The Role of Residue Acidity on the Stabilization of Vaterite by Amino

Article pubs.acs.org/crystal

The Role of Residue Acidity on the Stabilization of Vaterite by Amino Acids and Oligopeptides Matthew A. Hood, Katharina Landfester, and Rafael Muñoz-Espí* Max Planck Institute for Polymer Research, Ackermannweg 10, 55128 Mainz, Germany S Supporting Information *

ABSTRACT: Nature uses proteins containing acidic residues to stabilize thermodynamically unstable calcium carbonate polymorphs, producing complex composite structures and controlling their final morphology. Stabilization of vaterite, the most thermodynamically unstable polymorph of anhydrous calcium carbonate, is possible in the presence of soluble biogenic molecules. We analyze here, in a systematic manner, the effect of the side-chain acidity of different amino acids on vaterite stabilization by following the kinetics of calcium carbonate crystallization through the free calcium concentration, pH, and turbidity. Acidic residues from aspartic and glutamic acid showed the greatest stabilization of vaterite, while cysteine and serine only partially stabilize this polymorph. Using the method of direct mixing of calcium and carbonate ions, we were able to further tailor the kinetics of calcium carbonate crystal growth by choosing the carbonate source as either sodium bicarbonate or sodium carbonate. Finally, oligopeptides of two oppositely charged amino acids, aspartic acid and histidine, were selected to study the effect of the chain length on the interactions between additive and calcium carbonate. Control over the interactions between ions, crystal faces, and charged additives results in stabilizing vaterite, which provides an insight into biomineralization processes.

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aqueous Ca2+ solution, and (ii) direct mixing of solutions of calcium and carbonate ions. The “diffusion method” is slow, taking hours to days to fully form crystals.21,22 At this time scale, with increased time for additives and metal ions to interact, a dramatic effect on the final CaCO3 polymorphs and morphologies is observed. However, only a small amount of CaCO3 is produced, making the technique useful only for proof-of-concept experiments. The direct mixing method is scalable and quickly induces crystallization, because supersaturation is achieved upon mixing of the ions. The importance of the carbonate source selection in the direct mixing method has often been underestimated, although it determines the amount of available carbonate in solution. Unless the pH of the carbonate source is controlled, as is the case for systems in which additives are added to the carbonate and not to CaCl2, the pH profile of the reaction changes upon addition of either Na2CO3 or NaHCO3.23 The change in the pH of the reaction is minimized by the introduction of additives such as amino acids or peptides, which have a mild bufferlike behavior on the system. Other buffering agents are sometimes added, but these molecules may also interact with the growing CaCO3 crystals.24 In this work, we analyze the effect of different amino acids (aspartic acid, glutamic acid, cysteine, serine, histidine, and leucine) on the crystallization of CaCO3 under controlled

INTRODUCTION The ability of nature to control the morphology and polymorph selection of calcium carbonate (CaCO3) is important in the design of biological structural materials, including antlers, eggshells, and the shells of crustaceans and other sea creatures. Often, nature uses organic templates, composed of biogenic regulator molecules and insoluble substrates, in achieving the appropriate mixture of crystal habits and hierarchical order that produces materials with high hardness and toughness.1−7 In an effort to better understand biomineralization processes, several research groups have extracted peptides from mollusk shells and other invertebrates to investigate what properties allow them to have control over the calcium carbonate crystallization. A large number of acidic residues along these protein sequences were observed, from regions rich in glutamic and aspartic acids.8−10 These acid-rich moieties have demonstrated strong binding to calcium ions and charged CaCO3 surfaces. The preferential binding of acidic residues to metal ionseither free or, especially, at surfacesresults in an inhibition of calcite growth and vaterite dissolution.11−14 Synthetic analogues of biomineralization systems are useful in the determination of factors that control mineralization by acting as models for processes found in nature.15−20 In the laboratory, two approaches have been most commonly used to precipitate calcium carbonate: (i) the so-called “diffusion method”, based on the dissolution of gaseous CO2 (either originating from decomposition of ammonium carbonate or added directly as a gas) in an enclosed vessel containing an © 2014 American Chemical Society

