Mechanistic Approach to Predict the Combined Effects of Additives

Aug 23, 2016 - Polyelectrolyte films with carboxylic and/or amine groups serve as the organic template for mineralization, and amino acids and monosac...
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Mechanistic Approach to Predict the Combined Effects of Additives and Surface Templates on Calcium Carbonate Mineralization Josue A. Lopez-Berganza and Rosa M. Espinosa-Marzal* Civil and Environmental Engineering, University of Illinois at Urbana−Champaign, 205 North Matthews Avenue, Urbana, Illinois 61801, United States S Supporting Information *

ABSTRACT: The biomineralization of calcium carbonate is masterfully directed by organic macromolecules present in many organisms. In this biomimetic study, absorbance measurements accompanied by microscopy and infrared spectroscopy are used to evaluate the superposed effect of organic additives and surface chemistries on the kinetics of surface-directed nucleation and growth of calcium carbonate. Polyelectrolyte films with carboxylic and/or amine groups serve as the organic template for mineralization, and amino acids and monosaccharides as the selected solution additives. A grain-boundary kinetics model describes surface precipitation of calcium carbonate to provide a mechanistic insight into the precipitation pathway via two parameters, the near-surface supersaturation and the crystal number density. While an organic matrix rich in ternary amines strongly promotes vaterite nucleation, the selected carboxylic-enriched polyelectrolyte film significantly stabilizes ACC in the near-surface region, while it equally promotes vaterite and calcite nucleation. The combined effect of organic additive and surface template determines the near-surface supersaturation. Soluble additives can also be directly involved in surface nucleation if they strongly interact with the organic interface. Our mechanistic approach reveals two different precipitation pathways that result from the synergy between surface template and organic additives.

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INTRODUCTION Biomineralization is the process by which diverse organisms such as mollusks, sea urchins, sponges, and ascidians can form hard functional structures.1−5 The result of this process is a composite containing both a mineral phase and a small amount of organic component, with characteristics that differ from those of the abiotic minerals. Calcium carbonate is the most commonly synthesized biomineral by organisms in different taxa and has been the subject of extensive research for many decades,5−8 including many computational studies that focused on the early stages of biomineralization.9−15 Calcium carbonate occurs in three different crystalline polymorphs at ambient pressure (calcite, aragonite, and vaterite), two hydrated crystalline phases (monohydrocalcite and ikaite) and a less stable and more soluble amorphous form, ACC.2,3,5 Aggregation of prenucleation clusters (PNCs) into ACC has been proposed as an alternative (nonclassical) path to classical nucleation, which ocurrs by ion-by-ion attachment.16−18The pathway traversed to the stable crystalline form has thermodynamic origins and, thus, is dictated by the free-energy landscape of the system.19 However, in many cases, a less thermodynamically stable phase (e.g., ACC) nucleates first according to kinetics arguments (Ostwald step rule).2,20 Some studies demonstrate that ACC is a precursor of calcite,1,16,21 whereas others do not show a direct transformation of ACC into calcite, but instead, ACC dissolution and direct nucleation from solution occurring at organic interfaces.16,22 © XXXX American Chemical Society

According to the classical nucleation theory, the thermodynamic barrier for nucleation is reduced at surfaces that minimize the net interfacial energy γ of the forming nuclei (γ = γLS + h(γCS − γLS), with h a factor that depends on the aspect ratio of the nucleus, and γij the interfacial energy of ij = LC (liquid-crystal), CS (crystal-substrate), and LS (liquid-substrate), thereby leading to nucleation rates that can be higher than in the bulk.22 Studies of surface-templated precipitation of calcium carbonate have shown nucleation of vaterite, and calcite on different substrates under different solution conditions.22−28 Smeets et al. observed the growth of ACC particles (10−20 nm) in a polystyrenesulfonate (PSS) film by TEM, before crystals formed outside of the polymer matrix.29 It was proposed that the local supersaturation within charged polyelectrolytes can be higher than in the bulk, thereby promoting nucleation within the polymer, while the concentration outside the polymer was too small for nucleation.29 In contrast, the increase in nucleation barrier for calcite with the surface charge of various polysaccharide films suggested that, at high supersaturation, more hydrophilic organic templates (i.e., higher charge, and smaller γLS) could retard nucleation in agreement with the classical nucleation theory.30 Further, lowReceived: April 4, 2016 Revised: July 27, 2016

