Gel-Like Calcium Carbonate Precursors Observed by in situ AFM

Dec 6, 2016 - Departamento de Física, Universidad de Santiago de Chile, Avenida Ecuador 3493, Estación Central 9170124, Casilla 307, Correo 2, ...
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Gel-Like Calcium Carbonate Precursors Observed by in-situ AFM Stefan Leo Philipp Wolf, Leonardo Caballero, Francisco Melo, and Helmut Cölfen Langmuir, Just Accepted Manuscript • DOI: 10.1021/acs.langmuir.6b03974 • Publication Date (Web): 06 Dec 2016 Downloaded from http://pubs.acs.org on December 10, 2016

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Gel-Like Calcium Carbonate Precursors Observed by in-situ AFM Stefan L. P. Wolf[†], Leonardo Caballero[‡], Francisco Melo[‡] and Helmut Cölfen[†]* [†] Physical Chemistry, University of Konstanz, 78457 Konstanz, Germany [‡] Departamento de Física, Universidad de Santiago de Chile, Avenida Ecuador 3493, Estación Central 9170124, Casilla 307, Correo 2, Santiago, Chile Supporting information is available online

ABSTRACT: The debate about crystallization processes is still ongoing and non-classical crystallization mechanisms attract more and more attention. This work indicates that polymer induced liquid precursor (PILP) phases play a role for non-classical calcium carbonate crystallization and growth processes. Here we report the observation of gel-like precursors for the crystal growth on a calcite surface by means of an in-situ AFM study. These precursors spread out on the surface with time supporting their liquid character. This study will give new insights into biomineralization and crystallization processes in general.

The understanding of crystallization processes is of great significance for many fields of science and industry. The applications in industry range from purification over crystal engineering in pharmacy to the inhibition of nucleation events in pipelines.1, 2 Also the shape of colloidal particles, e.g. in pigments or varnishes, is very important for the processability of the final product.3 In nature, crystallization is essential for survival of many organisms. In the process of biomineralization, organisms are able to build carapace, spines, or in the case of vertebrates teeth or bones of complex shapes and most importantly with enhanced mechanical properties.4, 5 The formation mechanisms behind these complex shapes are still rarely understood and are still under debate.6-8 As the most abundant biomineral, calcium carbonate attracts the most attention of scientists. For over a century biomineralization was explained by means of classical nucleation theory – and calcium carbonate was the prime example for this theory – albeit it shows a huge discrepancy to experimental results.9-11

In contrast to that, Gebauer et al. demonstrated a cluster based nucleation pathway for CaCO312-14 named "non classical nucleation". Also, the subsequent crystal growth can follow non-classical crystal particle based pathways15 including oriented attachment16, 17 or mesocrystal formation.18, 19 This novel view also includes the presence of liquid precursors and amorphous intermediates.20-23 Such intermediates are long-time known to appear in protein crystallization as well.24 Gower et al. were the first to observe liquid like precursors for CaCO3 in the presence of Poly(aspartic acid) and named them therefore “polymer induced liquid precursors” (PILP).25-27 The postulation for a liquid-like species by Gower et al. was mainly based on the observation of thin films forming on a glass substrate.25 Bewernitz et al. showed by means of NMR spectroscopy the presence of different carbonate species in solution where the diffusion coefficient was correlated to a liquid dense phase.23 They also stated that such liquid precursors are also present without any additive so that they should be referred to polymer-stabilized precursors.23, 28-30 Such precursors are also intermediates in the crystallization of amino acids or other small molecules like dyes and in these cases, the liquid precursors could be isolated by centrifugation.3, 31 Nevertheless, a direct observation of liquid precursors for calcium carbonate or any other inorganic crystal system was not possible. However, molecular dynamic simulations indicate that such liquid species are present in nucleation events.29, 32 PILPs can be used for crystal growth by the addition of liquid precursors to a substrate or a seed crystal.33 A nanoscopic observation of the growth