Received: October 22, 2013 Revised: December 11, 2013 Published: February 7, 2014 1077

dx.doi.org/10.1021/cg401580y | Cryst. Growth Des. 2014, 14, 1077−1085

Crystal Growth & Design

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crystallization evolution was monitored, the reaction parameters were analogous to the rest of the crystallization experiments, but the total volume was 25 mL. In situ measurements were recorded under a N2 atmosphere to avoid the influence of CO2 from the environment. The vessel, with dilute CaCl2 and amino acid solutions, was purged with N2 for 10 min prior to the start of in situ recording. An initial baseline was recorded for 60 s prior to carbonate source addition. Turbidity measurements were recorded by a transmission setup. Light transmission measurements were conducted in the dark with a self-made setup composed of a He−Ne red laser source (JDSU, model 1145P, 633 nm, 25 mW), a reaction chamber under constant magnetic stirring (300 rpm), a filter (Schott) that reduces the intensity of the transmitted light by a factor of 100, and a photodiode detector (photosensitive area = 10 × 10 mm). The detected current is amplified by a transimpedance amplifier, coupled with a multimeter (Keithley 2010) connected to a computer for data acquisition. An initial baseline prior to crystallization was recorded for 60 s preceding the carbonate source addition, slowly by use of an Eppendorf pipet. Scattering data points were recorded every 3, 10, or 20 s, depending on the total duration of the experiment. Kinetics: Evaluation of Turbidity Data. The experimental turbidity curves were analyzed as previously reported25 to obtain quantitative parameters of the crystallization kinetics. Data for transmitted intensity (I) versus time were fitted to the empiric equation

parameters (supersaturation, ionic strength, and additive concentration) during the direct mixing of precursor solutions. The amino acids were chosen by selecting similar backbone and side-chain structures with increasing residue acidity. The kinetics of nucleation and growth was controlled by choosing either Na 2 CO 3 or NaHCO 3 as the carbonate source. Nucleation and crystal growth were monitored in situ by turbidity, and the interaction of amino acids with calcium ions during crystallization was monitored by a calcium-ion-selective electrode. Oligopeptides of two oppositely charged amino acids, aspartic acid (Asp) and histidine (His), were selected to study systematically the effect of their chain length on the binding to inorganic crystal surfaces. The tendency for increasing oligomer chain length to preferentially bind with a particular crystal face was monitored by evaluating the oligomer effect on nucleation and growth of CaCO3.

