The hidden structure of human enamel Beniash, Elia; Stifler, Cayla A; Sun, Chang-Yu ...
Nature communications,
09/2019, Volume:
10, Issue:
1
Journal Article
Peer reviewed
Open access
Enamel is the hardest and most resilient tissue in the human body. Enamel includes morphologically aligned, parallel, ∼50 nm wide, microns-long nanocrystals, bundled either into 5-μm-wide rods or ...their space-filling interrod. The orientation of enamel crystals, however, is poorly understood. Here we show that the crystalline c-axes are homogenously oriented in interrod crystals across most of the enamel layer thickness. Within each rod crystals are not co-oriented with one another or with the long axis of the rod, as previously assumed: the c-axes of adjacent nanocrystals are most frequently mis-oriented by 1°-30°, and this orientation within each rod gradually changes, with an overall angle spread that is never zero, but varies between 30°-90° within one rod. Molecular dynamics simulations demonstrate that the observed mis-orientations of adjacent crystals induce crack deflection. This toughening mechanism contributes to the unique resilience of enamel, which lasts a lifetime under extreme physical and chemical challenges.
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.
Calcite, aragonite, and vaterite are the three anhydrous polymorphs of calcium carbonate, in order of decreasing thermodynamic stability. Although vaterite is not commonly found in geological ...settings, it is an important precursor in several carbonate-forming systems and can be found in biological settings. Because of difficulties in obtaining large, pure, single crystals, the crystal structure of vaterite has been elusive for almost a century. Using aberration-corrected high-resolution transmission electron microscopy, we found that vaterite is actually composed of at least two different crystallographic structures that coexist within a pseudo-single crystal. The major structure exhibits hexagonal symmetry; the minor structure, existing as nanodomains within the major matrix, is still unknown.
Crystallization by particle attachment (CPA) of amorphous precursors has been demonstrated in modern biomineralized skeletons across a broad phylogenetic range of animals. Precisely the same ...precursors, hydrated (ACC-H₂O) and anhydrous calcium carbonate (ACC), have been observed spectromicroscopically in echinoderms, mollusks, and cnidarians, phyla drawn from the 3 major clades of eumetazoans. Scanning electron microscopy (SEM) here also shows evidence of CPA in tunicate chordates. This is surprising, as species in these clades have no common ancestor that formed a mineralized skeleton and appear to have evolved carbonate biomineralization independently millions of years after their late Neoproterozoic divergence. Here we correlate the occurrence of CPA from ACC precursor particles with nanoparticulate fabric and then use the latter to investigate the antiquity of the former. SEM images of early biominerals from Ediacaran and Cambrian shelly fossils show that these early calcifiers used attachment of ACC particles to form their biominerals. The convergent evolution of biomineral CPA may have been dictated by the same thermodynamics and kinetics as we observe today.
Do corals form their skeletons by precipitation from solution or by attachment of amorphous precursor particles as observed in other minerals and biominerals? The classical model assumes ...precipitation in contrast with observed “vital effects,” that is, deviations from elemental and isotopic compositions at thermodynamic equilibrium. Here, we show direct spectromicroscopy evidence in Stylophora pistillata corals that two amorphous precursors exist, one hydrated and one anhydrous amorphous calcium carbonate (ACC); that these are formed in the tissue as 400-nm particles; and that they attach to the surface of coral skeletons, remain amorphous for hours, and finally, crystallize into aragonite (CaCO₃). We show in both coral and synthetic aragonite spherulites that crystal growth by attachment of ACC particles is more than 100 times faster than ion-by-ion growth from solution. Fast growth provides a distinct physiological advantage to corals in the rigors of the reef, a crowded and fiercely competitive ecosystem. Corals are affected by warming-induced bleaching and postmortem dissolution, but the finding here that ACC particles are formed inside tissue may make coral skeleton formation less susceptible to ocean acidification than previously assumed. If this is how other corals form their skeletons, perhaps this is how a few corals survived past CO₂ increases, such as the Paleocene–Eocene Thermal Maximum that occurred 56 Mya.
As one of the most abundant materials in the world, calcium carbonate, CaCO
, is the main constituent of the skeletons and shells of various marine organisms. It is used in the cement industry and ...plays a crucial role in the global carbon cycle and formation of sedimentary rocks. For more than a century, only three polymorphs of pure CaCO
-calcite, aragonite, and vaterite-were known to exist at ambient conditions, as well as two hydrated crystal phases, monohydrocalcite (CaCO
·1H
O) and ikaite (CaCO
·6H
O). While investigating the role of magnesium ions in crystallization pathways of amorphous calcium carbonate, we unexpectedly discovered an unknown crystalline phase, hemihydrate CaCO
·½H
O, with monoclinic structure. This discovery may have important implications in biomineralization, geology, and industrial processes based on hydration of CaCO
.
