Biomimetic Precipitation of Nanostructured Colloidal Calcite Particles

Dec 20, 2007 - using scanning and transmission electron microscopy and X-ray diffraction. ... The precipitation of calcite particles of different size...
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CRYSTAL GROWTH & DESIGN

Biomimetic Precipitation of Nanostructured Colloidal Calcite Particles by Enzyme-Catalyzed Reaction in the Presence of Magnesium Ions

2008 VOL. 8, NO. 2 435–441

Ivan Sondi,*,† Srecˇo D. Škapin,‡ and Branka Salopek-Sondi§ Center for Marine and EnVironmental Research, and Department of Molecular Biology, Ru{er BoškoVic´ Institute, Zagreb, Croatia, and Department for AdVanced Materials, Jožef Stefan Institute, Ljubljana ReceiVed February 27, 2007; ReVised Manuscript ReceiVed October 12, 2007

ABSTRACT: A novel, bioinspired precipitation process, effectuated through the decomposition of urea by catalytically active CanaValia ensiformis urease (urea amidohydrolase; EC 3.5.1.5), in a solution of calcium and magnesium salts was used to precipitate uniform submicron-size, nanostructured calcium carbonate particles. The structure and morphology of the precipitates were investigated using scanning and transmission electron microscopy and X-ray diffraction. Their surface properties were investigated by electrophoretic mobilities and specific surface area measurements. These precipitates were formed through initial generation of a nanometer-scale, amorphous, metastable precursor phase, which, on aging, transforms into nanosize crystalline calcite and aggregates into nearly spherical nanostructured calcite particles. The presence of magnesium ions in combination with urease macromolecules was found to affect the nucleation process and inhibited the growth of the initially formed nanoparticles in solution. This nonclassical formation of calcite colloids, described as the biomimetic nanoscale aggregation route, supports the recently reaffirmed mechanism according to which carbonate colloids are produced through aggregation of preformed nanosize particles. Introduction The precipitation of calcite particles of different sizes, morphologies, and surface properties has been intensively investigated due to their importance in geo- and biosciences and in numerous industrial applications. Most of the previously reported research deals with micron-size calcium carbonate polymorphs, while the precipitation of uniform nanosize carbonate particles of controlled shape has received less attention.1–4 At present, neither standardized preparation processes nor the mechanisms determining size and shape of nanosize calcite particles are known. Recently, a new approach based on bioinspired microstructural processes and techniques, which are initiated or stimulated by biological systems, have been employed in the preparation of calcium carbonate precipitates.5–12 These procedures involve functional templates, often proteins or peptides, which are implicated in controlling nucleation, growth, and morphology of the precipitates.13–16 Several studies have shown that interfacial physicochemical interactions between these macromolecules and the inorganic phase control nucleation and growth phenomena of carbonate solids.6,8,11,13,17 Following this concept, recent progress in studies on carbonate precipitation was accomplished through the use of catalytically active proteins such as urease enzymes (urea amidohydrolases; EC 3.5.1.5).18–22 These proteins are generated by many bacteria, certain species of yeast, and a number of plants, allowing them to use exogenous and internally generated urea as a nitrogen source.23 The chemical, structural, and surface properties and the mode of action of ureases have been described elsewhere.24,25 It was already reported that calcium carbonate polymorphs of different sizes and shapes can be obtained by * Corresponding author. Mailing address: Center for Marine and Environmental Research, Ru{er Boškovic´ Institute, Bijenicˇka cesta 54, 10000 Zagreb, Croatia. Phone +385-1-4680-124. Fax: +385-1-4680-242. E-mail: [email protected]. † Center for Marine and Environmental Research, Ru{er Boškovic´ Institute. § Department of Molecular Biology, Ru{er Boškovic´ Institute. ‡ Jožef Stefan Institute.

