesocrystal structures similar to biominerals is usually ascribed to growth by the control of organic molecules. Biomimetic or bioinspired crystal growth of CaCO3 by artificial means is a well-known method to synthesize textured crystals, including mesocrystals. Various organic molecules, such as extracted proteins from biominerals25,33 and recombinant proteins,34 have been used for synthesis of the biomimetic mesocrystals. Water-soluble polymers35−40 and hydrogel matrices29,41−44 were also reported to promote the formation of CaCO3 mesocrystals. However, the structural difference in the textures depending on the organic molecules has been only slightly described.45 Several routes to the textured crystals or mesocrystals have been Received: March 23, 2015 Revised: July 11, 2015 Published: July 24, 2015 3755
DOI: 10.1021/acs.cgd.5b00407 Cryst. Growth Des. 2015, 15, 3755−3761
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JEOL JSM-7600-F) operating at 5 kV. Cross-sectional specimens (10 μm × 10 μm × 100 nm) of the biogenic and biomimetic calcites were prepared using a focused ion beam (FIB) (FEI QUANTA-3D-FEG) and were then observed using FETEM (FEI TECNAI-G2) operating at 200 kV. The specimens were roughly cut with a gallium ion beam irradiated at 30 nA and 30 kV, and then finally polished at 43 pA and 2 kV. The difference in distribution of the organic phase was quantitatively evaluated from the variation coefficient of white and black parts in the binarized TEM images by using image analysis software (Gimp-2) (Supporting Information). Powder XRD patterns were obtained using a Bruker D8 with Cu Kα1 radiation. The variance of the lattice spacing (Δd/d) of the samples was estimated with Williamson−Hall plots using XRD profiles (Supporting Information).48 Here, we adopted Warren’s method49 to correct the band broadening due to the effects from the instrument. The content of organic matter was evaluated by thermal gravimetry (TG) using an SII TG/DTA 6200. The samples were heated in air from 50 to 1000 °C for combustion of the organic matter.
proposed to involve oriented attachment of polymer-stabilized crystalline or noncrystalline nanoparticles28,29,46 and stepwise crystal growth with mineral bridges connecting nanoparticles.47 Addadi and co-workers proposed that the textured CaCO3 crystals are produced through a solid-state transformation of amorphous calcium carbonate (ACC) involving nanoparticle accretion.27−29 In spite of these efforts, the formation mechanism of biogenic and biomimetic textured crystals and mesocrystals has not yet been revealed. It is necessary to address the formation mechanism of the nanostructures to understand the biomineralization and development of the biomimetic process. In the present work, we synthesized various types of mesoscale textured calcites similar to those of biogenic crystals in CaCO3-based biominerals. The biomimetic mesoscopic textures depended on the state of the organic species that were contained in the supersaturated solutions. The dendritic growth on the nanoscale is essential for the production of strained bodies in the insoluble gel matrix, while the facet growth with soluble polymers is inferred to produce the textured calcite that has a continuous body including organic phases. These findings are important for fabrication of the organic-mediated mesostructured crystals.
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RESULTS AND DISCUSSION Characterization of Biominerals. Mesoscopically textured crystals have been regarded as a particular hierarchical architecture for CaCO3-based biominerals. The structural difference, including the distribution of organic phases and lattice strain, has been reported for calcite bodies of a fan mussel and a pearl shell.14 However, the presence of granular textures that is the essence of the mesocrystal or bridged nanocrystals was not clearly evaluated in the previous study. In the present work, we characterized the mesoscale textures of three kinds of biogenic calcite crystals from an avian eggshell and the prismatic layers of the fan mussel and the pearl oyster after removal of the organic substance with a NaClO solution. The mammillary layer of the eggshell was composed of grains ∼50 μm in diameter (Figure S1c). The columns ∼100 μm in diameter were obtained from two kinds of prismatic layers (Figure S1a,b). As shown in Figure 1, nanoscale grains 50−70 nm in diameter were observed on the surface and the cross section of the biogenic calcites (Figure 1a1−c1, a2−c2). The cross-sectional surfaces were prepared by cracking the crystal grains with a muddler. The granular textures were clearly observed after etching of the calcite bodies with a diluted acetic acid solution (Figure 1a3−c3). Here, the crystal surface was mildly etched with 0.1 wt % acetic acid solution at room temperature for 4 h. Therefore, these