Formation of Vaterite Mesocrystals in Biomineral ... - ACS Publications

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Formation of Vaterite Mesocrystals in Biomineral-like Structures and Implication for Biomineralization Yu-Ying Wang,† Qi-Zhi Yao,‡ Han Li,† Gen-Tao Zhou,*,† and Ying-Ming Sheng† †

CAS Key Laboratory of Crust-Mantle Materials and Environments, School of Earth and Space Sciences, and ‡School of Chemistry and Materials Science, University of Science and Technology of China, Hefei 230026, P. R. China ABSTRACT: Vaterite mesocrystals with a hexagonal prism structure were successfully achieved in the presence of sodium citrate (SC) and sodium dodecyl benzenesulfonate (SDBS) by use of a gas-diffusion method at room temperature. X-ray powder diffraction (XRD), Fourier transform infrared spectroscopy (FT-IR), transmission electron microscopy (TEM), selected area electron diffraction (SAED), thermogravimetric analysis (TGA), nitrogen physisorption analysis, and fieldemission scanning electron microscopy (FESEM) equipped with energy-dispersive X-ray (EDX) were used to characterize the hexagonal prisms. XRD and FESEM results reveal that the superstructures are composed of hundreds of well-stacked nanoflakes, which construct the laminated hexagonal prism of vaterite. TEM and SAED analyses show that the hexagonal prism has the same crystallographic symmetry as single-crystal vaterite, confirming that the hexagonal prismatic architectures are orientationally aligned mesocrystals of vatreite. However, no hexagonal prism structures can be produced only with SC or SDBS, indicating that the cooperation of SC and SDBS is indispensable to the formation of hexagonal prismatic vaterite mesocrystals. The hexagonal prism mesocrystals of vaterite exhibit remarkable similarity to the nacreous layers of vaterite in freshwater cultured pearls from mussels and the columns/lamellae of vaterite in bivalve in architectures. Therefore, the current study on vaterite mesocrystals will be helpful for us to mimic and learn from nature and may provide another pathway toward full insight into biomineralization mechanism. shells,21 in fish otoliths,15,22,23 and in inorganic tissues like gallstones and human heart valves14,24 and is also mediated by soil bacteria.16,25 Biogenic vaterite also has been found as the only mineral component of endoskeleton in the body spicules and tunic spicules of the solitary ascidian Herdmania momus.2,3,14 Furthermore, biogenetic vaterite is usually exquisitely shaped and is significantly different in its appearance from its abiotic counterpart.2,3,19,26,27 Usually, unstable vaterite precipitates in a spherical shape when grown in laboratory from supersaturated solutions.28,29 Nevertheless, biogenetic vaterite crystallizes in more complex habits than its synthetic counterpart, such as tablets, fibers, and botryoidal habits with lamellar superstructures.14,15,18,19 For example, the vaterite crystals deposited in lackluster pearls show a tablet structure, which has a hierarchy similar to that of nacre with the “brick-andmortar” structure.18,19 The vateritic spicules of H. momus demonstrate a unique architecture composed of microsized, hexagonally faceted thorns organized in partial spirals along the cylinder-like polycrystalline body of the spicule.2,3 These unique and frequently beautiful morphologies that characterize biogenetic vaterite have long been a source of fascination. To date, numerous studies have suggested that morphology and

1. INTRODUCTION Biomineralization is a widespread phenomenon in nature, leading to the formation of a variety of solid inorganic structures by living organisms, including intracellular crystals in prokaryotes, exoskeletons in protozoa, spicules, lenses, bones, teeth, statoliths and otoliths in invertebrates, and pathological biominerals such as gallstones, kidney stones, and oyster pearls.1−3 These biominerals are usually inorganic−organic hybrid composites and fascinate many researchers due to their seemingly well-designed morphologies and hierarchical structures.2−8 Calcium carbonate (CaCO3), occurring geologically as main mineral constituents of sedimentary rocks and biologically as inorganic components in the skeletons of many mineralizing organisms,2,3,7−9 is one of the most abundant minerals in nature. It has three anhydrous crystalline polymorphs: rhombohedral calcite, orthorhombic aragonite, and hexagonal vaterite.10−13 Of them, calcite is thermodynamically the most stable one, followed by aragonite and then vaterite, which is the least stable one. Therefore, the natural occurrence of unstable vaterite is rare relative to stable calcite and metastable aragonite. However, biogenetic vaterite shows high stability compared to its abiotic counterpart due to its strong association with biological activities, and has been of great interest.2,3,14−20 It has been documented that vaterite biomineralization widely occurs in freshwater cultured pearls from mussels,17−19 in larval snail © 2015 American Chemical Society

Received: November 22, 2014 Revised: March 6, 2015 Published: March 12, 2015 1714

