H. Henry Teng

Formation of chiral morphologies through selective binding of amino acids to calcite surface steps

Many living organisms contain biominerals and composites with finely tuned properties, reflecting a remarkable level of control over the nucleation, growth and shape of the constituent crystals. Peptides and proteins play an important role in achieving this control. But the general view that organic molecules affect mineralization through stereochemical recognition, where geometrical and chemical constraints dictate their binding to a mineral, seems difficult to reconcile with a mechanistic understanding, where crystallization is controlled by thermodynamic and kinetic factors. Indeed, traditional crystal growth models emphasize the inhibiting effect of so-called ‘modifiers’ on surface-step growth, rather than stereochemical matching to newly expressed crystal facets. Here we report in situ atomic force microscope observations and molecular modelling studies of calcite growth in the presence of chiral amino acids that reconcile these two seemingly divergent views. We find that enantiomer-specific binding of the amino acids to those surface-step edges that offer the best geometric and chemical fit changes the step-edge free energies, which in turn results in macroscopic crystal shape modifications. Our results emphasize that the mechanism underlying crystal modification through organic molecules is best understood by considering both stereochemical recognition and the effects of binding on the interfacial energies of the growing crystal.

Kinetics of calcite growth: Surface processes and relationships to macroscopic rate laws

This study links classical crystal growth theory with observations of microscopic surface processes to quantify the dependence of calcite growth on supersaturation, σ, and show relationships to the same dependencies often approximated by affinity based expressions. In situ Atomic Force Microscopy was used to quantify calcite growth rates and observe transitions in growth processes on {104} faces in characterized solutions with variable σ. When σ < 0.8, growth occurs by step flow at surface defects, including screw dislocations. As σ exceeds 0.8, two-dimensional surface nucleation becomes increasingly important. The single sourced, single spirals that are produced at lower σ were examined to measure rates of step flow and the slopes of growth hillocks. These data were used to obtain the surface-normal growth rate, Rm, by the pure spiral mechanism. The dependence of overall growth rate upon dislocation source structure was analyzed using the fundamentals of crystal growth theory. The resulting surface process-based rate expressions for spiral growth show the relationships between Rm and the distribution and structures of dislocation sources. These theoretical relations are upheld by the process-based experimental rate data reported in this study. The analysis further shows that the dependence of growth rate on dislocation source structures is essential for properly representing growth. This is because most growth sources exhibit complex structures with multiple dislocations. The expressions resulting from this analysis were compared to affinity-based rate equations to show where popular affinity-based rate laws hold or break down. Results of this study demonstrate that the widely used second order chemical affinity-based rate laws are physically meaningful only under special conditions. The exponent in affinity-based expressions is dependent upon the supersaturation range used to fit data. An apparent second order dependence is achieved when solution supersaturations are very near equilibrium and growth occurs only by simple, single sourced dislocation spirals. These findings indicate the need to apply caution when deducing growth mechanisms and rate laws from temporal changes in bulk solution chemistry. Observations of various types of surface defects that give rise to step formation suggest that popular ‘rate laws’ are sample-dependent composites of rate contributions from each dislocation structure.

Reversed calcite morphologies induced by microscopic growth kinetics: Insight into biomineralization

Abstract This experimental investigation of calcite growth quantifies relationships between solution supersaturation and the rates of step advancement. Using in situ fluid cell atomic force microscopy (AFM), we show that the movement of monomolecular steps comprising growth hillocks on {10 1 4} faces during the growth of this anisotropic material is specific to crystallographic direction. By quantifying the sensitivity of step growth kinetics to supersaturation, we can produce spiral hillocks with unique geometries. These forms are caused by a complex dependence of step migration rates, vs+ and vs−, upon small differences in solution chemistry as they grow normal to the conventional fast ([ 4 41]+ and [48 1 ]+) and slow ([ 4 41]− and [48 1 ]−) crystallographic directions. As solute activity, a, decreases, vs+ and vs− converge and growth hillocks express a pseudo-isotropic form. At still lower supersaturations where a approaches its equilibrium value, ae, an inversion in the rates of step advancement produces hillocks with unusual reversed geometries. Comparisons of the kinetic data with classical theoretical models suggest that the observed behavior may be due to minute impurities that impact the kinetics of growth through blocking and incorporation mechanisms. These findings demonstrate the control of crystallographic structure on the local-scale kinetics of growth to stabilize the formation of unusual hillock morphologies at the near-equilibrium conditions found in natural environments.