In contrast to synthetic materials, materials produced by organisms are formed in ambient conditions and with a limited selection of elements. Nevertheless, living organisms reveal elegant strategies ...for achieving specific functions, ranging from skeletal support to mastication, from sensors and defensive tools to optical function. Using state-of-the-art characterization techniques, we present a biostrategy for strengthening and toughening the otherwise brittle calcite optical lenses found in the brittlestar Ophiocoma wendtii. This intriguing process uses coherent nanoprecipitates to induce compressive stresses on the host matrix, functionally resembling the Guinier–Preston zones known in classical metallurgy. We believe that these calcitic nanoparticles, being rich in magnesium, segregate during or just after transformation from amorphous to crystalline phase, similarly to segregation behavior from a supersaturated quenched alloy.
Many biogenic minerals are composed of aggregated particles at the nanoscale. These minerals usually form through the transformation of amorphous precursors into single crystals inside a privileged ...space controlled by the organism. Here, in vitro experiments aimed at understanding the factors responsible for producing such single crystals with aggregated particle texture are presented. Crystallization is achieved by a two‐step reaction in which amorphous calcium carbonate (ACC) is first precipitated and then transformed into calcite in small volumes of water and in the presence of additives. The additives used are gel‐forming molecules, phosphate ions, and the organic extract from sea urchin embryonic spicules ‐ all are present in various biogenic crystals that grow via the transformation of ACC. Remarkably, this procedure yields faceted single‐crystals of calcite that maintain the nanoparticle texture. The crystals grow predominantly by the accretion of ACC nanoparticles, which subsequently crystallize. Gels and phosphate ions stabilize ACC via a different mechanism than sea urchin spicule macromolecules. It is concluded that the unique nanoparticle texture of biogenic minerals results from formation pathways that may differ from one another, but given the appropriate precursor and micro‐environment, share a common particle accretion mechanism.
Single calcite crystals are grown by amorphous calcium carbonate (ACC) particle‐accretion using a synthetic procedure inspired by biogenic systems. The transformation of solid ACC particles in the presence of certain additives retards the classical dissolution‐precipitation process facilitating growth by a particle‐mediated process. The results provide a mechanistic understanding of biogenic and synthetic single crystal growth.
Nacre, the iridescent outer lining of pearls and inner lining of many mollusk shells, is composed of periodic, parallel, organic sheets alternating with aragonite (CaCO3) tablet layers. Nacre tablet ...thickness (TT) generates both nacre's iridescence and its remarkable resistance to fracture. Despite extensive studies on how nacre forms, the mechanisms controlling TT remain unknown, even though they determine the most conspicuous of nacre's characteristics, visible even to the naked eye.
Thermodynamics predicts that temperature (T) will affect both physical and chemical components of biomineralized skeletons. The chemical composition of biominerals is well-established to record environmental parameters, and has therefore been extensively used in paleoclimate studies. The physical structure, however, has been hypothesized but never directly demonstrated to depend on the environment. Here we observe that the physical TT in nacre from modern and fossil shallow-water shells of the bivalves Pinna and Atrina correlates with T as measured by the carbonate clumped isotope thermometer. Based on the observed TT vs. T correlation, we anticipate that TT will be used as a paleothermometer, useful to estimate paleotemperature in shallow-water paleoenvironments. Here we successfully test the proposed new nacre TT thermometer on two Jurassic Pinna shells. The increase of TT with T is consistent with greater aragonite growth rate at higher T, and with greater metabolic rate at higher T. Thus, it reveals a complex, T-dependent biophysical mechanism for nacre formation.
•We show that nacre tablet thickness (TT) correlates with formation temperature (T).•The TT vs. T correlation can be used as a thermometer to measure paleo-temperatures.•This is a physical, not a chemical proxy, and thus is less sensitive to diagenesis.
Although calcareous anatomical structures have evolved in diverse animal groups, such structures have been unknown in insects. Here, we report the discovery of high-magnesium calcite CaMg(CO
)
armor ...overlaying the exoskeletons of major workers of the leaf-cutter ant Acromyrmex echinatior. Live-rearing and in vitro synthesis experiments indicate that the biomineral layer accumulates rapidly as ant workers mature, that the layer is continuously distributed, covering nearly the entire integument, and that the ant epicuticle catalyzes biomineral nucleation and growth. In situ nanoindentation demonstrates that the biomineral layer significantly hardens the exoskeleton. Increased survival of ant workers with biomineralized exoskeletons during aggressive encounters with other ants and reduced infection by entomopathogenic fungi demonstrate the protective role of the biomineral layer. The discovery of biogenic high-magnesium calcite in the relatively well-studied leaf-cutting ants suggests that calcareous biominerals enriched in magnesium may be more common in metazoans than previously recognized.
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