Calcium Carbonate Crystallization in the Presence of Casein

Article pubs.acs.org/crystal

Calcium Carbonate Crystallization in the Presence of Casein Yan Liu, YongJian Cui, HuiYuan Mao, and Rong Guo* College of Chemistry and Chemical Engineering, Yangzhou University, Yangzhou 225002, P. R. China S Supporting Information *

ABSTRACT: Phosphoproteins have specific and prominent influences on mediating the crystallization of calcium carbonate. In this research, a new kind of calcium carbonate crystal with a novel self-organized spiky dumbbell-like superstructure was synthesized in the presence of one typical phosphoprotein-casein. A complex self-assembly process for the formation of the hierarchical superstructures in the presence of casein has been proposed. The effects of the concentration of calcium ion, the reaction time, and temperature are investigated. The results indicate that phosphate groups of casein play important roles in directing growth and self-assembly of hierarchical superstructures. Our studies may contribute to the understanding of the specific role of phosphoprotein in the biomineralization process. We also believe that our studies will provide new insights into controlling the structure and morphology of minerals under easily attainable reaction conditions in the presence of phosphoprotein.

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INTRODUCTION Highly complicated structures of biominerals that exhibit fascinating morphologies with outstanding mechanical properties are ubiquitous in biological systems.1−4 A key principle in the nature biomineralization is the involvement of biological macromolecules such as proteins, lecithin, and carbohydrate that have high binding affinity to the surface of crystallites, which leads to control and directing of the crystallization of minerals.5−10 Understanding the specific role of biological macromolecules in controlling and regulating the crystallization of minerals is of much importance in many fields of research. CaCO3 has been widely studied as an attractive model mineral because it is one of the most abundant biominerals produced by organisms.11−14 CaCO3 has three anhydrous crystalline phases (calcite, aragonite, and vaterite) and two hydrated phases (mono- and hexahydrate). Calcite and aragonite are by far the most common and stable forms, whereas vaterite, a less stable polymorph from the viewpoint of thermodynamics, also plays key roles in biological life and health. To investigate the mechanism of the biomineralization process, proteins have been used to induce the nucleation and growth of CaCO3 crystals in vitro.15−19 For instance, proteins isolated from abalone nacre can affect the shape of the calcite growth step and roughen a calcite surface.20 Wang et al. found that the mixing of Na2CO3 with CaCl2 in an aqueous solution led to the formation of stable spherical vaterites in the presence of ovalbumin.21 The stabilizing effect of ovalbumin could arise from the strong binding between carboxylate groups of ovalbumin and the calcium ions on the CaCO3 surface. Cheng et al. reported that CaCO3 with a hollow structure and rice-like shape can be obtained in the presence of silk fibroin.22 It has been demonstrated that protein molecules not only act as templates for inducing nucleation of crystals and modulating their orientation but also direct the assembly of nanoscale © 2012 American Chemical Society

particles to form hierarchical superstructures. All of these studies indicate that the mineralization process controlled by proteins depends much on the protein properties (electrical charge density, conformation, phosphorylation, and hydrophobicity). However, the information concerning the mineralization mechanism controlled by proteins with different structures has remained limited. Thus, the further understanding of the role of proteins with different structures involved in the CaCO3 formation will lead to a better understanding of the complex biomineralization process. It has been found that phosphonates adsorb to ionic crystals much more strongly than other additives. They preferentially interact with kinks on the crystal nucleus surface and thus efficiently inhibit crystal growth.9,31 Compared with proteins containing no phosphonate groups, phosphoproteins might have specific and prominent influences on mediating the mineralization process of biominerals. It has been demonstrated that phosphorylated proteins are associated with stable crustacean ACC.23 Recently, Bentov et al. found that phosphoamino acid moieties in phosphoproteins play a major role in the control of spherical ACC formation and stabilization.24 Most recently, we have reported the formation of ACC with hierarchical superstructures in the presence of amphiphilic phosphoprotein-casein at low temperature.25 Casein can be assumed to take a key role during ACC superstructure formation where it serves as an effective stabilization agent for ACC and assembles spherical ACC particles into ACC superstructures. This re-emphasizes once again the specific role of phosphoprotein in biomineralization.25 However, there are limited systematical experiments that Received: September 13, 2011 Revised: August 22, 2012 Published: August 27, 2012 4720

