Molecular Mechanism of Crystal Growth Inhibition at the Calcium

Feb 11, 2016 - A detailed investigation at the atomistic level of the specific interactions taking place at the interface in solution is then needed t...
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Molecular Mechanism of Crystal Growth Inhibition at the Calcium Oxalate/Water Interfaces Leila Salimi Parvaneh,†,‡ Davide Donadio,*,§ and Marialore Sulpizi*,‡ †

Max Planck Institute for Polymer Research, Ackermannweg 10, 55128 Mainz, Germany Johannes Gutenberg University Mainz, Staudinger Weg 7, 55099 Mainz, Germany § Department of Chemistry, University of California Davis, One Shields Ave., Davis, California 95616, United States ‡

ABSTRACT: Understanding the molecular mechanisms which nature uses to control biomineral growth is a fundamental science goal with profound medical implication. In the case of calcium oxalate, a microscopic understanding of the interactions which regulate the growth and stabilization of metastable phases would permit to inhibit the growth of the crystals which are the main components of kidney stones. Here we use ab initio molecular dynamics simulations to unravel how specific molecular interactions occurring on calcium oxalate dihydrate surface can promote an anisotropic crystal growth. We find that the calcium oxalate dihydrate (100) and (101) surfaces are both hydrophilic and solvated by a strongly bound layer of water; however, they exhibit important differences in their ability to bind water and small molecules such as acetate. In particular, on the (100) surface, the more exposed Ca2+ ions can more strongly bind to negatively charged groups, exerting a protecting action on the surface and preventing its further growth. This mechanism in turn would favor an anisotropic growth of the calcium oxalate dihydrate crystals in the [100] direction, as observed in experiments.

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media have been widely studied.10−17 In particular Jung and coworkers have investigated the impact of different concentration of biopolymer additives, such as polyaspartate, polyglutamate, and polyacrylate, on calcium oxalate crystal growth.14 The presence of acid-rich polymeric additives is able to stabilize the metastable phases COD and COT, preventing the conversion to the thermodynamically stable phase COM. In particular the structural shift from COM to COD occurs gradually when increasing the polymeric additive concentration, with COD crystals exclusively crystallized beyond a certain critical concentrations of the additives. The critical concentration actually depends on the specific additive, showing that the specific molecular interactions determine the capability to control the crystallization.14 The pH of thesolution also plays a critical role: indeed at low pH COM is stabilized, while at intermediate (high) pH the metastable phases COD and COT appear.16 Possibly this is related to the fact that at intermediate/ basic pH deprotonated acidic residues exhibit greater affinity toward specific CaOx crystal planes, in turn inhibiting growth along specific crystal directions and therefore promoting the growth of metastable phases.13,18 It was recently observed13 that the stability of the formed phase increased dramatically with increasing the chain length of the peptides, with almost no conversion of the COD metastable phase for the case of the

INTRODUCTION The interactions between ions or molecules and crystalline interfaces play a crucial role in both natural and synthetic growth processes yielding materials with unique structural properties. Biological control of crystal morphology and structure is well-known in nature,1 a specific example being the role of mollusk shell macromolecules in determining crystal structure of calcium carbonate.2 In the case of calcium oxalate (CaOx), CaC2O4, the main component of kidney stones, two urinary constituents, a small organic anion, citrate, and a protein, osteopontin, can inhibit the growth and change the gross morphology of calcium oxalate crystals.3−5 Understanding the molecular mechanisms of biological control over CaOx crystallization is therefore central to the development of effective stone disease therapies and can help define general strategies for synthesizing biologically inspired materials. CaOx crystallization also plays an important role in water related industries, where CaOx appears as scale deposition on critical industrial equipment, such as heat exchangers, boilers, and sewage pipes, causing efficiency problems and energy losses.6−8 Calcium oxalate crystallizes in three different hydrated forms, calcium oxalate monohydrate (COM) (CaC2O4·H2O), calcium oxalate dihydrate (COD) (CaC2O4·2H2O), and calcium oxalate trihydrate (COT) (CaC2O4·3H2O). COM is the thermodynamically stable phase and occurs in kidney stones about twice as frequently as COD.9 However, asymptomatic crystals in urine are also common and are typically COD. The effects of biopolymers on calcium oxalate crystallization in aqueous © 2016 American Chemical Society

