Additive Speciation and Phase Behavior Modulating Mineralization

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Additive Speciation and Phase Behavior Modulate Mineralization Ashit Rao, Yu-Chieh Huang, and Helmut Cölfen J. Phys. Chem. C, Just Accepted Manuscript • DOI: 10.1021/acs.jpcc.7b02635 • Publication Date (Web): 07 Sep 2017 Downloaded from http://pubs.acs.org on September 12, 2017

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The Journal of Physical Chemistry C is published by the American Chemical Society. 1155 Sixteenth Street N.W., Washington, DC 20036 Published by American Chemical Society. Copyright © American Chemical Society. However, no copyright claim is made to original U.S. Government works, or works produced by employees of any Commonwealth realm Crown government in the course of their duties.

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The Journal of Physical Chemistry

Additive Speciation and Phase Behavior modulate Mineralization ASHIT RAO†,‡, YU-CHIEH HUANG†,, AND HELMUT CÖLFEN*,†, †

Physical Chemistry, Department of Chemistry, Universitätsstr. 10, University of Konstanz,

Konstanz 78464, Germany. ‡

Freiburg Institute for Advanced Studies, Albert-Ludwigs-Universität Freiburg, Freiburg 79104,

Germany.

ACS Paragon Plus Environment


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ABSTRACT Natural and synthetic composite materials as yet elude a complete understanding of formation mechanisms from organic and inorganic constituents. Addressing the interactions between organic additives and metastable inorganic precursors during mineral nucleation and growth is a critical challenge. In this study, we elucidate additive-controlled mineralization by a novel approach for the in-situ continuous monitoring of a widely-applied diffusion-based methodology, assisted by the quantitative assessment of mineral nucleation. The formation of amorphous superstructures is attributed to a complex interplay between mineral species and additives viz. ions, ion-clusters and mineral precursors as well as a unique phase behavior of the additive molecules relative to the maturing mineral phase. A pH-dependent conditioning of nucleation and demixing of transient liquid-like additive-ion complexes are shown to play critical roles in tuning mineral architecture. Thus, the modulation of mineral precursors and mineralization conditions by additive species determine material composition and morphology.


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INTRODUCTION Additive-controlled nucleation and growth often produce intricate morphologies that are atypical of geological euhedral counterparts.1-2 The complex architectures underlying synthetic and biogenic minerals lead to interesting physical properties.1, 3-4 Although the properties of synthetic composites are approaching those of biogenic counterparts, a limited understanding of the mechanisms underlying natural and chemical routes represents a lacuna in the field of material science.5-10 Therefore a holistic understanding of the stages of material formation viz. nucleation, phase transformation, oriented attachment and the subsequent schemes of crystallization can offer an enhanced control over material properties such as composition, shape and structure.11 Bio-inspired materials frequently utilize calcium carbonate (CaCO3) as a model system because of its prevalence as an inorganic constituent in biogenic minerals.2 Further CaCO3 is industrially relevant as a construction and filler material and also in scale formation. Of its several forms, amorphous precursors of CaCO3 are adeptly utilized by Nature to produce minerals with fascinating morphologies and orientations.10, 12-14 This is exemplified by the fine structure of the calcitic sea urchin skeletal elements and hierarchical aragonitic biominerals.15-18 The associated structure-property relations have inspired synthetic counterparts with remarkable physical properties such as materials mimicking the hierarchical organization of nacre and microlens arrays motivated by skeletal elements.19-24 However due to the dynamic nature of organicinorganic interactions as well as the metastable nature of intermediate phases, the formation mechanisms of mineral structures remain debated. Of the several methods for CaCO3 synthesis (including the double diffusion25 and Kitano26 routes), gas diffusion is a widely applied technique for investigating additive-controlled crystal growth. During gas diffusion, mineral precipitation is achieved by exposing a mixture of Ca2+ ions and additives to decomposing