Surface site-specific interactions of aspartate with calcite during dissolution; implications for biomineralization

Abstract Calcite occurs widely as a mineral component in the exoskeletons and tissues of marine and freshwater invertebrates. Matrix macromolecules involved in regulating the biological growth of calcite in these organisms are known to share a carboxylic-rich character that arises from an abundance of the acidic amino acids aspartate (Asp) and glutamate (Glu). This study determines the interactions of Asp with calcite {101̄4} faces during dissolution using in situ fluid-cell atomic force microscopy (AFM) and macroscopic ex situ optical methods. In control experiments, etch-pit morphologies produced_by dissolution in simple undersaturated solutions reflect the inherent symmetry of the {101̄4} faces with a rhombus form. With the introduction of Asp. surface site reactivities are modified to yield isosceles triangular etch pits and hillocks. With continued exposure to Asp-bearing solutions, these triangular pits coalesce and the surface evolves into a network of interconnected tetrahedral etch hillocks. The component tetrahedral “sides”have Miller-Bravais indices of (0001), (1̄101), and (01̄11). These faces intersect the (101̄4) face in the [01̄0], [451̄], and [4̅11] directions to compose the tlnee edges of the triangular etch pits. Structural and stereochemical contraints suggest that the (1̄101) and (01̄11) faces in the hillock are a combination of corresponding faces from the {1102} and {1̄100} crystallographic forms. Results of this dissolution study are consistent with previous growth experiments showing that Asp causes preferential development of the {0001} and possibly the {1̄100} forms of calcite. These observations support mechanisms proposing that the new forms are stabilized by the molecular recognition of Asp functional groups for specific surface sites. Because Asp stabilizes identical faces during growth and dissolution, we suggest that dissolution studies offer an alternative means of determining the crystal forms that develop during biomineralizing processes and a more direct means of identifying those surface sites involved. We demonstrate that the stability of crystallographic directions expressed by step edges is controlled by the relative reactivities of surface sites. Our findings yield new insights into surface structure controls on mineral reactivity.

Resolving orthoclase dissolution processes with atomic force microscopy and X-ray reflectivity

Abstract Direct measuremens of orthoclase (001) were performed using in situ atomic force microscopy (AFM) and synchrotron X-ray reflectivity to reveal the A-scale dissolution process as a function of pH and temperature. Distinct processes were observed, involving mainly terrace roughening at pH = 1.1 and step motion at pH = 12.9. A gel-like surface coating was observed to form at acidic pH under slow fluid flow-rate conditions. No coating was observed either at alkaline pH or at acidic pH under high fluid flow-rate conditions. The corresponding dissolution rates were measured directly at pH = 1.1 and 12.9 at ∼50°C using real-time X-ray reflectivity measurements, and reacted interface structures were derived from crystal truncation rod measurements after reaction at both acidic and alkaline pH. Our observations reveal, under these experimental conditions, that 1) orthoclase dissolution is controlled by at least two separate surface reactions having distinct reactive sites; 2) dissolution is stoichiometric at alkaline pH and only minimally nonstoichiometric (limited to one unit-cell depth) at acidic pH; previously identified nonstoichiometric layer thicknesses derived from macroscopic measurements are associated with the formation of the gel-like coatings; 3) dissolution rates measured at freshly cleaved (001) surfaces are comparable to those derived from steady-state powder dissolution rates for both alkaline and acidic pH; and 4) elevated transient dissolution rates are not observed for freshly cleaved surfaces but are obtained under alkaline conditions after reacting the orthoclase (001) surface at acidic pH. These observations clarify differences in orthoclase dissolution mechanisms as a function of pH, demonstrate the utility of AFM and X-ray scattering methods for measuring A-scale structures and face-specific dissolution rates on single crystals and place new constraints on the understanding of alkali feldspar weathering processes.