Received: December 21, 2015 Revised: February 5, 2016 Published: February 11, 2016 4410

DOI: 10.1021/acs.jpcc.5b12474 J. Phys. Chem. C 2016, 120, 4410−4417

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The Journal of Physical Chemistry C

the different surfaces. We indeed find a remarkable difference between the two investigated surfaces of COD, and our simulations indicate that acetate can bind more favorably to the (100) surface. This means that the side chain interaction has a key role in discriminating between the two investigated surfaces.

longest chain. In particular it was found that an increase in the chain length favors the formation of tetragonal COD. The same group also observed an elongation of the (100) face in COD crystals in samples prepared with an increasing chain length, which indicates a predominant specific adsorption of the oligopeptide on this face and a promotion of the growth in the [001] direction. These studies suggest that the side chain groups may establish relatively strong interaction with the crystal facets and with the ions in solution, thus shifting the thermodynamic equilibrium. Moreover, the (bio)-polymers may have a preferential binding to certain crystal planes with respect to others, depending on both the molecular details of the side chains and on their length, so to inhibit growth along specific crystallographic directions and to modify the relative growth. This means that in solution kinetically controlled growth may take place. However, to date, research on CaOx growth modification by proteins and small molecules has not resolved the molecular-scale control mechanisms. A detailed investigation at the atomistic level of the specific interactions taking place at the interface in solution is then needed to shed light on the microscopic origin of both the stabilization of metastable phases and anisotropic growth. Although there has been extended theoretical investigation of the interaction of calcium carbonate with water19,20 and polyelectrolytes,21−25 much less analysis has been carried out for calcium oxalate. Atomistic simulations have been so far mostly limited to the COM phase. In particular, the adsorption of osteopontin,26 glutamic acid,27 and citrate28 on different facets of COM has been addressed. These studies have identified, e.g., a facespecific adsorption motif in osteopontin and delineated separate roles for carboxylate and phosphate groups in the inhibition of crystal growth. The interaction of poly acrylate with COD (100) was also modeled to support the experimental observation of anisotropic growth, yet without considering a solvated surface.16 Our aim here is to characterize the surfaces of the metastable COD in water and their interaction with additives, and to find a rationale for the different growth morphologies. Specifically, the first question that we want to address regards the solvation of the different crystal surfaces. COD surfaces are hydrophilic and may establish strong interaction with the solvent, water in particular, which is present in physiological conditions. The structure of interfacial water can change depending on the chemical composition and the structure of the surface and has a significant role on the nucleation and crystal growth of inorganic materials in the presence of organic molecules.29−31 For this purpose we will provide an ab initio molecular dynamics (MD) description of COD(100)/water and COD(101)/water interfaces. Density functional theory (DFT) based MD simulations are particularly suitable for this purpose, since they do not involve any force field parametrization and are, therefore, sufficiently transferable to investigate complex heterogeneous environments, such as mineral/water/polymer interfaces. Our second aim is to quantify the interaction of COD surfaces with carboxylic groups, which characterize the side-chains of several (bio)molecules and polyelectrolytes, from citrate to (poly)aspartate, (poly)acrylate, and (poly)glutamate. Indeed the carboxylic group plays a key role in the growth shape and stabilization. We have chosen the acetate anion as a minimal model for the polymer side chain and we have investigated the interaction of acetate with both solvated COD(100) and COD(101). To quantify the strength of acetate adsorption at the COD/water interface we have calculated the acetate binding free energy to

