Adam F. Wallace

Crystallization by particle attachment in synthetic, biogenic, and geologic environments

Growing crystals by attaching particles Crystals grow in a number a ways, including pathways involving the assembly of other particles and multi-ion complexes. De Yoreo et al. review the mounting evidence for these nonclassical pathways from new observational and computational techniques, and the thermodynamic basis for these growth mechanisms. Developing predictive models for these crystal growth and nucleation pathways will improve materials synthesis strategies. These approaches will also improve fundamental understanding of natural processes such as biomineralization and trace element cycling in aquatic ecosystems. Science, this issue 10.1126/science.aaa6760 Materials nucleate and grow by the assembly of small particles and multi-ion complexes. BACKGROUND Numerous lines of evidence challenge the traditional interpretations of how crystals nucleate and grow in synthetic and natural systems. In contrast to the monomer-by-monomer addition described in classical models, crystallization by addition of particles, ranging from multi-ion complexes to fully formed nanocrystals, is now recognized as a common phenomenon. This diverse set of pathways results from the complexity of both the free-energy landscapes and the reaction dynamics that govern particle formation and interaction. Whereas experimental observations clearly demonstrate crystallization by particle attachment (CPA), many fundamental aspects remain unknown—particularly the interplay of solution structure, interfacial forces, and particle motion. Thus, a predictive description that connects molecular details to ensemble behavior is lacking. As that description develops, long-standing interpretations of crystal formation patterns in synthetic systems and natural environments must be revisited. Here, we describe the current understanding of CPA, examine some of the nonclassical thermodynamic and dynamic mechanisms known to give rise to experimentally observed pathways, and highlight the challenges to our understanding of these mechanisms. We also explore the factors determining when particle-attachment pathways dominate growth and discuss their implications for interpreting natural crystallization and controlling nanomaterials synthesis. ADVANCES CPA has been observed or inferred in a wide range of synthetic systems—including oxide, metallic, and semiconductor nanoparticles; and zeolites, organic systems, macromolecules, and common biomineral phases formed biomimetically. CPA in natural environments also occurs in geologic and biological minerals. The species identified as being responsible for growth vary widely and include multi-ion complexes, oligomeric clusters, crystalline or amorphous nanoparticles, and monomer-rich liquid droplets. Particle-based pathways exceed the scope of classical theories, which assume that a new phase appears via monomer-by-monomer addition to an isolated cluster. Theoretical studies have attempted to identify the forces that drive CPA, as well as the thermodynamic basis for appearance of the constituent particles. However, neither a qualitative consensus nor a comprehensive theory has emerged. Nonetheless, concepts from phase transition theory and colloidal physics provide many of the basic features needed for a qualitative framework. There is a free-energy landscape across which assembly takes place and that determines the thermodynamic preference for particle structure, shape, and size distribution. Dynamic processes, including particle diffusion and relaxation, determine whether the growth process follows this preference or another, kinetically controlled pathway. OUTLOOK Although observations of CPA in synthetic systems are reported for diverse mineral compositions, efforts to establish the scope of CPA in natural environments have only recently begun. Particle-based mineral formation may have particular importance for biogeochemical cycling of nutrients and metals in aquatic systems, as well as for environmental remediation. CPA is poised to provide a better understanding of biomineral formation with a physical basis for the origins of some compositions, isotopic signatures, and morphologies. It may also explain enigmatic textures and patterns found in carbonate mineral deposits that record Earth’s transition from an inorganic to a biological world. A predictive understanding of CPA, which is believed to dominate solution-based growth of important semiconductor, oxide, and metallic nanomaterials, promises advances in nanomaterials design and synthesis for diverse applications. With a mechanism-based understanding, CPA processes can be exploited to produce hierarchical structures that retain the size-dependent attributes of their nanoscale building blocks and create materials with enhanced or novel physical and chemical properties. Major gaps in our understanding of CPA. Particle attachment is influenced by the structure of solvent and ions at solid-solution interfaces and in confined regions of solution between solid surfaces. The details of solution and solid structure create the forces that drive particle motion. However, as the particles move, the local structure and corresponding forces change, taking the particles from a regime of long-range to short-range interactions and eventually leading to particle-attachment events. Field and laboratory observations show that crystals commonly form by the addition and attachment of particles that range from multi-ion complexes to fully formed nanoparticles. The particles involved in these nonclassical pathways to crystallization are diverse, in contrast to classical models that consider only the addition of monomeric chemical species. We review progress toward understanding crystal growth by particle-attachment processes and show that multiple pathways result from the interplay of free-energy landscapes and reaction dynamics. Much remains unknown about the fundamental aspects, particularly the relationships between solution structure, interfacial forces, and particle motion. Developing a predictive description that connects molecular details to ensemble behavior will require revisiting long-standing interpretations of crystal formation in synthetic systems, biominerals, and patterns of mineralization in natural environments.