Controls by saturation state on etch pit formation during calcite dissolution

Dissolution experiments were conducted on {1014} cleavage faces of calcite at various under-saturations to determine how the saturation state controls etch pit formation. Experimental observations were made by using in situ fluid cell Atomic Force Microscopy. Three dissolution modes were observed. When the saturation index Ω > 0.541, no etch pit formation was seen and dissolution primarily occurred at existing steps. When Ω decreased to Ωc = 0.541–0.410, the first visible pits appeared and continuous reduction in saturation state slowly increased the pit density on terraces while dissolution simultaneously proceeded at step edges. Finally, when the saturation state fell below Ωmax = ∼0.007, a precipitous increase in pit density took place that sharply contrasted to the ordered fashion of pit formation observed at saturation conditions above this level. These observations are interpreted to be two-dimensional and unassisted pit formation at Ω 0.541. The values of Ωc are in good agreement with the dislocation theorys predicted critical under-saturations for pit formation at line dislocations. The occurrence of Ωmax is not directly predicted but is a logical consequence of dissolution thermodynamics. These findings suggest that (1) dissolution near and far from equilibrium (i.e., Ω > Ωc, Ω < Ωmax) is not controlled by dislocations, therefore (2) dislocation density should significantly impact dissolution rate only in the saturation range of Ωmax < Ω < Ωc; (3) dissolution kinetics and chemical affinity of dissolution reactions should have a non-linear relationship: at sufficiently close to equilibrium, when dislocations cannot open up to form etch pits, the dissolution kinetics will be limited by the number of existing steps; at far from equilibrium, when pits are able to form in defect-free regions, the dissolution rate will be capped by the maximum number of achievable steps. These findings may provide explanations for several well-observed geochemical relationships, including the weak dependence of dissolution rate upon dislocation density in distilled water and the ‘plateau’ behavior of dissolution kinetics both near and far from equilibrium. The explosive occurrence of unassisted pit nucleation at Ω ∼ Ωmax is not predicted by the current dissolution rate equations. This suggests that an accurate ‘general’ rate law describing universal dissolution processes has yet to be developed.

Atomic-scale structure of the orthoclase (001)-water interface measured with high-resolution x-ray reflectivity.

In situ X-ray specular reflectivity and atomic force microscopy were used to determine the structure of the orthoclase (001) cleavage surface in contact with deionized water at 25°C. These are the first in situ measurements of the orthoclase–water interface structure performed to Angstrom-scale resolution. The orthoclase (001) cleavage surface has minimal roughness, and only one of two possible surface terminations is exposed. The X-ray data show that (1) the silica network at the orthoclase surface is terminated by an oxygen-containing species (e.g., O or OH) having a coverage of 1.9 ± 0.25 ML (the expected coverage is 2.0 ML, where 1 ML = 1 atom/55.76 A2), (2) the outermost layer of K+ ions have been removed with a derived coverage of 0.0 ± 0.08 ML (the bulk truncated K+ coverage is 1.0 ML), and (3) a complex relaxation profile affecting the near-surface structure propagates ∼26 A into the orthoclase with a maximum relaxation of ∼0.15 A near the surface. These data are inconsistent with K+ ion depletion below the topmost K+ layer. These results provide a new baseline for understanding the initial steps of the feldspar dissolution process, demonstrate the power of combining X-ray scattering techniques with scanning probe microscopies for understanding the intrinsic characteristics of complex mineral–water interface systems, and suggest a new approach for understanding feldspar dissolution mechanisms.

Cellular dissolution at hypha- and spore-mineral interfaces revealing unrecognized mechanisms and scales of fungal weathering

Fungus-mineral interactions play unparalleled roles in shaping the planet Earth but are underappreciated relative to bacterial influences. Unique to fungus, but largely unknown, are the interfacial processes and extensiveness of hypha- versus spore-mineral interactions given the associated turgor pressure differences and the vast contact areas between mycelia and minerals in the critical zone. Here we examine lizardite [Mg3Si2O5(OH)4] dissolution by single cells of a native fungal strain using confocal laser scanning microscopy, atomic force microscopy, and transmission electron microscopy–energy dispersive X-ray spectroscopy to explore the mechanism, driving force, and magnitude of the interfacial reactions. Results from our inspection showed (1) significant pH reduction in the vicinity of cells upon mineral surface attachment, (2) exclusive Fe loss from the mineral at the cell-mineral interfaces, and (3) destruction of the mineral crystal structure below the area colonized by hyphae but not that by spores. Compared to the results from bulk experiments and at the mineral-water interface, these observations indicate that (1) only attached cells release siderophores and (2) biomechanical forces of hyphal growth are indispensable for fungal weathering and strong enough to breach the mineral lattice. Estimated mineral mass loss at the interface suggests that cellular dissolution can ultimately account for ∼40%–50% of the overall bio-weathering, significantly larger than the previous estimate of ∼1% contribution.