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ammonium carbonate in a desiccator. Seemingly simple, crystal growth via gas diffusion is susceptible to multiple factors including the rate of ammonium carbonate decomposition, desiccator volume, the gas-liquid interfacial area, initial Ca2+ concentration and stirring conditions, which together affect nucleation rates and supersaturation.27-28 Notable observations derived by applying this methodology include additive concentration dependent polymorph behavior29, crystal organization by oriented attachment30-31 as well as modulation of phase transitions and crystal morphology under confinement32-33. Of the several fascinating morphologies achieved by the gas-diffusion approach, hollow superstructures composed of amorphous CaCO3 (ACC) formed in the presence of inositol hexakisphosphate (IP6, phytic acid) are particularly interesting.34 Previous studies have reported crystalline calcareous hollow structures formed in the presence of double-hydrophilic block copolymers (DHBCs) and mixtures of DHBCs and surfactants.35-36 However in presence of IP6, unique material features are identified including a hollow spherical structure, enhanced stability of an amorphous mineral phase as well as a template-free synthesis approach.34 Alternative methods for the production of hollow particles typically require multiple steps for the removal of the particle core by chemical or physical treatment.37-39 In order to address the mechanisms underlying IP6-mediated superstructure formation, we describe the role of IP6 on the early stages of mineralization encompassing ion-complexation, interactions with ion-clusters, mineral nucleation and additive speciation, thereby providing a better understanding for the selective emergence of material composition and shape. To the best of our knowledge, this study presents novel in situ quantitative measurements of the free Ca2+ ion fraction for addressing the dynamics of additive-controlled mineral growth in the standard gas-diffusion methodology, circumventing tedious time-based sampling.


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EXPERIMENTAL SECTION Materials. For titration experiments, calcium chloride (CaCl2, Fluka, 1 M), sodium hydroxide (NaOH, Alfa Aesar, 0.01 M), hydrochloric acid (Merck, 1 M solution), sodium bicarbonate (anhydrous NaHCO3, Aldrich, ACS reagent), sodium carbonate (Na2CO3, Riedel de-Haën, ACS reagent),

and

sodium

chloride

(VWR

Prolabo,

99.9%)

are

used.

myo-Inositol

hexakis(dihydrogen phosphate) from Sigma (CAS Number 83-86-3) is used as the mineralization additive. Potentiometric titration. Potentiometric titrations are done by using an automated titration setup (Metrohm GmbH, Germany) operated by a software (Tiamo v2.2, Metrohm GmbH, Germany).40-41 During these experiments, the solution pH and free Ca2+ concentrations are continuously monitored by a flat membrane glass electrode (Metrohm, No. 6.0256.100) and a polymer-based ion-selective electrode (ISE; Metrohm, No. 6.0508.110), respectively. Calcium chloride (10 mM) solution is dosed at a constant rate of 0.01 mL/min to carbonate buffer (10 mM, 20 mL) under constant stirring at 800 rpm. A fixed pH is maintained by the automatic counter-titration of NaOH (10 mM). The Ca2+-ISE is calibrated by titrating CaCl2 into water. Samples collected at different time intervals are centrifuged at 16000 g for 30 min and the free IP6 contents in the supernatants are estimated by using a colorimetric assay.42 Development of pH and free Ca2+ ions during gas diffusion. The experimental set-up for continuous in situ monitoring of solution pH and free Ca2+ ion concentration uses (A) a pH electrode (Metrohm, No. 6.0256.100) and (B) an ion-selective electrode (Metrohm, No. 6.0508.110), respectively. Solutions containing CaCl2 (10 mM) and IP6 (7.5 mM) and also appropriate reference solutions are applied for mineralization. Details of the experimental set-up are provided in Figure S1. Samples from the gas diffusion experiments are quenched using



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absolute ethanol43 and analyzed using a Perkin Elmer Spectrum 100 spectrometer operated in an attenuated total reflection configuration. Sample compositions are analyzed by means of thermogravimetric analyses (TGA, Netzsch, Selb, Germany). Measurements from 293 to 1273 K are performed at a heating rate of 5 K/min under a constant oxygen flow. Infiltration of mineral precursor in pores of track etched membranes. Polycarbonate tracketch membranes (pore size 5 µm, IsoporeTM, Millipore) are infiltrated with the ethanol quenched product of a gas diffusion reaction performed for 1 h. The infiltrated membranes are washed with ethanol and placed in a humidified closed desiccator containing a vial of ammonium carbonate. After incubation (16 h), the membranes are washed with water and dissolved by sonication in dichloromethane. Resultant particles are analyzed by TEM using a Libra120 (Zeiss SMT, Jena Germany) instrument operated at 120 kV with a beam current of about 4 µA.