dx.doi.org/10.1021/cg3005213 | Cryst. Growth Des. 2012, 12, 4720−4726

Crystal Growth & Design

Article

Figure 1. SEM images (a,b) and TEM image (c) of CaCO3 obtained in the presence of 2.0 g L−1 casein at 25 ± 1 °C, [CaCl2] = 20 mM; HRTEM images (d−f) and SAED pattern (inset) obtained from the area marked with real line circle (d,f) and dashed circle (e) in panel c. White circular regions in panel f are amorphous parts. purchased from Sigma. Analytical grade sodium carbonate and calcium chloride were purchased from Shanghai Chemical Reagent Co. and used as received without further purification. Distilled water was used as the solvent. Experimental Procedures. In a typical procedure, 1 mL of 1 M CaCl2 aqueous solution was added to 49 mL of 2.0 g/L soluble casein aqueous solution. After stirring for 30 min, 50 mL of sodium carbonate solution (20 mM) was added into the above solution. After stirring for 3 h, the obtained precipitate was centrifuged and rinsed several times with ethanol and distilled water and dried at room temperature for at least 48 h. Characterization. X-ray powder diffraction (XRD) patterns were recorded using a Bruker D8 Advanced XRD diffractometer with Cu Kα radiation at a scanning rate of 0.04 deg·s−1. Scanning electron microscope (SEM) images were taken with a JEOL JSM-6700FXIB, fitted with a field emission source, and working at 20 kV. All samples were mounted on copper stubs and sputter-coated with gold prior to examination. Infrared spectroscopic analysis was performed in transmission mode (FT-IR) using a Nicolet Aexus 470, with scanning from 4000 to 500 cm−1 by using KBr pellets. Transmission electron microscopy (TEM) images were obtained on a 150 kV H-800 microscope. High-resolution transmission electron microscopy (HRTEM) and selected-area electron diffraction (SAED) images were recorded by using a JEM-2010 UHR high-resolution transmission electron microscope (Japan Electron Co.).

reproduce CaCO3 with complex structures and morphologies in the presence of phosphoprotein.23,26−28 In addition to a high content of acidic amino acid residues,29,30 casein proteins have several phosphoserine residues. Thus, casein has the ability to bind calcium ions via phosphate groups of phosphoserine residues in addition to acidic amino acid residues,32,33 which will influence the crystallization process of CaCO3 uniquely. In the present work, we continue to investigate the influence of the phosphoprotein-casein on the crystallization of CaCO3 systematically. Mineralization of CaCO3 with novel hierarchical spiky dumbbell-like structures has been obtained in the presence of casein. The influences of reaction time, temperature, and reagent concentration on the mediation of the phase transformation and morphology change of CaCO3 crystals in the presence of casein have been investigated systematically. Our studies will contribute to understand the biomineralization, with the benefits of not only uncovering the mechanism adopted by proteins but also applying them to the synthesis of materials with exquisite morphology and specific textures.

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EXPERIMENTAL SECTION

Materials. Casein (isoelectric point (pI) = 4.5 and average molecular weight (MW) = 2.1 kDa) and dephosphorylated casein were 4721



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Figure 2. XRD pattern (a), FT-IR spectra (b), and thermogravimetric trace (c) of CaCO3 obtained in the presence of 2.0 g L−1 casein at 25 ± 1 °C; [CaCl2] = 20 mM. C, calcite phase (JCPDS card: 05-0586); V, vaterite phase (JCPDS card: 33-0268).