DOI: 10.1021/cg501707f Cryst. Growth Des. 2015, 15, 1714−1725

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Crystal Growth & Design Table 1. Morphological Properties of the CaCO3 Obtained under Various Experimental Conditionsa

a

sample

conc of Ca2+ (mM)

conc of SDBS (mM)

conc of SC (mM)

time (h)

morphology

phaseb

1 2 3 4 5 6 7 8 9 10

10.0 10.0 10.0 10.0 10.0 10.0 10.0 10.0 10.0 10.0

10.0 0.0 0.0 2.0 5.0 15.0 10.0 10.0 10.0 10.0

20.0 0.0 20.0 20.0 20.0 20.0 5.0 10.0 15.0 30.0

24 24 24 24 24 24 24 24 24 24

hexagonal prism rhombohedral spindle-like hexagonal flake hexagonal flake/prism hexagonal prism flake and flower-like flower-like hexagonal prism/flake hexagonal flake

V C C V (major) + C V (major) + C V V+C C C (major) + V V+C

For all samples, the initial pH of the mineralization solution is 8.0. bAbbreviations: V, vaterite; C, calcite. 2.2. Preparation. The biomimetic mineralization of CaCO3 was carried out by a CO2 gas diffusion technique36 in a closed desiccator at ambient conditions. In a typical experiment, 0.2941 g of SC (20.0 mM) and 0.1742 g of SDBS (10.0 mM) were first dissolved in 50 mL of deionized water with vigorous stirring by a magnetic stirrer at room temperature. Then, 0.0555 g of CaCl2 was added to the solution and the mixture was stirred for 10 min to form a homogeneous solution. The solution was transferred to a 50 mL beaker with a piece of glass substrate (1.8 cm × 1.8 cm) on the bottom for collecting the crystals. The pH of the solution was adjusted to 8.0 using a diluted HCl or NaOH solution. Finally, the beaker was covered with Parafilm punched with five needle holes and then put in a desiccator. Ten grams of crushed ammonium carbonate was placed at the bottom of the desiccator as the source of CO2, and a bottle (100 mL) of H2SO4 (98%) was also placed in the desiccator to absorb NH3 vapor. After 24 h of incubation, the beaker was taken out, and the glass substrate was separated from the mineralized solution, rinsed thoroughly with anhydrous ethanol several times to remove the polymers possibly adsorbing on the surfaces of the mineralized product, and allowed to dry at room temperature for characterization. The precipitated CaCO3 in beaker was also isolated by centrifugation and washed three times by anhydrous ethanol, and then dried in a vacuum oven overnight at 25 °C. To investigate the effect of concentration of the organic components (SDBS and SC) on the formation of CaCO3, a series of comparative experiments with different concentrations of SDBS and SC were also carried out. All of the experimental conditions and corresponding morphologies of the products are listed in Table 1. 2.3. Characterization. Several analytical techniques were used to characterize the mineralized products. Scanning electron microscopy (SEM) analysis was performed on a field emission SEM microscope (TESCAN MIRA 3) equipped with energy-dispersive X-ray (EDAX, GENESIS APEX), with the operation acceleration voltage of 5 kV. The samples for SEM analysis were coated with a thin film of platinum to increase the conductivity. Energy-dispersive X-ray spectroscopy (EDX) was applied for elemental composition analysis of the mineralized products. The powder X-ray diffraction (XRD) patterns were recorded with a Philips X’Pert ProSuper X-ray diffractometer equipped with graphite monochromatized Cu Kα irradiation (λ = 0.154056 nm), employing a scanning rate of 0.02°·s−1 in the 2θ range 10−70°. FT-IR spectra were recorded on a Nicolet Impact 400 FT-IR spectrometer from 4000 to 400 cm−1 at room temperature. Transmission electron microscopy (TEM) and selected area electron diffraction (SAED) were performed on a JEOL-2010 (JSM) microscope at an accelerating voltage of 200 kV. In order to analyze the internal structure of vaterite crystals, samples were embedded in epoxy resin and ultramicrotomed by cryosection system (Leica EM FC7 UC7) for the TEM measurements. Nitrogen sorption data were performed at a Micromeritics Tristar II 3020M automated gas adsorption analyzer utilizing Barrett−Emmett−Teller (BET) calculations for surface area and Barrett−Joyner−Halenda (BJH) calculations for pore size distribution for the adsorption branch of the isotherm. Thermogravimetric analysis was carried out under a

orientation of biogenetic vaterite are directed by organic molecules such as proteins and glycoproteins.2,3,19,23,26,27 For instance, in fish otoliths, organic matrix existed between the vaterite layers have a large content of acidic amino acids, such as glycine, glutamic acid, and aspartic acid.23 In freshwater cultured pearls, a large amount of organic molecules containing S and P have been found to exist between the vaterite platelets.19 A general consensus is that polyanionic macromolecules, such as proteins, can induce the nucleation of special polymorph and control the unique morphogenesis of biogenic minerals with their carboxylate, sulfate and/or sulfonic groups, phosphate.1,23,30−33 Therefore, investigating the effect of structure-specific organic/biological model additives on crystallization and morphogenesis of vaterite is important to understand both the unique morphogenesis and biomineralization mechanism. Here, the biomimetic growth of CaCO3 was carried out by a classic CO2 gas diffusion technique, and sodium citrate (SC) and sodium dodecyl benzenesulfonate (SDBS) were selected as model organic additives to influence the crystallization and growth of CaCO3. Citrate with three −COO− groups has been identified as playing critical roles in interfering with crystal thickening and stabilizing apatite nanocrystal sizes in bone,34,35 and SDBS is an anion surfactant with a headgroup of sulfonic group. Therefore, they may mimic the mineralization of certain functional groups in macromolecules associated with biomineralization. The well-defined hexagonal prisms of vaterite mesocrystals stacked by hundreds of nanoflakes subunits can be successfully achieved in the presence of SC and SDBS. Because of the remarkable resemblance of the vaterite hexagonal prism-like mesocrystals to the vaterite nacreous layers in freshwater cultured pearls or to the columnar/lamellar vaterite in the bivalve, current results may bring new insights about biomineralization.