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at a concentration of 14 mM. Selected tests were performed at other concentrations of CaCl2 and Na2CO3 (2, 10, and 50 mM). The solutions were filtered using a 0.2 μm Nylon filter (Fisherbrand) prior to use. Polyelectrolyte solutions (1 mg/mL) were prepared by overnight sonication in a 500 mM NaCl solution at 60 °C and filtered IAP prior to use. The supersaturation σ = ln K , where IAP is the ion

energy barriers for nucleation were found to correlate well with strong crystal−substrate binding.31 Highly sulfated and carboxylated saccharides and carboxylated amino acids are commonly found in mineralizing macromolecules and are thought to play an active role in the biomineralization process.30−32 Systematic in situ potentiometric titration experiments have shown that amino acids and carbohydrates can modify the early stages of precipitation.32,33 The action of amino acids is manifold, including association with calcium ions, (de)stabilization of PNCs, nucleation inhibition or promotion, adsorption on precursors, and influence on local structure of nucleated particles and solubility.32−38 For example, aspartic acid, glutamic acid, and serine can stabilize PNCs and retard ACC nucleation at pH 9.75;32 glycine reduces ACC solubility, perhaps as a result of incorporation into the mineral. Similar experiments using carbohydrates as bulk additives demonstrated additive-dependent effects on calcium carbonate precipitation, which were attributed to stereochemistry, additive moieties, and the nature of glycosidic linkages.33 For example, arabinose was shown to strongly stabilize PNCs and to promote direct nucleation of vaterite from solution at pH 9.75, i.e., without involving ACC as a kinetically preferred precursor; in contrast, glucose and mannose promoted ACC nucleation. Soluble additives have also been observed to bind selectively to certain crystal faces, modifying textures, morphologies, and even mechanical properties.39,40 The joint effect of an insoluble protein matrix and soluble organic additives has been studied in systems mimicking natural biomineralization.41−44 It has been proposed that insoluble proteins primarily provide the nucleating sites, whereas the soluble additives are responsible for the morphology of the final crystal phase. However, the complexity of the system (proteins) used in those studies prevented more detailed insight and mechanistic understanding. Thus, the combined effect of soluble additives and organic interfaces on the kinetics of calcium carbonate nucleation and growth has not yet been fully understood.39 In this work, two well-characterized polyelectrolyte films provide the organic substrate for mineralization. The effects of substrate in conjunction with organic additives on precipitation kinetics of calcium carbonate were investigated via real-time absorbance measurements combined with microscopy, and IR spectroscopy. Further insight into the mechanisms underlying mineralization was obtained by modeling surface-precipitation kinetics.

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activity product and Ks is the solubility product, was calculated with respect to ACC, calcite, and vaterite using Visual MINTEQ v 3.1 (Table S1 in Supporting Information (SI)). Preparation of Surface-Adsorbed Polyelectrolyte Films. The optical thickness of the adsorbed polyelectrolyte films was measured by Multiple-Beam Interferometry with a Transmission Interferometric Adsorption Sensor (TInAS).45 TInAS allows for fast (2 Hz) readings of the interference pattern generated by white light passing through the substrate, which consists of a borosilicate-glass coverslip, a 25 nm aluminum mirror and a ∼3 μm sputtered amorphous silica surface. The fluid cell has a total volume of ∼20 μL and is composed of the silica substrate on the bottom, a template metal spacer that holds an O-ring in the middle, and a fused silica window that is connected to inlet and outlet tubing. Unidirectional constant flow (0.15 mL/min) into the cell is established using a peristaltic pump (ISMATEC IP). White light (Techniquip, FOI-150, USA) travels through the multiple layers of the TInAS sensor and generates an interference spectrum, which is collected with a spectrometer (Ocean Optics USB-2000+) and transmitted digitally to a computer. The silica substrates were cleaned using UV−ozone cleaning (30 min), sonication in toluene (10 min), isopropanol (10 min), ethanol (10 min), and a second UV− ozone cycle (30 min). A reference spectrum was collected prior to polymer adsorption to establish a baseline. During polymer adsorption, the software gives deviations from the baseline as the optical (dry) film thickness of the adsorbed polymer layer. Two polyelectrolyte films were selected: poly(ethylene imine) (PEI) and a two-layer film composed of poly(allylalmine hydrochloride) (PAH) and poly(acrylic acid) (PAA). At the end of polymer adsorption, the fluid cell was rinsed for ∼20 min to remove weakly adsorbed polymer. The absence of desorption of the films was also confirmed in CaCl2 solutions. The thickness of the adsorbed polymer films on the window was determined by ellipsometry (Gaertner Scientific, L116C, USA) in air. The polarizer was set to 45° and the incidence angle to 70°. LGEMP (Gaertner Scientific, USA) software was used for data collection. Absorbance Measurements. The TInAS fluid cell was modified with double-inlet tubing joining ∼5 mm before the fluid cell entrance to introduce two separate solutions. The stock solutions were continuously pumped for 1 h at constant flow rate on both surface films, thereby maintaining constant solution conditions in the cell during precipitation. Reference measurements were performed on bare (polymer-free) substrates. The pH of the effluent stream was recorded during the experiment (Mettler-Toledo, Seven Compact S220, USA). The initial pH of the CaCl2 solution was adjusted, if needed, to keep the pH of the effluent at 9.25 ± 0.23. Various flow rates (q) were tested but the results discussed here correspond to the optimal flow rate of 0.15 mL/min; lower flow rates led to sporadic clogging of tubing with precipitate and to unsteady flow in the cell, while an increase to 0.30 mL/min led to occasional removal of small crystals and ACC from the surface. Calcium carbonate precipitation in the fluid cell gradually decreases the transmitted light intensity into the spectrometer. The corresponding absorbance during precipitation is given by