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METHODS DFT-based Born−Oppenheimer molecular dynamics (BOMD) simulations were performed in order to unravel the atomistic structure of the COD/water interface and to provide the binding structure and free energy of acetate at the COD/water interface. We used the generalized gradient approximation exchange-correlation functional by Perdew-Burke-Ernzerhof (PBE)32 including Grimme (D3) corrections for van der Waals interactions.33 All the calculations have been carried out with the CP2K/Quickstep package,34 which is based on the hybrid Gaussian and plane wave method.35 The interaction of the valence electrons is described by analytic Goedecker, Teter, and Hutter (GTH) pseudopotentials,36 a double-ζ valence polarized (DZVP) Gaussian basis set was chosen for the real space representation of the valence electrons, while plane waves up to a cutoff energy of 280 Ry were used to expand the density in reciprocal space. The Γ-point only was considered. All the BOMD simulations were performed in the canonical NVT ensemble, using the Nose-Hoover thermostat37,38 to keep the average temperature at 330 K. The BOMD equations of motion were integrated using a time step of 0.5 fs. As a starting point of our simulations we used the crystallographic coordinates of bulk COD from Tazzoli and Domenghetti.39 COD is a tetragonal crystal with I4/m (C4h) space group, where the calcium ions is coordinated to six oxygens belonging to four oxalic groups and to two crystallographic water molecules. The chemical formula for COD is (CaC2O4·(2+x)H2O) with x ≤ 0.5. Tazzoli and Domenegetti found x = 0.3739 and recently Izatulina et al. also suggested x = 0.13−0.37.40 According to the crystal structure in ref 39, zeolitic water is present in the channels, which are formed by calcium ions, oxalate ions and crystallographic water molecules. For simplicity, in our calculations we did not consider the zeolitic water (x = 0) as this is not directly involved in the specific interactions characterizing the COD/ water surface. Both the COD(100) and COD(101) surfaces were cut in such a way to obtain neutral and nonpolar surfaces (Figure 1). Cleavage along the (100) plane would result in polar surfaces: to remove net polarization, we redistributed half of the calcium atoms from the calcium terminated surface to the oxalate terminated one. The resulting surface density of calcium ions

Figure 1. Sideview of calcium oxalate dihydrate (100) (a) and (101) (b). 4411

DOI: 10.1021/acs.jpcc.5b12474 J. Phys. Chem. C 2016, 120, 4410−4417

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The Journal of Physical Chemistry C on the (100) surface is 3.3/nm2 and on the (101) surface is 2.3/nm2. The COD(100) surface was subsequently hydrated with 111 water molecules and the COD(101) surface with 116 water molecules, respectively. When negatively charged acetate ions are introduced, total charge neutrality is obtained either by adding a neutralizing background (as in the case of the calculation of the binding free energy of acetate to COD) or by adding an equivalent number of sodium counterions in solution. The simulation cell sizes are 32.514 × 12.371 × 14.714 Å3 for COD(100)/water and 14.393 × 12.371 × 32.514 Å3 for COD(101)/water and periodic boundary conditions were employed, so that mineral and water slabs extend periodically in the x and y directions, while they are alternating in the z direction. The thickness of the water slab between two COD surfaces is ∼2 nm, which is sufficient to avoid interactions between images and to have a middle layer of water with bulklike properties. No position constraints were used in the simulations. After 5−10 ps of equilibration in the NVT ensemble, 20 ps were collected for data analysis. Free energies were obtained by thermodynamic integration using the Bluemoon ensemble approach,41 where the distance between the carbon atom of the carboxylate group of the acetate and the calcium ion is identified as reaction coordinate. The free energy was then calculated by integrating the average constraint force, f(r) with respect to the constrained distance, according to ΔA = −

a→b

∫a

oxalate ions which are expected to strongly interact with water, as shown in Figure 1. As COD surfaces come in contact with water, strong interactions between the surface ions and the water molecules are established. Figure 2 shows a density map

Figure 2. Density map of the first adsorbed layer of water molecules on (a) calcium oxalate dihydrate (100) and (b) calcium oxalate dihydrate (101) surfaces. Calcium atoms are in yellow, oxygen atoms in red, and carbon atoms in cyan.

of the first adsorbed layer of water on the (100) and (101) surfaces, which shows that water molecules can bind to both calcium and oxalate ions on both surfaces. The very localized density also suggests that both surfaces are hydrophilic and no exchange of water in the first adsorbed layer occurs during the simulation time (∼20 ps). To get a deeper insight into interfacial water ordering, we have also calculated the average water dipole orientation at the interface. In particular in Figure 3b the average cosine of the angle between the water molecule dipole and the surface normal is plotted as a function of the distance from COD(100) and COD(101) surfaces, respectively. Indeed the water molecules present a strong dipole orientational ordering,

b

⟨f (r )⟩ dr

(1)