biogenic calcite crystals have an internal structure showing granular textures similar to those of the surfaces. On the other hand, the granular textures were not observed on or in a geological single crystal of calcite (Iceland spar) (Figure S5a). The spot patterns of electron diffraction within the scope of a circle 2 μm in diameter, which were assigned to the calcite lattice, were obtained from FIB-cut platy samples of the granular structures (Figure 1a4−c4, inset). This means that the grains were arranged in the same crystallographic direction, like a single-crystalline body. The presence of an organic phase in the crystalline bodies is shown as white parts in binary pictures obtained from TEM images of the FIB-cut plates (Figure 1a4−c4), as reported in the previous article.14 The biogenic calcite crystals contained 1−2 wt % of organic matter according to the TG analysis (Figure S6). These contrasts were not observed on the geological calcite (Figure S5a3). Discrete organic phases ∼5 nm in diameter were homogeneously distributed in the continuous inorganic matrix of the fan mussel. On the other hand, the organic phases were localized in the crystalline bodies of the pearl shell and the eggshell. Linear aggregation of the impurities
EXPERIMENTAL SECTION
Materials. Three kinds of biogenic calcite crystals in CaCO3-based biominerals were used for characterization of the granular textures. The prismatic layers of a pearl oyster (Pinctada fucata) and a fan mussel (Atrina pectinata) were mechanically separated from the aragonite nacreous layers. These prismatic layers of shells and an avian eggshell (Gallus gallus domesticus) were immersed in a 5 vol % NaClO (Kanto Chemical) aqueous solution for 2 days to remove organic substances, and the samples were then washed with purified water. Synthesis. CaCl2·2H2O (Kanto Chemical), (NH4)2CO3 (Kanto Chemical), agar (Kanto Chemical, agarose ∼70 wt %, agaropectin ∼30 wt %), poly(acrylic acid) (PAA, Mw: 2000) (Sigma-Aldrich), and hexyltrimethylammonium bromide (CTA) (Tokyo Chemical) were used without further purification. Several kinds of biomimetic calcite crystals were produced using a supersaturated solution system. The PAA-mediated calcite (CaCO3/PAA) was produced in an aqueous solution containing CaCl2·2H2O (10 mmol/dm3) and PAA (0−50 mmol/dm3). The agar-mediated calcites (CaCO3/agar-sol, CaCO3/ agar-gel, and CaCO3/agar-gel/CTA) were grown in the solution containing CaCl2·2H2O (50 mmol/dm3) and a certain amount of agar powder (0−8.0 wt %) and CTA (0−1000 mmol/dm 3 ). A homogeneous solution was prepared by stirring at about 90 °C. After agar dissolved completely, the solution was put in a refrigerated chamber for gelation. However, the aqueous solution containing 0.1 wt % of agar was not solidified, even after aging. These solutions and hydrogels were sealed with (NH4)2CO3 for 1−4 days in a glass vessel. Precipitates in the solutions and hydrogels were washed with hot water and then air-dried at 60 °C. Epitaxial growth was performed on a seed of a calcite single crystal (Iceland spar) 1−5 mm in size using a solution containing CaCl2· 2H2O (1 mmol/dm3), agar (8.0 wt %), and CTA (1000 mmol/dm3). The seed calcite was washed with purified water several times and fixed on a glass substrate. After the agar was completely dissolved, the calcite seed was soaked in the solution. The prepared gel, including the seed, was sealed with (NH4)2CO3 for 24 h in a glass vessel. The crystals grown on the seed calcite were washed with hot water and air-dried at 60 °C. Characterization. The CaCO3 particles were analyzed using fieldemission scanning electron microscopy (FESEM), field-emission transmission electron microscopy (FETEM), optical microscopy (OM), and powder X-ray diffraction analysis (XRD). The samples were coated with osmium using a plasma coater (Vacuum Device HPC-1SW) and were then observed using FESEM (FEI Sirion and 3756
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formation of granular textures with no relation to the lattice strain. We observed the nanoscale granular textures on the surfaces and the cross-sectional views of the biogenic calcites shown in the present work. The electron diffraction patterns indicate that the nanograins were arranged in the same crystallographic direction. However, the distribution of the organic phase and the magnitude of lattice strain in the biogenic calcite crystals indicate the variation of the granularly textured bodies in biominerals. The prismatic layer of the fan mussel is basically composed of the low-strain textured calcite that has a monocrystalline body including homogeneously distributed tiny organic inclusions. The presence of the granular textures suggests that the organic inclusions network through the entire body. The presence of organic matter in the granular texture was revealed by chemical etching (Figure 