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Molecular Modulation of Calcite Dissolution by Organic Acids Congmeng Wu,† Xiaoqiang Wang,† Kang Zhao,† Meiwen Cao,† Hai Xu,*,† Daohong Xia,† and Jian R. Lu*,‡ †
State Key Laboratory of Heavy Oil Processing and the Centre for Bioengineering and Biotechnology, China University of Petroleum (East China), Qingdao 266555, People’s Republic of China ‡ Biological Physics Group, School of Physics and Astronomy, University of Manchester, Schuster Building, Manchester M13 9JP, United Kingdom
bS Supporting Information ABSTRACT: Dissolution of the calcite (104) surface in aqueous solution in the presence of 10 organic acids has been studied using fluid-cell atomic force microscopy (AFM) in vitro. Etch pit morphology varies as species conformation changes. [421] steps appeared in the presence of each of Gly, L-Glu, L-Lys, malonate, and succinate. The overall shape of etch pits became hexagonal in Gly, malonate, and succinate, while a pseudotriangular shape in L-Glu solution and a sectorial shape in L-Lys solution were observed, primarily as a result of molecular chirality. Unexpectedly, [010] instead of [421] steps emerged in L-Asp solution, giving a trapezoidal pit shape. Despite the differences in molecular structure of 6-aminohexanoate, acetate, oxalate, and glutarate, these molecules did not show any influence on pit morphology, revealing that solid/fluid recognition must depend on the geometry of additives, especially the distance between functional groups. We show that both the ammonium and the carboxylate groups are active in surface binding and that the organic acids tend to bind through more than one functional group to the calcite face. Our AFM results confirm the crucial role of geometrical matching between calcite and modifiers and show that step edge reactivity, stereochemical correspondence, electrostatic attraction, and molecular chirality play a secondary role in surface modification. This conclusion will give guidelines for synthesizing bioinspired materials with specific shape.
1. INTRODUCTION Despite its importance, there lacks an in-depth understanding of the mechanistic models applicable to biomineralization.1 This hinders the harnessing of biomineralization reactions for in vitro synthesis of novel materials. It is generally recognized that the stereochemical recognition relationship between crystal steps and organic modifiers is the key to the effects of biomolecules, although other factors such as geometrical matching and electrostatic interaction also play a role in the inorganic/organic interaction at the interface.25 Previous studies68 have paid much attention to the influence of aspartic acid-rich (Asp-rich) proteins or peptides and found that the efficacy of these acidic biomolecules derives from the strong affinity of functional carboxylates to calcium ions. Results from these studies also show that organicinorganic recognition are direction-specific and dependent on molecular characters such as chirality, hydrophilicity, net charge, and chain length.3,8 Although some correlations between morphology and molecular characteristics have been established, thorough interpretations of step-modifier interactions as well as a detailed understanding of the individual role of functional groups remain elusive. Amino acids are the basic building blocks of proteins and carry some functional groups that are the same as macromolecules but in a much shorter backbone structure. Amino acids are therefore ideal probes for crystalfunctional group interactions. r 2011 American Chemical Society
Sometimes, however, growth experiments in the presence of amino acids or peptides hardly show few differences in modified morphologies, and the rounding of steps do not always point to a specific crystallographic direction.5,6 On the contrary, dissolution experiments have the advantages of stabilizing definite step edge directions for some additives and also consume less time than growth studies.9,10 Herein, we have carried out a series of fluidcell atomic force microscopic (AFM) experiments on calcite (104) surface in the presence of organic acids (five of which are amino acids) in an aqueous environment. In situ AFM opens a valuable window for monitoring the dynamics of crystal growth and dissolution at the micro- or nanoscale.11 Given the ubiquity and abundance of calcite in nature, it is this material that has been the main focus in the development of theories concerning biomineralization.5,1218 All of the organic acids tested were chosen so as to select particular differences in their effects.