For the calculation of the acetate binding free energy to COD(100) 16 values of the constrained distance were chosen in the range from 2.82 to 5 Å, while for the acetate binding free energy to COD(101) ten values of the constrained distance were chosen in the range from 3 to 5 Å. For COD(100) in the closest contact region (2.82−3.22 Å) the distance intervals were separated by 0.8 Å (except 0.1 Å for 2.9 to 3) and then 0.14 Å for 3.22 to 3.5, 0.12 Å for 3.5 to 3.62, 0.18 Å for 3.62 to 3.80 and 0.2 Å for 3.80 to 5 Å were considered for (100). For COD(101) in the closest contact region (3−3.44 Å) the distance intervals were separated by 0.2 Å for 3 to 3.2, 0.1 Å for 3.2 to 3.3 and 0.14 Å for 3.3 to 3.44 and then 0.2 Å for 3.44 to 3.84 Å, 0.16 Å for 3.84 to 4, 0.24 Å for 4 to 4.24, 0.4 Å for 4.24 to 4.64, and 0.36 Å for 4.64 to 5 Å were considered. For each constrained distance 2 ps were used for equilibration, then the average constraint force f(r) was calculated using a sampling time window of 8 to 15 ps depending on the observed convergence of the constraint force. The errors were estimated from block data analysis.

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RESULTS AND DISCUSSION Water Structure at the COD/Water Interfaces. Both COD(100) and COD(101) surfaces are stable when they come in contact with water. In particular, both surfaces do not undergo major structural relaxations, and the ionic positions in the topmost layer remain very close to those of the optimized geometry in gas phase. The average mean squre displacement of all the ions positions in the solvated system with respect to the geometry optimized gas phase position is 0.73 Å for (100) and 0.63 Å for (101) surface. Our first aim is to elucidate the water structure at the COD/water interface in order to understand if, e.g., a specific plane exhibits a more structured or ordered layer of adsorbed water. Indeed both COD(100) and COD(101) surfaces are characterized by exposed Ca2+ and

Figure 3. (a) θ is the angle between the water molecule dipole and the surface normal is shown. (b) Orientation of water molecules at calcium oxalate dihydrate (100) (blue line) and (101) (red line) interfaces. (c,d) Density map of distribution of first adsorbed layer of water molecules on COD(100) (c) and COD(101) (d) interfaces. Calcium atoms are in yellow, oxygen atoms in red, and carbon atoms in cyan. 4412