Microscopic Evidence for Liquid-Liquid Separation in Supersaturated CaCO3 Solutions

Making Crystals The initial transition from a disordered solution to the formation of nuclei that grow into crystals continues to be a puzzle. Recent experiments suggested the formation of stable ordered clusters that appear prior to the formation of the first nuclei. Wallace et al. (p. 885; see the Perspective by Myerson and Trout) used molecular dynamics to look at the potential structure and dynamics of these clusters and lattice gas simulations to explore the population dynamics of the cluster populations prior to nucleation. A liquid-liquid phase separation process was observed whereby one phase becomes more concentrated in ions and becomes the precursor for nuclei to form. The preordering seen during calcium carbonate crystallization may be due to a liquid-liquid separation process. [Also see Perspective by Myerson and Trout] Recent experimental observations of the onset of calcium carbonate (CaCO3) mineralization suggest the emergence of a population of clusters that are stable rather than unstable as predicted by classical nucleation theory. This study uses molecular dynamics simulations to probe the structure, dynamics, and energetics of hydrated CaCO3 clusters and lattice gas simulations to explore the behavior of cluster populations before nucleation. Our results predict formation of a dense liquid phase through liquid-liquid separation within the concentration range in which clusters are observed. Coalescence and solidification of nanoscale droplets results in formation of a solid phase, the structure of which is consistent with amorphous CaCO3. The presence of a liquid-liquid binodal enables a diverse set of experimental observations to be reconciled within the context of established phase-separation mechanisms.

Carboxylated molecules regulate magnesium content of amorphous calcium carbonates during calcification

With the realization that many calcified skeletons form by processes involving a precursor phase of amorphous calcium carbonate (ACC), a new paradigm for mineralization is emerging. There is evidence the Mg content in biogenic ACC is regulated by carboxylated (acidic) proteins and other macromolecules, but the physical basis for such a process is unknown. We test the hypothesis that ACC compositions express a systematic relationship to the chemistry of carboxyl-rich biomolecules. A series of inorganic control experiments were conducted to establish the dependence of Mg/Ca ratios in ACC on solution composition. We then determined the influence of a suite of simple carboxylated organic acids on Mg content. Molecules with a strong affinity for binding Ca compared with Mg promote the formation of Mg-enriched ACC that is compositionally equivalent to high-magnesium calcites and dolomite. Measurements show Mg/Ca ratios are controlled by a predictable dependence upon the binding properties of the organic molecules. The trend appears rooted in the conformation and electrostatic potential topology of each molecule, but dynamic factors also may be involved. The dependence suggests a physical basis for reports that specific sequences of calcifying proteins are critical to modulating mineralization. Insights from this study may provide a plausible explanation for why some biogenic carbonates and carbonaceous cements often contain higher Mg signatures than those that are possible by classical crystal growth processes. The findings reiterate the controls of microenvironment on mineralization and suggest an origin of compositional offsets, or vital effects, long recognized by the paleoclimate community.