Figure 1. Developments of free Ca2+ ions in aqueous solutions without IP6 (black continuous) and with 75 µM IP6 at pH 7 (gray continuous), pH 8 (gray dotted) and 9 (gray dash-dot).


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RESULTS AND DISCUSSION Ion-complexation and IP6 Speciation. By continuously monitoring the development of free Ca2+ content using an ion-selective electrode at constant pH, we assess ion complexation by IP6 earlier described44 as:

+ 6 ⇋ 6 + 2

(1)

Consistent with previous studies45-46, the complexation of Ca2+ ions is found to be pH-dependent with increased binding capacities at higher pH values. From the offset in initial development of free Ca2+ ions, a maximal value of about 5.1 Ca2+ ions bound to an IP6 species is determined at pH 9.0. At pH 8.0 and 7.0, about 4.4 and 1.8 Ca2+ ions bind to an IP6 molecule, respectively (Figure 1). A lower than expected complexation (i.e. 6 mol Ca2+ for each mol of IP6) is attributed to the pH-related speciation of phosphate groups to dianion forms as well as the conformational constraints of binding sites.47 At pH 9.0, the most abundant species (IP6-11H; IP610

H2; IP6-9H3) present partially deprotonated phosphate groups (Figure S2). The co-existence of

multiple IP6 species with distinct states of deprotonation may contribute to a ‘polymer structure’ wherein Ca2+ ions lead to the bridging of metal-IP6 complexes.48-49 Given that pH governs the nature of intermediate mineral phases,43, 50-51 its additional role in tuning additive speciation and related poly-/flexi-dentate interactions appears crucial. Therefore we probe the effects of IP6 on mineral nucleation under conditions of constant pH. Assessing Mineral Nucleation. Since early mineral events are key to understanding biogenic and synthetic mineral structures52-53, we quantitatively assess the effects of IP6 on CaCO3 nucleation.40 Plots representing the development of free Ca2+ ions are evident of the potent inhibition of nucleation by IP6 (Figure 2). The inhibitory activity is quantified from a scaling



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factor (F) value, which is defined as the quotient of the mean time required for the nucleation in presence of an additive and that of the corresponding reference.54 At pH 9.0, F values of 1.8 and 2.8 are estimated at 7.5 and 75 µM IP6, respectively. With 750 µM IP6, nucleation is not observed for extended periods in experiments conducted up to 22 h. The estimated ion-binding capacity in carbonate-free solutions at pH 9.0 is inconsistent with the degree of inhibition towards mineral nucleation. Therefore there are contributions from multiple factors for the delayed onset of nucleation such as an additive-mediated colloidal stabilization of mineral precursors.6, 41, 54 At pH 9.75, IP6 has similar effects towards nucleation for which F values of 1.9, 2.2 and 3.4 are estimated at 7.5, 75 and 750 µM additive concentrations, respectively for primary nucleation. At higher IP6 concentrations, secondary nucleation events are prominent (arrows, Figure 2B). Corresponding F values of 4.1 and 5.8 are observed at 75 and 750 µM IP6, respectively for the secondary nucleation events. This shows that primary as well as secondary nucleation of mineral particles are inhibited by IP6 in a concentration dependent manner. Observations of secondary nucleation for certain anionic additives (such as poly(acrylic) acid and sodium tripolyphosphate) suggest a preferential adsorption of additives to pre-nucleation clusters in comparison to the nucleated mineral particles.41 During the formation of a mineral phase, the released additive molecules transiently stabilize ion clusters formed during the continuous addition of Ca2+ ions to an excess of carbonate species.41 To validate this hypothesis, we apply a colorimetric method to estimate the development of Ca2+bound IP6 contents in course of titration-based mineralization (Figure S3, S4). During the prenucleation stage, the binding of Ca2+ ions by IP6 species attains a maximum and decreases prior to the primary nucleation event. This reflects a competitive association of Ca2+ ions with additive


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molecules and carbonate species, favoring ion-association towards the onset of nucleation, which may be expressed as: 6 + ⇋ 6 +

(2)