2. METHODS A 3 3 2 cm3 crystal of optical-quality Iceland spar from Ward’s Scientific, Mexico, was washed consecutively by ethanol, 1% Received: March 31, 2011 Revised: May 16, 2011 Published: May 18, 2011 3153
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Crystal Growth & Design hydrochloric acid, and deionized water (Milli-Q water, resistivity g 18.2 MΩ cm). The washing procedure was done twice, and the crystal was then completely dried under a flowing N2 stream. The cleaned crystal of Iceland spar was then placed on a clean substrate and cleaved by scalpel scoring along the cleavage plane. Because the cleavage plane (104) requires a minimal energy for initiating a cleavage, it is easy to generate rhombohedral fragments with six crystallographically equivalent {104} facets. The cleaved fragments (2 2 1 mm3) were handled with tweezers to avoid contamination, and a jet of N2 was applied to remove small particles from the cleaved surfaces. L-Aspartic acid (L-Asp), L-glutamic acid (L-Glu), and L-lysine (L-Lys) (purity g99.5%) were purchased from GL Biochem (Shanghai), and glycine (Gly) (purity g99.5%), 6-aminohexanoic acid (purity g98.5%), and sodium acetate (purity g99.0%) were purchased from Sinopharm Chemical Reagent. Oxalic acid, malonic acid, succinic acid, and glutaric acid (purity g99.0%) were purchased from Acros. Stock solutions were made using deionized water, and all of the organic acid solutions had a concentration of 100 mM, which was sufficient for observing morphological changes. Before AFM operation, the pH of all of the solutions was adjusted to 6.5 by adding reagent grade diluted NaOH or HCl solutions. We chose a pH of 6.5 for the dissolution experiments because it is close to the physiological environment. The ionic formulas and pKa values of all of the organic acids used are listed in Table S1 of the Supporting Information. A previous study measured the point of zero charge (pHpzc) for calcite (104) surface to be 9.5.19 Therefore, under the experimental conditions, the calcite (104) surface was positively charged, while the zwitterion form of amino acids and the ionized form of carboxylic acids dominated in the solutions. All of the organic acids were negatively charged except L-Lys and 6-aminohexanoic acid. All in situ AFM images were captured at room temperature in contact mode by a Nanoscope IVa scanning probe microscope (Digital Instruments, Santa Barbara, CA), equipped with a J-type scanner (maximum scan area 125 125 μm2) and gold-coated Si3N4 tips with a nominal spring constant of 0.06 N/m. A fleshly cleaved calcite sample (2 2 1 mm3) was anchored onto a steel puck, and then the O-ring in the liquid cell was placed on top of the calcite (104) face and aqueous solutions continuously flowed into the cell by sucking solution from the outlet of the fluid cell using a peristaltic pump. In this way, leakage of liquid from the fluid cell could easily be avoided. When the fluid cell and delivery pipes were filled with the desired solution, the fluid flow was stopped and surface features of the calcite were then mapped continuously using AFM. Prior to each run, the piezoelectric scanner was calibrated in the x, y, and z directions to ensure the authenticity of the surface morphology. AFM images were collected using scan rates of 520 Hz and a resolution of 512 512, while minimizing the tipsurface force to avoid any artifactual effects on the crystal morphology. Prior to injection of additives, deionized water was allowed to flow over the calcite cleavage face so that the orientation of the calcite dissolution surface was established.
3. RESULTS Upon the introduction of deionized water, calcite surface dissolution proceeds simultaneously by etch pit nucleation and step retreat. Successive retreat of steps leads to deepening of pits and coalescence of nearby pits, yielding a microtopography of interconnected etch pits. The shapes of these etch pits are rhombohedral, and this agrees well with the previous results.16 Because of the differences in step edge geometry and kink site structure, the Æ441æ rhombus developed in pure water is composed of two distinct pairs of step edges, the obtuse steps and the acute ones, both of which are symmetrically related by a c-glide plane. The two obtuse steps [481]þ and [441]þ are crystallographically equivalent as are the two acute ones, [481] and
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Figure 1. Deflection mode AFM images of the calcite (104) face observed in aqueous solutions at a pH of 6.5 in the presence of (a) deionized water, (b) 100 mM glycine, (c) 100 mM L-aspartic acid, (d) 100 mM L-glutamic acid, (e) 100 mM L-lysine, and (f) 100 mM 6-aminohexanoic acid. (a1f1) Captured within 0.5 min of modifier injection; (a2f2) 10 min later; (a3f3) more than 30 min later. Note that the observed pit shapes became stable after 30 min.
[441]. Four internal angles can be formed by the intersection of step edges, and the value of these angles is either 78 or 102 (Figure 3A), corresponding to the unit cell.20 Orientation of the calcite sample is illustrated in Figure 1a1 by dashed lines. There are two obtuse steps on the lower part and two acute ones on the upper side, and all of the AFM images shown here possess the same orientation for convenience. Rounding of the obtuse obtuse corner was observed in pure water after tens of minutes, suggesting that impurity effects become evident with increasing 3154
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Crystal Growth & Design undersaturation21 and no specific crystallographic directions apart from Æ441æ were observed at any stage. In the presence of Gly, the calcite cleavage face took on a hexagonal shape in several minutes (Figure 1b2), as a result of the expression of the [421] direction before reaching stability. The intrinsic steps [481] and [441] characteristic of pure water still exist in Gly solution, regardless of the appearance of newly formed [421] step edges. From Figure 1b3, further exposure to Gly led to the narrowing of the upper part of the hexagon, contributing to a sharpening of the corner at the top. The step edges of [421] became curved on the upper side, while the [481] and [441] steps started to diminish. All of these effects make the hexagon asymmetrical in regard to the [010] direction, but it remains symmetrical with respect to the c-glide plane. As shown in Figure 1c1, c2, and c3, upon the introduction of L-Asp into the calcitewater system, the (104) surface immediately exhibits