Kinetics of amorphous silica dissolution and the paradox of the silica polymorphs

The mechanisms by which amorphous silica dissolves have proven elusive because noncrystalline materials lack the structural order that allows them to be studied by the classical terrace, ledge, kink-based models applied to crystals. This would seem to imply amorphous phases have surfaces that are disordered at an atomic scale so that the transfer of SiO4 tetrahedra to solution always leaves the surface free energy of the solid unchanged. As a consequence, dissolution rates of amorphous phases should simply scale linearly with increasing driving force (undersaturation) through the higher probability of detaching silica tetrahedra. By examining rate measurements for two amorphous SiO2 glasses we find, instead, a paradox. In electrolyte solutions, these silicas show the same exponential dependence on driving force as their crystalline counterpart, quartz. We analyze this enigma by considering that amorphous silicas present two predominant types of surface-coordinated silica tetrahedra to solution. Electrolytes overcome the energy barrier to nucleated detachment of higher coordinated species to create a periphery of reactive, lesser coordinated groups that increase surface energy. The result is a plausible mechanism-based model that is formally identical with the classical polynuclear theory developed for crystal growth. The model also accounts for reported demineralization rates of natural biogenic and synthetic colloidal silicas. In principle, these insights should be applicable to materials with a wide variety of compositions and structural order when the reacting units are defined by the energies of their constituent species.

Kinetics of Silica Nucleation on Carboxyl- and Amine-Terminated Surfaces: Insights for Biomineralization

An in situ, atomic force microscopy- (AFM-)-based experimental approach is developed to directly measure the kinetics of silica nucleation on model biosubstrates under chemical conditions that mimic natural biosilica deposition environments. Relative contributions of thermodynamic and kinetic drivers to surface nucleation are quantified by use of amine-, carboxyl-, and hybrid NH(3)(+)/COO(-)-terminated surfaces as surrogates for charged and ionizable groups on silica-mineralizing organic matrices. The data show that amine-terminated surfaces do not promote silica nucleation, whereas carboxyl and hybrid NH(3)(+)/COO(-) substrates are active for silica deposition. The rate of silica nucleation is approximately 18x faster on the hybrid substrates than on carboxylated surfaces, but the free energy barriers to cluster formation are similar on both surface types. These findings suggest that surface nucleation rates are more sensitive to kinetic drivers than previously believed and that cooperative interactions between oppositely charged surface species play important roles in directing the onset of silica nucleation. Further experiments to test the importance of these cooperative interactions with patterned NH(3)(+)/COO(-) substrates, and aminated surfaces with solution-borne anionic species, confirm that silica nucleation is most rapid when oppositely charged species are proximal. By documenting the synergy that occurs between surface groups during silica formation, these findings demonstrate a new type of emergent behavior underlying the ability of self-assembled molecular templates to direct mineral formation.

A unifying model for Neoproterozoic–Palaeozoic exceptional fossil preservation through pyritization and carbonaceous compression

Soft-tissue fossils capture exquisite biological detail and provide our clearest views onto the rise of animals across the Ediacaran-Cambrian transition. The processes contributing to fossilization of soft tissues, however, have long been a subject of debate. The Ediacaran Gaojiashan biota displays soft-tissue preservational styles ranging from pervasive pyritization to carbonaceous compression, and thus provides an excellent opportunity to dissect the relationships between these taphonomic pathways. Here geochemical analyses of the Gaojiashan fossil Conotubus hemiannulatus show that pyrite precipitation was fuelled by the degradation of labile tissues through bacterial sulfate reduction (BSR). Pyritization initiated with nucleation on recalcitrant tube walls, proceeded centripetally, decelerated with exhaustion of labile tissues and possibly continued beneath the BSR zone. We propose that pyritization and kerogenization are regulated principally by placement and duration of the decaying organism in different microbial zones of the sediment column, which hinge on post-burial sedimentation rate and/or microbial zone thickness.

Influence of ion-associated water on the hydrolysis of Si-O bonded interactions.