Figure 2. Development of free Ca2+ concentration in carbonate buffer for titrations performed at (A) pH 9.0 and (B) pH 9.75. Plots represent experiments without additive (black) and with varying content of IP6 viz. 7.5 µM (continuous gray), 75 µM (dotted gray) and 750 µM (dash-dot gray). However the titration profiles suggest the intermediate existence of organic-inorganic complexes consisting of Ca2+ ions as well as carbonate and additive species. This is supported by the inhibition of nucleation by IP6 being inconsistent with the estimated degree of Ca2+ ion complexation, the emergence of secondary nucleation events and the distinct developmental trends of bound Ca2+ in reference and IP6-containing titrations during the pre-nucleation stage (Figure S5). The formation of these organic-inorganic complexes is represented as:

+ + 6 + + ⇋ 6 + 2 +

(3)

where (i.e. x>0, z>0 and x>z). Therefore the decrease in bound IP6 prior to nucleation reflects a phase behavior of additive species based on the displacement of IP6 from additive associated



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Ca2+ ions and ion clusters (Figure S4). Additive incorporation within the nucleated amorphous particles appears energetically less favorable. The preferential association of IP6 with ions and ion clusters relative to the mineral phase also explains the extended transient stabilization of ionclusters during the post-nucleation regime and the prominence of secondary nucleation events (Figure 2). Depending on the mineralization scheme, an analogous additive phase behavior might operate for phase transformations from liquid- or gel-like to crystalline phases during mineral growth55-57. The slopes of the linear pre-nucleation regimes for free Ca2+ development elucidate the stability of PNCs.41 At pH 9.0, the slopes of the pre-nucleation stages in presence of IP6 indicate a minor shift in equilibrium towards free Ca2+ with respect to the additive-free reference titrations. At pH 9.75, this effect is diminished at corresponding additive contents. Considering the changes in nucleation time and stability of ion-clusters, the additive produces significant pH dependent effects. Distinct pH related trends for mineral nucleation are also noted in the presence of certain complex additives such as polysaccharides51. A pH difference of ∆0.75 is not expected to have a significant effect on the deprotonation states of IP6 (Figure S2). This is validated by the similar development of IP6 equivalence points in DI water and carbonate solutions within the experimentally accessed pH range (Figure S6). An alternate explanation for these pH dependent effects is the distinct composition of PNCs43, 58. We speculate that the specific occurrence of secondary nucleation at pH 9.75 is due to the significantly higher fraction of carbonate species in the buffer. Under statistical assumptions, at higher pH i.e. in scarcity of bicarbonate ions, the charged state of cluster species composed of Ca2+ and CO32- might favor divalency. These states appear energetically more favorable for IP6 binding, in comparison to ion clusters containing bicarbonate species that might also accommodate monovalent states. This explanation conforms


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to the initial offset in Ca2+ development at pH 9.0 as well as the secondary nucleation at pH 9.75, representative of preferential additive-Ca2+ and additive-PNC interactions respectively. Although this hypothesis requires experimental validation especially in view of the structural dynamism of cluster species, supporting evidence comes from the high solubility of IP6 salts with monovalent cations (eg. K+) in comparison to those with divalent cations such as Ca2+. Counter intuitive to the notion of mineralization solely driven by complexation of single ion species, the titration analyses suggest that the composition and equilibria associated with ion-clusters critically affect additive-controlled nucleation processes. Solubility products for mineral phases nucleated in the presence of IP6 are determined (Figure S7). Note that these values reflect the most soluble of all phases present at a given time point. Reference experiments performed at pH 9.75 and 9.0 yield respective solubility products of 3.8x10-8 and 3.0x10-8 M2 consistent with previous studies.40, 43 IP6 markedly affects the products nucleated depending on experimental pH and additive concentration. At pH 9.0, IP6 produces values of a post-nucleation solubility product similar to the reference levels, gradually approaching about 2.6x10-8 M2 (indicating a transient amorphous form or the formation of crystalline forms such as vaterite). At pH 9.75, the solubility of nucleated products varies in a concentration dependent manner. At low IP6 concentration (7.5 µM), the solubility product of the initially nucleated particles (3.8x10-8 M2) suggests ACC nucleation, consistent with reference experiments. At higher additive concentrations, an increase in the solubility products of the initially nucleated phase is observed, corresponding to about 3.9x10-8 and 4.5x10-8 M2 for titrations containing 75 and 750 µM IP6, respectively. For 750 µM IP6-containing titrations, the post-nucleation solubility product for the secondary nucleation event is about 8.0x10-8 M2 (i.e. at 30000 sec), which is lower than that of the initially nucleated phase (9.5x10-8 M2). Since the