a dissolution behavior different from pure water followed by the expression of some new step edges. The shape of the etch pits changes successively from symmetric rhombus through elongated rhombus (Figure 1c1), pentagon (Figure 1c2), and asymmetric trapezoid (Figure 1c3). The trapezoid form lasts for a long time, up to 12 h. Step edge vectors for the newly expressed steps are [010], [411], and [461] (see Figure 3), which is generally consistent with previous studies.9,22 The newly developed pit shape was no longer symmetrical with regard to the c-glide plane, presumably resulting for the chirality of Asp. The (104) plane intersects the (001), (011), and (112) planes at [010], [411], and [461] directions, respectively. Therefore, the (001) and (011) planes must have been stabilized by L-Asp.9 The two expressed [411] step edges are parallel to each other. For convenience, the shorter one is denoted as [411]a because it lies on the acute side, and the longer one is denoted as [411]o because it lies on the obtuse side. It is clear from the AFM images in Figure 1c that the emergence of the [010] step was much slower than that of the [461] and [411] steps, indicating that L-Aspcalcite interaction along the [010] direction is relatively weak or progresses at a lower rate.9 It is noteworthy that the expression of [010] was direction specific because it was expressed on the acute side of the pits rather than the obtuse side. The measured angles between step edges composing the pits are approximately 120 between [010] and [411]a, 60 between [010] and [411]o, 73 between [461] and [411]o and 107 between [461] and [411]a step edge vectors, which correspond well with values calculated from the crystal structure as shown in Figure 3. The deviations in angles between the measured and theoretical values may be the result of mass transfer limitation or thermal drift of the AFM scanner. Further exposure to L-Asp under static conditions did not cause curvature of the obtuse obtuse corner, implying that a different dissolution mechanism dominates in L-Asp solution. The etch pits developed in L-Glu solution were quite different from those in L-Asp despite the small difference in side chain length. Within tens of seconds of the injection of L-Glu, Figure 1d1 shows curvature at the [441]/[481]þ corner, while other steps are not affected. After several minutes, the effect became more apparent with three step directions of the original Æ441æ rhombus being affected except [481], before the surface finally took on a pseudotriangular shape (Figure 1d3). The corresponding crystallographic directions are [481], [411]o, and [421], and the measured angle between [481] and [411]o is 93. Similarly, this measured angle is slightly deviated from the theoretical one as shown in Figure 3. Surprisingly, the [010]
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Figure 2. Deflection mode AFM images of the calcite (104) face observed in aqueous solutions at 6.5 in the presence of (a) 100 mM sodium acetate, (b) 100 mM oxalic acid, (c) 100 mM malonic acid, (d) 100 mM succinic acid, and (e) 100 mM glutaric acid. (a1e1) Captured within 0.5 min of modifier injection; (a2e2) after a further 10 min; (a3e3) after more than 30 min. Note that the pit shape became stable after 30 min.
direction, which was expressed in L-Asp, was not expressed in L-Glu solution. On the contrary, the new step edge vector [421] progressively emerged in L-Glu. It should be noted that the step edges along [421] were curved, unlike the straight ones in Gly, malonate, or succinate. The overall effects caused by L-Glu were much stronger on the left part of the pits, and the [421] step edge only appeared on the left side, never on the right side. Long time exposure to L-Glu did not lead to the straightening of the [421] step side. On the introduction of L-Lys solution, the etch pit morphology maintained a rhombic form, and there was no discernible effect in the first 10 min (Figure 1e1). However, 30 min later, the [421] step emerged on the left part of the pits, and the pit shape changed to sectorial and then was stable. On the introduction of 6-aminohexanoic acid, there were no discernible changes in the surface features. The (104) face retained a rhombohedral pattern without expression of newly formed step 3155
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Figure 3. Summary of the effects of organic acids on calcite etch pit shape at solution pH of 6.5: (A) deionized water, (B) Gly or malonate or succinate, (C) L-Asp, (D) L-Glu, (E) L-Lys, and (F) acetate or oxalate or glutarate or 6-aminohexanoate. The theoretical values of angles between step edges are depicted in the figure, and only the newly expressed step edge vectors are labeled for (B), (C), (D), (E), and (F).
edges. Longer exposure to 6-aminohexanoic acid only caused rounding of the obtuseobtuse corner, which is similar to the changes in pure water. No other modifications were observed with time. The weak effects of 6-aminohexanoic acid are quite different from those of the other four amino acids. In an attempt to find structure-related differences in etch pit morphology, five kinds of carboxylic acids were chosen for AFM study. Only two of them affected pit morphology. In Figure 2, the [421] direction appeared and coexisted with intrinsic Æ441æ steps in both malonic acid and succinic acid, a behavior that is similar to that of Gly. The hexagons clearly developed in malonic and succinic acid and were more regular than those developed in Gly after 30 min. The [421] step edges remained perfectly straight even after long exposure to malonate or succinate (Figure 2c3 and d3), which is different from Gly (Figure 1b3). The overall shape maintained the standard hexagonal pattern. The effects of malonate and succinate were almost the same, the only difference being in the ratio ([421] step length)/(Æ441æ step length). Surprisingly, acetate, oxalic acid, and glutaric acid showed no effect on pit morphology, and the calcite surface maintained its rhombohedral pattern (Figure 2). The influences of all of the organic acids are summarized in Figure 3. It is evident that chiral molecules like L-Asp, L-Glu, and L-Lys are symmetry-breaking, while achiral molecules like Gly, malonic acid, and succinic acid are symmetry-retaining with regard to the c-glide plane. Only for L-Asp is the expression of [010] step, which is direction specific. Molecules with different functional groups may have different or identical modifying effects.
