A fundamental question in biomineralization is the nature of the first-formed mineral phase. In vertebrate bone formation, this issue has been the subject of a long-standing controversy. We address ...this key issue using the continuously growing fin bony rays of the Tuebingen long-fin zebrafish as a model for bone mineralization. Employing high-resolution scanning and transmission electron microscopy imaging, electron diffraction, and elemental analysis, we demonstrate the presence of an abundant amorphous calcium phosphate phase in the newly formed fin bones. The extracted amorphous mineral particles crystallize with time, and mineral crystallinity increases during bone maturation. Based on these findings, we propose that this amorphous calcium phosphate phase may be a precursor phase that later transforms into the mature crystalline mineral.
Guanine crystals are widely used in nature to manipulate light. The first part of this feature article explores how organisms are able to construct an extraordinary array of optical “devices” ...including diffuse scatterers, broadband and narrowband reflectors, tunable photonic crystals, and image‐forming mirrors by varying the size, morphology, and arrangement of guanine crystals. The second part presents an overview of some of the properties of crystalline guanine to explain why this material is ideally suited for such optical applications. The high reflectivity of many natural optical systems ultimately derives from the fact that guanine crystals have an extremely high refractive index—a product of its anisotropic crystal structure comprised of densely stacked H‐bonded layers. In order to optimize their reflectivity, many organisms exert exquisite control over the crystal morphology, forming plate‐like single crystals in which the high refractive index face is preferentially expressed. Guanine‐based optics are used in a wide range of biological functions such as in camouflage, display, and vision, and exhibit a degree of versatility, tunability, and complexity that is difficult to incorporate into artificial devices using conventional engineering approaches. These biological systems could inspire the next generation of advanced optical materials.
How are organisms able to construct and control diffuse scatterers in white spiders, broadband and narrowband reflectors in fish scales, tunable photonic crystals in chameleons and copepods, and image‐forming mirrors in scallop eyes? Just by varying the size, morphology, and arrangement of the guanine crystals in their cells.
Abstract Lamellar bone is a major component of most mammalian skeletons. A prominent component of individual lamellae are parallel arrays of mineralized type I collagen fibrils, organized in a ...plywood like motif. Here we use a dual beam microscope and the serial surface view (SSV) method to investigate the three dimensional collagen organization of circumferential lamellar bone from rat tibiae after demineralization and osmium staining. Fast Fourier transform analysis is used to quantitatively identify the mean collagen array orientations and local collagen fibril dispersion. Based on collagen fibril array orientations and variations in fibril dispersion, we identify 3 distinct sub-lamellar structural motifs: a plywood-like fanning sub-lamella, a unidirectional sub-lamella and a disordered sub-lamella. We also show that the disordered sub-lamella is less mineralized than the other sub-lamellae. The hubs and junctions of the canalicular network, which connect radially oriented canaliculi, are intimately associated with the disordered sub-lamella. We also note considerable variations in the proportions of these 3 sub-lamellar structural elements among different lamellae. This new application of Serial Surface View opens the way to quantitatively compare lamellar bone from different sources, and to clarify the 3-dimensional structures of other bone types, as well as other biological structural materials.
The biological approach to forming crystals is proving to be most surprising. Mollusks build their shells by using a hydrophobic silk gel, very acidic aspartic acid rich proteins, and apparently also ...an amorphous precursor phase from which the crystals form. All this takes place in a highly structured chitinous framework. Here we present ideas on how these disparate components work together to produce the highly structured pearly nacreous layer of the mollusk shell.
Mollusk shell nacre is full of surprises: Here ideas are presented on how disparate components like a hydrophobic silk gel, highly acidic proteins, and possibly an amorphous, transient mineral precursor phase are assembled within a chitinous scaffold to produce the pearly nacreous layer of a mollusk shell (shown here).
Many organisms form crystals from transient amorphous precursor phases. In cases where the precursor phases were imaged, they were seen to consist of nanosphere particles. Interestingly, some mature ...biogenic crystals also have a nanosphere particle morphology, but some are characterized by crystallographic faces that are smooth at the nanometer level. There are also biogenic crystals that have both crystallographic faces and nanosphere particle morphology. This highlight presents a working hypothesis, stating that some biomineralization processes involve growth by nanosphere particle accretion, where amorphous nanoparticles are incorporated as such into growing crystals and their morphology is preserved upon crystallization. This process produces biogenic crystals with a nanosphere particle morphology. Other biomineralization processes proceed by ion-by-ion growth, and some cases of biological crystal growth involve both processes. We also identify several biomineralization processes which do not seem to fit this working hypothesis. It is our hope that this highlight will inspire studies that will shed more light on the underlying crystallization mechanisms in biology.