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second nucleation event occurs in presence of an initially formed ‘seed’ phase, the newly formed mineral products exhibit a lower solubility product. Significantly higher than the reference values, these solubility products hint towards the presence of distinct forms of amorphous CaCO3. Given the polyamorphic nature of CaCO3 precursors9-10, the mineral phase appears to undergo a transformation cascade towards more stable amorphous forms in the course of nucleation (Figure S7). This phenomenon might contribute to the structural emergence of hollow particles from products of nucleation wherein the sacrificial core presents a higher solubility relative to shell material. Since gas diffusion experiments performed in presence of IP6 produce a kinetically stabilized form of ACC34, it must be noted that the mineralization scheme can deviate significantly with regards to experimental methodologies. Titration-based experiments described here are conducted at a constant pH buffered using an excess of bicarbonate and carbonate ions under conditions of constant stirring. In contrast, gas diffusion experiments are typically performed applying an initial excess of Ca2+ ions without external agitation. Therefore, we extend our study to diffusion-based mineral nucleation and growth.

Figure 3. Continuous evolution of (A) pH and (B) free Ca2+ content in reference (black) and additive-containing (gray) gas diffusion experiments. Dotted lines represent IP6 containing solutions without Ca2+ ions.


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Probing Diffusion-based Mineral Growth. Gas diffusion is the most prevalent technique to evaluate the effects of additives on mineral structure and form. However an intrinsic lack of control over pH development and diffusion conditions lead to ‘black-box’-like conditions and difficult to access formation mechanisms27. To elucidate IP6 mediated mineral superstructures, we continuously monitor gas diffusion experiments for pH and free Ca2+ concentrations (Figure 3) as an improvement of the on-line pH monitoring and offline calcium and carbonate determination experiments reported before.27 Another advantage is the selective determination of the free Ca2+ ion fraction, which is not associated with counter-ion and additive species. This provides an understanding of the equilibrium between free and bound Ca2+ ions during gas diffusion based mineralization. In situ measurements reveal that distinct pH profiles develop in presence of the additive (Figure 3A). Without IP6, the pH rapidly increases during the first 5 h to about pH 9.8 and remains constant. With IP6, the initial pH value is much lower (pH 7), increasing to pH 8.4 at 4 h and then steadily to about pH 9.1 at 22 h. This corresponds to a significant pH change of ∆pH 2 in presence of additive relative to the reference values (i.e. ∆pH 1), hinting towards the contribution of bicarbonate ions during the early stages of additivecontrolled diffusion-based mineralization. A previous study investigating the carbonation of calcium hydroxide solutions also identifies a strong pH-related speciation of carbonate ions during mineral nucleation59. Experiments conducted without either Ca2+ ions or IP6 produce a disposition towards rapid pH increase. This indicates that additive-ion associates produce a pH buffering effect via the deprotonation of the phosphate oxygens of IP6. Coupled with the quantitative assessment of mineral nucleation under fixed pH conditions, the continuous in situ measurements show that mineralization additives affecting pH (via buffering or ioncomplexation) can modulate the mineralization reaction in terms of stability of mineral



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precursors, nucleation behavior and poly(a)morph selection. In additive-free systems, pH is a critical factor affecting the nature of mineral precursors such as liquid phases and ACC.43, 60 In the presence of additives for diffusion based mineralization, the role of solution pH encompasses the speciation of additives molecules (Figure S2) as well as the modulation of additive-ion complexes as dynamic reservoirs of mineral precursors. Considering the development of free Ca2+ ions in additive-free gas diffusion experiments (Figure 3B), distinct regimes are identified corresponding to (i) an initial rapid decrease, (ii) a slow decrease until about 12 h, (iii) followed by a rapid decrease until 22 h. Relative bound Ca2+ fractions of about 30, 82 and 99.8 % are estimated at the end of these stages. In view of the recent advances pertaining to nucleation and crystallization,8,