4. DISCUSSION Steps associated with slower retreat rates will be those that are ultimately expressed, whereas those with faster retreat rates will grow out of existence.23 Thus, the finally preserved steps are those that are most stable and whose retreat velocities are the lowest. It can be therefore inferred that [481] and [441] steps
Figure 4. Atomic structure of the calcite (104) surface, top view. Dark green, Ca in plane; white, C in plane; yellow, O in plane; light red, O below the plane; red, O above the plane.27
have lower retreat rates in deionized water in comparison with [010] and [421] steps; that is, [010] and [421] steps are too active to be protected in pure water and disappear rapidly. The relatively higher stability of [481] and [441] steps and the lower stability of [010] and [421] steps in water can be interpreted in terms of calcite atomic structure. Unlike the alternate arrangement of Ca atoms and CO3 groups in the [481] and [441] directions, both [010] and [421] steps are bonded by either Ca atoms or CO3 groups (Figure 4). The CaCa distance is 4.05, 4.99, and 6.43 Å along the [421], [010], and Æ441æ directions, respectively. Thus, more Ca atoms are available for surface interactions at either [010] or [421] steps than at Æ441æ steps, and atoms along these two crystallographic directions also share a more polarized surrounding. These structural characteristics are 3156
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Figure 5. Solution stability constants (log K) for calcium chelating.29,3133
therefore responsible for the relatively higher energy of the [010] and [421] steps, and they can only be stabilized by adding foreign additives such as maleic acid,24 fluoride ion,10 and lithium ion.25 However, metal cations or anions are so small that they can easily incorporate into bulk structure,26 but amino acids are too big to enter the bulk of crystal,5 and they tend to adsorb onto the crystal surface through binding with their functional groups. From the AFM results, Gly, L-Asp, L-Glu, L-Lys, malonate, and succinate bring about visible modifications, while 6-aminohexanoate, acetate, oxalate, and glutarate show no influence on pit morphology. These variations in etch pit morphology induced by diverse organic acids illustrate that surface reactions are highly species specific. The expression of new step edges shows that the relative activity of step edges or step edge energy can be changed in the presence of organic acids. The expression of the [421] step in the presence of each of Gly, L-Glu, L-Lys, malonate, and succinate implies that step retreat perpendicular to the [421] direction is relatively slowed by these five organic acids through organic/inorganic interactions. The expression of the [010], [411], and [461] steps in L-Asp solution is similar. No modifying effects were observed for the other four organic acids, that is, 6-aminohexanoic acid, acetic acid, oxalic acid, and glutaric acid. These additives are evidently unable to stabilize any new steps besides Æ441æ. There are three possible explanations, no interaction between crystal face and the four additives, surface interactions that are too weak to stabilize new steps, or surface interactions only between Æ441æ steps and the four additives. No matter how the surface reaction proceeds, the only definite rule is that the ratio of v(new steps)/v(Æ441æ) has to be reduced for any new steps to be expressed.23 Surface reaction between crystal and additives may result from four mechanisms, surface complexation, electrostatic attraction, geometrical matching, and stereochemical correspondence, all of which have been discussed previously.23,28,29 However, the order
of importance of these four mechanisms for organic acids is not yet known. There is no agreement whether these organic acids are bound by one or more functional groups to the calcite (104) surface,23 nor is there agreement about the role of NH3þ in surface binding. For an isolated (104) layer (Figure 6A), each Ca atom in bulk is coordinated with six O atoms from different CO3 groups, four of which are coplanar while the other two are in planes below and above. Because of the breaking of ionic bonds between Ca and O atoms during cleavage, the cleaved (104) surface produces one dangling bond for each Ca site on surface (Figure 6B) and two dangling bonds for Ca atoms that are located at step edges of Æ441æ (Figure 6D), making them easy to form complexes with chelating ligands. A previous study30 has found that relaxation of the calcite (104) face is negligible after cleavage and it is hydrated in water in the form of two surface species, that is, >CaOH and >CO3Hþ, where “>” designates surface-bound. Depending on solution pH, >CaOH dominates in the basic regime, while >CO3Hþ dominates in the acidic regime. Thus, to bind Ca atoms on the (104) face, additives have first to replace the OH, for which water molecules compete with additives. One commonly accepted model is surface complexation where surface complexes are formed through chelating ligands. Surface complexation on the calcite (104) face can be represented as follows: > Ca þ H2 O T >CaOH þ Hþ
ð1Þ
> Ca þ L T > CaL
ð2Þ
where “>” again designates a surface-bound Ca atom and L stands for ligand. It is then suggested that the strength of surface chelation can be estimated in terms of the stability constant, log K, of the related Ca-additive complex in solution. Only those that 3157
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Figure 6. Atomic structure of a calcite {104} monolayer showing (A) atomic surroundings of step edges of an octagonal etch pit; (B) one dangling bond for Ca1; (C) three dangling bonds for Ca2; (D) two dangling bonds for Ca3; and (E) three dangling bonds for Ca4. Dark green, Ca in plane; light green, Ca below the plane; white, C in plane; light white, C below the plane; yellow, O in plane; light red, O below the plane; red, O above the plane. Dangling bonds of each atom are represented in the picture.27