Previous studies show the demineralization of biogenic, amorphous, and crystalline forms of silica is enhanced in the presence of alkali and alkaline earth cations. The origins of this effect are difficult to explain in light of work suggesting predominantly weak outer-sphere type interactions between these ions and silica. Here we investigate the ability of M(II) aqua ions to promote the hydrolysis of Si-O bonded interactions relative to ion-free water using electronic structure methods. Reaction pathways for Si-O hydrolysis are calculated with the B3LYP and PBE1PBE density functionals at the 6-31G(d) and 6-311+G(d,p) levels in the presence of water, and both inner- and outer-sphere adsorption complexes of Mg(2+)(6H(2)O) and Ca(2+)(6H(2)O). All reaction trajectories involving hydrated ions are characterized by one or more surmountable barriers associated with the rearrangement of ion-associated water molecules, and a single formidable barrier corresponding to hydrolysis of the Si-O bonded interaction. The hydrolysis step for outer-sphere adsorption is slightly less favorable than the water-induced reaction. In contrast, the barrier opposing Si-O hydrolysis in the presence of inner-sphere species is generally reduced relative to the water-induced pathway, indicating that the formation of inner-sphere complexes may be prerequisite to the detachment of Si species from highly coordinated surface sites. The results suggest a two-part physical model for ion-promoted Si-O hydrolysis that is consistent with experimental rate measurements. First, a bond path is formed between the cation and a bridging oxygen site on the silica surface that weakens the surrounding Si-O interactions, making them more susceptible to attack by water. Second, Si-O hydrolysis occurs adjacent to these inner-sphere species in proportion to the frequency of ion-associated solvent reorganization events. Both processes are dependent upon the particular ion hydration environment, which suggests measured cation-specific demineralization rates arise from differential barriers opposing reorganization of ion-associated solvent molecules at the silica-water interface.

Thermally-induced structural and chemical alteration of organic-walled microfossils: an experimental approach to understanding fossil preservation in metasediments.

The identification and confirmation of bona fide Archean-Paleoproterozoic microfossils can prove to be a challenging task, further compounded by diagenetic and metamorphic histories. While structures of likely biological origin are not uncommon in Precambrian rocks, the search for early fossil life has been disproportionately focused on lesser thermally altered rocks, typically greenschist or lower-grade metamorphism. Recently, however, an increasing number of inferred micro- and macrofossils have been reported from higher-grade metasediments, prompting us to experimentally test and quantify the preservability of organic-walled microfossils over varying durations of controlled heating and under two differing redox conditions. Because of their relatively low-intensity natural thermal alteration, acritarchs from the Mesoproterozoic Ruyang Group were chosen as subjects for experimental heating at approximately 500°C, with durations ranging from 1 to 250 days and in both oxic (normal present day conditions) and anoxic conditions. Upon extraction, the opacity, reflectivity, color, microchemistry, and microstructures of the heated acritarchs were characterized using optic microscopy, scanning electron microscopy, Raman spectroscopy, and X-ray photoelectron spectroscopy. The results differ for acritarchs prepared under oxic vs. anoxic conditions, with the anoxic replicates surviving experimental heating longer and retaining biological morphologies better, despite an increasing degree of carbonization with continuous heating. Conversely, the oxic replicates show aggressive degradation. In conjunction with fossils from high-grade metasediments, our data illustrate the preservational potential of organic-walled microfossils subjected to metamorphism in reducing conditions, offer insights into the search for microfossils in metasediments, and help to elucidate the influence of time on the carbonization/graphitization processes during thermal alteration.