MATERIALS AND METHODS

The following chemicals were used without any further purification: calcium chloride dihydrate (Sigma-Aldrich, ≥99%), sodium carbonate (Sigma-Aldrich, 99.95−100.05% dry basis), sodium chloride (EMD, min 99%), sodium hydroxide (Sigma-Aldrich, ≥97%), poly(ethylene imine) solution (PEI) (Sigma-Aldrich, 750 000 g/mol, 50% wt in H2O), poly(acrylic acid) (PAA) solution (Polysciences, Inc., 30 000 g/ mol, 30% wt in H2O), poly(allylalmine hydrochloride) (PAH) (SigmaAldrich 17 500 g/mol), L-serine (Sigma-Aldrich, ≥99%), glycine (Sigma-Aldrich, ≥98.5%), L-aspartic acid (Sigma-Aldrich, ≥98%), Lglutamic acid (Sigma-Aldrich, ≥99%), D-(−)-arabinose (SigmaAldrich, ≥98%), D-(+)-glucose (Sigma-Aldrich, ≥99%), and D(+)-mannose (Sigma-Aldrich, ≥99%). Solutions of calcium chloride were prepared with Milli-Q water at concentrations of 14 mM, while the additive concentration (amino acid or monosaccharide) was set to 20 mM in the CaCl2 solution, hence in molar excess with respect to Ca2+ to maximize calcium− additive interactions. Sodium carbonate was dissolved in Milli-Q water

⎛ S − Dλ ⎞ Aλ = − log10⎜ λ ⎟ ⎝ Rλ − Dλ ⎠

(1)

where Aλ is the absorbance at a given wavelength, Sλ is the light intensity, Rλ is the reference intensity before crystal precipitation, and Dλ is the background intensity. The absorbance was collected by OceanView (Ocean Optics, v 1.5.0, USA), and a wavelength of λ = 530 nm was selected for the analysis (Δ = A530). B

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Figure 1. Microscopy images during calcium carbonate precipitation in a sandwiched solution between two polymer-coated substrates after 5 min: (a) PAH/PAA (green) and (b) PEI (red). The circles designate vaterite (in yellow), calcite (in blue), and ACC (in red). (c) ATR-IR spectroscopy of the calcium carbonate solution between polymer-coated coverslip and ATR diamond crystal after 5 min (dashed) and 30 min (solid). Solution concentration: 7 mM CaCO3, 14 mM NaCl. Scale bar = 50 μm. compare across conditions, the zeta potential was normalized by the square of the diameter, which is denoted as “surface potential”.

The measured absorbance over time includes the contribution of the precipitate in the bulk solution and on bottom and top surfaces of the cell. A final rinsing step with water was performed to remove the precipitated minerals in the bulk solution, i.e., to record solely the absorbance of the surface precipitate. A silica nanoparticle suspension (diameter = 12 nm) was injected into the fluid cell until a constant absorbance reading was achieved; the suspension was then exchanged by water at the selected flow rate, which led to a decrease of the absorbance. The residence time was determined as the time required for the absorbance to recover the baseline in water and is ∼ 1.5 min. Flow Imaging Microscopy. The TINAS flow cell was fixed to the stage of an optical microscope (Leica, DM 1750 M and MC 170 HD, Germany) to visualize the precipitation on bottom and upper substrates with time under the same conditions as in the absorbance measurements. After each experiment, Raman microspectroscopy (Nanophoton, RAMAN-11, Japan) was applied to identify the crystalline phase of single crystals grown on upper and bottom substrates. A 532 nm laser was used with exposure times between 10 and 20 s. RAMAN Data Viewer software was used to collect point measurements and correct the baseline of the measurement. The crystal number density at the end of the experiment was determined by counting the number of crystals on both bottom and upper substrates of the fluid cell window using ImageJ (U.S. National Institute of Health, v 1.49, USA) on light microscopy images; the polymorph distribution of calcite and vaterite crystals was obtained by dividing by the total number of crystals. Three representative pictures per experimental condition were typically analyzed. The early stage of precipitation was also investigated under nonflow conditions by combining ATR-IR (Perkin Elmer, Frontier, USA and Pike Technologies, GladiATR, USA) and optical microscopy to determine the amorphous and crystalline phases that precipitate with time. The two solutions (0.5 μL of each stock solution with a concentration of 14 mM) were sandwiched between two coverslips (Warner Instruments, No. 2 Glass Coverslip, USA) for microscopy or between coverslip and ATR crystal for IR spectroscopy, both coated with the selected polyelectrolyte films, and sealed with silicone vacuum grease (Dow Corning, high-vacuum grease) to avoid evaporation; polyelectrolyte adsorption onto the coverslips was confirmed by ellipsometry. Dynamic Light Scattering (DLS). The hydrodynamic diameter and electrophoretic mobility (EPM) of PEI and PAA were examined with a Zetasizer (Malvern, ZS90, UK) at the wavelength of 633 nm and the scattering angle of 90°. The reference measurements were conducted in 1 mM polymer solution with CaCl2 (7 mM), and with CaCl2 (7 mM)+NaCl (10 mM) solutions, the latter to mimic the ionic strength of aspartic and glutamic acid, and the pH was adjusted to 9.25 with NaOH. Hydrodynamic diameter and electrophoretic mobility were measured with each additive (10 mM) in the polymer solution (1 mM) with CaCl2 (7 mM); three replicate samples were examined right after sample preparation. The zeta potentials of the polymers were calculated from the EPM following Ohshima’s method.46−48 To