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EXPERIMENTAL SECTION

Materials. NaHCO3 (≥99.5%) and Na2CO3 (≥99.5%) were acquired from Fischer Scientific. CaCl2·2H2O (≥99%), 3 M KCl solution, L-leucine (Leu, 99.5%), L-histidine (His, 99.5%), L-serine (Ser, 99.5%), L-cysteine (Cys, 98.5%), L-glutamic acid (Glu, 99.5%), Laspartic acid (Asp, 99.5%), N,N-dimethylformamide (DMF, ≥99.8%), trifluoroacetic acid (TFA, 99%), N,N-diisopropylethylamine (DIPEA, 99.5%), piperazine (99%), N-methylpyrrolidone (NMP, 99.5%), triisopropylsilane (TIS, 99%), ethyl (hydroxyimino)cyanoacetate (Oxyma Pure, 97%), and O-(benzotriazol-1-yl)-N,N,N′,N′-tetramethyluronium hexafluorophosphate (HBTU, ≥98%) were purchased from Sigma Aldrich. Wang resins containing aspartic acid or histidine, N-Fmoc-aspartic acid(O-tert-butyl)-OH, and N-Fmoc-histidine(Ntrityl)-OH were purchased from Novabiochem. KOH was acquired from Riedel deHaën. Milli-Q water (18.5 Ω·m) was used in all experiments. Microwave-Controlled Solid-Phase Peptide Synthesis and Peptide Purification. The pentamer, decamer, and eicosamer oligopeptides of aspartic acid and histidine were prepared with a CEM Liberty peptide synthesizer. DMF and NMP were used as solvents and the standard CEM Liberty coupling protocols were followed. To achieve 1 mmol of oligomer, preloaded Wang resins containing 0.7 mmol/g aspartic acid and 0.8 mmol/g histidine were used. The amino acid (0.2 M in DMF) coupling was facilitated by use of Oxyma Pure/HBTU (0.5 M in DMF) and DIPEA (2 M in NMP). Deprotection and release of the different oligomers from the Wang resins was accomplished by 24 h treatment with a cleavage solution containing 95% TFA, 2.5% TIS (as a scavenger), and 2.5% H2O. The products were filtered and then precipitated in cold diethyl ether and centrifuged before lyophilization. The chemical purity of the oligopeptides was characterized by HPLC. Crystallization Experiments. Crystallization of CaCO3 was carried out by direct addition of concentrated carbonate solutions (1 M) in equal molar ratios to CaCl2 solutions containing different amino acid concentrations (from 10 to 50 mM) and types (Leu, His, Ser, Cys, Glu, and Asp). The amino acids were added to the CaCl2 solution at molar ratios of 2:1, 1:1, and 1:10 (amino acid:Ca2+). In all crystallization reactions the final volume was maintained at 50 mL. The pH values of the CaCl2/amino acid solutions were set at 8.5 by addition of KOH. The ionic strength was adjusted with KCl (final KCl concentration 30 mM). After addition of the carbonate source, the reaction vessels were sealed with a screw-on lid to prevent any CO2 exchange with the environment. After the CaCO3 crystallization, the samples were washed by centrifugation at 4000 rpm for 30 min at 20 °C in a Rotixa 50 RS swinging-bucket rotor centrifuge. The supernatant was discarded and the samples were dried overnight under vacuum at room temperature. The free calcium-ion concentration and pH were simultaneously measured by use of a combined polymer membrane calcium-ion selective electrode (Metrohm) and a pH electrode (Mettler Toledo) connected to a Titrando titrator unit 836 (Metrohm). While

I(t ) = t0 + (tend − t0)

tn B + tn n

(1)

in which the parameters t0 and tend correspond to the initial and final values, respectively, of the intensity within the fast growing interval (corresponding to the limits of the peak of the first derivative of the curves), and B and n are fitting constants. From the change in transmission per time unit, which correlates to the desupersaturation rate, a precipitation rate r was calculated according to r=−

dI(t ) nBnt (n − 1) = (tend − t0) n dt (B + t n)2

(2)

The maximum value of the precipitation rate, rmax, which corresponds to the slope at the inflection point, was determined from the minimum of the derivative curves. From the rates in the absence (rblank) and in the presence (rmax) of an additive, an “inhibition efficiency” R with values ranging between 0 and 1 can be calculated:

R=

rblank − rmax rblank

(3)

Characterization Techniques. X-ray diffraction (XRD) was performed by use of a Guinier imaging plate camera (G670) from Huber with an X-ray source producing a Cu Kα wavelength of 1.5406 Å. The morphology of the crystals was investigated by scanning electron microscopy (SEM) on a Zeiss 1530 LEO Gemini microscope with an accelerating voltage of 1 kV and a working distance of ∼3 mm. The samples were prepared by dilution of crystals with ethanol to a final concentration of ∼1.0 wt % solid content and then drop-cast onto silicon wafers and allowed to dry under ambient conditions. No metal coating was used for evaluation.