11

ion-associates and amorphous

particles are most representative phases in the first and second regimes. This is supported by considering the average solubility of solid ACC (about 3.4 ± 0.4 ×10-8 M2) based on potentiometric titration studies40,

43

as well as stoichiometric Ca2+ and CO32- contents in the

mineral phase, which theoretically predict free Ca2+ contents of about 1.8×10-4 M. Experimental values being significantly higher than the expected free Ca2+ contents indicate that PNCs and soluble transient phases are prevalent during the initial regime of diffusion-based CaCO3 formation. In the presence of IP6, distinct trends are observed for the development of free Ca2+ ions (Figure 3). The initial free ion content is about hundred-fold lower than that of reference experiments with Ca2+ alone. Initially about 99.5 % of total Ca2+ is IP6 bound, which is due to the remarkable ion-complexation capacity of the additive. With the gradual decomposition of ammonium carbonate, the rise in pH enhances ion complexation leading to a minimum in free Ca2+ contents at about 8 h, corresponding to 99.9 % of total Ca2+ being associated with IP6 and counter-ions. Since IP6 is a potent stabilizer of ACC34, the steady increase in free Ca2+ content


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after 10 h infers the predominance of ACC in the system. This is confirmed by polarization light microscopy, which indicates the presence of amorphous particles at 5 h of gas diffusion experiments (Figure S8). The detected values are 10-fold lower than those corresponding to the solubility of ACC and thus represent equilibrium free Ca2+ contents overall affected by ionassociation as well as ion complexation regulated by the IP6 species. The in situ observations of diffusion-based mineralization reveal that PNCs and amorphous mineral precursors are prevalent during diffusion-based mineral growth. In gas diffusion experiments, the initially formed IP6-Ca2+ complexes serve as a source of mineral precursors, subsequently incorporating carbonate and also bicarbonate species. On these lines, the role of bicarbonate ions in stabilizing a mineral precursor in form of a condensed liquid phase is possible60. On account of ammonia diffusion, the increase in pH through the reaction course favors IP6 deprotonation and is expected to enhance ion-complexation. However the increase in free Ca2+ during the late stages of mineralization reflects the competitive association of Ca2+ ions with carbonate and IP6 species under conditions of supersaturation, as suggested by equilibria (2) and (3). In course of nucleation, IP6 is expelled from growing mineral, representing the demixing of a solid mineral and a soluble IP6-rich phase. Diffusion-based mineralization is highly susceptible to kinetic effects such as diffusion limitation.21 Under stirring conditions, the changes in free Ca2+ content and pH are rapid (Figure S9), which suggest that the conditions of diffusion critically affect the mineralization process. Titration-based assays and in-situ monitoring of gas diffusion validate that additive speciation and ion-complexation modulate mineral nucleation. We further investigate the chemical compositions of intermediates formed during diffusion experiments. IR spectra for samples at different time periods of mineralization exhibit certain peaks representative of IP6 speciation61



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(Figure S10). In the 1 h sample, peaks at 940, 990 and 1067 cm-1 are assigned to νas(P-OH), νas(P-O in PO32-) and νs(P-O in HPO3-), respectively. The peak at 940 cm-1 indicates partially deprotonated IP6 species due to the low pH conditions during initial stages of gas diffusion (Figure 3). Subsequent samples do not exhibit this peak but a major peak at 982 cm-1 indicative of νas(P-O in PO32-). This confirms a dynamic speciation of IP6 and the emergence of the completely deprotonated form of IP6 in course of the diffusion-based mineralization. Presence of CaCO3 is only detected in 6, 18 and 48 h samples as shown by corresponding ν3 peaks between 1439 and 1450 cm-1. FTIR spectra also present broad bands between 3000 and 3700 cm-1 indicating additive- and mineral-associated hydration. Thermogravimetric analyses are also performed (Figure S11). IP6 hinders the quantification of mineral composition because of coinciding stages of mass losses associated with ring decomposition reactions.44,

62

However

under mineralization conditions, samples at 6 and 16 h present enhanced mass losses at about 650-700°C indicating CaCO3 decomposition to CaO. The mass losses at about 400°C indicate a certain co-association of IP6 with the mineral phase.62 Thus the in situ investigations on mineral formation provide indications of an intermediate phase containing IP6 and ion species that serves as a precursor for the mineral superstructure.