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mechanism of such liquid precursors is, however, still an open challenge. To investigate these liquid precursors we used in-situ atomic force microscopy (AFM). It is a well-established technique to observe interactions of proteins or small molecules with different surfaces.34-36 In situ AFM is also well suited to observe crystal growth processes directly in solution.37-39 In this study, the growth behavior of liquid-like species on a calcite {104}5 surface was observed using in situ AFM. Experimental All used chemicals were of analytical grade and used without further purification. The growth solutions were prepared by adding 0.1 ml of a 0.01 M NaOH solution to 5 ml of a 0.01 M solution of calcium chloride. Afterwards a volume of 0.06 ml of a 1 mg/ml PAA (M = 1200 g/mol) was added to the solution under stirring. Finally, 0.2 ml of a 10 mM NaHCO3 solution was added to the reaction mixture. Note that the solution is still clear and shows no precipitate. Test experiments were carried out by depositing the solution onto a freshly cleaved calcite crystal (Ward 's Scientific, Chihuahua, Mexico), and by following the dynamics of cluster formation through atomic force images in the tapping mode. The selected surface is the plane {104} of the calcite crystal. Small crystals of 2mm by 2mm side and 0.5mm thickness were obtained by cleavage. Through the inspection under the optical microscope, crystals exhibiting the smallest amount of macroscopic terraces in the {104} face were selected for experiments. Each crystal sample was fixed at the center of a circular glass plate, 15 mm in diameter and 1 mm in thickness by a small wax droplet. In addition, this plate serves as the bottom lid of the fluid cell. Solution is injected by means of a syringe pump. A force volume technique in the tapping mode was used to obtain force curves. Force data were obtained automatically in a 64x64 grid and at 60 nm steps resolution (total scan area of about 4 µm x 4 µm). Every row was obtained at a rate of about of 1/min. Approaching and retraction speed was 1.5 µm/s. For tapping images an OTR8 (from Bruker) cantilever of 0.15 N/m spring constant and reflecting coating were used.

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Results and Discussion The liquid-like precursors are synthesized by the simple mixing of poly(acrylic acid), calcium chloride and sodium bicarbonate (cf. Experimental). Directly after mixing deposition of precursors on the calcite surface can be observed. The properties of these droplets are still not completely investigated due to the small existence region in the phase diagram and their instability. To examine in some detail the properties of the precursors, we first performed an indentation type test. Figure 1 presents a typical precursor profile over which force curves are obtained. Forces are presented as function of the distance between the hard substrate and the cantilever tip. It is seen that in all sectors of this precursor, the approaching curves show a small but abrupt attraction that occurs when the tip makes contact with the precursor surface. This is an indication of the existence of adhesion between the tip and the precursor. After this contact, the precursors deform elastically if they are thin enough, which is seen since the force increases with decreasing tip surface distance.

Figure 1 Height image of one precursor droplet (top) and the corresponding height profiles immediately after solution infiltration.

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Figure 2 In-situ AFM height (a & d), phase (b & e) and adhesion images (c & f) of a calcite surface shortly after infiltration of the solution. Numbers in the force-distance curves label the circles in the AFM height and phase images. Circles 2 & 5 show a clean calcite reference surface. Blue: approach to the surface, red: tip retraction from the surface. (small drift downward, visible in panels c and f, is because adhesion maps are not taken simultaneously with height and phase images

Note that the force increases very rapidly when the tip gets closer to the underlying calcite crystal that is much harder than the precursor. In general, thicker areas of the precursors are more easily indented by the cantilever tip and are prone to exhibit large hysteresis in the force curves (see SI Figure S1 for force distance curves at the different positions of the droplet.).

In Figure 2, the addition of the new species to the calcite {104} surface at very early stages is presented as observed by in situ AFM at lower magnification. In the height images, (a) and (d), some plain spots indicated by the white circles (1, 3, 4, 6, 7 & 8) can be seen. Careful inspection of these regions shows relatively smooth surfaces compared to the surrounding surface.

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The newly appeared species show a softer behavior clearly visible in the phase image as indicated in Figure 2(b) and 2(e) (circles 1, 3, 4, 6, 7 & 8). The force-distance curves (1 to 8; related to circles 1-8) show a different behavior for the approach (blue) and the retract (red) curves, which is not observed for the “clean” surface (circles 2 & 5).