have a K2 greater than K1 are able to substitute the >CaOHþ form on the surface.9 As shown in Figure 5, most of the additives that modify pit morphology have larger stability constants than the >CaOH complex. However, some of those like L-Lys with lower stability also affect pit morphology. On the other hand, the stability constant for the Caoxalate complex is 3, but our AFM study indicates that oxalic acid has no effect on pit morphology. Thus, despite the fact that chelating ligands can alter the microscopic mechanism of calcite dissolution, as documented by Perry et al.,34 the differences between the surface/ligand interaction and the solution ion/ligand interaction may make it difficult to relate the above stability constants to etch pit shape. Looking more directly at the surface interaction, the results for acetate suggest that a single carboxylate is unable to stabilize any steps other than Æ441æ. Acetate contains only one functional group (COO), and the carboxylate is able to coordinate with the Ca atom, but the CH3 group is inactive with respect to the surface. Three possibilities for the carboxylatecalcium binding are that only the carbonyl oxygen is bound to the Ca atom, only the hydroxyl oxygen is bound to the Ca atom, or that both oxygens are bound to a single Ca atom. Computer modeling35 suggested that methanoic acid adsorbs to a (104) surface by bridging two surface Ca atoms with a strong interaction with the carbonyl oxygen and a weaker one with the hydroxyl oxygen. The estimated CaO distances are 2.21 and 3.01 Å, respectively. Experimental results36 showed that the OO distance in acetate is 2.18 Å (Figure 7), which makes bridging possible in both [010] and [421] directions. However, neither of these emerged in the AFM experiments. This indicates that a single carboxylate is not sufficient, because only the carbonyl oxygen is strongly coordinated and the hydroxyl oxygen is only fixed by H-bonding with surface CO3Hþ or H2O molecules; that is, it is only held effectively by a single bond, and
this is not enough to stabilize new step edges by acetate or any single COO. The occurrence of the [421] direction in the presence of Gly, L-Glu, L-Lys, malonate, and succinate must then be ascribed to the combined effect of a carboxylate with one or more of the additional functional groups in these molecules. Similarly, the emergence of the [010] step in L-Asp solution must also be ascribed to a cooperative contribution of more than one functional groups. Thus, only a multiple bonded mode of attachment for the above organic acids on the calcite surface is tenable. Although the four dicarboxylic acids are negatively charged with the same pair of functional groups, their consequences for dissolution are widely different. What is most noticeable is that the ones that have a three- or four-carbon chain have strong effects on pit morphology, while those with shorter or longer chains have no influence. Apart from confirming that electrostatic attraction on its own is not effective in stabilizing, this strongly indicates that some degree of geometrical matching is important. Figure 7 shows that the carbonyl oxygens in the two carboxylate groups in oxalate, malonate, succinate, and glutarate are separated by 3.18, 3.43, 4.45, and 5.29 Å, respectively, and the two hydroxyl oxygens are separated by 3.12, 4.24, 4.49, and 7.25 Å, respectively. This means that malonate and succinate match relatively well with the [421] step edges, while oxalate and glutarate have a poorer match. Given that only malonate and succinate affect the morphology, the geometrical matching between adjacent Ca atoms and the two carboxylates must play a central role in the stabilization of the [421] step. Figure 6 shows that Ca atoms at step edges have a bonding environment different from those that lie on the (104) surface. Each surface Ca atom (Ca1 in Figure 6) has one dangling bond pointing upward, while each Ca atom at the [010] (Ca2 in Figure 6) or [421] (Ca4 in Figure 6) step edges has three dangling bonds. 3158
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Figure 7. Energy-optimized geometry of organic acids in aqueous solution, with OO and NO distances in angstroms. The one for acetate is a direct experimental result.36 Those for Gly,37 6-aminohexanoate,38 oxalate,39glutarate,38 succinate,38 malonate,38 and L-Asp40 are direct molecular modeling results, and the conformers of succinate, malonate, and L-Asp are in general agreement with experiment.4143 The one for L-Glu is a combined result from experiment and molecular modeling.4447 Note that the conformer of Gly in aqueous solution is almost the same as on calcite (104) surface,37,4850 and it can therefore be assumed that the (104) surface exerts little effect on the conformations of these organic acids in solution. Cartesian coordinates of the organic acids in the figure are available in Table S2 of the Supporting Information. The most stable conformer of L-Lys in aqueous solution was not found in the published literature and is not shown here.
This enables each Ca atom at [010] or [421] to form up to three chemical bonds with an additive molecule. Thus, step edge Ca atoms can have alternative binding geometries with a single carboxylate, either through a monodentate mode (bound to one oxygen of the carboxylate) or through a bidentate mode (bound with two oxygens of the carboxylate). Molecular modeling studies have provided some information about binding geometries of organic acids to calcite,35,37,51 silicon,52 fluorapatite,53 and hydroxyapatite54,55 surfaces. These show that both the carboxylate and the ammonium groups can coordinate with Ca atoms. The preferred view of the mechanism is that proton transfer occurs at the hydroxyl oxygen enabling H-bonding between hydroxyl oxygen and surface CO3Hþ groups or between hydroxyl oxygen and H2O molecules. Hydrogens of the NH3þ group are also capable of H-bonding with carbonate oxygens or H2O molecules. However, the carboxyl group is a highly polar functional group because of the presence of both the strongly polarized carbonyl (CdO) group and the hydroxyl (OH) group. Electron density can be drawn from the hydroxyl hydrogen through the conjugated carboxyl group, allowing the easy release of the proton from the hydroxyl oxygen, which can then participate in H-bonding. Dudev et al.56,57 have systematically investigated the factors that control the carboxylate-binding mode. Their results indicated that a key factor is the availability and type of interactions between the metal-free carboxylate O atom and its neighbors. If a hydrogen bond is formed between metal-free carboxylate O and its neighbors (such as water molecules), then the monodentate mode is preferred over the bidentate. Katz et al.58 found that only monodentate binding occurs if the Ca2þ coordination number is 6. All of these arguments are consistent with a preferred monodentate binding for Cacarboxylate. This still leaves open the question as to which of the carboxylate oxygens is bound because both the carbonyl Ocarbonyl O and the hydroxyl Ohydroxyl O distances in malonate and succinate satisfy the required geometrical match along the [421] direction.