1a3). The fibrils were suggested to be formed from the organic inclusion through the etching process.15 Thus, the granular texture can be regarded as a monocrystalline body including homogeneously distributed organic inclusions. On the other hand, the organic phases were localized with relatively high strain in the crystalline bodies of the pearl shell and the eggshell. One of the authors14 showed that the subgrains were found to be divided by the highly strained parts in the pearl shell. Thus, the calcite bodies of the biominerals consist of the granular textures that are separated with the definite organic phases and the strained crystalline layers. The grains are basically arranged in the same crystallographic direction through strained interphases. Biomimetic Production of Various Mesoscopic Textures. Since CaCO3-based biominerals commonly contain acidic polymers and polysaccharides, poly(acrylic acid) (PAA) and agar have been used as a typical substitution for biomimetic or bioinspired production of CaCO 3 in aqueous systems.29,39−42 In the present work, we produced mesoscopic granular textures similar to those of biominerals with organic molecules. Figure 2 shows the textured bodies of artificial calcite crystals grown in a supersaturated solution containing PAA (Mw: 2000, 50 mmol/dm3), a low concentration (0.1 wt %) of agar (sol), and a high concentration (8.0 wt %) of agar (gel) with and without a cationic organic molecule (CTA) (1000 mmol/dm3). The granular textures were basically observed on and in the calcite bodies grown with the organic molecules. The crystals prepared with PAA (CaCO3/PAA) exhibited grains 30−60 nm in size on the surface and the cross section (Figure 2b1,b2; Figure S9b). The particles formed in the agar sol (CaCO3/agar-sol) were rhombohedra covered with {104} having pores of several tens of nanometers (Figure 2a1; Figure S9a). The cross-sectional image of the crystals indicates the presence of nanograins 50−100 nm in diameter (Figure 2a2). The crystals grown in the agar gel (CaCO3/agar-gel) consisted of inhomogeneous grains 120−330 nm on the surface and 60−190 nm on the cross section (Figure 2d1,d2; Figure S9d). The grains of 60−180 nm in size were observed on the surface and cross section of the crystals formed in the agar gel containing CTA (CaCO3/agar-gel/CTA) (Figure 2c1,c2; Figure S9c). The granular textures appeared clearly after chemical etching of all the biomimetic crystal bodies (Figure 2a3−d3). The granular textures were not observed on calcite crystals grown in the absence of organic molecules (Figure S5b1−b3). The spot patterns of electron diffraction that were assigned to the calcite lattice were obtained from all of the FIB-cut platy samples having mesoscopic textures (Figure 2a4−d4 inset). This means that the calcite crystals have the single-crystalline feature,
Figure 1. SEM images of the surface (a1, b1, c1), the cross section (a2, b2, c2), and the etched surfaces (a3, b3, c3); the binarized pictures of TEM images and the electron diffraction patterns (inset) (a4, b4, c4); and the values of lattice strain and heterogeneity (a5, b5, c5) for the prismatic layer of fan mussel (a1−a5), the prismatic layer of pearl oyster (b1−b5), and the mammillary layer of eggshell (c1−c5). Enlarged SEM and original TEM images were shown in Supporting Information (Figures S2 and S4).
was perpendicular and parallel to the c axis of calcite in the pearl shell and the eggshell, respectively. The difference in distribution of the organic phase was quantitatively supported by the coefficient of variation (CV) for the white and black parts in the binary images (red bars in Figure 1a5−c5). The CV, which is defined as the ratio of the standard deviation to the mean, is used as an indicator of the homogeneity of organic molecules (Supporting Information). The lattice strain of the biogenic calcite was estimated from the XRD profiles (Figures S7 and S8) with Williamson−Hall plots (blue bars in Figure 1a5−c5). Relatively high strain values were obtained for the calcite bodies of the pearl shell and the eggshell. On the other hand, the strain of calcite in the fan mussel was as small as the value (0.045 ± 0.023%) in Iceland spar regardless of the presence of the granular texture. Therefore, the interaction of the organic molecules with the crystalline units induces the 3757
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Figure 2. SEM images of the surface (a1−d1), the cross section (a2− d2), and the etched surfaces (a3−d3); the binarized pictures of TEM images and the electron diffraction patterns (inset) (a4−d4); and the values of lattice strain and heterogeneity (a5−d5) for CaCO3/agar-sol (a1−a5), CaCO3/PAA (b1−b5), CaCO3/agar-gel/CTA (c1−c5), and CaCO3/agar-gel (d1−d5). Enlarged SEM and original TEM images of a1−d1 and a4−d4 were shown in Supporting Information (Figures S3 and S4).