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The Journal of Physical Chemistry C which is modulated by the local positive (calcium ions) and negative (oxalate ions) charge on the surface. The average dipole orientation of water on COD(100) surface exhibits a first negative peak, i.e., water dipoles pointing toward the surface plane, and a second positive peak, i.e., water dipoles pointing outward. Alternate dipole ordering extends beyond the first layer of interfacial water, as fluctuations of smaller amplitude also characterize the second layer. In contrast the dipole of water at COD(101) surface exhibits only a marked outward orientation limited to the first interfacial layer, and no regular amplitude fluctuations farther away from the surface. To achieve a more comprehensive view, we computed the interfacial water orientation “in plane”, as a function of the location on the surface. In Figure 3(c,d) the density map of the average cosine for the first adsorbed layer of water is reported. The positive values for cos θ (orange) indicate an average dipole orientation pointing out of the surface into the solvent, while negative values (green) correspond to dipoles pointing toward the surface. The alternation of green and orange spots suggests that the local order is determined by the binding of water to calcium and oxalate ions, respectively, although overall there is no net water orientation in the direction perpendicular to the surface. In particular, on the COD(100) surface the first negative peak in Figure 3(b) can be associated with waters that bind to the oxalate (hydrogen bonds) and the subsequent positive peak to the waters that point toward Ca2+, and have therefore opposite orientation. Both the COD(100) and COD(101) surfaces exhibit strong interactions between exposed Ca2+ ions and water. On COD(100) two inequivalent Ca2+ ions, labeld as Ca(1) and Ca(2) characterize the topmost layer. Instead on COD(101) four Ca2+ lay in the top layer: Ca(1) and Ca(2), respectively Ca(3) and Ca(4) have equivalent positions (see Figure 1). The solvation structure of such ions represents an important element to understand the ability of small (and large) molecules to bind to the surface. In particular it is important to understand if significant differences characterize the solvation structure of Ca2+ ions belonging to the COD(100) and COD(101) surfaces. To this purpose we have calculated the radial distribution functions (RDFs) between Ca2+ and water oxygen, and we have compared them for the two different surfaces. From Figure 4 we observe that for both surfaces the RDFs are characterized by an intense first peak, located around 2.4 Å. The coordination numbers of water oxygen to Ca2+ are reported in Table 1 together with the number of oxalate oxygen atoms coordinating to calcium from the crystal. An interesting difference here is that the Ca2+ ions on the COD(100) surface are more exposed to the solvent: they have a lower coordination from oxalate oxygens and a higher coordination to solvent oxygens (on average 2−4 water molecules can bind to the surface Ca2+). In contrast on COD(101) a higher coordination from the oxalate oxygens is complemented by a reduced solvation from water (on average only 1−2 water molecules can bind to the surface Ca2+). The more exposed Ca2+ ions on the COD(100) suggests that on this surface Ca2+ ions can more easily (and strongly) bind to negatively charged molecules. This, in turn, would also suggest that the COD(100) surface can be more easily covered by negatively charged molecules or side chains. However, in order to further support this prediction a direct calculation of the binding free energy for an adsorbing, negatively charged, molecule is required, as it is discussed in the next section.

Figure 4. Radial distribution functions (RDFs) and integrated numbers between calcium ions and water oxygen atoms. (a) RDF for Ca(1) (blue line) and Ca(2) (red line) at the calcium oxalate dihydrate (100) interface. (b) RDF for Ca(1) and Ca(2) (blue line) and Ca(3) and Ca(4) (red line) at the calcium oxalate dihydrate (101) interface. Calcium labels according to Figure 1.

Table 1. Coordination Numbers of Calcium Ions on COD(100) and COD(101) with Oxygens from the Crystal (Namely Oxygen from Oxalate and Crystallographic Waters) and Oxygens from Solution COD(100)/water

O(crystal)

OW(SOL)

Ca(1) Ca(2) COD(101)/water

4 5 O(crystal)

4 2 OW(SOL)

Ca(1),Ca(2) Ca(3),Ca(4)

6 7

2 1

Acetate Binding at the COD/Water Interfaces. As mentioned in the introduction one of our aims is to understand the interaction of polyelectrolytes with carboxylated side chains with COD crystal faces. Here the acetate anion serves as an analogue for the carboxylate group. In the following we estimate the binding energy of acetate to two different surfaces, namely COD(100) and COD(101) in order to (i) elucidate the most favorable binding configuration and (ii) estimate differences in the binding free energy. For this purpose we performed constrained MD, where, starting from an equilibrated binding configuration, the distance of the carboxylate from the Ca2+ ion on the surface is gradually increased. We considered as model systems the COD(100)/water and COD(101)/water interfaces, where one acetate binds to the most exposed Ca2+ ion (this is Ca(1) according to the labeling in Figure 1). Although we start with similar configurations for acetate at both interfaces, after 10 ps of equilibration we find that on COD(100) acetate binds in a bidentate fashion (two carboxylate oxygens coordinate the Ca2+ ion), while on 4413

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The Journal of Physical Chemistry C COD(101) it binds in a monodentate fashion (only one carboxylate oxygen coordinates the Ca2+ ion). A typical configuration for the two interfaces is reported in Figure 5.

Figure 5. (a) Acetate adsorbs in a bidentate configuration at the calcium oxalate dihydrate (100)/water interface. (b) Acetate adsorbs in a monodentate configuration at the calcium oxalate dihydrate (101)/water interface. Crystallographic water are omitted for clarity.