The carbonyl oxygen of methanoic acid was found by simulation to interact more strongly than hydroxyl oxygen with Ca atoms on calcite (104) surface.35 Xiang et al.59 also used simulation to show that the order of binding strength in glutamic Ca2þ binding in the gas phase is carbonyl O > amino N > hydroxyl O. On the basis of the carbonyl binding being the strongest of the three, the malonate should bind more strongly than Gly, and it should bond through the carbonyl groups not the hydroxyls. This is consistent with the observation that the [421] step edge developed in malonate is straighter than that in Gly. The difference in binding strength between CaO(CdO) and CaN can be rationalized as follows. The nitrogen atom is less accessible than the carbonyl oxygen because of the steric hindrance exerted by the three hydrogens of the NH3þ group, and the electrostatic repulsion between NH3þ and CaOHþ is also unfavorable for CaN interaction.35 Hence, two binding geometries can be suggested for malonate (Figure 8) and succinate. In mode a, the two carbonyl oxygens form bonding with adjacent Ca atoms at a [421] step edge, while the two hydroxyl oxygens H-bond with H2O in bulk solution. In mode b, the two carbonyl oxygens are bound with adjacent Ca atoms at a [421] step edge; one hydroxyl oxygen points upward and H-bonds with H2O in bulk solution (it is too far away from surface CO3Hþ37), and the other hydroxyl oxygen H-bonds with a surface CO3Hþ with or without proton transfer. Figure 4 shows that the three oxygen atoms bound with one carbon share the same CO bond length of 1.29 Å. One lies in the (104) plane, while the other two are below and above. Thus, only the O atom of the CO3 group that sits in or above the (104) plane is able to accept protons from water or from the carboxyl group so as to H-bond with hydroxyl oxygen. Moreover, the protruding O will be more active than the in-plane O for H-bonding because it has one dangling bond, while the in-plane O has no dangling bond (Figure 6). Our proposed structure in Figure 8 therefore allows greater possibility for proton transfer from the acidic COOH group to the protruding O. 3159
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Figure 8. Schematic diagram of malonate binding at a [421] step edge. H-bonds are represented as dotted lines, and CaO bonds are represented in stick form.
Figure 9. Schematic diagram for Gly binding at a [421] step. H-bonds are represented by dotted lines, and CaO and CaN bonds are represented in stick form.
The carbonyl Ocarbonyl O distances of succinate and glutarate also satisfy the geometrical matching at the [010] steps, but this was not expressed in the AFM images. This can be interpreted in terms of step edge reactivity and stereochemical correspondence. As the [421] steps have a much more polarized surrounding than [010] and there is a different arrangement of O atoms along the two directions (Figure 4), there will be a difference in CaO(CdO) binding and different atomic surroundings for H-bonding. It is clear that single carboxylate is unable to stabilize the [010] or [421] directions, so the stabilization of [421] in Gly solution must be a combined result of R-COO and R-NH3þ. The similarity of the molecular skeleton of Gly and malonate (Figure 7) suggests that they should behave similarly, as observed, if the positively charged NH3þ group can play a similar
but slightly weaker role to the COO group. Because they are oppositely charged, it seems that electrostatic interaction is no longer important for surface binding. Possible binding geometries for Gly are illustrated in Figure 9. The binding of carboxylate to the Ca atom is the same as for malonate, while the ammonium group can bind to a Ca atom by N as well as H-bonding with a surface CO3 group or H2O molecules. In mode a, N and carbonyl O are both bound to Ca atoms, and the hydroxyl O forms an H-bond with a surface CO3Hþ. Mode b is almost the same as mode a with an additional H-bond between the amino H and carbonate O, and in mode c, the N and carbonyl O are still bound to Ca atoms, but amino H and hydroxyl O H-bond with H2O. Instead of [421], L-Asp brings about the expression of [010]. If R-NH3þ in L-Asp (Figure 7) does not function as a participant in surface binding, then the modifying effect of L-Asp would be the 3160
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Crystal Growth & Design same as that of succinate or malonate. The difference means that the R-NH3þ of L-Asp should play a part, which promotes the expression of [010] instead of [421]. The main difference between the [010] and [421] directions is the arrangement of O atoms, and therefore there is a different atomic surrounding for H-bonding (Figure 4). The distribution of oxygen atoms along the [010] has a higher density than that in [421] direction, and this makes O atoms more available along the [010] steps. We note that the mechanism of the L-Asp interaction with [010] has nothing to do with chirality because [010] is also expressed anisotropically in D-Asp at pH 6.5 (data not shown). Molecular modeling6 suggests that five H2O molecules have to be replaced at obtuse steps for Asp-step interactions, while only four H2O molecules need to be replaced at acute steps. Reduced displacement of adsorbed waters by L-Asp at the acute steps leads to a lower energy barrier for interaction and therefore produces negative interaction energy (acute versus obtuse steps). Thus, the [010] step is always expressed on the acute side of the etch pits. In addition to [010], the step edges [461] and [411] were also stabilized by L-Asp, which is generally consistent with a recent study.22 Ca atoms in the [461] direction are separated