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RESULTS AND DISCUSSION When casein was used as an additive, the crystallization of CaCO3 results in crystals that exhibit an unusual morphology, that is, a spiky dumbbell-shaped particle around 5.5 μm in length and 3.5 μm in width is found (Figure 1a). These spearlike branches grew radially from the dumbbell-shaped core with diameters of 0.3−1.0 μm at the root and lengths of 0.5−4.0 μm from the root to the tip. The magnified SEM image (Figure 1b) reveals that the surface of the dumbbell-shaped body is rather rough. More detailed information about the spiky dumbbell-like superstructure can be further provided by TEM, HRTEM, and SAED analyses. Figure 1c shows the TEM image of the final product. It reveals the product with spiky dumbbell shapes, which is the same as the SEM results. Figure 1d−f shows the typical HRTEM image and SAED patterns taken from the area shown in Figure 1c. According to the typical HRTEM image from the edge of the spike, the value of the lattice spacing of 0.23 nm measured in the HRTEM image (Figure 1d) is consistent with that of (113) interplane spacing of calcite (JCPDS card No. 05−0586). There also exist amorphous phases in the spike as shown in the area enclosed in white circles in Figure 1f. The SAED pattern (Figure 1d, inset) of a single spike shows the polycrystalline nature. The values of the d spacing are ca. 0.30, 0.23, and 0.19 nm, corresponding to the (104), (113), and (116) planes of the calcite crystal, and ca. 0.33 and 0.18 nm, corresponding to the (112) and (118) planes of the vaterite crystal. These results are in good agreement with the following XRD results. The typical SAED pattern from the edge of the dumbbell body shows diffraction rings typical of calcite and vaterite crystals of random orientation (Figure 1e, inset), which indicates the overall polycrystalline characteristics of the calcite and vaterite. The value of the lattice spacing of 0.23 nm measured in the HRTEM image (Figure 1e) is also consistent with that for the (113) interplane spacing of calcite. Accordingly, both the spike and the dumbbell body are polycrystalline characteristics of the calcite and vaterite. Figure 2a shows the XRD pattern of CaCO3 precipitates, revealing reflection peaks for calcite and vaterite crystals. The phase of the product was also confirmed by the FTIR spectrum (Figure 2b). The presence of peaks at 875 and 712 cm−1 can be assigned as the characteristic peaks for calcite, and the characteristic peak at 745 cm−1 can be indexed as the characteristic peak for vaterite.34−36 FTIR results also confirm that the CaCO3 sample can be indexed as a mixture of calcite and vaterite, which is consistent with the XRD result. The

particle morphology (including size and shape) remains almost unchanged during the ripening (Figure S1a, Supporting Information). Also, according to the FT-IR analysis (Figure S1b, Supporting Information), the fraction of vaterite stabilized by casein remains almost unchanged during the ripen process, and there is no evident indication of vaterite to calcite transformation. The occurrence of polymorphs of the crystalline and different phases of calcium carbonate could be due to the energy barrier to nucleation for these phases, which is an expression of Ostwald’s step rule.38,39 Vaterite is a metastable phase that usually transforms to the thermodynamically most stable calcite phase. Some organic additives, such as glutamic acid,14 aspartic acid,15 ovalbumin,21 and PAMAM dendrimers13 can retard or prohibit such phase transformation. Similarly, casein can protect the crystal surface of the vaterite phase by interfacial adsorption and stabilize the unstable phase. It can be seen from Figure 2b the infrared data display clearly the CONH band at 1654 cm−1, confirming that casein molecules remain attached in the separated samples. The thermogravimetraic analysis (TGA) results further support the existence of casein in the resulting CaCO3 precipitates. CaCO3 precipitates mineralized in the presence of casein show the weight loss of 9.1 wt % at around 250−500 °C due to the decomposition of protein (Figure 2c). Notably, the weight loss of ca. 4.6% at the first stage is due to water and alcohol dissipation.21 The results indicate that the presence of casein has a stabilizing effect on the unstable vaterite phase, blocking its transition to the calcite phase. CaCO3 that mineralized without casein results in the formation of large rhombohedral calcite crystals with an average size over 25 μm (Figure S2, Supporting Information), revealing casein has a significant influence on the crystalline CaCO3. Casein's isoelectric point is 4.6, and at pH values greater than this, it is negatively charged. Notably, casein has several phosphoserine residues in addition to a high content of acidic amino acid residues (such as glutamic acid and aspartic acid residues). Thus, casein has the ability to bind calcium ions via both phosphate groups of phosphoserine and carboxylate groups of acidic amino acid residues. This will influence the crystallization process of CaCO3 in the presence of casein. To determine which interaction (the interaction between calcium ions and phosphate groups or carboxylate groups) plays a crucial role in the stabilization of vaterite, a controlled experiment using the dephosphorylated casein as an additive was performed. The CaCO3 products are mainly elliptical-like aggregates around 3.0 μm in length and 1.8 μm in width with clearly calcite crystal faces (Figure 3a). Obviously, the vaterite 4722