The binding free energy curves of acetate to both surfaces are reported in Figure 6, along with the free energy profile of

Figure 7. Snapshots illustrating the different types configurations for acetate at the calcium oxalate dihydrate/water interface. The snapshots are extracted from the trajectories generated to calculate the binding free energy. (a) Bidentate, (b) monodentate, (c) solvent separated ion pair for acetate binding to the (100) surface, (d) contact ion pair, (e) transition state, and (f) solvent separated ion pair for the (101) surface.

resembles closely that obtained for pairing acetate to Ca2+ in solution, where two minima (bidentate and monodentate) were also found for the contact ion pair (CIP) configuration. Such similar behavior is not surprising, if we consider that on the COD(100) the Ca2+ ion is mostly exposed to the solvent, with only partial screening from the solid. Conversely, the free energy profile for the COD(101) surface is qualitatively different, since it only presents a single minimum for the contact ion pair configuration, located at a slightly larger interatomic distance (∼3.4 Å), much shallower than the corresponding CIP minimum for acetate binding to COD(100). In the case of the COD(101) surface, Ca2+ is less exposed, partially screened by oxalate ions in the crystal, and, consequently, it is less prone to bind charged carboxylate groups. Snapshots of the monodentate CIP, the transition state and the SIP of acetate at COD(101) are presented in Figure 7(d−f). This sequence of snapshots unravels the bonding/ release mechanism of acetate at COD surfaces at atomistic level. In fact, the transition state between CIP and SIP, shown in Figure 7(e), corresponds to a change in the coordination of calcium to water: when acetate forms a direct contact to calcium, one of its neighboring water molecules is released into the solution. This molecular mechanism underlies the origin of the stability of the acetate/COD complex. If we compare the number of water molecules coordinated to the surface Ca2+ before and after the binding of acetate we find that for both COD(100) and COD(101) two water molecules are displaced. In the case of Ca2+ on COD(100) two oxygens from acetate complete the coordination shell, leading to an overall 8-fold

Figure 6. Binding free energy of acetate to calcium oxalate dihydrate surfaces as a function of the distance between the most exposed calcium ion and the acetate carbon. Black dashed line: calcium-acetate in water; blue line: acetate binding to calcium oxalate dihydrate (100); red line: acetate binding to calcium oxalate dihydrate (101).

acetate binding to a Ca2+ ion in solution, as obtained from our previous work.42 For all the three profiles in Figure 6 the reaction coordinate on the x-axis is the distance between the surface Ca2+ and the acetate carbon. All the three curves have been aligned using the shallow minimum that corresponds to the solvent separated ion pair (SIP). First of all, we notice that there is a remarkable difference between the binding free energy profile of acetate to the two COD surfaces. Binding of acetate to COD(100) is stronger than to COD(101), with a difference of about 12 ± 6 kJ/mol. Moreover, in the case of COD(100) the free energy profile is characterized by two nearly equivalent minima located at 3.0 and 3.3 Å, which correspond to the bidentate and monodentate configurations, respectively (Figure 7 a,b). The shape of this free energy curve 4414