2. EXPERIMENTAL SECTION 2.1. Chemicals. All chemicals are commercially available and analytical grade used as received without further purification. Sodium citrate (C6H5Na3·2H2O), sodium dodecyl benzenesulfonate (SDBS), ammonium carbonate ((NH4)2CO3), and calcium chloride (CaCl2) were purchased from Sinopharm Chemical Reagent Co., Ltd. Deionized water was used in all experiments. Analytical grade hydrochloric acid (HCl) and sodium hydroxide (NaOH) were used to adjust the pH whenever necessary. All glassware (beakers and small pieces of glass substrates) were cleaned and sonicated in anhydrous ethanol for 30 min, rinsed thoroughly with deionized water, further soaked in a solution of HNO3−H2O2−H2O (1:1:1, V:V:V), and then rinsed with deionized water and finally dried in air with anhydrous ethanol. 1715


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Crystal Growth & Design

Figure 1. Typical FESEM images of hexagonal prisms formed in the presence of [SDBS] = 10.0 mM, [sodium citrate] = 20.0 mM, and [Ca2+] = 10.0 mM for 24 h (sample 1), where (a) shows the panoramic image. Inset: the energy-dispersive X-ray (EDX) spectroscopic analysis, (b) and (c) closeup of an individual hexagonal prism, and (d) the higher magnification of the profile of a hexagonal prism.

Figure 2. Representative XRD pattern (a) and FT-IR spectrum (b) of sample 1. stream of air, at a heating rate of 10 °C/min using a TA Instruments (SDT Q600). To investigate the interaction between SDBS and SC, nuclear magnetic resonance (NMR) and ultraviolet absorption (UV) were applied. The proton NMR spectra were recorded of the additives dissolved in D2O on an AV 600 MHz instrument, at 300 K. Chemical shifts are reported in ppm (δ) relative to internal tetramethylsilane (TMS) at 0.00 ppm. The UV spectra were recorded on a Hitachi UV4100 spectrophotometer at room temperature in a 1 cm quartz cuvette.

3. RESULTS Figure 1 presents FESEM images of the mineralized product (sample 1 in Table 1) obtained in the presence of 20.0 mM SC and 10.0 mM SDBS. The panorama image (Figure 1a) shows that all of the particles exhibit well-defined hexagonal prism structures. Corresponding EDX analysis (Figure 1a, inset) demonstrates that the prism-like structures contain C, O, and Ca, as well as a small amount of Na, Si, Pt, and S, where the element Si comes from glass substrate and Pt from the sample 1716


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Figure 3. Representative TEM images (a and c) and SAED patterns (b and d) of sample 1.

mmc (JCPDS file 33-0268). Nevertheless, the (004) and (008) reflections in this sample are particularly strong and sharp compared with the standard diffraction pattern of vaterite (JCPDS file 33-0268). The stronger (004) and (008) reflections are most likely related to the preferential orientation of vaterite along the [001] direction, indicating that the hexagonal prisms may be stacked layer by layer along the [001] direction of vaterite crystal (e.g., Figure 1b,c). Moreover, all diffraction peaks are strong and sharp, also indicating that the assembled vaterite subunits are well crystallized. The corresponding FT-IR spectrum is exhibited in Figure 2b. The vibrational bands at 1086, 876, and 743 cm −1 can unambiguously be assigned to carbonate symmetric stretching (ν1 mode), carbonate out-of-plane bending (ν2 mode), and inplane bending (ν4 mode) vibrations of vaterite, respectively.29,37 No characteristic peaks belonging to aragonite at 713 and 700 cm−1, as well as calcite at 713 and 876 cm−1, were detected, further demonstrating that the hexagonal prism is the pure phase of vaterite.13,32 In addition, the broad band centered at 3450 cm−1 (between 3550 and 3200 cm−1) is the stretching vibrating absorption peak of O−H bond.38,39 The bands