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Figure 3. SEM images of CaCO3 samples obtained in the presence of 2.0 g L−1 dephosphorylated casein (a) and casein (b) at 25 ± 1 °C. (a) [CaCl2] = [Na2CO3] = 20 mM; (b) [CaCl2] = 20 mM, [Na2CO3] = 40 mM.

phase induced by the casein molecules disappears once the protein is dephosphorylated. The results, hence, confirm that the stabilization of vaterite could only be achieved by the strong binding of phosphate groups of casein to the calcium ions on the CaCO3 surface. Notably, casein has a large number of carboxyl groups (17% Asp and 23% Glu of all residues in casein) and a low content of phosphate groups (2.5%). However, compared with the acidic amino acid residues, phosphate groups in casein play a more crucial role in the formation and stabilization of vaterite. This confirms that the electrostatic attraction between phosphate groups and Ca2+ is stronger than that between the carboxylate group and Ca2+.9,31,37 In addition, the presence of excess CO32− in the solution has a significant effect on the crystallization process of CaCO3. For example, when the molar ratio CO32−/Ca2+ is increased from 1:1 to 2:1, elliptical-like aggregates consisting of rhombohedra are observed (Figure 3b). FT-IR and XRD results show that the CaCO3 sample prepared is pure calcite (data not shown). Here, an excess of CO32− induces a net negative surface charge of the growing nanoparticles, such that electrostatic interactions with the phosphate group of casein are significantly reduced and that the calcite crystals are obtained. To further demonstrate the details of the growing process, we conducted the effects of ion concentration and temperature on the crystallization of CaCO3 in the presence of casein. The variation of Ca2+ concentration can effectively modulate the morphologies and phase modifications of CaCO3. When the calcium ion concentration is decreased to 5 mM, spherical particles of 0.7−1.5 μm in diameter connected with each other are observed (Figure 4a). XRD results indicate that the obtained particles consist mainly of vaterite with only a small fraction of calcite (curve a in Figure 5). When the concentration of Ca2+ is up to 60 mM, the as-prepared CaCO3 sample is composed of spherical particles (Figure 4b). XRD results show that the polymorph of CaCO3 product is

Figure 5. XRD patterns of CaCO3 samples obtained in the presence of 2.0 g L−1 casein at different ion concentrations. [CaCl2] = 5 mM (a) and 60 mM (b).

pure calcite (curve b in Figure 5). Here, at low Ca2+ ion concentration, the decrease of the supersaturation makes the crystallization controlled by the protein more efficient, resulting in the formation of spherical vaterite. At high Ca2+ ion concentration, the higher supersaturation of CaCO3 at the onset of precipitation leads to a faster nucleation as well as growth rate and a less controlled crystallization process, which allows the formation of spherical calcite particles. Generally, temperature is believed to have a great impact on the crystal forms of the final products. We have carried out analogous experiments at different temperatures. Figure 6a

Figure 6. SEM images of CaCO3 samples obtained in the presence of 2.0 g L−1 casein at different reaction temperatures: (a) 10 ± 1 °C and (b) 50 ± 1 °C. [CaCl2] = 20 mM.

shows that the dumbbell-like microparticles are produced at 10 ± 1 °C. The average length and width of the dumbbell-like microparticle is about 1.3 and 0.8 μm, respectively. An enlarged micrograph indicates that the resulting dumbbell-like assembly is built up of numerous small nanoparticles with the particle size of 15−25 nm (inset in Figure 6a). The CaCO3 sample prepared at 10 ± 1 °C in the presence of casein is almost vaterite as indexed in the FTIR results shown in Figure S3, Supporting Information. Even though the dumbbell-like crystalline particles have been formed in many earlier studies,40−44 the dumbbell-like vaterite composed of primary nanoparticles in protein aqueous solution has been rarely observed. With the reaction temperature increasing to 50 ± 1 °C, spherical particles with broad size distribution are obtained (Figure 6b). An enlarged micrograph (inset in Figure 6b) suggests that the particles also exhibit a rough outer surface. The CaCO3 sample obtained at 50 ± 1 °C can be indexed as calcite mainly (Figure S3, Supporting Information). However, the CaCO3 samples formed without any additives at different