concentration of the organic additives. The textured crystals with homogeneously distributed organic phases with a low lattice strain similar to that in the fan mussel are grown with soluble macromolecules, such as PAA and a low concentration of agar. The insoluble gel matrix promotes the formation of mesoscale granular textures with locally distributed organic phases with a relatively large lattice strain, which are analogous to the mesoscopic textures of the pearl shell and the eggshell. The presence of the cationic molecule improves the homogeneity of the size of the grains and pores in the textures. However, the effect was not observed upon the addition of CTA without agar gel (Figure S9e). These results suggest that the organic electrolyte combined with the agar gel network controls the crystalline morphology. Growth of Mesoscopic Granular Textures. In previous work, the presence of polyelectrolytes and gel matrices induced the formation of mesostructured crystals similar to those in biominerals.29,39−42 However, the formation process has not been sufficiently clarified. In the current work, we showed that two kinds of typical textured crystals were grown with various kinds of organic molecules. The textured calcites with
although the granular textures are clearly observed on and in their bodies. The binary TEM images of the FIB-cut plates indicate the presence of an organic phase as white parts in the artificially grown calcite crystals (Figure 2a4−d4). In the crystals of CaCO3/PAA and CaCO3/agar-sol, the organic phases ∼5 nm in diameter were homogeneously distributed in the samples. On the other hand, the organic impurities were localized in the crystalline bodies of CaCO3/agar-gel and CaCO3/agar-gel/ CTA. The impurities were linearly aligned in the body of the calcite crystal. These features of the organic phase are similar to those of the high-strain calcite in the pearl shell and the eggshell. The CV of white and black parts in the binary images supports the difference in the distribution of the organic phases (red bars in Figure 2a5−d5). The lattice strain in the calcite crystals of CaCO3/PAA and CaCO3/agar-sol was as small as the value in Iceland spar. On the other hand, relatively high strain values were obtained for the calcite bodies of CaCO3/ agar-gel and CaCO3/agar-gel/CTA (blue bars in Figure 2a5− d5). These results indicate that two kinds of typical textured calcite crystals are produced by changing the kind and 3758
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branches mainly grew in two directions (Figure 3b2). The calcite body was relatively porous in the outer layer (Figure 3b2) and dense in the inner part (Figure 3b3). These results suggest that the branches formed by the dendritic growth are thickened though the lateral growth with prolonging of the reaction period. Thus, the dense structure was formed in the inner part. Figure 4a illustrates the formation process of the mesoscopic texture with segregated organic phases and lattice strains.
segregated organic phases and lattice strains were formed in the gel matrix. The faceted units were definitely grown in the dense agar gel containing CTA. The architecture of the textured calcite provides clues to the process. However, it is generally difficult to observe the growth structures of textured calcites in the homogeneous system. Therefore, we utilized the epitaxial growth of the mesostructured calcite on a single crystal as a seed to clarify the formation process including the growth direction. As shown in Figure 3a1−a4, the branching structure
Figure 4. Formation processes of the high-strain mesoscopic granular textures divided with locally distributed organic phases (a) and the low-strain textures having a homogeneous distribution of organic molecules (b). Nanoscale dendritic growth of calcite occurs with the gel matrix. The branches then thicken, and the textured body is formed through the fusion of the branches. Facet growth of calcite crystal occurs with the segregation of specific soluble organic species.