preparation of SEM analysis, indicating the hexagonal prisms should be calcium carbonate. In particular, the presence of S and Na in the EDX spectrum may show that there are traces of organic additives SDBS and SC occluded into the hexagonal prism structures, indicating that the prism-like structures are a biomineral-like organic−inorganic composite. The further magnified SEM images in Figure 1b,c unambiguously show that the prism-like structure is a quite regular hexagonal prism with sharp facets and edges. The angles of adjacent edges are close to 120°, corresponding to the habit of hexagonal symmetry (Figure 1b). Moreover, the hexagonal prism is about 3 μm in lateral length and 4 μm in height (Figure 1b,c). The locally magnified images (inset in Figure 1c,d) further exhibit that the prism is stacked by hundreds of nanoflakes subunits, and the thicknesses of the nanoflakes are ca. 40−50 nm. Phase composition for sample 1 was identified by XRD and FT-IR techniques, and the results are presented in Figure 2. The XRD result reveals that the hexagonal prismatic architectures are pure hexagonal vaterite with the lattice parameters a = 7.147 Å, c = 16.917 Å, and space group P63/ 1717


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Crystal Growth & Design detected at 2920 and 2851 cm−1 can be assigned to the asymmetric and symmetric stretching vibrations of the C−H groups from organic components, respectively.36,39 In particular, the trace bands of the sulfonic acid group at 1170 cm−1 and carboxyl group at 1736 cm−1 are also detected, indicating that the organic additives are intimately bound with the mineralized structures even after extensive washing.40−42 Therefore, the FESEM, XRD, and FT-IR analyses demonstrate that the mineralized product is an organic−inorganic composite hexagonal prism of vaterite. The morphology and microstructure of the hexagonal prismatic vaterite was further examined by TEM and SAED. Figure 3a,b depicts the TEM image and representative SAED pattern of an ultrathin section detached from a typical prism in sample 1 by a 10 min of ultrasonication. The TEM image (Figure 3a) indicates that this thin section is constructed of obvious nanoflake-like subunits. Moreover, a remarkable number of interstices can be seen within the bulk, suggesting a crystallization pathway based on the aggregation of subunits. The SAED pattern (Figure 3b) of the whole area of Figure 3a shows a set of elongated diffraction spots, and the spots can be indexed as vaterite viewed from the [001] zone axis. The appearance of periodic elongated diffraction spots indicates that the hexagonal prism is stacked by nanoflake subunits, and the crystallographic directions of the nanoflakes in the hexagonal prism are not random but are roughly arranged in the same orientation. Each vaterite prism can be considered as an aggregate consisting of nanoflakes that share the same 3D orientations. The internal structure of vaterite crystals was also investigated using TEM of an ultrathin section prepared using cryosection system, where the vaterite sample was embedded in epoxy resin and ultra-microtomed (Figure 3c,d). The image of TEM (Figure 3c) further demonstrates that the thin section is constructed of obvious nanoflake-like subunits. The SAED analyses from the different areas in Figure 3c render the same diffraction patterns of single crystal, and the representative SAED pattern taken from the boxed area in Figure 3c is shown in Figure 3d. The SAED results from the interior of the prismlike structure further confirm that the crystallographic orientations of all the nanoflakes in each hexagonal prism are parallel to each other. Therefore, the TEM and SAED analyses reveal that the hexagonal prismatic vaterite is mesocrystal. The hexagonal prism-like vaterite was also characterized by use of TG-DTA, and the corresponding results are illustrated in Figure 4. There are three stages of weight loss in the thermogram curve. The first slow weight loss with a total 1.06 wt % occurs from room temperature to 150 °C, which can be attributed to the evaporation of the adsorbed water.39 The second apparent weight loss of 1.87 wt % and the corresponding exothermic peak centered at 422 °C in the DTA curve can be assigned to the combustion and removal of the organic components (SC and SDBS) adsorbed/anchored in the mineralized product, which corresponds to the EDX (Figure 1a, inset) and FT-IR (Figure 2b) results. The last weight loss (∼41.98 wt %) in the temperature range of 550− 800 °C should be attributed to the decomposition of CaCO3 to CaO and CO2. This is further supported by the significant endothermic peak at 730 °C in the DTA curve. Therefore, TGDTA analyses support again that the obtained vaterite can be regarded as an organic−inorganic composite including approximately 1.87 wt % organics. Usually, mesopores and defects under preservation of a collective crystal orientation are believed to be important

Figure 4. TG curve (black line) and DTA curve (red line) of sample 1 in air atmosphere.

characteristics of mesocrystals.43,44 Therefore, mesoporous structure in sample 1 was demonstrated by gas sorption experiments according to BET. Representative N2 sorption isotherm and the corresponding BJH pore size distribution curve are plotted in Figure 5, panels a and b, respectively. The adsorption/desorption hysteresis loops mainly present in the

Figure 5. Nitrogen adsorption−desorption isotherms (a) and pore size distribution (b) of sample 1. 1718