Figure 3 the time evolution of precursors followed during 6 days (Day 1: after 2h of solution infiltration). Each row indicates AFM 2 images of height, phase and adhesion maps (at resolution of 128x128pixels ). The adhesion map is made by plotting the force of adhesion, Fadh at each point. Corresponding adhesion histograms and typical force curves are also shown. Lowest row indicates time evolution of total width of zone 1 and the thickness of precursor layer as defined in the right panel.

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This feature can be explained by a gel-like structure where the AFM-tip is adhered by the growing species. The adhesion images, Figures 2(c) and 2(f), constructed by extracting, at each point the adhesion energy, Wad from the adhesion force Fad (see Supporting Information), perfectly correlate to the phase images and smooth area in height images. In detail, first when the AFM-tip approaches the species on the surface, the tip slightly compresses the nanosized species until it hits the underlying calcite surface (4 & 6). During the retraction step, the tip is going the same way back but a significant adhesion force is observed before leaving the new growth species. This adhesive behavior is not observed for the clean surface, Figure 2(b) and 2(e), circles 2 and 5, and can be explained assuming a gel-like behavior of the precursors. We notice that none of these features are observed in control experiments performed on calcite surface under the conditions described above but in the absence of PAA. Similarly, further controls performed with all components, with exception of NaHCO3, did not show the presence of soft droplets. Approaching force curves such as 4 & 6, allow for the estimation of the Young modulus, YP, of the precursors through a fitting procedure (cf. Supporting Information). We obtained YP = 2 MPa, which is about two orders of magnitude lower than that of a relatively soft rigid material but is in the typical range of hydrogels like for example 0.91 +/- 0.14 MPa for a poly(acrylic acid) hydrogel.40 Interestingly, the shape and the range of the penetration in curves 2 & 5 (zones free of precursors) indicate the presence of a thin and soft layer of Calcite of thickness about 10 nm (for details see supplemental material). The Young’s modulus of this layer is about 10 MPa, and this softness can be attributed to the crystal roughness developed during the surface solution contact. However, other effect can not be ruled out. Notice that force curves 1, 3, 7 & 8, do not reveal a soft layer in approaching because the precursors are very thin in such areas. However, a strong adhesion in retraction is clearly visible. A complete exploration of the distribution of stiffness and

adhesion over the surface of a single precursor is given as Supporting Information. In order to check the mechanical stiffness of macroscopic samples of Calcite type gels, PAA-CaCO3 hydrogels where prepared,41 using PAA of large molecular weight (Mw ~ 100,000 g/mol), and independent measurements of Young’s modulus were performed. Slopes extracted from stress versus strain curves lead to values of Young’s modulus in the range of 50kPa (cf. Supporting Information), which is significantly smaller than values obtained for droplets through indentation methods. This difference in bulk modulus is likely due to the fact that calcium carbonate hydrogels, based on large molecular weight PAA, are spongy structures compared to precursors droplets. To compare the growth behavior of these gel-like structures with the results reported by Gower et al. for the thin film formation by the PILP phase, the solution was kept over several days on top of the calcite surface and analyzed again by in-situ AFM. The obtained results are shown in Figure 3. After the solution is injected into the cell, the slow evolution of the surface is followed through atomic force images in the tapping mode and indentation series for six days. A set of data is taken every day (data for day 1 are taken 2h after injection) and force curves analyzed. Each raw image in Figure 3 presents AFM images indicating height, phase and adhesion map, followed by the adhesion histogram and typical force curves in approaching and retraction. Adhesion diminishes with time. However, analysis (not shown) of height images, in low 2 resolution (128x128pxl ) indicates roughly that while no significant change of the precursor diameter occurs in time, the surface roughness diminishes by a factor 2 within a period of 6 days. As precursors age, force curves present interesting features (see rightmost panels in Fig. 3). In approaching a first zone (zone 1) in which the force grows linearly with penetration progressively develops. As the tip approaches further, a different zone in which the force increases very rapidly with penetration is clearly visible (zone 2). The latter can be associated with a plastic zone due to the progressive penetration of the tip into the precursor through plastic deformation whereas the former is expected to result from either elastic or hyper elastic deformations. The strong increase of