homogeneous precipitation in solutions of calcium salts through the enzyme-catalyzed decomposition of urea at room temperature.19 The role of urease in the formation of strontium and barium carbonates,20 and of their mixed compounds,21 was also investigated. Next to a catalytic function in the decomposition of urea, ureases also exert significant influence on the crystal phase formation and shaping of carbonate precipitates. A recent study by the present authors has exemplified the role of the primary protein structure (amino acid sequences) of ureases on the phase formation and morphological properties of the precipitates.22 During the homogeneous precipitation of anhydrous mixed Ca-Mg carbonates by an enzyme-catalyzed reaction, nanosize calcite particles appeared at an early stage of the precipitation process.21 Following up on this work, the new bioinspired strategies for the preparation of uniform, nanostructured, and submicron-size calcium carbonate particles, based on enzymatic activity of CanaValia ensiformis urease in aqueous solution containing urea, magnesium, and calcium salts, were investigated. This study contributes to the understanding of the biomimetic mechanism that leads to a new approach for the synthesis of nanostructured biomineralized precipitates. Specifically, it describes the complex biomimetic mechanism that involves the simultaneous inhibitory effect of magnesium ions on the crystal growth of initially formed nanocrystallites and their subsequent aggregation that, finally, govern the formation of submicronsize and nanostructured colloidal carbonates. Experimental Section Materials. Reagent-grade calcium and magnesium chloride and urea were obtained from the Aldrich Chemical Co. and used without further purification. Stock solutions of these reactants were freshly prepared and filtered through 0.22 µm Millipore membranes before use. Urease (Lot 21K7038, molecular weight 470 000 Da), purchased from Sigma Co., was fractionated from C. ensiformis (Jack Bean) meal extract and with activities of 45 U mg-1 of dry weight. Preparation and Characterization of the Precipitates. Experimental conditions, particularly concentrations of urease, were chosen

10.1021/cg070195n CCC: $40.75  2008 American Chemical Society Published on Web 12/20/2007

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Table 1. Composition of Solutions for the Precipitation of Calcium Carbonate Solids sample

[CaCl2] mol dm-3

[MgCl2] mol dm-3

[urea] mol dm-3

[urease] mg cm-3

1 2 3 4 5

0.25 0.25 0.25 0.25 0.25

0 0 0.1 0.25 0.25

0.5 0.5 0.5 0.5 0.5

0,5 1 1 1 1.5

according to previous studies that indicate the concentration range that should be used to obtain amorphous and nanosized solids.19,22 The reacting solutions containing calcium, magnesium chloride, and urea were kept in tightly stoppered Erlenmeyer flasks and saturated with nitrogen before a measured amount of urease solution was injected. The mixtures were then kept at room temperature, from 2 min to 1 h, with gentle stirring. The concentration of calcium chloride was 0.25 mol dm-3, and that of urea was 0.50 mol dm-3, while the concentrations of urease and magnesium chloride were varied from 0.5 to 1.5 mg cm-3 and from 0 to 0.25 mol dm-3, respectively (Table 1). All experiments were performed at 25 °C. The onset of precipitation was determined by the appearance of milky clouds (whiting) in the reacting solutions. The obtained precipitates were sequentially filtered and washed with deionized water to remove urease and the excess of calcium and magnesium salts. This procedure stops the formation of the new solid phase. The wet precipitates were analyzed immediately. The size and the morphology of the precipitates obtained were examined by scanning and transmission electron microscopy (SEM and TEM). The particle size of precipitates was obtained from SEM micrographs using the software Image Tool for Windows (version 2.0), while data were analyzed by means of the software Origin 7.0. Chemical composition was determined by energy dispersive X-ray analyses (EDX) using Noran Tracor (series II, Tracor Northern) software. The crystalline phases of carbonate precipitates were analyzed by X-ray powder diffraction (XRD) using a D4 Endeavor, Bruker AXS instrument, and identified according to the JCPDS powder diffraction files. The diffraction peaks on the XRD patterns were coded as follows: A-amorphous phase, C-calcite. The particle size of crystallites was determined by the XRD Debye–Scherrer equation and cross-referenced by TEM. Specific surface area measurements (SSA) of the freeze-dried powder of carbonate solids were made by the single-point nitrogen adsorption technique, using a Micromeritics FlowSorb II 2300 instrument. Electrokinetic measurements of carbonate particles as a function of pH were made in 10-3 mol dm-3 aqueous NaCl solution by using a Malvern Nanosizer instrument.