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view of the structure (inset in Figure 7a) clearly reveals that the calcite crystal is elongated along the crystallographic c-axis with three {10.4} faces on each end of the formed crystal. The formation of elongated calcite prisms indicates that SC molecules interact preferentially with calcite faces paralleling to the c direction. However, when 2.0 mM of SDBS was introduced to this mineralization system, the XRD analysis (Figure 6b) shows that vaterite and calcite coexist in the mineralized product (sample 4). FESEM observation (Figure 7b) indicates that the flake-like crystals with a diameter of about 5−10 μm appear in the presence of 2.0 mM SDBS and 20.0 mM SC, and most of them exhibiting hexagonal structures. Combined with the XRD analysis (Figure 6b), the hexagonal flake-like particles can be identified as vaterite. This is similar to the hexagonal plate-like mesocrystals of vaterite obtained in the presence of a N-trimethylammonium derivative of hydroxyethyl cellulose in morphology.46 Besides, hexagonal/truncated trigonal plates of calcite, which expose the unusual (001) face, was also observed (inset in Figure 7b). This truncated calcite morphology has also been obtained in the presence of polystyrenesulfonate (PSS) molecules containing a sulfonate group.47 The unusual expression of the (001) face in the calcite can be attributed to preferential interactions of SDBS molecules with the (001) face, because the {0001} faces of calcite are polar and consist of alternate layers of Ca2+ and CO32− ions.48 Further increasing concentration of SDBS to 5.0 mM leads to the formation of massive vaterite and minor calcite (sample 5, Figure 6c). FESEM images show that besides hexagonal flakelike crystals some of crystals are assembled into hexagonal prism structures (Figure 7c and its inset). In particular, the uniform hexagonal prism-like vaterite can be formed with 10.0 mM of SDBS and 20.0 mM of SC (Figures 1 and 2). Moreover, with the SDBS concentration being sequentially increased to 15.0 mM, pure hexagonal prism-like vaterite is also obtained (Figures 6d and 7d). It appears that in the presence of SC raising the concentration of SDBS facilitates the formation of hexagonal prismatic vaterite (e.g., Figures 1, 6, and 7). Similarly, the influence of SC on the polymorph selection and morphogenesis of mineralized products was also investigated under the same mineralization conditions (samples 7−10 in Table 1). In the absence of SC, Ca2+ and SDBS immediately precipitate after mixing, and thus the subsequent experiments are not carried out. After 5.0 mM of SC was added into the mineralization solution (sample 7), nevertheless, 24 h of mineralization leads to a binary mixture of vaterite and calcite (Figure 8a). FESEM image (Figure 9a) shows that a number of flake-like crystals (indicated by red arrows) and flower-like crystals (indicated by white arrows) coexist. When the concentration of SC is increased to 10.0 mM, XRD analysis confirms that pure phase of calcite is obtained (Figure 8b), and FESEM observations unveil that all the calcite exhibits the hierarchical rose-like architectures (Figure 9b and its inset). Nevertheless, as the SC concentration further increases to 15.0 mM, the product (sample 9) turns into a mixture of vaterite and calcite again (Figure 8c). A mass of hexagonal prism crystals (vaterite) and a few quasi hexagon-shaped crystals (calcite) can be observed in the FESEM images (Figure 9c and its insets). Moreover, the well-defined hexagonal prism-like structures of vaterite are formed when the SC concentration increases to 20.0 mM (Figures 1 and 2). However, with further increasing SC concentration to 30.0 mM, the product (sample 10) is also composed of vaterite and calcite (Figure 8d). The FESEM analyses reveal that hexagon-like calcite flakes and

range of 0.4−1.0 P/Po. The N2 isotherm of sample 1 is a type IV isotherm with a type H3 hysteresis loop, indicating that the sample has a mesoporous structure.39,45 In addition, the pore size distribution curve of the hexagonal prism (Figure 5b) is determined from the adsorption branch of the isotherm. The pore size distribution peaks are centered at 5 and 10 nm, respectively. These mesopores may come from the interstitial voids of the packed primary nanoparticles within the hexagonal prismatic architectures. The BET surface area of the hexagonal prismatic vaterite calculated from N2 isotherms is 5.09 m2/g, and the total pore volume is about 0.02 cm3/g. In a word, the results of TEM, SAED, TG-DTA, and BET confirm that the vaterite hexagonal prisms are mesocrystals consisting of oriented nanoflakes and organics. Moreover, to understand the formation details of the hexagonal prism-like vaterite, a series of comparative experiments with various concentrations of SDBS or SC were performed while keeping other conditions constant. Prior to these experiments, a blank experiment was performed without any organic additives. The XRD and SEM results show that in the absence of SC and SDBS (sample 2 in Table 1) the mineralized product is well developed calcite rhombohedra terminated by {10.4} planes (data not shown). However, marked changes in phase and morphology can be observed with the addition of the organic additives. Figures 6 and 7 show the

Figure 6. XRD patterns of the products obtained at the SDBS concentration of 0.0 mM (a), 2.0 mM (b), 5.0 mM (c), and 15.0 mM (d), while the SC concentration was kept at 20 mM (samples 3−6).