A working hypothesis for the understanding of amorphous-to-crystalline transformations in biogenic skeletal materials formed through transient amorphous precursor phases.
The fresh water fish neon tetra has the ability to change the structural color of its lateral stripe in response to a change in the light conditions, from blue‐green in the light‐adapted state to ...indigo in the dark‐adapted state. The colors are produced by constructive interference of light reflected from stacks of intracellular guanine crystals, forming tunable photonic crystal arrays. We have used micro X‐ray diffraction to track in time distinct diffraction spots corresponding to individual crystal arrays within a single cell during the color change. We demonstrate that reversible variations in crystal tilt within individual arrays are responsible for the light‐induced color variations. These results settle a long‐standing debate between the two proposed models, the “Venetian blinds” model and the “accordion” model. The insight gained from this biogenic light‐induced photonic tunable system may provide inspiration for the design of artificial optical tunable systems.
Color switch: The physical mechanism of the light‐triggered color change in the lateral stripe of the neon tetra is controlled by changing the tilt angle of the guanine crystal arrays. It is shown that the color change can be described by the “Venetian blinds” model.
Globally, soil organic matter (SOM) contains more than three times as much carbon as either the atmosphere or terrestrial vegetation. Yet it remains largely unknown why some SOM persists for ...millennia whereas other SOM decomposes readily--and this limits our ability to predict how soils will respond to climate change. Recent analytical and experimental advances have demonstrated that molecular structure alone does not control SOM stability: in fact, environmental and biological controls predominate. Here we propose ways to include this understanding in a new generation of experiments and soil carbon models, thereby improving predictions of the SOM response to global warming.
Males of sapphirinid copepods use regularly alternating layers of hexagonal-shaped guanine crystals and cytoplasm to produce spectacular structural colors. In order to understand the mechanism by ...which the different colors are produced, we measured the reflectance of live individuals and then characterized the organization of the crystals and the cytoplasm layers in the same individuals using cryo-SEM. On the basis of these measurements, we calculated the expected reflectance spectra and found that they are strikingly similar to the measured ones. We show that variations in the cytoplasm layer thickness are mainly responsible for the different reflected colors and also that the copepod color strongly depends on the angular orientation relative to the incident light, which can account for its appearance and disappearance during spiral swimming in the natural habitat.
Vision mechanisms in animals, especially those living in water, are diverse. Many eyes have reflective elements that consist of multilayers of nanometer‐sized crystalline plates, composed of organic ...molecules. The crystal multilayer assemblies owe their enhanced reflectivity to the high refractive indices of the crystals in preferred crystallographic directions. The high refractive indices are due to the molecular arrangements in their crystal structures. Herein, data regarding these difficult‐to‐characterize crystals are reviewed. This is followed by a discussion on the function of these crystalline assemblies, especially in visual systems whose anatomy has been well characterized under close to in vivo conditions. Three test cases are presented, and then the relations between the reflecting crystalline components and their functions, including the relations between molecular structure, crystal structure, and reflecting properties are discussed. Some of the underlying mechanisms are also discussed, and finally open questions in the field are identified.
The reflectors used in animal eyes to form images, increase photon‐capture, or to regulate light‐exposure are stunning examples of advanced biogenic materials. The optical properties of these reflectors depend on the structure, morphology, and hierarchical organization of the constituent organic crystals.
Bone is the most widespread mineralized tissue in vertebrates and its formation is orchestrated by specialized cells – the osteoblasts. Crystalline carbonated hydroxyapatite, an inorganic calcium ...phosphate mineral, constitutes a substantial fraction of mature bone tissue. Yet key aspects of the mineral formation mechanism, transport pathways and deposition in the extracellular matrix remain unidentified. Using cryo-electron microscopy on native frozen-hydrated tissues we show that during mineralization of developing mouse calvaria and long bones, bone-lining cells concentrate membrane-bound mineral granules within intracellular vesicles. Elemental analysis and electron diffraction show that the intracellular mineral granules consist of disordered calcium phosphate, a highly metastable phase and a potential precursor of carbonated hydroxyapatite. The intracellular mineral contains considerably less calcium than expected for synthetic amorphous calcium phosphate, suggesting the presence of a cellular mechanism by which phosphate entities are first formed and thereafter gradually sequester calcium within the vesicles. We thus demonstrate that in vivo osteoblasts actively produce disordered mineral packets within intracellular vesicles for mineralization of the extracellular developing bone tissue. The use of a highly disordered precursor mineral phase that later crystallizes within an extracellular matrix is a strategy employed in the formation of fish fin bones and by various invertebrate phyla. This therefore appears to be a widespread strategy used by many animal phyla, including vertebrates.
PDF