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the force in zone 2 is then due to the tip reaching the hard substrate. These two zones are also observed in retraction. Different zones and force features are summarized in lower panels in Fig. 3. The lower panel in Figure 3 shows that both, the total width (zone1 plus zone2) and the width of zone1, increase with time. Since force is sensitive to both, the first contact with the surface and the hard substrate, it is natural to identify the extension of the penetration force as the thickness of the layer precursor. Simple analysis of these quantities in time (lower panels, fig.3) indicates that thickening of the precursors takes place at a rate of about 1.4 nm/hr. It is worth noting that the long range of the force on retraction curves indicates that the precursor surface can deform significantly under pulling before tip detachment actually occurs. An estimate of this deformation can be obtained by subtracting δtotal in approach to δtotal in retraction. From the corresponding panels in Fig. 3, we see that these distances differ in about 50nm. This is consistent with the observation of a relatively high adhesion and the soft character of precursors. Indeed, through a rough estimate, from maximum adhesion force (5nN) and tip size (about 20nm), we found that the tensile stress near the tip can reach values greater than 10MPa, which implies that typical strain is very large (given the relatively low value of the measured YP of about 1MPa), which would produce precursor elongation likely exceeding the typical distance of the problem (tip radius of curvature). In order to follow in time the mechanical feature of the softer layer of zone 1, we define a relative stiffness of this layer as the slope of force penetration curve K=ΔF/Δδ, (see fig. 3, lower panel, for definition). At early stages of growth by precursors, the average of K is about 0.02 N/m and fluctuates significantly. However, fluctuations decrease and stabilize to about 20% after the day 2. Overall, average K does not change with time, and its value is kept close to 0.02 N/m, suggesting that the growth continues by addition of precursors on top. It is worth noting that further analysis42 of force curves demonstrated that Young’s modulus of precursors surfaces ranges from 1 MPa to 2 MPa, which is close to the average value obtained from fit of force curves in the case of thin precursors.

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These observations are in complete agreement with the postulated mechanism by Gower.25 Furthermore, such a crystal growth cannot be explained by the classical Kossel layer by layer growth43 because an ion-by-ion growth mechanism would lead to distinct layers with steps or kinks rather than to complete precursor species addition in the micrometer range. Conclusion In conclusion, we showed here for the first time that gel-like precursors – which were likely liquid before they encountered the surface – are a possible crystal growth species in inorganic crystal systems, like they appear in protein crystallization where such intermediates are well known.44 This supports a non-classical crystal growth pathway involving micron-sized species as materials reservoir for crystal growth. Such liquid growth species would be a possibility to explain the growth of the elaborate and complex biomineral architectures and also be a unique precursor to realize a plethora of complex shapes of synthetic crystals.

ASSOCIATED CONTENT Supporting Information Information about the calculations of the Young’s modulus sample preparation and precursor analysis. This material is available free of charge via the Internet at http://pubs.acs.org

AUTHOR INFORMATION Corresponding Author E-mail: [email protected]

Present Addresses [‡]

S. L. P. Wolf , Prof. Dr. Helmut Cölfen Physical Chemistry University of Konstanz Universitätsstr. 10, 78457 Konstanz (Germany) [‡]

L. Caballero , Prof. Dr. F. Melo Departamento de Física Universidad de Santiago de Chile, Avenida Ecuador 3493, Estación Central 9170124, Casilla 307, Correo 2, Santiago (Chile) .

Author Contributions ‡These authors contributed equally.

Notes The authors declare no competing financial interests.

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ACKNOWLEDGMENT We gratefully thank the DAAD for support of this work within the ALECHILE program project ID 56236541. We thank José Luis Arias Bautista for fruitful discussions on the experimental data. F. Melo and L. Caballero kindly acknowledge Anillo ACT1412 Conicyt-Chile for support.

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43. Kossel, W., Zur Energetik von Oberflächenvorgängen. Annalen der Physik 1934, 413 (5), 457-480. 44. Kuznetsov, Y. G.; Malkin, A. J.; McPherson, A., The liquid protein phase in crystallization: a case study—intact immunoglobulins. J. Cryst. Growth 2001, 232 (1–4), 30-39.

Liquid-like precursors sediment on a surface and start to densify over time to thin film on the surface. This behavior served by in-situ AFM.

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calcite generate a was ob-