Search

Biomineralized structures are complex functional hierarchical assemblies composed of biomineral building blocks joined together by an organic phase. The formation of individual mineral units is governed by the cellular tissue component that orchestrates the process of biomineral nucleation, growth, and morphogenesis. These processes are imprinted in the structural, compositional, and crystallographic properties of the emerging biominerals on all scales. Measurement of these properties can provide crucial information on the mechanisms that are employed by the organism to form these complex 3D architectures and to unravel principles of their functionality. Nevertheless, so far, this has only been possible at the macroscopic scale, by averaging the properties of the entire composite assembly, or at the mesoscale, by looking at extremely small parts of the entire picture. In this study, the newly developed synchrotron-based dark-field X-ray microscopy method is employed to study the link between 3D crystallographic properties of relatively large calcitic prisms in the shell of the mollusc Pinna nobilis and their local lattice properties with extremely high angular resolution down to 0.001°. Mechanistic links between variations in local lattice parameters and spacing, crystal orientation, chemical composition, and the deposition process of the entire mineral unit are unraveled.

Biomineralized structures are complex functional hierarchical assemblies composed of biomineral building blocks joined together by an organic phase. The formation of individual mineral units is governed by the cellular tissue component that orchestrates the process of biomineral nucleation, growth, and morphogenesis. These processes are imprinted in the structural, compositional, and crystallographic properties of the emerging biominerals on all scales. Measurement of these properties can provide crucial information on the mechanisms that are employed by the organism to form these complex 3D architectures and to unravel principles of their functionality. Nevertheless, so far, this has only been possible at the macroscopic scale, by averaging the properties of the entire composite assembly, or at the mesoscale, by looking at extremely small parts of the entire picture. In this study, the newly developed synchrotron-based dark-field X-ray microscopy method is employed to study the link between 3D crystallographic properties of relatively large calcitic prisms in the shell of the mollusc Pinna nobilis and their local lattice properties with extremely high angular resolution down to 0.001°. Mechanistic links between variations in local lattice parameters and spacing, crystal orientation, chemical composition, and the deposition process of the entire mineral unit are unraveled.

Crystallization by particle attachment (CPA) is a gradual process where each step has its own thermodynamic and kinetic constrains defining a unique pathway of crystal growth. An important example is biomineralization of calcium carbonate through amorphous precursors that are morphed into shapes and textural patterns that cannot be envisioned by the classical monomer-by-monomer approach. Here, a mechanistic link between the collective kinetics of mineral deposition and the emergence of crystallographic texture is established. Using the prismatic ultrastructure in bivalve shells as a model, a fundamental leap is made in the ability to analytically describe the evolution of form and texture of biological mineralized tissues and to design the structure and crystallographic properties of synthetic materials formed by CPA.

Crystallization by particle attachment (CPA) is a gradual process where each step has its own thermodynamic and kinetic constrains defining a unique pathway of crystal growth. An important example is biomineralization of calcium carbonate through amorphous precursors that are morphed into shapes and textural patterns that cannot be envisioned by the classical monomer-by-monomer approach. Here, a mechanistic link between the collective kinetics of mineral deposition and the emergence of crystallographic texture is established. Using the prismatic ultrastructure in bivalve shells as a model, a fundamental leap is made in the ability to analytically describe the evolution of form and texture of biological mineralized tissues and to design the structure and crystallographic properties of synthetic materials formed by CPA.

Crystallization by particle attachment (CPA) is a gradual process where each step has its own thermodynamic and kinetic constrains defining a unique pathway of crystal growth. An important example is biomineralization of calcium carbonate through amorphous precursors that are morphed into shapes and textural patterns that cannot be envisioned by the classical monomer-by-monomer approach. Here, a mechanistic link between the collective kinetics of mineral deposition and the emergence of crystallographic texture is established. Using the prismatic ultrastructure in bivalve shells as a model, a fundamental leap is made in the ability to analytically describe the evolution of form and texture of biological mineralized tissues and to design the structure and crystallographic properties of synthetic materials formed by CPA.