Figure 4. SEM images of CaCO3 samples obtained in the presence of 2.0 g L−1 casein at different ion concentrations. [CaCl2] = 5 mM (a) and 60 mM (b). 4723



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Figure 7. TEM and SEM images of CaCO3 samples produced in the presence of 2.0 g L−1 casein at the early reaction stages. The reaction time is (a) 0, (b) 5, (c) 10, (d,e) 20, and (f) 30 min.

and 1.0 μm. The particulate primary building blocks can be discerned from the image (Figure 7b). After 10 min of reaction, short branches emanating from the dumbbell-like particle are produced (Figure 7c). When the reaction time is prolonged to 20 min, more superstructures with spear like branches appear (Figure 7d). The surface of the dumbbell-like particle becomes smoother compared with the sample shown in Figure 7b. The average length and width of the dumbbell-like particle increases to 5.3 and 2.8 μm, respectively. From the magnified SEM image shown in Figure 7e, the branch is built up of numerous small nanoparticles with the particle size of about 15 nm. The length and the diameter of the branches both increase with time. Thirty minutes later, the formed superstructure (Figure 7f) resembles in shape and size the spiky dumbbell-like particles in the final product shown in Figure 1a, that is, the particles do not further grow in the remaining time of the reaction. This means that the aggregation of the primary particles into the final hierarchical superstructure is relatively fast. However, as TEM and SEM investigations potentially suffer from drying artifacts, we performed time-dependent DLS on a crystallizing solution to study the growth of the crystallites in solution. According to DLS measurements (Figure S4a, Supporting Information), a 2 g/L casein solution contains casein submicelles and casein micelles with hydrodynamic radii of ∼18 and ∼200 nm, respectively. The addition of calcium ions to the colorless casein solution induces a bluish color in the mixture immediately. DLS results show that the addition of calcium ions make the two size distribution peaks shift to 75

reaction temperatures all display rhombohedral calcite morphology (data not shown). It is well-known that vaterite transforms readily and irreversibly into the stable calcite form through a solvent-mediated process.45,46 The recrystallization rate of smaller building blocks obviously slows down and keeps for a longer period at a metastable state at a lower reaction temperature. Thus, vaterite becomes a dominant phase at low temperature. When the reaction temperature increases, the rate of recrystallization process can be accelerated. This contributes to the dissolution of the metastable CaCO3 crystals formed at an early reaction stage, which is helpful for the formation of calcite. Furthermore, too fast of a reaction rate at high temperature is disadvantageous for the oriented aggregation of these building units, which leads to irregular or spherical particles. To obtain more evidence for the formation of spiky dumbbell-like particles, the phase and morphological development of CaCO3 at different crystallization times was examined. The representative TEM and SEM images of the products obtained at the early stages of the superstructure formation are presented in Figure 7. At the beginning of the process (sample taken immediately after initiating the mineralization process, t = 0), it seems that the first species to form are amorphous calcium carbonate particles. This is in good agreement with the generally accepted process of calcium carbonate crystallization in the presence of additives.23,24 After 5 min of reaction, the products are spherical particles with size of 1.2 μm and dumbbell-like particles with an average length and width of 2.2 4724



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and 330 nm (Figure S4b, Supporting Information), which is caused by the binding of calcium ions to caseins.47,48 Upon the addition of NaCO3 (Figure S4c, Supporting Information), the onset of nanoparticle formation (RH = 30 nm; because the aggregation of particles is fast, this is the first data point acquired by DLS) is followed by the fast aggregation with time (Figure S4d, Supporting Information). Compared with the distribution peaks shown in Figure S4a,b, Supporting Information, it can be seen that the distribution peaks corresponding to casein aggregates disappear, which indicates that the structure of casein micelles is destroyed by the formation of CaCO3 nanopaticles. The primary nanoparticles vanish after about 20 min, and only larger aggregates are found (Figure S4e, Supporting Information), indicating the unstable character of the small particles and their aggregation into larger particles. Maybe the bigger particles in sediment are lost from solution detection. Figure 8 shows the typical IR spectra of CaCO3 with the reaction time. It seems that the first species to form are

