The image-forming mirror in the eye of the scallop Palmer, Benjamin A.; Taylor, Gavin J.; Brumfeld, Vlad ...
Science (American Association for the Advancement of Science),
12/2017, Letnik:
358, Številka:
6367
Journal Article
Recenzirano
Scallops possess a visual system comprising up to 200 eyes, each containing a concave mirror rather than a lens to focus light. The hierarchical organization of the multilayered mirror is controlled ...for image formation, from the component guanine crystals at the nanoscale to the complex three-dimensional morphology at the millimeter level. The layered structure of the mirror is tuned to reflect the wavelengths of light penetrating the scallop’s habitat and is tiled with a mosaic of square guanine crystals, which reduces optical aberrations. The mirror forms images on a double-layered retina used for separately imaging the peripheral and central fields of view. The tiled, off-axis mirror of the scallop eye bears a striking resemblance to the segmented mirrors of reflecting telescopes.
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.
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.
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.
Fish have evolved biogenic multilayer reflectors composed of stacks of intracellular anhydrous guanine crystals separated by cytoplasm, to produce the silvery luster of their skin and scales. Here we ...compare two different variants of the Japanese Koi fish; one of them with enhanced reflectivity. Our aim is to determine how biology modulates reflectivity, and from this to obtain a mechanistic understanding of the structure and properties governing the intensity of silver reflectance. We measured the reflectance of individual scales with a custom-made microscope, and then for each individual scale we characterized the structure of the guanine crystal/cytoplasm layers using high-resolution cryo-SEM. The measured reflectance and the structural-geometrical parameters were used to calculate the reflectance of each scale, and the results were compared to the experimental measurements. We show that enhanced reflectivity is obtained with the same basic guanine crystal/cytoplasm stacks, but the structural arrangement between the stack, inside the stacks, and relative to the scale surface is varied when reflectivity is enhanced. Finally, we propose a model that incorporates the basic building block parameters, the crystal orientation inside the tissue, and the resulting reflectance and explains the mechanistic basis for reflectance enhancement.
Vibrational spectroscopy in the electron microscope would be transformative in the study of biological samples, provided that radiation damage could be prevented. However, electron beams typically ...create high-energy excitations that severely accelerate sample degradation. Here this major difficulty is overcome using an 'aloof' electron beam, positioned tens of nanometres away from the sample: high-energy excitations are suppressed, while vibrational modes of energies <1 eV can be 'safely' investigated. To demonstrate the potential of aloof spectroscopy, we record electron energy loss spectra from biogenic guanine crystals in their native state, resolving their characteristic C-H, N-H and C=O vibrational signatures with no observable radiation damage. The technique opens up the possibility of non-damaging compositional analyses of organic functional groups, including non-crystalline biological materials, at a spatial resolution of ∼10 nm, simultaneously combined with imaging in the electron microscope.
An ugly duckling grows into a swan: Many organisms grow their crystalline mineral phases through the secondary nucleation of nanospheres made of an amorphous precursor phase. Stable amorphous calcium ...carbonate biominerals were used to induce a similar transformation in vitro. The amorphous nanospheres underwent a solid‐phase transformation that resulted in highly ordered calcite crystals composed of aggregated particles (see SEM image).
Light‐induced tunable photonic systems are rare in nature, and generally beyond the state‐of‐the‐art in artificial systems. Sapphirinid male copepods produce some of the most spectacular colors in ...nature. The male coloration, used for communication purposes, is structural and is produced from ordered layers of guanine crystals separated by cytoplasm. It is generally accepted that the colors of the males are related to their location in the epipelagic zone. By combining correlative reflectance and cryoelectron microscopy image analyses, together with optical time lapse recording and transfer matrix modeling, it is shown that male sapphirinids have the remarkable ability to change their reflectance spectrum in response to changes in the light conditions. It is also shown that this color change is achieved by a change in the thickness of the cytoplasm layers that separate the guanine crystals. This change is reversible, and is both intensity and wavelength dependent. This capability provides the male with the ability to efficiently reflect light under certain conditions, while remaining transparent and hence camouflaged under other conditions. These copepods can thus provide inspiration for producing synthetic tunable photonic arrays.
Male sapphirinids have the remarkable ability to change their reflectance spectrum in response to changes in the light conditions. This change is reversible, and is both intensity and wavelength dependent.
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