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RESULTS AND DISCUSSION Calcium carbonate typically crystallizes in the form of three anhydrous polymorphs, of which calcite is the most thermodynamically stable and vaterite the least.12,26 Recently, vaterite has been observed to contain two interspersed crystal structures.27 Previous reports have shown that acidic amino acids preferentially bind to the calcite crystal faces, retarding their growth.28 Therefore, the stabilization of vaterite crystals in the presence of additives is indicative of a good interaction between the additive molecule and the crystal faces. We carried 1078



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nucleation and growth kinetics observed, in comparison to carbonate, as will be discussed in the next section. Analysis of the samples by XRD indicated that only calcite was obtained in the control sample prepared in the absence of any additive. Vaterite was the only polymorph present upon the addition of aspartic and glutamic acids, as shown in Figure 1. Cysteine and

out in situ and ex situ measurements to evaluate the conditions in which amino acids affect the nucleation and growth of calcium carbonate. Effect of Amino Acid Structure on Crystallization. Amino acids can act as molecular modulators by complexing Ca2+ or CO32− ions free in solution or present at crystal faces.11,26,29−34 Excluding glutamic acid, all amino acids used in our experiments have a side chain consisting of a methylene unit prior to their distinct residues: 2-ethyl, imidazole, hydroxyl, thiol, and carboxylate for Leu, His, Ser, Cys, and Asp, respectively (Table 1). Glutamic acid has a very similar Table 1. Chemical Structure and Isoelectric Point of Amino Acids Used and Corresponding Kinetic Parametersa

a

Kinetic parameters are from turbidity measurements (precipitation rate, rmax, and inflection point, tinfl) at an [amino acid]:[Ca2+] ratio of 2:1.

Figure 1. XRD patterns for CaCO3 samples prepared by addition of NaHCO3 in the presence of different amino acids at an amino acid-tocalcium ratio of 2:1. (V) vaterite; (C) calcite; (*) KCl.

structure to aspartic acid but contains an additional methylene unit in its side chain. The chemistry of the residues confers different properties to the amino acids. The residue of leucine is hydrophobic, while that of histidine is basic. Serine and cysteine have two polar residues (although the thiol of cysteine means it may also behave like an acidic side chain), which may take part in dipole interactions or hydrogen bonding with the species of calcium carbonate.35 Glutamic and aspartic acids were selected as negatively charged acidic molecules and have been shown to have the greatest effect on the nucleation and growth of calcium carbonate.31,32 All amino acids were used in their levorotatory chiral form in order to prevent any effect that might exist due to chirality of the molecules and subsequent oligomeric chains.29,33 Amino acids, which possess at least two charged species (the C-terminus and N-terminus), have a potential significant charge, determined by their pKa values (Supporting Information, Table S1). The pKa values also give a sense of the amount of charged species able to interact with ions at a particular pH.36 When the zwitterionic character of the amino acids is taken into account, it is more convenient to compare the isoelectric points (pI) of the amino acids, defined as the pH at which the net electrical charge of the molecule is 0 (see Table 1). Solutions containing an amino acid-to-calcium ratio of 2:1 were stirred for 1 h, prior to the addition of NaHCO3, to allow for the complexation of the calcium ions. Bicarbonate was selected as the carbonate source because of the slower

serine were also able to stabilize vaterite crystals, but a mixture of vaterite and calcite crystals was present. In contrast, the presence of histidine and leucine had no effect on vaterite stabilization, and calcite was the only phase observed in the diffractograms. The stabilization of vaterite followed the series Asp > Glu > Cys > Ser > His > Leu, which correlates with the acidity of the amino acid residue. The kinetics of nucleation and crystal growth was evaluated by turbidity measurements, presented in Figure 2a. In the turbidity curves, which show transmitted light as a function of time, a marked delay in the onset represents a longer induction time and is related to a slower kinetics of the nucleation. The longer induction time can be explained by stronger interactions between the amino acid and the Ca2+ ions, which decreases the availability of calcium in the crystallization environment. If nucleation and growth processes could be strictly separated, the nucleation would be finished after the induction time, and the shape of the decay curve should be related to the specific interactions of amino acid molecules with growing crystal faces. Unfortunately, in real systems, the nucleation process does not necessarily stop when growth starts. Therefore, turbidity curves include both processes. The overall inhibition of an additive can be quantified by the so-called “inhibition efficiency”, R, defined as indicated in eq 3. Table 1 lists the values of the precipitation rates (rmax) and the inflection points of the fastest-growing regions of the curves (tinfl.). The greatest hindering of the nucleation, judged from the induction times, was observed for 1079