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The Journal of Physical Chemistry C coordinated ion, while in the case of Ca2+ on COD(101) one oxygen atom from acetate enters the ion coordination shell, leading to an overall 7-fold coordination. This means that on both surfaces the binding is the result of an entropic stabilization of the bound configuration. In other words, the liberation of water molecules from the hydration shells of the components (surface and Ca2+) is the driving energy source for the binding. A similar mechanism was found for binding of multivalent ions onto polyelectrolytes.43,44 However, adsorption on COD(100) is overall more favorable thanks to the enthalpic contribution coming from the bidentate configuration. Indeed we find, from gas phase geometry optimization, that for acetate binding to COD(100) the bidentate configuration is 97 kJ/mol more stable than the monodentate one. Although COD(100) and COD(101) are both hydrophilic important differences exist in their ability to bind water and small molecules such as acetate. In particular the stronger affinity of acetate for COD(100) would suggest that molecules with carboxylate groups can exert a stronger protecting action on such a surface, inhibiting its further growth. This would introduce an asymmetry in the growth of the two different facets eventually promoting elongated needle-like shapes. Increasing Acetate Concentration: Surface Coverage. As a last step of our analysis we investigate the effect of varying the concentration of acetate bonded to COD surfaces. For this purpose we have considered two additional systems, where the number of acetate molecules is raised to two and four molecules per surface, respectively. In the case of the COD(100) interface it is possible to obtain a stable configuration with three/four acetate molecules binding on the most exposed Ca2+ ions Figure 8(a,b). However, in the case of (101) the surface can accommodate only two/three acetate molecules Figure 8(c,d). In both cases the exact number of acetate molecules bound to the surface depends on the counterions position, which are added to maintain the overall cell neutrality. Indeed a higher surface coverage is obtained, e.g., when Na+ counterions are located in close proximity to the surface, since they can contribute to the partial screening of acetate negative charge, therefore reducing the acetate−acetate repulsion at the interface. Specifically, for COD(100), we could observe that if a Na+ ion is close to the surface (average distance from surface 1.3 Å) the binding of four acetate molecules is possible Figure 8(b). Instead when the counterions are further away from the surface (average distance of the Na+ counterions 8.4 Å), only three acetate bind to the surface while one moves to in the bulk solution Figure 8(a). In the case of COD(101) a Na+ close to the surface (average distance from surface 1.4 Å) permits to adsorb three acetates Figure 8(d). Indeed when a forth molecule is placed in the proximity of the surface, it readily detaches and moves toward the bulk water. Instead when the counterions are all far away from the surface (average distance 8.8 Å) only two acetate molecules bind to the surface Figure 8(c). Our results show that the acetate coverage has an important dependence on the local ionic strength of the growing solution.

Figure 8. Snapshots illustrating the different binding configurations for the adsorption of four acetate molecules at the calcium oxalate dihydrate/water interface. (a) COD(100)/water: 3 acetate binding to the surface; 4 Na+ counterions in the solution (simulation time 17 ps); (b) COD(100)/water: 4 acetate binding to the surface; 1 Na+ close to the surface and 3 Na+ in the solution (simulation time 17 ps); (c) COD(101)/water: 2 acetate binding to the surface; 4 Na+ counterions in the solution (simulation time 13 ps); (d) COD(101)/water: 3 acetate binding to the surface; 1 Na+ close to the surface and 3 Na+ in the solution (simulation time 13 ps). Calcium atoms are in yellow, oxygen in red, carbon in cyan and sodium in blue.

negatively charged acetate. Such adsorbed molecules can also exert a protecting action on the surface preventing a further growth of the covered surface. This also means that if acetate can more strongly bind to the COD(100) surfaces, it can eventually more strongly inhibit its further growth. Our results suggest that this could be already a determining element to promote anisotropic growth along the (101) direction. Further investigation is certainly required to address the role of polypeptide backbones when polyelectrolytes and polypeptides, e.g., polyacrylate, polyglutamate, or polyaspartate, are considered. However, for this purpose larger models and simplified empirical potentials will be required. This will be subject of a future investigation.

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AUTHOR INFORMATION

Corresponding Authors

*E-mail: [email protected]. Tel: +1-530-754-1040. *E-mail: [email protected]. Tel: +49-6131-39-23641.

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CONCLUSIONS Summarizing our results we can conclude that although the COD(100) and COD(101) are both hydrophilic and solvated by a strongly bound layer of water, important differences exist in their ability to bind water and small molecules such as acetate. In particular since the Ca2+ ions are more exposed on the COD(100) surface they can also more strongly bind to the

Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS We would like to thank Rafael Muñoz-Espi ́ for interesting discussion of the experimental data, and Jens Kahlen for help with the initial setup. All of the simulations were performed on 4415

DOI: 10.1021/acs.jpcc.5b12474 J. Phys. Chem. C 2016, 120, 4410−4417

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The Journal of Physical Chemistry C

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the Rechenzentrum Garching of the Max Planck Society and Mogon ZDV cluster oof Johannes Gutenberg University, Mainz.

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DOI: 10.1021/acs.jpcc.5b12474 J. Phys. Chem. C 2016, 120, 4410−4417