Serpentine Dissolution in the Presence of Bacteria Bacillus mucilaginosus

Dissolution of serpentine in the presence of soil bacteria Bacillus mucilaginosus is examined through solution chemistry analysis, X-ray diffraction and 3D X-ray microscopy. Microbe-mineral interactions were carried out by incubating serpentine powder and the bacteria for 30 days. Measured Mg concentrations in the culture media were significantly higher than that in any of the control experiments at any time during the experiments. However, the behavior of the Mg/Si ratio was similar to what was known for inorganic dissolution of silicate minerals. XRD analysis revealed increased quantity of amorphous components in the reacted mineral samples, and tomography images showed a very porous and powdered appearance of the dissolved serpentine grains. These data suggest the dissolution probably proceeds through an incongruent route. Further, these observations imply that there is little genetic control by the microbes during the bacteria-mineral interaction; rather, the accelerated dissolution results primarily from a biologically induced process. Finally, the observed pH decrease, the presence of carboxylic acid, ketone, aldehyde, phenol, and alcohol in the metabolites suggests that organic acids and ligands secreted by the bacteria are largely responsible for the accelerated mineral dissolution.

Solution-chemistry control of Mg2+-calcite interaction mechanisms: Implication for biomineralization

Abstract We investigated the effect of Mg2+ on calcite hillock growth over a broad range of solution conditions in terms of supersaturation (Ωcalcite) and Mg/Ca ratios using atomic force microscopy and secondary ion mass spectrometry. We found that both the incorporation pattern/incorporated Mg2+ quantity in the hillock structure and the Mg2+-induced morphological change of the hillock surface showed strong dependence of the growth conditions. Specifically, when Mg/Ca was high (i.e., >5) and Ωcalcite was low (i.e., ~0.45), Mg2+ was predominantly incorporated into the negative sectors of the hillock structure, resulting in gradual loss of step structure and morphological amorphism on these vicinal surfaces. When Mg/Ca and Ωcalcite were in intermediate ranges (i.e., Mg/Ca < 5, and 0.45 < Ωcalcite < 1), the originally straight edges of the hillock steps exhibited curvatures of varying degrees and formed “tear-drop” morphologies. It is noted that such “tear-drop” morphology was stable within the duration of the experiments and did not evolve into other surface patterns. By contrast, when both Mg/Ca and Ωcalcite were high (i.e., Mg/Ca > 5, and Ωcalcite > 1.1), the growing hillocks experienced two phases of morphological changes, initiated with the formation of “tear-drops” followed by the development of linear ruptures along [481] and [441] directions. And the occurrence of these ruptures segmented the hillock surface effectively into multiple isolated plateaus. Significantly, we revealed the underlying mechanisms for these condition-specific effects of Mg2+ on calcite growth, which mainly resulted from the interplay among three major factors: (1) the size-mismatch between Mg2+ and Ca2+ that causes structural strains in magnesian calcite and leads to morphological amorphism in high-Mg carbonate; (2) the asymmetry of the calcite crystal structure that sets a physical limitation for Mg2+ incorporation patterns in the hillock structure; and (3) the step advancing rate (i.e., the calcite growth kinetics) that affects both Mg2+ incorporation and the accommodation of Mg2+-induced structural strains in the hillock structure. Detailed discussions were given for each growth scenario. The results of our study provide a theoretical base to decipher the roles of Mg2+ in CaCO3 mineralization, and thus, have important implication for a range of processes that involve the growth of Mg-Ca-CO3 systems, such as biomineralization, carbon capture and storage, and scale controls in industrial settings.