Figure 9. Scheme of the formation process of spiky dumbbell-shaped superstructure obtained in the presence of 2.0 g L−1 casein at 25 ± 1 °C.

large number of these nanocrystals due to the reduced nanocrystals and the lower aggregation velocity (Figure 9c). At this stage, the attachment of the nanocrystals would preferentially occur at the relatively more active sites of the dumbbell-like particles at proper reaction conditions (such as proper reaction temperature and ion concentration). This selective attachment process of nanocrystals continues, and the spear-like branches are formed and grow longer until all the nanocrystals are consumed (Figure 9d). Meanwhile, the body of dumbbell-like particles still undergoes the Ostwald ripening process at the cost of the smaller nanoparticles, and the size of the as-obtained dumbbell-like particle increases with the reaction time. The aggregation is energetically favored because the formation of larger crystals can greatly reduce the interfacial energy of small primary nanoparticles. Generally, van der Waals force is believed to drive the aggregate growth of nanostructures in biomimetic mineralization. Here, in addition to van der Waals force, the hydrophobic interaction between casein molecules may be one of the main driving forces for the nanoparticle aggregation because of the amphiphilic caseincapped on CaCO3 surface. The structures and the crystalline evolution process of the superstructures suggest that the formation mechanism is a typical nonclassical pathway of crystallization, including the self-assembly and the transformation of amorphous precursors. The mode of self-assembly of nanoscale building blocks under control of casein agrees well with the growth model proposed by Colfen et al.49

Figure 8. FTIR spectra of CaCO3 samples at the early reaction stages. The reaction time is (a) 0, (b) 5, and (c) 30 min.

amorphous calcium carbonate particles. Immediately, ACC transforms into vaterite and calcite. The phase fraction of calcite to vaterite then increases, and finally remains almost unchanged with the reaction time. Just as discussed above, casein has the ability to bind calcium ions via both phosphate groups of phosphoserine, and carboxylate groups of acidic amino acid residues. The strong adsorbed casein can protect the crystal surface of the vaterite phase by interfacial adsorption and stabilize the unstable phase. Furthermore, compared with CaCO3 formed in the presence of dephosphorylated casein, the crystallization of CaCO3 regulated by casein depends much on the electrostatic attraction between phosphate groups and calcium ions. In addition to the role of the stabilization of the vaterite phase, the presence of casein is undoubtedly vital in the formation of spiky dumbbell-like superstructure. On the basis of the above experimental observation, the stepwise formation process could be described as follows. Initially, the amorphous CaCO3 particle is formed in the presence of casein (Figure 9a). Immediately, some amorphous nanoparticles are transformed into CaCO3 nanocrystals. Almost simultaneously, the amorphous nanoparticles and early formed nanocrystals aggregate into the dumbbell-like particles very quickly (Figure 9b). After this stage, the subsequent nanocrystals may gradually attach to the dumbbell-like particle instead of the sharp aggregation of a

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CONCLUSIONS The protein template for the mineralization of CaCO3 usually contains acidic amino acid residues such as aspartic acid and glutamic acid residues. Interestingly, this work found that protein with both phosphate groups and acidic amino acid residues can control the mineralization of CaCO3 more specially. The novel morphology, dumbbell-like particles with spear-like branches, has been formed in casein aqueous solution, which is determined to be a vaterite and calcite mixture. The interaction between phosphate groups of casein and calcium ions plays a critical role in organizing calcium carbonate on the microscopic level. In addition, the adsorption of casein molecules onto a certain crystal face leads to the generation of the least stable vaterite. Calcium carbonate complex architectures with different morphologies, including dumbbell-like, spherical-like, and elliptical-like aggregates, were 4725



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constructed under the influence of casein by tuning the experimental conditions such as temperature, concentration of Ca2+, etc.

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ASSOCIATED CONTENT

S Supporting Information *

Additional information as noted in the text. This material is available free of charge via the Internet at http://pubs.acs.org.

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AUTHOR INFORMATION

Corresponding Author

*Tel: +86-514-87971802. Fax: +86-514-87311374. E-mail: [email protected]. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work was supported by the National Nature Science Foundations of China (20803061 and 21073156) and PAPD. REFERENCES

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Calcium Carbonate Crystallization in the Presence of Casein

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