Bonded interactions in silica polymorphs, silicates, and siloxane molecules

Abstract Experimental model electron density distributions obtained for the silica polymorphs coesite and stishovite are comparable with electron density distributions calculated for various silicates and siloxane molecules. The Si-O bond lengths and Si-O-Si angles calculated with first-principles density functional theory methods as a function of pressure are also comparable with the bond lengths and angles observed for coesite and quartz within the experimental error. The similarity of the topological properties of the Si-O bonded interactions and the experimental and the geometry-optimized structures for the silica polymorphs provide a basis for understanding the properties and crystal chemistry of silica. The agreement supports the argument that the bulk of the structural and physical properties of the silica polymorphs are intrinsic properties of molecular-like coordination polyhedra such that the silica polymorphs can be pictured as “supermolecules” of silica bound by virtually the same forces that bind the Si and O atoms in simple siloxane molecules. The topology of the electron density distribution is consistent with the assertion that the Si-O bonded interaction arises from the net electrostatic attraction exerted on the nuclei by the electron density accumulated between the Si and O atoms. The correlation between the Si-O bond length and Si-O-Si angle is ascribed to the progressive local concentration of the electron density in the nonbonded lone pair region of the O atom rather than to a bonded interaction that involves the d-orbitals on Si. The accumulation of deformation electron density, Δρ(r), in the bonded and nonbonded regions of the Si-O bond, the close proximity of the bond critical point, rc, of the bond with the nodal surface of the Laplacian and the negative value of the total energy density are taken as evidence that the bond has a nontrivial component of shared character. For M-O bonded interactions for first and second row metal atoms bonded to O, ∇2ρ(rc) is positive and increases linearly as ρ(rc) and G(rc)/ρ(rc) both increase and as the value of H(rc) decreases; the greater the shared character of the interaction, the larger the values of both ∇2ρ(rc) and G(rc)/ρ(rc). In addition, a mapping of ∇2ρ(r) serves to highlight those Lewis base domains that are susceptible to electrophilic attack by H, like the O atoms in coesite involved in bent Si-O-Si angles; the narrower the angle, the greater the affinity for H. On the basis of the net charges conferred on the Si and O atoms and the bonded radii of the two atoms, the Si-O bond for stishovite, with six-coordinated Si and three-coordinated O, is indicated to be more ionic in character than that in quartz with four-coordinated Si and two-coordinated O. Unlike the conclusion reached for ionic and crystal radii, it is the bonded radius of the O atom that increases with the increasing coordination number of Si, not the radius of the Si atom. The modeling of the electron density distributions for quartz, coesite, and beryl as a function of pressure suggests that the shared character of the bonded interactions in these minerals increases slightly with increasing pressure. The insight provided by the calculations and the modeling of the electron density distributions and the structures of the silica polymorphs bodes well for future Earth materials studies that are expected to improve and clarify our understanding of the connection between properties and structure within the framework of quantum mechanical observables, to find new and improved uses for the materials and to enhance our understanding of crystal chemistry and chemical reactions of materials in their natural environment at the atomic level.

Role of directed van der Waals bonded interactions in the determination of the structures of Molecular arsenate solids

Bond paths, local energy density properties, and Laplacian, L(r) = -wedge(2)rho(r), composite isosurfaces of the electron density distributions were calculated for the intramolecular and intermolecular bonded interactions for molecular solids of As(2)O(3) and AsO(2) composition, an As(2)O(5) crystal, a number of arsenate molecules, and the arsenic metalloid, arsenolamprite. The directed intermolecular van der Waals As-O, O-O, and As-As bonded interactions are believed to serve as mainstays between the individual molecules in each of the molecular solids. As-O bond paths between the bonded atoms connect Lewis base charge concentrations and Lewis acid charge depletion domains, whereas the O-O and As-As paths connect Lewis base pair and Lewis acid pair domains, respectively, giving rise to sets of intermolecular directed bond paths. The alignment of the directed bond paths results in the periodic structures adopted by the arsenates. The arrangements of the As atoms in the claudetite polymorphs of As(2)O(3) and the As atoms in arsenolamprite are similar. Like the As(2)O(3) polymorphs, arsenolamprite is a molecular solid connected by relatively weak As-As intermolecular directed van der Waals bond paths between the layers of stronger As-As intramolecular bonded interactions. The bond critical point and local energy density properties of the intermolecular As-As bonded interactions in arsenolamprite are comparable with the As-As interactions in claudetite I. As such, the structure of claudetite I can be viewed as a stuffed derivative of the arsenolamprite structure with O atoms between pairs of As atoms comprising the layers of the structure. The cubic structure adopted by the arsenolite polymorph can be understood in terms of sets of directed acid-base As-O and base-base O-O pair domains and bond paths that radiate from the tetrahedral faces of its constituent molecules, serving as face-to-face key-lock mainstays in forming a periodic tetrahedral array of molecules rather than one based on some variant of close packing. The relatively dense structure and the corrugation of the layers in claudetite I can also be understood in terms of directed van der Waals As-O bonded interactions. Our study not only provides a new basis for understanding the crystal chemistry and the structures of the arsenates, but it also calls for a reappraisal of the concept of van der Waals bonded interactions, how the structures of molecular solids are viewed, and how the molecules in these solids are bonded in a periodic structure.