XRD patterns and SEM images of the CaCO3 samples mineralized for 24 h at SDBS concentrations of 0.0, 2.0, 5.0, or 15.0 mM (samples 3−6 in Table 1) while maintaining the SC concentration at 20.0 mM. The XRD result (Figure 6a) demonstrates that the product (sample 3) is pure calcite phase only with 20.0 mM of SC. The corresponding FESEM image in Figure 7a shows that the regular elongated calcite crystals are obtained. The elongated calcite crystals have an average length of about 20 μm with an aspect ratio of ∼4 (the aspect ratio defined as a ratio of length to diameter of the crystal). A closer 1719


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Figure 7. SEM images of the products obtained at the SDBS concentration of 0.0 mM (a), 2.0 mM (b), 5.0 mM (c), and 15.0 mM (d), while the SC concentration was kept at 20 mM (samples 3−6). The smooth faces in panel b (inset) are ascribed to the {10.4} family, as indicated by arrows.

some disc-like vaterite aggregates with rough appearances coexist, and no prism-like vaterite mesocrystals are visible in this case (Figure 9d and its insets). Therefore, the concentration of SC also has a significant effect on the phase and morphology of CaCO3. Furthermore, no hexagonal prism structures can be obtained only in the presence of SC or SDBS, indicating that SC and SDBS do cooperate to induce the formation of hexagonal prismatic vaterite. Although various physical properties such as conductance, viscosity, and surface tension can give some information about intermolecular interactions between the component molecules,49,50 spectroscopic methods such as NMR, UV have been considered to be the most appropriate for the purpose.51,52 Thus, 1H NMR and UV techniques were applied here to identify the interaction between SC and SDBS in solution. Figure 10a depicts 1H NMR spectra of SDBS and the mixture of SDBS and SC in D2O at 300 K. The structural formula of SDBS is also inset in Figure 10a. Corresponding to the aromatic ring in the headgroup of SDBS, there are two clusters signals: the peaks at the chemical shift of about 7.6 ppm in Figure 10a correspond to the H-1 of CH groups and those at about 7.1 ppm correspond to the H-2.51 To carefully inspect the 1H signals, the abscissa and vertical axes of the 1H NMR spectra in Figure 10a have been zoomed in, and the range of the abscissa axis is from 6.5 to 8, the vertical axis from −50 to 300 (inset in Figure 10a). Strikingly, the two signals of aromatic ring (H-1 and H-2) clearly show upfield shifts when SDBS is mixed with SC. It is sufficient to assume that the variations of

Figure 8. XRD patterns of the products obtained at the SC concentration of 5.0 mM (a), 10.0 mM (b), 15.0 mM (c), and 30.0 mM (d), while the SDBS concentration was kept at 10 mM (samples 7−10).

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Figure 9. SEM images of the products obtained at the SC concentration of 5.0 mM (a), 10.0 mM (b), 15.0 mM (c), and 30.0 mM (d), while the SDBS concentration was kept at 10 mM (samples 7−10). The smooth faces in panels c and d (inset) are ascribed to the {10.4} family, as indicated by arrows.

received considerable attention in recent years. Mesocrystals are quasi-single crystals comprising ordered assemblies of small, anisotropic, and vectorially aligned nanoparticles, which are usually interconnected by the binding affinity between the polymer molecules anchored/adsorbed to the nanoparticles. Therefore, mesocrystals often behave as an entirely new class of porous materials superstructures.43,55,63,64 Moreover, in the absence of any organic additives, various mesocrystal structures such as fluorapatite and aragonite mesocrystals can also be formed.62,65 In this case, the intrinsic anisotropic dipole−dipole interactions from the assembled subunits are believed to be the driving force for the formation of mesocrystals.62,65−67 Interestingly, mesocrystal structures have also been widely found in biominerals.5,7,17,68−71 For example, aligned nanoparticle building units were already found in a sea urchin spine and sponge spicules,71 and also found in the tablets of aragonite-type nacre.5 However, due to the complexity of biomineral systems and the difficulty of observing structure formation starting on the nanoscale in living systems, not much is known yet about the formation mechanisms of mesocrystals in biominerals. The exact formation mechanism of a mesocrystal still remains to be explored for biominerals, as pointed out by Song and Cölfen (2010).61 In our experiment, well-defined hexagonal prismatic vaterite stacked by hundreds of small nanoflakes subunits has been obtained in the presence of 20.0 mM SC and 10.0 mM SDBS (Figures 1 and 2). TEM and SAED analyses (Figure 3) confirm that the hexagonal

the chemical shifts reflect changes in the local environment of the observed nuclei, suggesting that SC changes the aggregation properties of SDBS in solution. The UV spectra shown in Figure 10b further confirm this assumption. It can be seen that the peak of SDBS at 220 nm for benzene ring decreases and moves to longer wavelength when SC is added into the solution. The absorption peak shift can be ascribed to the interaction of SC with the benzene ring of SDBS,53 indicating that the microenvironment around SDBS is changed. Therefore, the 1H NMR and UV analyses (Figure 10) indicate that the strong interactions between SC and SDBS occur in solution. It is the strong interactions between SC and SDBS that can cooperatively influence the formation of hexagonal prismatic vaterite mesocrystals.