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of R against the isolectric point (pI) of the amino acids, shown in Figure 2b, is a clear indication of the dependency of crystal growth on the acidity of the residue of the amino acid used as an additive. Despite its basic residue, histidine has an inhibition effect, which may be related to the interaction of the basic side chain with HCO3− and CO32−, as well as their complexes with calcium ions.37 Leucine has by far the weakest influence due to the hydrophobicity of the residue. The combined evaluation of XRD and turbidity data indicates that the greater the inhibitory efficiency of the additive, the greater its ability to stabilize vaterite, which is directly related to the degree of side-chain acidity. SEM images of the dried crystals, shown in Figure 3, displayed the typical morphologies of the observed polymorphs: rhombohedra of calcite crystals and small crystallites of vaterite, which frequently organize into spherulites. Large amounts of amino acid cause imperfections on the surface of the calcite crystals (observed as pits) and also lead to aggregation of the vaterite crystallites in nonspherical morphologies. These variations from ideal morphologies are in agreement with the postulated binding of the amino acid molecules to the growing surfaces of calcium carbonate. Effect of Amino Acid Concentration and Carbonate Source on Crystallization. The effect of amino acid concentration on nucleation and growth of CaCO3, with the addition of bicarbonate, was investigated by changing the amino acid concentration with respect to the Ca2+ ions in solution. For all experiments, the calcium concentration, [Ca2+], was maintained at 10 mM and the [amino acid]: [Ca2+] ratios were 1:1 and 1:10. XRD patterns of the samples indicated that the stabilization of vaterite decreased with decreasing amino acid concentration (Supporting Information, Figure S1). At a molar ratio of 1:1, vaterite is completely stabilized by aspartic acid, while a mixture of vaterite and calcite is now obtained in the presence of glutamic acid. In comparison, cysteine and serine are no longer able to stabilize vaterite, as calcite is the only polymorph observed from the XRD. At a molar ratio of 10:1, aspartic acid is the only amino acid able to partially stabilize vaterite (a mixture of vaterite and calcite is observed). The results indicate how critical the amino acid concentration is in stabilizating polymorphs. The pH of the environment has an effect on the growth of calcium carbonate even in the absence of any additive and is related to the dissociation equilibria of carbonate in solution.38

Figure 2. (a) Evolution of turbidity for the crystallization of CaCO3 in the presence of different amino acids at an amino acid-to-calcium ratio of 2:1. (b) Variation of the inhibition efficiency with isoelectric point.

aspartic and glutamic acids, followed by cysteine, serine, histidine, and finally leucine. The same order is followed by the values of R, mainly indicative of the inhibition of growth, and the highest values were obtained for glutamic (R = 0.87) and aspartic (R = 0.90) acids. The representation of the values

Figure 3. SEM images of samples prepared in the presence of (a) aspartic acid, (b) cysteine, and (c) leucine at an amino acid-to-calcium ratio of 2:1. 1080