Results A modified, rapid homogeneous precipitation process, under the conditions summarized in Table 1, was used in the preparation of calcite particles from reacting solutions, containing urea, urease, magnesium, and calcium chloride. Precipitates were rapidly formed with the onset of precipitation in only 2 min. The pH of the reacting solutions changed from the initial 6.7 to 8.7 at the end of the precipitation process. Figure 1 shows that there was no significant change in the rate of calcium carbonate formation with time at the same concentration of urease. In addition, the yields of precipitated solid phases obtained under otherwise the same experimental conditions, in the absence (Table 1, sample 2) and in the presence (Table 1, sample 4) of magnesium ions, were almost the same. In contrast, with prolonged reaction times, the presence or absence of magnesium ions in the reacting solutions caused discernible differences in the size and shape of precipitates obtained. SEM micrographs, displayed in Figure 2, and particle size distribution histograms, shown in Figure 3, demonstrate the effect of time of aging on the formation, morphology, and the size of calcium carbonate precipitates obtained in reacting

Figure 1. Time-dependent changes of the weight and the yield of calcium carbonate solids precipitated in the presence (O) and in absence of magnesium ions (b) (Table 1, samples 2 and 4).

solutions containing 0.25 mol dm-3 of magnesium ions (Table 1, sample 4). Approximately 10 min after the reacting components were mixed, ultrafine, uniform, and nonaggregated particles, with modal diameters around 130 nm, were observed (Figures 2a and 3). The XRD pattern of this solid, taken in the wet state immediately after separation from the reacting solution, showed them to be nearly spherical and amorphous (Figure 4, spectrum a). After prolonged reaction times, under otherwise identical conditions, the particles changed profoundly. Thus, after 30 min of reaction time, the formation of nonaggregated and ultrafine calcite particles still proceeded (Figure 2b). However, an increase in the particle sizes from ∼130 to 300 nm was observed for precipitates obtained after 10 and 30 min (Figure 3). The latter precipitates still exhibited amorphous structures, while a small amount of crystalline calcite appeared (Figure 4, spectrum b). On continuous aging, after 60 min of reaction time, the size of particles taken from the reacting solutions increased to ∼ 500 nm, and they became partially aggregated (Figure 2c). The XRD data (Figure 4, spectrum c) of this solid exhibited a characteristic spectrum of well-defined calcite structures. Notably, the XRD peaks of the latter precipitate were significantly widened, indicating that the spherical submicron particles are built of nanosize crystallites. Applying the Debye-Scheerer equation, their size was estimated to be ∼10 nm. More detailed morphological and structural analyses of these spheroids, taken at a higher TEM magnification and accomplished by SAED data, additionally confirms that the spheroids are built of slightly textured nanosized calcite monocrystals (Figure 5). This observation is in agreement with XRD data. EDX revealed that this solid contained ∼2 mol % of Mg (Figure 6). On the basis of the relation between the interplanar spacing d (104) and the composition of the anhydrous Ca-Mg carbonates,26 it was estimated that these precipitates should be designated as a low magnesium calcite. In contrast, on aging in reacting solution without magnesium ions, but otherwise under the same experimental conditions (Table 1, sample 2), a discontinuity in the precipitation process appeared after 30 min of reaction time, when large calcite particles of undefined morphology (Figure 7b) with modal diameters of 3-4 µm (Figure 8) were precipitated. The precipitates obtained after 60 min of reaction time had the morphology of irregular spherical particles and twinned sequentialgrowth rhombohedra (Figure 7c), both with an approximate size of ∼30 µm. In comparison with the solids obtained from the reacting solution containing magnesium ions, the XRD patterns of the latter precipitates were not broadened,

Precipitation of Nanostructured Colloidal Calcite Particles

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Figure 3. Particle size distribution histograms of calcium carbonate precipitates evaluated from the corresponding SEM micrographs shown in Figure 2a,b. The solid lines are Gaussian fittings of the data.