by 15.72 Å, and those at [411] steps are separated by 9.51 Å. Such a long distance is apparently beyond the bridging capability of L-Asp molecules, but the structure at the higher index steps is less easy to interpret. The etch pits developed in L-Glu took on a different morphology from L-Asp, although the functional groups are the same. In L-Glu solution, [461] and [010] steps were not observed, and [481] was not affected. The equilibrium shape was a pseudotriangle, consisting of [411]o, [481] and the curved [421] steps (Figures 1 and 3). We attribute the expression of [421] to the joint effects of R-COO and R-NH3þ just as in Gly. The step edge bending probably arises from the R group of L-Glu. Geometrical matching is not satisfied for the two carbonyl oxygens in L-Glu (separated by 5.94 Å in Figure 7), and only the distance between R-COO and R-NH3þ groups match well with the [421] (the NO(CdO) distance is 3.54 Å in Figure 7). The γ-COO group can assist in enantiospecific binding, which leads to asymmetrical expression of the [421] step edges with respect to the c-glide plane. Because modification is more severe on the left part of the etch pits, the morphological symmetry about the c-glide plane is also destroyed, showing that the anisotropic expression of the [421] step edge results from molecular chirality. [411]o was present in both L-Asp and L-Glu, so the stabilization of [411]o in L-Glu may share the same interaction mechanism as that in L-Asp. The etch pit shape evolved in L-Lys solution appears most similar to that in L-Glu. As shown in Figure 1e, only [421] was expressed on the left part of the etch pits; the other original Æ441æ steps were unaffected and coexist with the newly expressed [421] step. The effect was less than for L-Glu because the longer chain of the R group leads to worse geometrical matching and the ε-NH3þ at the end of the R group in L-Lys is relatively less active than γ-COO for surface binding. Hence, the expression of [421] results from the cooperative binding of R-COO and R-NH3þ groups. It is worth noting that positively charged L-Lys (the calcite (104) surface is positively charged at a pH of 6.5) still exerts an influence on pit morphology and the newly expressed step was also direction specific. This suggests that electrostatic attraction plays a weak role in surface interaction and the dominant role is still geometrical matching for the L-Lys-calcite system because 6-aminohexanoate with one less R-NH3þ than
ARTICLE L-Lys
showed no effect. The qualitative conclusion is that R-amino acids whose side chain is longer than that of Asp should induce a modification similar that of to Glu or Lys, with a onesided expression of the [421] step, which is sensitive to molecular chirality. In addition, the functional group on the side chain in L-Glu and L-Lys must be involved in surface binding. Otherwise, the etch pit shape cannot be enantiospecific and should be the same as in Gly.51 The distance of NO(CdO) in 6-aminohexanoate is 7.72 Å (Figure 7), which sits between 6.84 Å (double the N O(CdO) distance in Gly) and 8.10 Å (double 4.05 Å) and therefore matches with two alternate Ca atoms at the [421] step. However, [421] was never observed in 6-aminohexanoate, implying that geometrical matching is only effective for adjacent Ca sites. In addition to the surface reactions discussed above, a recent study has indicated that organic modifier such as L-Asp affects the surface diffusion of calcium and carbonate ions through rearrangement of the structure of water bound on the calcite surface, thereby affecting the kinetics of calcite growth.60 This again implies the multiplicity of the effects of modifiers, including chemical, structural, thermodynamic, and kinetics factors, as suggested by Orme et al.5 However, the direct observation of etch pit morphology in the presence of organic acids from this work suggests the paramount role of geometrical matching in surface modification during dissolution.
5. CONCLUSIONS The differences in developed etch pit morphology between L-Asp and L-Glu, Gly and 6-aminohexanoate, oxalate and malonate, and succinate and glutarate highlight the paramount importance of geometrical matching in organic/inorganic recognition. Furthermore, step edge reactivity, stereochemical correspondence, and molecular chirality are also important, while electrostatic interaction plays a minor role. Chiral molecules will break the symmetry of etch pit with regard to the c-glide plane, and the anisotropic appearance of new steps primarily arises from stereochemical correspondence between the surface and molecules. Comparison of the results between L-Asp and succinate, L-Glu and glutarate, and L-Lys and 6-aminohexanoate demonstrates the significant role of R-NH3þ in surface bindings. Single carboxylate is incapable of stabilizing new step edges; amino acids and carboxylic acids prefer to use at least two functional groups to bind to the crystal surface or at step edges. The R-NH3þ group in amino acid is also active in calcite surface binding and can play a similar part to the COO group. Basic amino acids like L-Lys also have the potential for surface modification, although the effect is not as strong as the acidic ones. Simple carboxylic acids such as malonic acid and succinic acid can mimic the functions of amino acids at the crystal surface and may therefore serve as substitutes for amino acids in biomaterial fabrication. ’ ASSOCIATED CONTENT
bS
Supporting Information. Ionic formulas and pKa values, and the Cartesian coordinates for the optimized geometries of all of the organic acids in aqueous solution. This material is available free of charge via the Internet at http://pubs.acs.org.