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Carbonate, CO32−, is in equilibrium with HCO3− and H2CO3, which evolves into CO2 gas. Thus, the pH of the solution determines the availability of CO32− ions. To ensure total deprotonation of the carboxylate group in the amino acids, a pH of 8.5 was chosen for the initial solution in our experiments, which implies that nearly all of the carbonate is in the HCO3− form. Slower reaction kinetics was achieved by reducing the availability of CO32−. NaHCO3 as the carbonate source must first be deprotonated prior to reacting with Ca2+ to form CaCO3. HCO3− is univalent and may interact with the amino acids. In addition, HCO3− has been shown to form a metastable Ca(HCO3)2 in solution, which reduces the amount of available CO32−, thus reducing the speed of CaCO3 formation. This reduced speed increases the time in which amino acids can interact with ions and crystal faces. In comparison, Na2CO3 fully disassociates to CO32−. At a pH of 8.5, protonation of the CO32− does occur but is competitive with the reaction with Ca2+ to form calcium carbonate. By choosing the carbonate source, we are able to control the reaction kinetics of calcium carbonate precipitation. Crystallization experiments, at an amino acid-to-calcium ratio of 2:1, were carried out with Na2CO3. XRD patterns of dried samples prepared from Na2CO3, presented in Figure 4, show

The kinetics of crystallization of calcium carbonate in the presence of either NaHCO3 or Na2CO3 was monitored by turbidity measurements for systems containing aspartic acid at concentrations of 20, 10, and 1 mM, corresponding to amino acid-to-calcium ratios of 2:1, 1:1, and 1:10, respectively. Aspartic acid was chosen as an additive because it has the strongest influence on calcium carbonate crystallization, as proven previously. The evolution of the curves is shown in Figure 5a,b.

Figure 4. XRD patterns for CaCO3 samples prepared by addition of Na2CO3 in the presence of different amino acids at an amino acid-tocalcium ratio of 2:1. (V) vaterite; (C) calcite; (*) KCl.

that the calcite polymorph is more prevalent than in the case of samples prepared from NaHCO3. Aspartic acid is able to stabilize vaterite completely. However, diffractograms of samples prepared with glutamic acid display a mixture of vaterite and calcite. In the presence of serine and cysteine, the patterns displayed reflections only for calcite crystals. As the concentration of amino acid decreased from 10 to 1 mM, vaterite stabilization further decreased (Supporting Information, Figure S2).

Figure 5. Evolution of turbidity for crystallization of CaCO3 samples in the presence of varying aspartic acid concentrations with addition of (a) NaHCO3 and (b) Na2CO3. (c) Dependence of inhibition efficiency (R) on aspartic acid concentration with addition of NaHCO3. The added lines in panel b are to aid the eye and do not represent a fit. 1081



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Figure 6. Evolution of relative calcium concentration and pH for crystallization of CaCO3 in the presence of selected amino acids with addition of (a, c) NaHCO3 and (b, d) Na2CO3.

are useful indicators of the overall state of the free-ion concentration in solution. It should be noted that Ca2+-selective electrodes do not identify what is occurring with the Ca2+ ions but only whether they are in their free form. Thus, we cannot determine if the Ca2+ ions are being used in nucleation and growth of calcium carbonate, being bound to amino acids, or forming complexes with additional ions. The initial values of Ca2+ ions registered by the Ca2+-selective electrode varied from the added concentration of 10 mM, depending on the addition of amino acid and the type of amino acid. In the case of aspartic acid, the displaced initial value of [Ca2+] was ∼6 mM, while in the presence of His and Leu, values between 8 and 10 mM were measured. This is consistent with the fact that Ca2+ ions have a strong binding to acidic amino acid residues like that of aspartic acid. To allow a comparison of the concentration curves, the relative Ca2+ concentration (i.e., [Ca2+]/[Ca2+]0, where [Ca2+] is the measured concentration at a certain time and [Ca2+]0 the initial concentration) was used. In situ measurement of pH is critical for evaluating the effect of the carbonate source addition on the reaction. It is expected that the pH profile of the solutions will change with the addition of NaHCO3 or Na2CO3, as there will be a change in the equilibrium of CO32− ions such that protons may be either released or taken up from solution. Figure 6 compares the change in the relative Ca 2+ concentration and pH with time when either Na2CO3 or NaHCO3 is added. With the addition of bicarbonate, there is an initial drop in the calcium concentration, followed by a tapering till a plateau is reached. In experiments in which Na2CO3 was added, the decrease in the free calcium was much faster than for those with bicarbonate solutions: bicarbonate solutions still had more than 50% of the relative Ca2+ ions available after 3600 s, while the carbonate solutions were completely devoid of free Ca2+ at the same time.