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RESULTS

Polyelectrolyte Film Adsorption. The adsorption kinetics of the two selected polyelectrolyte films (PEI and PAH/PAA) on the bottom substrate (silica) of the fluid cell was measured in situ prior to each mineralization experiment; representative adsorption curves are shown in Figure S1. The optical dry thicknesses for PEI, PAH, and PAA-films are 0.99 ± 0.41, 1.13 ± 0.43, and 3.29 ± 0.34 nm, respectively. The dry thickness of the polymer films adsorbed onto the upper surface (glass) was determined ex situ by ellipsometry to be 4.5 ± 0.8 nm for PAH/PAA-films, and hence in good agreement with the optical thickness on the bottom surface. The dry thickness of PEI could not be determined with accuracy by ellipsometry due to the close match between its refractive index and that of the substrate. The optical thickness D is proportional to the adsorbed dry mass per unit area according to the de Feijter equation,49 Mdry = D(n − nw)/(dn/dc), which leads to 67 ng/cm2 for PEI, 363 ng/cm2 for PAA, and 132 ng/cm2 for PAH. The charge density of functional groups at a specific pH can be determined according to αpMdryNNA/Mpol, where NA is the Avogadro number, Mpol the number molecular weight of the polymer, N the polymerization degree, α the ionization degree at each specific pH, and p the number of protonated or deprotonated functional groups per monomer (4 ternary amines for PEI, 1 carboxylic group for PAA, and 1 amine group for PAH). The parameters used for the calculation are in the SI (Table S2). At a pH of 9.25, the charge densities are −30 and +5 per nm2 for PAA and PAH, respectively, and +3 per nm2 for PEI. A surface charge of ∼ −0.5 per nm2 and of ∼ −0.04 per nm2 has been reported for the reference silica substrate50 and borosilicate glass,51 respectively, at pH 9 and 10 mM ionic strength. Adsorption of Additives on PEI and PAA. Zeta potential and hydrodynamic size of PEI and PAA macromolecules in two electrolyte solutions (as reference) and with the additives are shown in Figure S2 (SI). Although the zeta potential is not a measure of the adsorbed mass, it gives qualitative information about interactions between solutes and polymers. The hydrodynamic size of PEI significantly increased with aspartic acid and mannose, and marginally with glutamic acid, glucose, and arabinose, which indicates that PEI aggregation is mediated by the additive (Figure S2a). The surface potential, which considers the change in size, strongly decreases with respect to the reference for all additives, except for serine (Figure S2b). Adsorption can lead to a decrease in surface potential per unit C

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S4). Exceptions were observed for aspartic and glutamic acid, which fully inhibited ACC nucleation on both polymer films, and serine that also hindered ACC nucleation on PAH/PAAfilms. A selection of microscopy images is shown in Figure S4. Note that under nonflow conditions, the concentration decreases during crystal growth, and hence the solution becomes saturated after a short time. In contrast, the concentration and supersaturation remain constant in the flow cell, if the system is in steady state, and mineralization can be investigated for longer time spans, but we do not get spectroscopic information. Snapshots of calcium carbonate precipitation over time on glass and on PEI- and PAH/PAAfilms in the fluid cell (flow rate = 0.15 mL/min) are shown in Figure 2.