Figure 2. Scanning electron micrographs of calcium carbonate particles obtained by aging a solution containing 0.5 mol dm-3 urea, 0.25 mol dm-3 CaCl2, 0.25 mol dm-3 MgCl2, and 1 mg cm-3 C. ensiformis urease at 25 °C for (a) 10 min, (b) 30 min, and (c) 60 min (Table 1, sample 4).

indicating the formation of only micron-size crystallites (Figure 9, spectrum c). The change in size and morphology of the precipitates was also followed by a rapid change in their surface properties. Figure 10 displays the change in SSA of solids obtained, after various reaction times, in reaction mixtures with and without magnesium ions. As expected, these results follow the SEM observations and granulometric characteristics of the respective precipitates. The SSA values for precipitates obtained after 10

Figure 4. XRD patterns of calcium carbonate precipitates obtained by aging a solution containing 0.5 mol dm-3 urea, 0.25 mol dm-3 CaCl2, 0.25 mol dm-3 MgCl2, and 1 mg cm-3 C. ensiformis urease at 25 °C for (a) 10 min, (b) 30 min, and (c) 60 min (corresponding SEM micrographs are shown in Figure 2a-c).

min of reaction time were 46 and 42 m2g-1, respectively. There is significant evidence of a decrease in the SSA from 46 to 14 m2 g-1 for precipitates obtained from reacting solutions containing magnesium ions and from 42 to almost 1 m2 g-1 for those without magnesium ions. Electrophoretic mobility measurements of the calcite precipitated from solution containing magnesium ions, after 60 min of reaction (Table 1, sample 4), showed the

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Figure 5. Transmision electron micrograph of spherical calcium carbonate particles obtained by aging a solution containing 0.5 mol dm-3 urea, 0.25 mol dm-3 CaCl2, 0.25 mol dm-3 MgCl2, and 1 mg cm-3 C. ensiformis urease at 25 °C for 60 min (corresponding SEM micrographs are shown in Figure 2c). The inset displays selected area electron diffraction (SAED) data.

Figure 6. EDX spectrum of calcium carbonate particles obtained by aging a solution containing 0.5 mol dm-3 urea, 0.25 mol dm-3 CaCl2, 0.25 mol dm-3 MgCl2, and 1 mg cm-3 C. ensiformis urease at 25 °C for 60 min (corresponding SEM and TEM micrographs are shown in Figures 2c and 5).

particles to be negatively charged over the whole investigated pH range from 6 to 10.5 (Figure 11). Discussion This study is based on previous research on the role of catalytically active ureases in preparation of carbonate particles of various structures and morphological properties.19–22 Its results, in comparison with previous studies, demonstrate that the precipitation of uniform, colloidal, and nearly spherical calcite particles, built of nanosize subunits, can be achieved by biomimetically tailored precipitation processes, in solutions containing a combination of calcium and magnesium salts, effectuated by decomposition of urea by C. ensiformis urease. However, the conditions under which such solids could be obtained were rather restrictive in terms of the concentration of urease, reaction time, and the presence of magnesium ions.

Figure 7. Scanning electron micrographs of calcium carbonate particles obtained by aging a solution containing 0.5 mol dm-3 urea, 0.25 mol dm-3 CaCl2, and 1 mg cm-3 C. ensiformis urease at 25 °C for (a) 10 min, (b) 30 min, and (c) 60 min (Table 1, sample 2).