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Figure 4. Representative TEM images of rod-shaped amorphous structures formed in track etched membranes after (A, B) 24 h and (C, D) 72 h of mineralization. Scale bars represent (A, C) 1µm and (B, D) 200 nm. Liquid-like Organic-Inorganic Microphase. Metallogel materials have been reported for Fe3+-IP6 complexes based on the multidentate properties of IP663. To elucidate the role of a liquid- or gel-like mineral precursors in the emergence of hollow particles34, track-etched membranes are infiltrated using a quenched gellike product obtained prior to substantial mineralization (i.e. at 1 h) in gas diffusion experiments and then exposed to ammonium carbonate vapors. Previous studies have demonstrated that liquid-like precursor phases of certain minerals can infiltrate pores by capillary action and yield crystalline rods.64 EDS mapping of infiltrated membranes show phosphorous rich regions corresponding to the membrane pores (Figure S12). This suggests that a transient IP6-containing phase with a dense liquid- or gel-like state exists during the initial regime of diffusion



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experiments. Membrane dissolution after exposure to ammonium carbonate vapors yield particles exhibiting rod-like morphologies (Figure 4; Figure S13). The corresponding SAED pattern confirms an amorphous nature. At higher magnification, the rods show an inhomogeneous, porous structure. Estimated rod thickness of about 4.2±0.6 µm indicates volume shrinkage during phase transformation (membrane pore diameter, 5 µm). This reflects a structural consequence of the discharge of additives and water from a dense liquid-/gel-like precursor.65-66 Assuming a uniform cylindrical shape and negligible shrinkage along the rod length for simplicity, the volume loss during ACC formation from the precursor phase is approximately 38%. Considering the void spaces in the rods (Figure 4), the actual volume shrinkage is greater. A minimal volume change of 38% is comparable to those reported for the transformation of monohydrated ACC to calcitic rods. From the volume change and an approximated mass loss during phase transformation based on the TGA, the following equation is applied to estimate the density of the IP6-Ca2+ constituted precursor phase: = where = density, m = mass and V = volume of the respective initial precursor phase and hydrated ACC product. From the literature value of hydrated ACC ( =1.49 g/mL67) and mass loss of about 15% during ACC formation (ie. / from TGA profiles and reported maximal ACC thermal stability of 290°C68), the density of the precursor phase is determined to be about 1.2 ± 0.11 g/mL. This value is intermediate to the density of IP6 with stoichiometric bound Ca2+ (1.0039 g/mL) at the concentrations present in the gas diffusion experiment and the density of ACC (1.49 g/mL), indicating a liquid-like precursor phase constituted of carbonate and IP6 species, Ca2+ ions and a significant degree of hydration. With evidence of a liquid-like microphase constituted of ion-additive complexes, a possible mechanism for the emergence of


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the hollow-particle morphologies34 is the interfacial ripening of precursor droplets that serve as sacrificial templates (Figure 5). Note that the size distribution of ACC particles was unaffected by dichloromethane treatment (Figure S14). This alleviates concerns about an enhanced solubility of ACC in dichloromethane affecting morphological investigations and density estimations.



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Figure 5. Schematic representation of mineralization involving liquid-like droplets composed of hydrated IP6-Ca2+-CO32- complexes (A) (i) confined within membrane pores by capillarity, (ii) forming porous amorphous rods post-mineralization and (B) in bulk solution, the droplets serve as a sacrificial template for (i) interfacial ACC formation, (ii) leading to hollow particles. Colors represent an IP6-rich liquid-like mineral precursor (pink) and amorphous CaCO3 (orange).


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Figure 6. Representative TEM images of samples from the diffusion-based mineralization reaction. The respective reaction time-points are (A) 5 min, (B, D, E) 30 min and (C, F, G) 90 min. Scale bars represent (A) 2 µm, (B, C) 500 nm and (D-G) 100 nm.