area, either owing to the negative charge of the adsorbed molecule (e.g., for the two acids), or if the adsorbed molecule is uncharged (e.g., zwitter serine and glycine, and the monosaccharides). The results indicate either weak or no adsorption of serine on PEI. Note that since extrinsic compensation of PAH-charges is unlikely,52 the interaction between PAH/PAA-films and additives is mainly dictated by PAA. Hence, PAA, instead of PAH/PAA, was selected for these studies, which simplifies the interpretation of DLS results. Figure S2c shows the size of the PAA globules. Ca2+ bridging is responsible for the enormous increase in size of the PAA globules in the reference solutions (410 and 935 nm, respectively), while the macromolecule size is ∼6 nm in the absence of Ca2+. The remarkable decrease in the size of PAA-Ca2+ globules by the additives is consistent with additive adsorption on the polymer via Ca2+ bound to PAA, which releases Ca2+-bridges with some PAA globules. Note that Ca2+-bridging leads to a minor surface potential of PAA in the reference solutions, while the surface potential becomes more negative with all additives (Figure S2d). A weaker adsorption of arabinose and glucose is plausible, based on the less negative surface potential compared to mannose, serine, and glycine. Flow Imaging Microscopy. The initial stage of calcium carbonate precipitation on both polyelectrolyte films was studied by combining optical microscopy and ATR-IR spectroscopy under nonflow conditions. On PAH/PAA-films two solid phases were visible: one that grew with time, and another one composed of a large amount of tiny particles distributed uniformly that was present from the beginning (Figure 1b) and completely dissolved after ∼11 min. Due to the resolution of optical microscopy, the nucleation pathway of these solids could not be resolved. IR spectroscopy (Figure 1c) showed a pronounced peak at ∼840−850 cm−1 after ∼2 min, which was attributed to the presence of uniformly distributed ACC.3 The signal was weak due to the large solution-to-solid ratio, which also prevented the crystalline phase from being detected through a peak at 712 or 745 cm−1 for calcite or vaterite, respectively (see the low crystal density). During precipitation, this peak shifted to larger wavelength numbers, indicating the increase in crystallinity in the sample,3,53 while calcite and vaterite were observed to grow with time (Figure 1b). Further, crystal growth was concurrent with the dissolution of ACC on PAH/PAA-films. Raman microspectroscopy unambiguously confirmed the soluble phase to be ACC on PAH/PAA-films but at a higher concentration (50 mM) (Figure S3). On PEI-films the amount of ACC was smaller than on PAH/PAA-films, and it completely vanished within ∼5 min (see Figure 1a). Smaller ACC particles could be present ( σCs > 0.6 reported in ref 62, and our own measurements (GC ∼ 3.28 nm/s) assuming saturation with respect to ACC. This yields GCi = G0i(σCs )3.12 for calcite, with G0i = 0.0232 nm/s. We are aware that this is a strong simplification, since the growth rate depends on the growth mechanism; we assume the crystals are perfect cubes for simplification. The fitting parameters in eqs 5, 6, 8, and 9 are the surfaceregion supersaturation (σs) and the induction time. The crystal number densities (NVB and NCB ) were obtained from microscopy images (Figure 7a,b). Shorter experiments (15 min and 30 min) showed that the relative polymorph distribution of calcite and vaterite was maintained approximately constant during the course of precipitation (Figure S15), and hence, NVB and NCB were assumed to remain constant with time. Figure 8a shows

[I B(R2 − y 2 ) dt ]

(3)

This considers that nucleation or growth cannot happen in areas already occupied by other crystals. The volume fraction of vaterite with respect to the volume of solution is obtained by integration of Ac:

∫0

⎡ ⎡ ⎨ 1 − exp⎢ −π ⎢ ⎪ ⎣ ⎣ ⎩

(5)

(2)

ϕV = OvB

G(t − τ ) ⎧ ⎪

Flow imaging microscopy only shows a short nucleation event at the beginning of the experiment (Figure S5). In the limit of site saturation (SS), i.e., if nucleation occurs in Δt ∼ 0, eq 5 can be simplified to

where IB = IB(τ) is the nucleation rate per unit surface area. The intersection is a circle with nonzero area if t > τ + y/G given by ac = π(R2 − y2) (see inset in Figure S16). The subindex e in eq 2 means that the overlap between crystals, as well as phantom nuclei, is included in the so-called “extended” area Aec. Assuming that the nuclei are distributed randomly on the surface, the true areal fraction Ac crossed by the plane y of all crystals growing from the same substrate is given by59 Ac = 1 − exp( −Ace )

∫0

(4)

where OBv is the surface area per unit volume of solution and the upper limit of the integral, ymax, is given by the crystal radius. To apply this model to mineralization on the polyelectrolyte films, we extend the concept of surface to a near-surface region perturbed by the film. Accordingly, nucleation can happen throughout the polyelectrolyte film. For hemispherical crystals H

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Figure 8. (a) Calculated near-surface supersaturation for vaterite (σVS , yellow) and calcite (σCS , blue), and (b) estimated interfacial energy of vaterite (γv, yellow) and calcite (γc, blue) on PEI-films in the absence and the presence of additives: serine, glycine, aspartic acid (Asp), glutamic acid (Glu), glucose, mannose, and arabinose.