4. DISCUSSION In the crystallization process of inorganics, two basic mechanisms have been proposed, including classical and nonclassical crystallizations.11,54−58 With regard to the classical crystallization, the growth of crystals is typically considered to occur via atom-by-atom addition to an existing nucleus or template. In contrast to the classical mechanism of atom/ molecule mediated growth of a single crystal, the particle mediated growth and assembly mechanisms are summarized as “non-classical crystallization”, including the processes like oriented attachment and mesocrystal formation.43,54,55,59−62 As one way of nonclassical crystallizations, mesocrystals have 1721


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nanoparticles or promoted by the interactions between surface-anchored ligands.74,75 The SDBS molecule has a hydrophobic tail, so the adsorbed/anchored organic additives can assist the self-assembly and induce the formation of mesocrystal structures by van der Waals force and/or hydrogen bonds among them. Besides, the strong dipole−dipole interactions along the crystallographic c direction may also contribute to the formation of hexagonal prismatic vaterite mesocrystals.29 Therefore, the driving force controlling the selfassembly process of hexagonal prismatic vaterite mesocrystals may originate from the van der Waals force and/or hydrogen bonds of the adsorbed/anchored organic molecules and the inherent anisotropic dipole−dipole interactions between the assembled subunits. In addition, the comparative experiments without SDBS and SC show that in the absence of organic additives, the same mineralization leads to only well-defined rhombohedral calcite (data not shown), suggesting that dissolved ammonia is not the critical factor for the phase variation of CaCO3 in present system. Nevertheless, the calcite elongated along the crystallographic c-axis with well-defined rhombohedral {10.4} caps on each end is formed only in the presence of SC (Figure 6a). The similarity of the results obtained in this study by applying SC with the ones reported in the presence of EDTA or malic acid may be originating from the presence of carboxylic groups in the molecular structure.76,77 The −COO− groups in SC can interact with the surface Ca2+ ions of CaCO3 crystals through electrostatic and/or bonding interactions.40,77,78 Therefore, the elongated morphology expressing {11.0} faces can be explained by the specific adsorption/binding of SC to the planes parallel to the c-axis of CaCO3 through the carboxylate groups. Nevertheless, with the increase of the SDBS concentration, vaterite becomes the dominant phase and the vaterite flakes gradually turn to hexagonal prism-like vaterite (Figures 1, 6, and 7), indicating that the formation of hexagonal prism may be via a process in which the flake-like particles gradually assemble into prism structures. Therefore, it is reasonable to conclude that SDBS is one of the key factors affecting the phase and morphology of CaCO3. Indeed, SDBS have always been selected to modify polymorph of CaCO3 and is believed to be in favor of the formation of metastable vaterite.79−81 For example, spherical vaterite was successfully fabricated with the addition of SDBS by rapidly mixing CaCl2 with Na2CO3 solutions.79 The transformation from aragonite to vaterite was also achieved with the assistance of SDBS using a 90 °C hydrothermal method.80 Hollow vaterite spheres were prepared in SDBS and aspartic acid binary-additive system by use of a rapid agitation method.81 In the present mineralization system, the polymorph change of CaCO3 from a pure calcite to vaterite dominated mixture and finally to pure vaterite can be nicely captured by the choice of a suitable content of SDBS and SC (Figures 1, 6, and 7). No hexagonal prism structures can be produced only with SC or SDBS. These results indicate that the coexistence of SC and SDBS is necessary for the formation of hexagonal prism-like vaterite. The 1H NMR and UV analyses (Figure 10) further demonstrate that SC can validly interact with SDBS in solution. Therefore, the change of phase and morphology of CaCO3 with the increasing of SC concentration may be attributed to the interactions of SC and SDBS (Figures 8 and 9). It has been reported that surfactants SDBS or SDS may bind into proteins or polymer molecules either as individual monomers or as the aggregates depending on the nature of the interaction and the surfactant concentration.50,82

Figure 10. 1H NMR spectra (a) and UV spectra (b) of the SDBS and the mixture of SDBS and SC.

prism has the same crystallographic symmetry as single-crystal vaterite. The EDX, FT-IR, and TG-DTA analyses (Figures 1a, 2b, and 4) suggest that the organics (∼1.87 wt %) are included in the prismatic vaterite. The BET measurements (Figure 5) further suggest that the vaterite is highly porous and has a large surface area. Therefore, the current experiments demonstrate that the hexagonal prism-like vaterite mesocrystals are formed by the oriented aggregation of vaterite flakes along its c direction. Nevertheless, it is well established that vaterite usually does not expose the highly polar {0001} faces as these would be composed of only carbonate or calcium ions in a hexagonal orientation, which would in the absence of specific organic/inorganic additives result in a too high surface energy.29,72 Moreover, the (001) face of vaterite can also be stabilized by the weakly adsorbed ammonium ions.72,73 Therefore, the fact that this face now becomes dominant in our experiment can be attributed to a sticking of the negatively charged carboxyl and/or sulfonic acid groups in the organic additives or the positively charged ammonia to the positively/ negatively charged {0001} planes, leading to a lowering of surface energy and inhibition of growth in this direction. Furthermore, in the presence of organic additives, it has been reputed that the subunit aggregation can be driven through the binding affinities between organic ligands with inorganic 1722


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sulfonic groups, which are closely associated with biomineralization of CaCO3. Therefore, this study on vaterite mesocrystals will be helpful for us to mimic and learn from nature and may bring new insights into the biomineralization.