In validation of the proposed mechanism, time-dependent TEM of samples from the diffusionbased mineralization is performed (Figure 6). During the nascent mineralization period, amorphous spherical structures, 50 to 200 nm in size are formed (Figure 6A), representative of the organic-inorganic microphase. The morphological features are similar to liquid-condensed phases formed during mineralization in an additive-free system69. In the next stage, the formation of an amorphous shell is observed (arrows, Figure 6B, D, E). This is suggestive of the interfacial demixing of additive-ion complexes towards an amorphous mineral shell and soluble IP6-ion complexes, driven by conditions of supersaturation (equilibria (2) and (3), Figure S4). Transitions in the hydration states of mineral precursors during the core-hollowing process were also proposed previously34. In view of the enhanced stability of amorphous mineral, a residual



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IP6 content inhibits the crystallization of the mineral shell. After 90 min, the progression of phase transition yields rattle-type or yolk-shell nanostructures with physically isolated core-shell constituents (Figure 6 C, F). In smaller particles (about 50 nm), the core is entirely consumed, producing a hollow particle (Figure 6G). This structural evolution identifies interfacial demixing of additive-ion complexes as a key mechanism that explains the emergence of hollow particles (Figure 5B). In some instances, interconnected yolk–shell structures are observed, reflecting the participation of partially coalesced droplets in the core-hollowing process (Figure S15). CONCLUSIONS Addressing the mechanisms underlying biomimetic and biogenic mineral growth is a challenge because of the metastable nature of intermediate phases. Here by utilizing a novel approach for in situ measurements of additive-controlled mineralization, we show that ion associates and transient liquid-like multicomponent phases play critical roles in diffusion-based mineral growth. Therefore, non-classical routes of nucleation and crystallization can be applied for addressing material forms and structures derived using this methodology. In the presence of IP6, the formation of hollow amorphous superstructures is attributed to multiple factors (Figure 5) viz. (i) the initial formation of hydrated IP6-ion complexes serving as a reservoir of Ca2+ ions, (ii) prevalence of initial low pH conditions that favor intermediate liquid-like mineral precursors, (iii) favorable association of IP6 with PNCs relative to the amorphous mineral resulting in a supersaturation- and pH-controlled ‘core-hollowing’ ripening process70 and (iv) a potent additive-mediated stabilization of ACC. This is a remarkable example of the multiple effects of a single additive on mineral nucleation and growth. Due to a pH-related speciation of additive molecules, distinct regimes of mineral growth emerge that favor microphase separation as shown for polymer-induced liquid precursor phases of CaCO3, as well as certain amino acids and


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pigments.71-74 Phase separation processes are suggested to play a role in biomineralization wherein macromolecules form liquid-like assemblies or gels, serving as templates and also condition biochemical environments in terms of local pH, ionic conditions, crowding and confinement.55, 75-77 Further investigations on intermolecular forces during microphase separation and the phase behavior of additives relative to the forming inorganic material can enable precise control over material architecture and composition. ASSOCIATED CONTENT Experimental details and supporting data for synthetic and analytical methods are provided. This material is available free of charge via the Internet at http://pubs.acs.org. AUTHOR INFORMATION Corresponding Author: [email protected] NOTES The authors declare no competing financial interest. ACKNOWLEDGMENTS A.R. acknowledges support from the Freiburg Institute for Advanced Studies. REFERENCES 1. Mann, S., Biomineralization: principles and concepts in bioinorganic materials chemistry. Oxford University Press: 2001; Vol. 5. 2. Lowenstam, H. A.; Weiner, S., On biomineralization. Oxford University Press: 1989. 3. Wegst, U. G.; Bai, H.; Saiz, E.; Tomsia, A. P.; Ritchie, R. O., Bioinspired structural materials. Nat. Mat. 2015, 14, 23-36. 4. Jackson, A.; Vincent, J.; Turner, R., The mechanical design of nacre. Proc. Roy. Soc. London B: Biol. Sci. 1988, 234 , 415-440. 5. Niederberger, M.; Cölfen, H., Oriented attachment and mesocrystals: non-classical crystallization mechanisms based on nanoparticle assembly. Phys. Chem. Chem. Phys. 2006, 8, 3271-3287. 6. Gebauer, D.; Kellermeier, M.; Gale, J. D.; Bergström, L.; Cölfen, H., Pre-nucleation clusters as solute precursors in crystallisation. Chem. Soc. Rev. 2014, 43, 2348-2371. 7. Gebauer, D.; Cölfen, H., Prenucleation clusters and non-classical nucleation. Nano Today 2011, 6, 564-584.



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Additive Speciation and Phase Behavior Modulating Mineralization

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