the near-surface supersaturation (σVS and σCs ) on PEI-films calculated with eqs. 6 and 9 for site saturation. Additive-Free Measurements. Figure S16a illustrates the good agreement between experimentally determined and calculated precipitation rate of vateritegiven as the volume fraction ϕ with time on PEI-films, assuming site saturation; the near-surface supersaturation is determined by the slope at large times in the steady state. The corresponding near-surface supersaturation that governs the growth of vaterite is σVS ∼ 3.0(0.4), and hence it is below the influent supersaturation (σVin ∼ 4.3). The large standard deviation is attributed to changes in pH. As noted earlier, bulk precipitation and the boundary layer are responsible for the drop in concentration close to the surface. We note that σVS is smaller than the supersaturation with respect to vaterite when the solution concentration is fixed by the solubility of ACC (σVACC ∼ 3.5) at pH 9.25. This suggests that the growth of vaterite is not dictated by ACC dissolution, which is consistent with flow imaging microscopy. The vaterite number density on PEI-films is about 5 times larger than on silica substrates. The PEI-film favors vaterite nucleation, perhaps by locally enhancing the concentration of the counterions (carbonate) that are electrostatically attracted to the protonated ternary amines in PEI with a surface charge of +3 nm−2 (−0.4 nm−2 for silica), similar to the scenario proposed by Smeets et al. in PSS.29 In fact, the lower growth rate of vaterite on silica compared to PEI-films (1.8 nm/s vs 5.2 nm/s) supports this argument. Further, active domains in polyelectrolytes take on structural conformations that actively bind counterions and they can act as preferred nucleation sites if a good interfacial match between the macromolecule and the crystal lattice is achieved.23,30,31 Note that ∼1 nm is the dry optical thickness, but the thickness of the hydrated polyelectrolyte can be in the range of ∼10 nm.63 This notably increases the probability of nucleation compared to a flat surface. Further, the PEI-film promoted vaterite nucleation, while only calcite was nucleated on silica (and glass). Vaterite was previously observed to form with linear PEI (with secondary amines), when calcium carbonate precipitation was induced via the diffusion method,25 but not for branched PEI with ternary amines, similar to the one used here, which promoted the formation of aggregated calcite rhombohedra. However, the solution conditions were very different, which can explain the different nucleation pathway in our experiments, as previously argued.22 Visible ACC clusters remained stabilized on PAH/PAA-films until the end of the experiment, indicating that the near-surface concentration was close to the solubility of ACC.22 In fact, the

measured growth rate of vaterite supports that the supersaturation is lower on PEI- than on PAH/PAA-films (∼5 vs ∼10 nm/s). However, despite the high supersaturation, the crystal density on PAH/PAA-films is about 1 order of magnitude smaller than on PEI-films (Figure 7a,b). This can be justified by the charge density of the polyelectrolyte films. For the PAH/PAA-film, it is well-known that part of the charge compensation occurs intrinsically, meaning that the positives charges of PAH (∼+4 nm−3) and the negative charges of PAA (∼−9 nm−3) partially compensate throughout the film, and only the net charge density (∼−5 nm−3) is compensated by the counterions (Ca2+) located within the upper region of the film.52 Hence, the charge density of the layer-by-layer film is reduced in comparison with a single-layer PAA-film. Higher binding strength and lower energy barrier for nucleation correlate with a decrease in charge of various polysaccharide templates,30 which was attributed to the reduction in hydrophilicity of the surface template. Since the charge density of PEI-films is smaller (∼+3 nm−3) than that of PAH/PAAfilms (∼−5 nm−3), a higher energy barrier for heterogeneous nucleation would be expected for PAH/PAA-films compared to PEI. Influence of Additives on Calcium Carbonate Precipitation on PEI- and PAH/PAA-Films. The additive influence on precipitation of calcium carbonate on PEI- and PAH/PAAfilms was demonstrated through changes in precipitation rate (Figure 6) and crystal number density (Figure 7). Figure 8a shows the near-surface supersaturation obtained by fitting the precipitation rate of calcium carbonate on PEI-films with the kinetics model (σVS , with respect to vaterite, in yellow; and σCS , with respect to calcite, in blue), the bars indicating the range for each parameter. All additives lead to a decrease of the nearsurface supersaturation with respect to the reference, which is consistent with the overall decrease in crystal number density. Several factors can justify the decrease in σVS compared to the reference (no additives).37,38 In fact, aspartic and glutamic acid can stabilize PNCs clusters,32 which is confirmed by the lack of turbidity of the effluent. Binding of additives to Ca2+ according to their association constant can further decrease the Ca2+ concentration. MINTEQ can predict the complexation between Ca2+ and some amino acids. At the pH of 9.25, in the presence of 10 mM glutamic acid, MINTEQ predicts the formation of 0.33 mM of Ca-glutamate that reduces calcium concentration and activity. Binding and the reduction of calcium activity is even stronger for aspartic acid because of its higher association constant.64 In the case of glycine, 0.168 mM of Ca-glycine+ complexes form in solution, i.e., weaker binding is predicted. A I

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similar effect is expected for serine,64 but a calculation was not possible because the association constants were not found. Calcium binding by the selected monosaccharides has been reported to be weaker than for amino acids due to the limited displacement of water in the hydration sphere of cations by the hydroxyl groups of the saccharides and to unfavorable steric arrangements.65−68 The main reason for the decrease in concentration by the monosaccharides is, thus, attributed here to the observed promotion of ACC nucleation in the bulk solution (turbidity of the effluent), especially by glucose, which rapidly decreases the solution concentration in the cell. Promotion of ACC nucleation in bulk solution by mannose and glucose has been previously reported,33 and explained to be induced by the enhanced aggregation between ion clusters. Arabinose was shown to stabilize PNCs at pH ∼ 9.75 in ref 33, but at the conditions of our experiments, it clearly promotes ACC nucleation in the bulk solution, as well. The precipitation kinetics on PAH/PAA-films is so slow that the equilibrium precipitation rate required to determine the near-surface supersaturation in steady state is not achieved during the experiment, and hence, supersaturation cannot be univocally determined. Although the decrease in Ca2+ activity induced by amino acids and monosaccharides and the stabilization of pre- or post-nucleation species are expected to be analogous to the experiments with PEI, the near-surface solution above the PAH/PAA-films is populated by ACC in presence of the monosaccharides and glycine, as shown by flow imaging microscopy; modeling attempts indicate that the measured precipitation rates are consistent with saturation of the near-surface solution with respect to ACC (Figure S19) with these additives. Interestingly, this suggests that the concentration at the organic interface is determined not only by the additive, but also by the surface-template properties, e.g., its charge density. The charge density is smaller for PEI- than for PAH/PAA-films, which would imply that lower near-surface supersaturation could be achieved on PEI-films, as we observe. About the Precipitation Pathway. According to the measured surface potential, all additives are expected to adsorb onto PEI- and PAH/PAA-films, and thus, they could theoretically participate on (heterogeneous) nucleation. Considering that the nucleation rate is given by31 IB =