In aqueous solution, the critical micelle concentration (CMC) of SDBS is measured to be about 1.6 × 10−3 mol/L.83 So SDBS occurs mainly as the aggregates rather than as the individual monomers in our experiments. Meanwhile, the aggregation states of SDBS would be influenced with the increase of the SC concentration. This may influence not only the polymorph section but also the size and morphology of CaCO3 (Figures 8 and 9). Therefore, the cooperative interactions between SDBS and SC play a vital role in the formation of the hexagonal prismatic vaterite mesocrystals. Noteworthy, the prism-like vaterite obtained here show a remarkable resemblance to the growth morphology of a vaterite nacreous layer in freshwater cultured pearls from mussels.18,19 The nacreous tablets in vaterite in freshwater cultured pearls have preferred orientation with the c-axis direction perpendicular to the tablet surface.19 The analogous structure has also been observed in the bivalve Corbicula f luminea.26,27 Frenzel and Harper characterized the microstructure of vateritic deformities occurring in the bivalve C. f luminea and found that columnar vaterite and lamellar vaterite are the most commonly observed microstructures in all parts of the shell.26 Further investigations of the columnar structure indicated that the vaterite crystallites within this structure have a common caxis orientation, and individual vaterite columns behaved as single crystals, but was internally composed of smaller irregularly shaped and slightly misaligned crystalline units.27 In particular, organic molecules were present largely as intracrystalline impurities or nanoscale phases in biological vaterite.19,26,27 This implies that the biomineralization of vaterite could be related to the organics. To date, it has been well established that the morphology and orientation of CaCO3 crystals in biominerals are directed by organic molecules, such as proteins, polysaccharides, and glycoproteins.1,8,23,31,84 Moreover, these proteins, polysaccharides, and glycoproteins are mainly hydroxylated, carboxylated, phosphated or sulfated or contain a mixture of these functional moieties, which may bind Ca2+ and could control crystal nucleation and growth by lowering the interfacial energy between the crystal and the macromolecular substrate.1,8,30,85 For example, Addadi et al. showed that a purified acidic glycoprotein from mollusk shells containing sulfate and carboxylate ligands can induce oriented calcite crystal growth.30 Aizenberg et al. found that macromolecules extracted from the ACC parts of sponges (Clathrina) and ascidians (Pyura pachydermatina) are glycoproteins rich in glutamic acid and hydroxyamino acids (which are potentially phosphorylated), while proteins extracted from the adjacent calcite phase are rich in aspartic acid.84,86 The polycarboxylated or sulfated polysaccharides have also been found in the calcium carbonate mineralized covering of coccoliths and can guide the development of the mineral phase.1,85,87 In particular, the water-soluble matrix (WSM) extracted from fresh water carp asteriscus (vaterite biomineral) can induce the formation of pielike vaterite in vitro by a biomimetic approach.23 Amino-acid analysis on asteriscus WSM shows that organic matrices have a large content of acidic amino acids, such as glycine, glutamic acid, and aspartic acid, indicating that the acidic amino acids have a great effect on vaterite crystal formation and stability.23 Beside, organic macromolecules rich in S and P have been detected between the vaterite platelets in freshwater cultured pearls, implying a stabilizing role of organic macromolecules with sulfate and/or sulfonic groups, phosphate for biological vaterite.19 Here, the organic additives used in our mineralization system are SC and SDBS contained carboxylate and

5. CONCLUSIONS In summary, vaterite mesocrystals in biomineral-like structures have been successfully harvested by a biomimetic process in solution with biomineralization-associated model organic additives. Our results show that organics with carboxyl and sulfonic groups play a vital role in the formation of biominerallike vaterite mesocrystals. The cooperative interactions between SDBS and SC lead to the formation of prism-like vaterite mesocrystals with the [001] preferential orientation. Since the architectures of the vaterite mesocrystals show remarkable analogy to the nacreous layers of vaterite in freshwater cultured pearls and the columns/lamellae of vaterite in bivalve, our study of this biomimetic mineralization may prove useful for a deeper understanding of biogenic mesocrystals. In addition, the produced hexagonal prism-like vaterite mesocrystals in the presence of SC and SDBS in this work would mimic the natural behavior of constructing three-dimensional (3D) nanostructures with controlled morphologies and may provide a new strategy for designing advanced materials with potentially novel and exciting properties.

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AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. Tel.: 86 551 63600533. Fax: 86 551 63600533. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work was partially supported by the Chinese Ministry of Science and Technology (No. 2011CB808800), the Natural Science Foundation of China (No. 41272054), and the Specialized Research Fund for the Doctoral Program of Higher Education (No. 20133402130007).

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REFERENCES

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Formation of Vaterite Mesocrystals in Biomineral ... - ACS Publications

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