There are two major processes that should be addressed to understand the mechanisms of formation of these precipitates. The first refers to the rapid formation of the nanosize amorphous precursor phase, and the second refers to simultaneous crystallization via a solid-state transformation pathway and nanoscale aggregation processes. What ensues is the formation of hierarchical, sub-micrometer-size, spherical structures. This complex, nonclassical course in formation of colloidal carbonates could be defined as biomimetic nanoscale aggrega-

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Figure 10. Change in specific surface area (SSA) of calcium carbonate solids obtained for various reaction times: (9) sample 4, Table 1; (0) sample 2, Table 1.

Figure 8. Particle size distribution histograms of calcium carbonate precipitates evaluated from the corresponding SEM micrographs shown in Figure 7a-c. The solid lines are Gaussian fittings of the data.

Figure 11. Electrophoretic mobility and ζ-potential of calcium carbonate particles obtained by aging a solution containing 0.5 mol dm-3 urea, 0.25 mol dm-3 CaCl2, 0.25 mol dm-3 MgCl2, and 1 mg cm-3 C. ensiformis urease at 25 °C for 60 min in 1 × 10-3 mol dm-3 NaCl solution as a function of pH.

Figure 9. XRD patterns of calcium carbonate precipitates obtained by aging a solution containing 0.5 mol dm-3 urea, 0.25 mol dm-3 CaCl2, and 1 mg cm-3 C. ensiformis urease at 25 °C for (a) 10 min, (b) 30 min, and (c) 60 min (corresponding SEM micrographs are shown in Figure 7a-c).

tion route, the one that in many instances explains the formation of complex biomineralized structures and their advantageous properties. The obvious question is: How does the presence of urease macromolecules and of magnesium ions in reacting solutions govern these processes and formation of precipitates? Protein macromolecules, in many cases, initiate solid phase formation, and furthermore, control the crystalline nature and morphology of inorganic precipitates.8,11,27–29 In reacting solutions, these phenomena are the consequence of physicochemical interactions between active functional groups of organic macromolecules at their surface and the “building components” (ions, complexes) of the nascent solids. The carboxyl-rich character of a protein resulting from the high abundance of negatively charged aspartic (Asp) and glutamic (Glu) acid residues, present at the surface of the molecules, is the most important factor in their biomineralization reactivity. Numerous studies14,30–33 have proved that amino acids act as primary active

sites in solution and at the interface of organic/inorganic biomineralizing structures. These provide preferential sites for nucleation by changing the interfacial energies, and by altering the growth rates of nascent solids. The distribution of Asp and Glu on the surface of C. ensiformis urease, used in this study, is shown in the CPH model displayed in Figure 12. Its amino acid sequence contains 12.8% Asp and Glu residues. The initial formation of the nanosize, amorphous, and metastable precursor phase may be the result of a strong interaction between Ca2+ and Asp and Glu at the urease surface, forming Ca2+/Asp and Ca2+/Glu multicarboxyl chelate complexes that act as organic templates and induce initial formation of the nanosize and amorphous precursor phase.34 This is in agreement with previous studies that have shown that the Asp residue controls the rate of nucleation, inhibits the growth of solids,31,34 and favors formation of the amorphous phase.22,35 The present study shows, however, that the presence and activity of Asp and Glu by themselves is not sufficient to inhibit the growth of the initially formed nanoparticles. Thus, with prolonged reaction times, the formation of micron-size near-spheres and sequential-growth rhombohedra of calcite solids occurs (Figure 7). This observation is also corroborated by the fact that the growth of the initially formed nanoparticles was inhibited in presence of magnesium ions (Figure 2). This finding highlights the importance of the presence of magnesium ions during the formation of nanosize precipitates. It has been documented that magnesium ions act

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Figure 12. CPH model of C. ensiformis urease (protein ID: AAA83831.1) showing (a) the tertiary structure of the protein displayed and colored according the secondary structure; (b) the distribution of Glu (blue) and Asp (red) residues on the surface of the urease molecule. The model was generated by using the Expasy online program: CPHmodels-2.0 for prediction of protein tertiary structure\48 and visualised by the RasWin 2.6 program.49 The template used for generating the C. ensiformis urease model was the 1S3T.pdb file for B. pasteurii urease, whose crystal structure has been solved.50 The amino acid identity between CanaValia urease and Bacillus urease is 58.6%.