PEI-films through the reduction of the interfacial energy to ∼94(11) mJ/m2. The estimated interfacial energy of vaterite at the organic interface is reduced by the adsorbed amino acids, arabinose and mannose (∼68(8)−86(16) mN/m in Figure 8b); the results for glucose should be taken into account with caution because they were very inconsistent, perhaps owing to the significant nucleation in the bulk solution. Interestingly, serine and glycine significantly reduce the interfacial energy of vaterite, which supports their adsorption on PEI, even if they do not alter the polymorph distribution. The estimated interfacial energy of calcite on PEI-films is higher than that of vaterite (125(10) mN/m in the absence of additives), in good agreement with literature, and it is reduced to 109 and 114 mN/m with glutamic and aspartic acid, respectively. The reasonable values for the interfacial energy obtained from the IB vs σS relation suggest that the nucleation of vaterite and calcite on PEI-films is consistent with classical nucleation theory, also in the presence of the selected additives. Although the exact role of ACC on nucleation cannot be directly observed in our experiments, we speculate that the decrease in nucleation barrier by the PEI in conjunction with additives could have prevented the nonclassical nucleation path to be followed. On PEI-films, the lower interfacial energy could facilitate direct nucleation of vaterite. Adsorbed additives to the polymer could further lower the interfacial energy of the organic interface, and alter the surface chemistry upon adsorption, thereby promoting a different polymorph, e.g., more calcite in the case of aspartic and glutamic acid, or still vaterite by serine and glycine. The interfacial energy of calcite and vaterite can be roughly estimated on PAH/PAA-films assuming σvs = 3.5, and it yields ∼131 and ∼104 mN/m, respectively, i.e., still consistent with classical nucleation theory; note that 125(10) mN/m and 94(10) mN/m were obtained on PEI-films, i.e., a bit smaller, indicating a lower nucleation barrier on PEI. Flow imaging microscopy also shows stable ACC above PAH/PAA-films with the three monosaccharides and glycine. Accordingly, the interfacial energies can be estimated, yielding ∼132 and 106 mN/m for calcite and vaterite, respectively, and hence, they remain unchanged, in contrast to the results with the same additives on PEI-films. This result might just be caused by a weak adsorption of the additives to PAA, and hence, it still requires further investigation. On the other hand, the higher interfacial energy, charge, and hydrophilicity of PAH/PAA-films could be the key to stabilize highly hydrated and lower interfacial-energy solids, e.g., ACC. ACC stabilization seems to correlate with a low precipitation rate on this surface template. Furthermore, the stabilization of PNCs by aspartic acid, glutamic acid, and serine seems to interfere with ACC stabilization by this organic interface, which greatly hinders precipitation. This suggests that ACC is directly involved in the precipitation pathway on PAH/PAA-films, and in the absence of ACC, precipitation is hindered. Other additives like monosaccharides and glycine do not alter ACC stabilization and interfacial energy, but they can influence the nucleation pathway by altering either the ACC structure or the surface chemistry for nucleation. It is also possible that surfacestabilized ACC on PAH/PAA-films could become a precursor for calcite and/or vaterite to surpass the higher energy barrier of this template, but our results do not provide any proof for this.

⎡ 256Ω2γ 3 ⎤ 3kT ⎥ exp⎢ − 5/3 ⎣ 27(kT )3 (σS)2 ⎦ πΩ η

where k is the Boltzmann constant, T the temperature, η the solution viscosity, and Ω the molecular volume, the interfacial energy γ of vaterite and calcite can be estimated with the fitted near-surface supersaturation. The surface density NB is related to IB through the time span, which is unknown. However, we note that changing the nucleating time from 0.1 to 5 min only changes the interfacial energy by 3 mN/m, and hence, we have assumed 1 min for the following estimations but we are aware about this uncertainty. For vaterite on PEI-films, γ is estimated to be ∼94(11) mJ/m2. Interfacial energies of vaterite in solution have been reported to be between 14 and 220 mJ/ m2,69−71 and hence, our values are well within the range. The interfacial energy of calcite in solution was reported to be ∼97− 160 mJ/m2 and to decrease to ∼72−81 mJ/m2 for growth on a surface template with carboxylic groups,22,31,69 indicating that the organic template can reduce the interfacial energy of calcite. Similarly, surface nucleation of vaterite could be favored on J