Basically, the textured crystal is formed through dendritic growth on a nanoscale. The presence of organic molecules induces the branching of the crystal growth. The rigid gel network of agarose performs as a physical impedance. The dominant growth direction of calcite is ⟨001⟩, although the stable face is {104}. The difference between the growth direction and the stable faces produced nanoscale steps on the crystal. Moreover, the branches grew in other directions. The nanoscale dendritic structures are formed through the densely branching growth in the gel matrix. The presence of a large amount of organic electrolytes, such as CTA, in the gel matrix promotes branching of the crystal by combination with the agar network. The branches then thicken, and the textured bodies are finally formed through the fusion of the branches. The lattice strains are deduced to be induced at the interface between the branches after the fusion. On the other hand, soluble polymers and a low concentration of agar cannot induce the definite branching growth, while the organic molecules are included through the facet growth of calcite (Figure 4b). Thus, the granular textures of the continuous body would be formed through facet growth with the segregation of specific soluble organic molecules as a mesoscopically networked inclusion. The analogy of the mesoscopic granular textures suggests that the biogenic calcites are formed through similar processes induced by soluble and/or insoluble biomolecules. Addadi and co-workers27−29 proposed that the mesoscopic textures of calcite crystals are formed by a two-step reaction. In
Figure 3. SEM observation of calcite crystals grown in the agar gel containing CTA (CaCO3/agar-gel/CTA) with (a1−a4) and without (b1−b3) the single-crystalline seed. Top view of the single-crystalline calcite after overgrowth (a1), microscopic image of the branching structures (a2), side view of the single-crystalline calcites after overgrowth (a3), and microscopic image of the branching structures (a4). Cross-sectional macroscopic image (b1) and microscopic images near the surface (b2) and near the core (b3).
was grown on a {104} face of the single crystalline calcite in agar gel. The repetition of light and dark in the polarized images was observed with rotation of the sample every 45° (Figure S10a1,a2). This indicates that the single-crystalline branches were formed through epitaxial growth on the mother crystal. The growth directions are deduced to be ⟨001⟩ and ⟨121⟩ (Figure 3a1−a4; Figure S10b1,b2,c1,c2) according to geometric consideration of the single crystal (Supporting Information). Therefore, the mesoscopic textures were formed on the basis of the dendritic crystal growth. Figure 3b1−b3 shows cross-sectional views of CaCO3/agar-gel/CTA grown for 96 h without the seed crystal. The branching structure from the core to the surface is recognized on the cross section. The 3759
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their model, partially stabilized ACC is first precipitated and then transformed into calcite. The formation of ACC particles is promoted by the presence of additives, such as gel-forming molecules, phosphate ions, and the organic extract from sea urchin embryonic spicules. The ACC nanospheres migrate to the surface of the growing crystal and are then crystallized. Propagation of crystallization was also supposed to occur in a biogenic calcite through secondary nucleation among individual nanoparticles of the disordered phase. The particle accretion mechanism yields faceted single crystals of calcite that maintain the mesoscopic textures. In the mechanisms proposed in the present study, the presence of ACC is not speculated for the formation of mesotextures. However, the possible implication of ACC is not denied in the models. Transient amorphous phases may be formed in the gel matrix ahead of the nanometric dendritic crystal growth involving high-strain mesoscopic granular textures divided by locally distributed organic phases (Figure 4a). Facet growth that provides lowstrain textures having a homogeneous distribution of organic molecules can be promoted by nanospheres stabilized by specific soluble organic species (Figure 4b). Further investigation is required for clarification of the effects of ACC on the formation of mesotextures in biological and biomimetic calcite crystals.
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CONCLUSIONS Various calcite crystals in several biominerals and artificially grown in biomimetic systems were characterized on the basis of their mesoscopic textures. We found the variation of the mesoscopically textured crystals having single-crystalline features: a low-strain body containing homogeneously distributed tiny organic inclusions and a high-strain body divided by locally distributed organic phases and lattice strains. The textured calcites were found to be formed through facet growth containing organic molecules and branching growth on nanoscale by specific interactions with soluble and insoluble organic molecules, respectively.
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ASSOCIATED CONTENT
S Supporting Information *
Additional notes and figures. The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.cgd.5b00407.
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AUTHOR INFORMATION
Corresponding Author
*E-mail:
[email protected]. Notes
The authors declare no competing financial interest.
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ACKNOWLEDGMENTS This work was partially supported by Grant-in-Aid for Scientific Research (No. 22107010) on Innovative Areas of “Fusion Materials: Creative Development of Materials and Exploration of Their Function through Molecular Control” (No. 2206) from the Ministry of Education, Culture, Sports, Science and Technology.
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REFERENCES
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DOI: 10.1021/acs.cgd.5b00407 Cryst. Growth Des. 2015, 15, 3755−3761
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