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’ AUTHOR INFORMATION Corresponding Author
*Tel.: (þ86)532-8698-1569 (H.X.), (þ44)-161-306-3926 (J.R.L.). E-mail:
[email protected] (H.X.),
[email protected] (J.R.L.).
’ ACKNOWLEDGMENT We thank Dr. Zijing Lin at the University of Science and Technology of China for providing the Cartesian coordinates of the lowest energy conformer of L-Asp in aqueous solution. We also thank Dr. R. K. Thomas, University of Oxford, for critical reading of this manuscript and for providing valuable comments. We are grateful for funding support from the National Natural Science Foundation of China (Grants No. 21071151) and the U.K. Engineering and Physical Sciences Research Council (EPSRC). ’ REFERENCES (1) Aizenberg, J. MRS Bull. 2010, 35, 323–330. (2) De Yoreo, J. J.; Dove, P. M. Science 2004, 306, 1301–1302. (3) De Yoreo, J. J.; Wierzbickib, A.; Dove, P. M. CrystEngComm 2007, 9, 1144–1152. (4) Qiu, S. R.; Wierzbicki, A.; Salter, E. A.; Zepeda, S.; Orme, C. A.; Hoyer, J. R.; Nancollas, G. H.; Cody, A. M.; De Yoreo, J. J. J. Am. Chem. Soc. 2005, 127, 9036–9044. (5) Orme, C. A.; Noy, A.; Wierzbicki, A.; McBride, M. T.; Grantham, M.; Teng, H. H.; Dove, P. M.; De Yoreo, J. J. Nature 2001, 411, 775–779. (6) Kim, I. W.; Giocondi, J. L.; Orme, C. A.; Collino, S.; Spencer Evans, J. Cryst. Growth Des. 2008, 8, 1154–1160. (7) Elhadj, S.; Salter, E. A.; Wierzbicki, A.; De Yoreo, J. J.; Han, N.; Dove, P. M. Cryst. Growth Des. 2006, 6, 197–201. (8) Elhadj, S.; De Yoreo, J. J.; Hoyer, J. R.; Dove, P. M. Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 19237–19242. (9) Teng, H. H.; Dove, P. M. Am. Mineral. 1997, 82, 878–887. (10) Vavouraki, A. I.; Putnis, C. V.; Putnis, A.; Koutsoukos, P. G. Cryst. Growth Des. 2010, 10, 60–69. (11) Teng, H. H. Spectroscopy 2005, 20, 16–20. (12) Hillner, P. E.; Gratz, A. J.; Manne, S.; Hansma, P. K. Geology 1992, 20, 359–362. (13) Stephenson, A. E.; De Yoreo, J. J.; Wu, L.; Wu, K. J.; Hoyer, J.; Dove, P. M. Science 2008, 322, 724–727. (14) Davis, K. J.; Dove, P. M.; De Yoreo, J. J. Science 2000, 290, 1134–1137. (15) Teng, H. H.; Dove, P. M.; Orme, C. A.; De Yoreo, J. J. Science 1998, 282, 724–727. (16) Teng, H. H. Geochim. Cosmochim. Acta 2004, 68, 253–262. (17) Teng, H. H.; Dove, P. M.; De Yoreo, J. J. Geochim. Cosmochim. Acta 1999, 63, 2507–2512. (18) Teng, H. H.; Dove, P. M.; De Yoreo, J. J. Geochim. Cosmochim. Acta 2000, 64, 2255–2266. (19) Churchill, H.; Teng, H.; Hazen, R. M. Am. Mineral. 2004, 89, 1048–1055. (20) Liang, Y.; Baer, D. R. Surf. Sci. 1997, 373, 275–287. (21) Harstad, A. O.; Stipp, S. L. S. Geochim. Cosmochim. Acta 2007, 71, 56–70. (22) Yoshino, T.; Kagi, H.; Kamiya, N.; Kokawa, R. J. Cryst. Growth 2010, 312, 1590–1598. (23) Teng, H. H.; Chen, Y.; Pauli, E. J. Am. Chem. Soc. 2006, 128, 14482–14484. (24) Hong, Q.; Suarez, M. F.; Coles, B. A.; Compton, R. G. J. Phys. Chem. B 1997, 101, 5557–5564. (25) Ruiz-Agudo, E.; Kowacz, M.; Putnis, C. V.; Putnis, A. Geochim. Cosmochim. Acta 2010, 74, 1256–1267. (26) Paquette, J.; Reeder, R. J. Geochim. Cosmochim. Acta 1995, 59, 735–749.
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