DOI: 10.1021/acs.cgd.6b00514 Cryst. Growth Des. XXXX, XXX, XXX−XXX

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precipitation rate, and this provides an estimation of the nearsurface supersaturation, and thereby, of the interfacial energy of vaterite and calcite. The results demonstrate the active role of both organic interface and organic solute on heterogeneous nucleation. Calcium carbonate mineralization is central to many natural processes occurring at or near the Earth’s surface. Complex proteins and other organic matter are involved in the mineralization process and the multiple interactions among the relevant players (ACC, water, ions, organic solutes and organic interfaces, and crystals) create a complexity that is key to determining the precipitation pathway. While surface chemistry is strongly simplified in our work by using model polyelectrolytes, certain complexity has been introduced through the entanglements between two polyelectrolytes with different functional groups and opposite charge; nature is even more complex. This work provides guidance to mechanistically understand the effect that organic matter can have on mineralization with implications on diverse fields ranging from design of biomimetic materials to understanding better biomineralization and the evolution of the Earth’s lithosphere.

It is also interesting that both vaterite and calcite nucleate on PAH/PAA-films. Nucleation of calcite on PAH/PAA-films is not surprising considering that acidic templates have been reported to promote proto-calcitic ACC.32 However, it is unlikely that the stabilized ACC is only a precursor of calcite, since as shown earlier, in the presence of glycine and arabinose, ACC was largely stabilized on PAH/PAA-films, but these additives did not promote calcite precipitation. Carboxylicterminated SAMs have also been shown to control crystal nucleation (surface density and plane)23 owing to the strong interaction between the carboxylic group and calcium, and under specific conditions to promote the epitaxial growth of calcite.72,73 Obviously, such an ordered nucleation and growth cannot happen within the carboxylic-rich polymer of this study, since macromolecules adopt a self-avoiding walk configuration to maximize their configurationally entropy, i.e., the disorder. In fact, the molecular weight of the polymer (macromolecule) has been shown to have a significant influence on the crystallization pathway,38 which can deviate from that on SAMs of small molecular-weight molecules. The nucleation of vaterite and calcite on PAH/PAA-films could indicate the presence of two different nucleation sites in the film or/and of two nucleation pathways. Since the two polymers, PAH and PAA, are expected to entangle with each other to partially satisfy their opposite charges within the film, a relevant amount of amine groups from PAH chains is present within the PAA layer.74 Perhaps, alternating charges and local changes of pH,17,55,75,76 i.e., local heterogeneities within the film with two functional groups, could be responsible for the observed polymorph distribution. This is an interesting suggestion that requires further investigation. This work highlights the complexity in the control that organic interfaces and solutes exert on surface mineralization. Our studies support previous work that remarks that an organic interface strongly affects nucleation, and can modify the precipitation pathway with respect to that happening in the bulk solution, for example, if it leads to a decrease in interfacial energy. The role of the additive is not limited to the crystal morphology, as previously proposed for complex systems (proteins), but it can be directly involved in heterogeneous nucleation, providing that a strong interaction with the organic interface exists. Nature might control the nucleation pathway by tuning the surface chemistry, e.g., via the adsorption of specific solutes on an organic interface, and thereby, altering the interfacial energy. Higher-interfacial-energy organic templates might impose an ACC-mediated pathway to crystallization, which can also be tuned by specific solutes. Our future work will be focused on providing more evidence for these suggestions.

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ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.cgd.6b00514. Calculated supersaturation by Visual MINTEQ, polyelectrolyte adsorption measured by TInAS, parameters for the calculation of the charge density of the polyelectrolyte films, size and surface potential of PEI and PAA, microscopy images of surface-precipitate, number of detected crystals as a function of time and representative image of bulk precipitate in flow imaging microscopy experiments, ACC dissolution during rinsing steps, Raman microspectroscopy of surface precipitate on PAA/PAH-films, absorbance raw data for the two polyelectrolyte films and for the glass substrate (reference), AFM and SEM images, time-evolution of crystal polymorphs on PEI and PAH/PAA-films, and representative fits to measured precipitation rates (PDF)

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AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. Tel: +1 217 607 3856. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This material is based upon work supported by the National Science Foundation under Grant No. CMMI-1435920. We also thank Yijue Diao for her help with Atomic Force Microscopy Imaging and DLS measurements, and Dr. Manfred D. Heuberger, Dr. Nicholas D. Spencer, and Martin Elsener for their support with the installation of TInAS at UIUC.

CONCLUSIONS Surface chemistry and additives are combined in an attempt to provide a general conceptual picture of biomineralization in which synergistic and competitive effects can be involved. We study surface-directed mineralization through high-resolution absorbance measurements and imaging microscopy to obtain the precipitation rate of calcium carbonate on various substrates and the polymorph distribution. Although the surface template plays an important role on determining the stable polymorph (mainly vaterite under the conditions of our experiments), as reported in other studies, we show that additives can also play a role in nucleation on the two (distinct) selected organic interfaces. We also propose a model to predict the surface-

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