Biomineralized structures are complex functional hierarchical assemblies composed of biomineral building blocks joined together by an organic phase. The formation of individual mineral units is governed by the cellular tissue component that orchestrates the process of biomineral nucleation, growth, and morphogenesis. These processes are imprinted in the structural, compositional, and crystallographic properties of the emerging biominerals on all scales. Measurement of these properties can provide crucial information on the mechanisms that are employed by the organism to form these complex 3D architectures and to unravel principles of their functionality. Nevertheless, so far, this has only been possible at the macroscopic scale, by averaging the properties of the entire composite assembly, or at the mesoscale, by looking at extremely small parts of the entire picture. In this study, the newly developed synchrotron-based dark-field X-ray microscopy method is employed to study the link between 3D crystallographic properties of relatively large calcitic prisms in the shell of the mollusc Pinna nobilis and their local lattice properties with extremely high angular resolution down to 0.001°. Mechanistic links between variations in local lattice parameters and spacing, crystal orientation, chemical composition, and the deposition process of the entire mineral unit are unraveled.

Biomineralized structures are complex functional hierarchical assemblies composed of biomineral building blocks joined together by an organic phase. The formation of individual mineral units is governed by the cellular tissue component that orchestrates the process of biomineral nucleation, growth, and morphogenesis. These processes are imprinted in the structural, compositional, and crystallographic properties of the emerging biominerals on all scales. Measurement of these properties can provide crucial information on the mechanisms that are employed by the organism to form these complex 3D architectures and to unravel principles of their functionality. Nevertheless, so far, this has only been possible at the macroscopic scale, by averaging the properties of the entire composite assembly, or at the mesoscale, by looking at extremely small parts of the entire picture. In this study, the newly developed synchrotron-based dark-field X-ray microscopy method is employed to study the link between 3D crystallographic properties of relatively large calcitic prisms in the shell of the mollusc Pinna nobilis and their local lattice properties with extremely high angular resolution down to 0.001°. Mechanistic links between variations in local lattice parameters and spacing, crystal orientation, chemical composition, and the deposition process of the entire mineral unit are unraveled.

Spherulites are radial distributions of acicular crystals, common in biogenic, geologic, and synthetic systems, yet exactly how spherulitic crystals nucleate and grow is still poorly understood. To investigate these processes in more detail, we chose scleractinian corals as a model system, because they are well known to form their skeletons from aragonite (CaCO3) spherulites, and because a comparative study of crystal structures across coral species has not been performed previously. We observed that all 12 diverse coral species analyzed here exhibit plumose spherulites in their skeletons, with well-defined centers of calcification (CoCs), and crystalline fibers radiating from them. In 7 of the 12 species, we observed a skeletal structural motif not observed previously: randomly oriented, equant crystals, which we termed "sprinkles". In Acropora pharaonis, these sprinkles are localized at the CoCs, while in 6 other species, sprinkles are either layered at the growth front (GF) of the spherulites, or randomly distributed. At the nano- and micro-scale, coral skeletons fill space as much as single crystals of aragonite. Based on these observations, we tentatively propose a spherulite formation mechanism in which growth front nucleation (GFN) of randomly oriented sprinkles, competition for space, and coarsening produce spherulites, rather than the previously assumed slightly misoriented nucleations termed "non-crystallographic branching". Phase-field simulations support this mechanism, and, using a minimal set of thermodynamic parameters, are able to reproduce all of the microstructural variation observed experimentally in all of the investigated coral skeletons. Beyond coral skeletons, other spherulitic systems, from aspirin to semicrystalline polymers and chocolate, may also form according to the mechanism for spherulite formation proposed here. STATEMENT OF SIGNIFICANCE: Understanding the fundamental mechanisms of spherulite nucleation and growth has broad ranging ap