When NaHCO 3 was added and the aspartic acid concentration decreased, there was an observable increase in calcium carbonate nucleation and growth, and the systems became turbid faster (approximated by the inflection point of the curves). In comparison, when Na2CO3 was added, the crystallization was substantial after a few seconds, with almost negligible induction times ( Glu > Cys > Ser > His > Leu, in accordance with the side-chain acidity. Using the direct mixing method, we also studied additional parameters for the stabilization of vaterite: available carbonate, which depends on the source; presence of an ionic strength adjuster, such as KCl; and Ca2+ supersaturation. As a method for extending the knowledge gained to systems of interest in nature and to highlight the impact of molecular weight on the interactions of ions and charged CaCO3 surfaces with homopolymers, two model oligopeptidic systems, oligo(aspartic acid) and oligohistidine, were investigated. It was shown that, with increasing molecular weight, the interactions between oligopeptides and both ions and charged growing surfaces increased, with drastic increases in nucleation and growth times. These results identify the origins of the interactions of peptides and proteins on the controlled expression of CaCO3 polymorphs with unusual morphologies that are found in nature.

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ASSOCIATED CONTENT

S Supporting Information *

Three tables, listing values of pKa for amino acids used and kinetics parameters from turbidity, and four figures, showing XRD patterns for lower amino acid concentrations, KCl-free crystallization, and higher supersaturation. This material is available free of charge via the Internet at http://pubs.acs.org.

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AUTHOR INFORMATION

Corresponding Author

*E-mail [email protected]; tel +49-6131-379410; fax +49-6131-379100. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS We thank Patricia Schulze and Dr. Adrian Fuchs, who helped with some experiments, Michael Steiert for his assistance with X-ray diffraction, and Beate Müller for the HPLC measurements.

Figure 8. Evolution of turbidity for crystallization of CaCO3 prepared in the presence of (a) oligo(aspartic acid) and (b) oligohistidine of different chain lengths. (c) Dependence of inhibition efficiency (R) on degree of polymerization for crystallization of CaCO3 in the presence of oligo(aspartic acid).

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REFERENCES

(1) Mann, S., Biomineralization: Principles and Concepts in Bioinorganic Materials Chemistry; Oxford University Press: Oxford, U.K., 2001. (2) Belcher, A. M.; Wu, X. H.; Christensen, R. J.; Hansma, P. K.; Stucky, G. D.; Morse, D. E. Nature 1996, 381, 56−58. (3) Aizenberg, J.; Lambert, G.; Weiner, S.; Addadi, L. J. Am. Chem. Soc. 2001, 124, 32−39. (4) Menahem, T.; Mastai, Y. J. Cryst. Growth 2008, 310, 3552−3556. (5) Obata, T.; Schoenefeld, S.; Krahnert, I.; Bergmann, S.; Scheffel, A.; Fernie, A. Metabolites 2013, 3, 168−184. (6) Scheffel, A.; Gruska, M.; Faivre, D.; Linaroudis, A.; Plitzko, J. M.; Schüler, D. Nature 2006, 440, 110−114.

of the calculated inhibition efficiencies on chain length, plotted in Figure 8c, can be fitted with the Langmuir isotherm of eq 4, which is an indication of the coverage of growing surfaces provided by longer peptides (see detailed values in Supporting Information, Table S3). The oligo(L-histidine)s, similarly to the monomeric amino acid His, do not seem to affect the kinetics of nucleation and growth significantly: His20 has only a slight retardation in the final nucleation of calcium carbonate. As was seen with the 50 mM supersaturated solutions, the interaction of His with negatively charged ions and crystals is confirmed, 1084



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