as a foremost modifier of calcite morphology in many natural environments.36 Recently, Meldurm and Hyde37 reported that magnesium ions, in combination with organic additives, affect calcite morphology by adsorption to specific crystal faces, altering nucleation and inhibiting crystal growth. This finding is in accordance with molecular dynamic simulations38 of the inhibitory effect of magnesium ions on calcite crystal growth. The above-described mechanisms determine the initial formation of amorphous and nanosize calcium carbonate particles and inhibit their further growth. Another important observation is the aggregation of these particles into hierarchical, submicronsize, and pseudospherical calcite particles. The latter model is inconsistent with conventional mechanisms that are primarily based on diffusion growth.39 The first observation of the involvement of aggregation processes in the formation of colloidal particles was presented already in the late 1960s.40 This significant finding has long remained neglected. Lately, a number of experimental and theoretical studies have dealt with the aggregation mechanisms in formation of colloidal particles by aggregation of preformed nanosize precursors.41–44 In spite of significant contributions of these research results, the models used have been based on a number of simplifying assumptions. For example, Privman and coworkers45 developed a kinetic model that explains the formation of colloidal dispersions, based on an experimental system of preparation of spherical gold particles. This model took into account the average particle size parameter, the width of the particle size distribution, and the time scale. The role of surface charge of particles was entirely neglected. For nanoparticles, the charge and the extent of their electrical double layer should be a major initiator of aggregation processes.46 The negative charge measured on the precipitates obtained in this study (Figure 11) is postulated to originate from the charge of the same sign on the nanoparticles. Since the aggregation obviously occurs, the conclusion is that the prevailing electrostatic barrier is not effective to prevent aggregation

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of the initially formed nanoparticles, the number of which in the reacting solution is continuously increasing. Recently, Kallay and Žalac46 have also shown that nanometer-scale particles cannot be stabilized by the electrostatic repulsion barrier since, at the same mass but higher number concentration, these aggregate more rapidly than larger colloidal particles. Theoretically, the main reason for that is the small size of nanoparticles in comparison to the extent of their diffuse double layers. Thus, these diffuse layers overlap entirely, and the interaction between nanoparticles could be considered as interaction between ions. The consequence is rapid aggregation of the preformed nanoclusters and formation of complex nanostructured submicronscale spheres. Thus, rather than accepting the conventional nucleation and growth mechanism, this study underscores the importance of nanoscale aggregation processes, and the formation of assemblies of nanoparticles as an alternative mechanism for carbonate particle growth, commonly encountered in biomineralizing systems.47 Additional, more focused and inherently more delicate experiments, directed to the better understanding of electrokinetic properties and of mutual interaction of nanosize precursors phases, are needed. Studies directed toward the very early stage of particle formation would clarify the role of aggregation processes at the nanoscale on the formation of carbonate colloids. Understanding and managing these processes will permit the preparation of nanosize calcium carbonate precipitates of desired sizes, shape, and surface properties. Although the preparation procedures of nanosize calcium carbonate precipitates are in their infancy, with no application yet reaching commercial applications, among many other possible routes of preparation, this study offers a new approach based on biomimetic processes. The development of new methods, capable of biomimeticaly generating nanosize calcium carbonate precipitates, with stringent control of their properties, would be required by specific needs in material science. The present study is also relevant in understanding the mechanism of formation of complex natural hybrid materials, found in bioinorganic structures generated through nanoparticle assemblies. Acknowledgment. This work was suported by the Ministry of Science, Education and Sports of the Republic of Croatia (Grants 098-0982934-2742, 098-0982913-2829, and 1190000000-1158), and by the Ministry of Higher Education, Science and Technology of the Republic of Slovenia (Grant P2-0091-0106).

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