Spherulites are radial distributions of acicular crystals, common in biogenic, geologic, and synthetic systems, yet exactly how spherulitic crystals nucleate and grow is still poorly understood. To investigate these processes in more detail, we chose scleractinian corals as a model system, because they are well known to form their skeletons from aragonite (CaCO3) spherulites, and because a comparative study of crystal structures across coral species has not been performed previously. We observed that all 12 diverse coral species analyzed here exhibit plumose spherulites in their skeletons, with well-defined centers of calcification (CoCs), and crystalline fibers radiating from them. In 7 of the 12 species, we observed a skeletal structural motif not observed previously: randomly oriented, equant crystals, which we termed "sprinkles". In Acropora pharaonis, these sprinkles are localized at the CoCs, while in 6 other species, sprinkles are either layered at the growth front (GF) of the spherulites, or randomly distributed. At the nano- and micro-scale, coral skeletons fill space as much as single crystals of aragonite. Based on these observations, we tentatively propose a spherulite formation mechanism in which growth front nucleation (GFN) of randomly oriented sprinkles, competition for space, and coarsening produce spherulites, rather than the previously assumed slightly misoriented nucleations termed "non-crystallographic branching". Phase-field simulations support this mechanism, and, using a minimal set of thermodynamic parameters, are able to reproduce all of the microstructural variation observed experimentally in all of the investigated coral skeletons. Beyond coral skeletons, other spherulitic systems, from aspirin to semicrystalline polymers and chocolate, may also form according to the mechanism for spherulite formation proposed here. STATEMENT OF SIGNIFICANCE: Understanding the fundamental mechanisms of spherulite nucleation and growth has broad ranging ap

Reef-building corals and their aragonite (CaCO3) skeletons support entire reef ecosystems, yet their formation mechanism is poorly understood. Here we used synchrotron spectromicroscopy to observe the nanoscale mineralogy of fresh, forming skeletons from six species spanning all reef-forming coral morphologies: Branching, encrusting, massive, and table. In all species, hydrated and anhydrous amorphous calcium carbonate nanoparticles were precursors for skeletal growth, as previously observed in a single species. The amorphous precursors here were observed in tissue, between tissue and skeleton, and at growth fronts of the skeleton, within a low-density nano- or microporous layer varying in thickness from 7 to 20 µm. Brunauer-Emmett-Teller measurements, however, indicated that the mature skeletons at the microscale were space-filling, comparable to single crystals of geologic aragonite. Nanoparticles alone can never fill space completely, thus ion-by-ion filling must be invoked to fill interstitial pores. Such ion-by-ion diffusion and attachment may occur from the supersaturated calcifying fluid known to exist in corals, or from a dense liquid precursor, observed in synthetic systems but never in biogenic ones. Concomitant particle attachment and ion-by-ion filling was previously observed in synthetic calcite rhombohedra, but never in aragonite pseudohexagonal prisms, synthetic or biogenic, as observed here. Models for biomineral growth, isotope incorporation, and coral skeletons' resilience to ocean warming and acidification must take into account the dual formation mechanism, including particle attachment and ion-by-ion space filling.

Reef-building corals and their aragonite (CaCO3) skeletons support entire reef ecosystems, yet their formation mechanism is poorly understood. Here we used synchrotron spectromicroscopy to observe the nanoscale mineralogy of fresh, forming skeletons from six species spanning all reef-forming coral morphologies: Branching, encrusting, massive, and table. In all species, hydrated and anhydrous amorphous calcium carbonate nanoparticles were precursors for skeletal growth, as previously observed in a single species. The amorphous precursors here were observed in tissue, between tissue and skeleton, and at growth fronts of the skeleton, within a low-density nano- or microporous layer varying in thickness from 7 to 20 µm. Brunauer-Emmett-Teller measurements, however, indicated that the mature skeletons at the microscale were space-filling, comparable to single crystals of geologic aragonite. Nanoparticles alone can never fill space completely, thus ion-by-ion filling must be invoked to fill interstitial pores. Such ion-by-ion diffusion and attachment may occur from the supersaturated calcifying fluid known to exist in corals, or from a dense liquid precursor, observed in synthetic systems but never in biogenic ones. Concomitant particle attachment and ion-by-ion filling was previously observed in synthetic calcite rhombohedra, but never in aragonite pseudohexagonal prisms, synthetic or biogenic, as observed here. Models for biomineral growth, isotope incorporation, and coral skeletons' resilience to ocean warming and acidification must take into account the dual formation mechanism, including particle attachment and ion-by-ion space filling.