ScienceWeek

BIOPHYSICS: PHOTONIC STRUCTURES IN BIOLOGICAL SYSTEMS

The following points are made by P. Vukusic and J.R. Sambles (Nature 424:852):

1) The natural world has exploited photonic structures since the Cambrian explosion: the sudden and enormous diversification of life that accompanied the start of the Cambrian period over 500 million years ago. Evidence from this era suggests that the co-development of predator and prey coloration, in step with their visual systems, resulted in the evolution of various life forms. Light can be a significant selection pressure for the evolution of certain animal groups, leading to the astonishing diversity of natural photonic structures present in the world today. Such structures might provide the inspiration for future technological applications.

2) Decades before the synthesis of fabricated photonic structures, studies were revealing the complex and elegant way in which it was accomplished naturally. Aquatic systems were the subject of many of the earliest studies. Crystal multilayer structures of guanine were identified as the key component of colored and broad-band silver reflections in many fish and also found to be a high-reflectance element in many bioluminescent organs and a sub-retinal component that assists with specialized marine vision(1). Recent interest in aquatic systems has revealed photonic structures of astonishing complexity. For example, arm ossicles from light-sensitive species of brittlestar, Ophiocoma wendtii, have regular arrays of inorganic microstructures with a characteristic double-lens design(2). These microlenses are photonic elements, each composed of single anisotropic calcite crystals that focus light towards nerve bundles of photoreceptors 4-7 microns below them inside the arm ossicle tissue. The design of the surface of each lens and the orientation of constituent calcite minimizes spherical aberration and birefringence that might otherwise degrade the optical function. Such microlens arrays assist in creating levels of light and shadow sensitivity that may serve to warn of the presence of predators.

3) Equally fascinating are the nanostructures found in the hair-like setae of many species of polychaete worm. In these creatures, a two-dimensional (2D) hexagonal lattice of voids within the cross-section of each seta creates a natural pseudo-photonic crystal fibre along its full length(3,4). The high spatial periodicity of this lattice generates a partial photonic bandgap (PBG) by which color is strongly Bragg-scattered in certain directions. As a consequence of this, strong iridescence is observed laterally. The biological significance of the centers, and therefore of the intricate structure, is understood to be visibility; this contrasts with the principal design purpose of recently developed synthetic photonic crystal fibers, which is to guide light longitudinally(5). The absence of centrally located defects within the natural photonic fibers examined so far, prevents light-guiding in these setae.

4) Iridescence is much more commonly encountered in terrestrial systems than in aquatic systems. The photonics associated with brightly colored birds and insects has been extensively studied for over a century but only recently have significant advances been made. Discoveries of partial PBG structures in Coleoptera and Lepidoptera highlight the breadth of nature's innovative use of light. Although certain systems, among them species of Coleoptera and Hymenoptera, display subtle coloration as a result of diffraction from surface periodicities, the majority of strong photonic effects arise in species that have evolved structures that have layers of alternately high and low refractive index. This leads to optical interference: an effect that pervades much of modern optics and the physics of which is well understood.

5) In summary: Millions of years before we began to manipulate the flow of light using synthetic structures, biological systems were using nanometer-scale architectures to produce striking optical effects. An astonishing variety of natural photonic structures exists: a species of Brittlestar uses photonic elements composed of calcite to collect light, Morpho butterflies use multiple layers of cuticle and air to produce their striking blue centers, and some insects use arrays of elements, known as nipple arrays, to reduce reflectivity in their compound eyes. Natural photonic structures are providing inspiration for technological applications.

References (abridged):

1. Denton, E. J. Reflectors in fishes. Sci. Am. 224, 64-72 (1971)

2. Aizenberg, J., Tkachenko, A., Weiner, S., Addadi, L. & Hendler, G. Calcitic microlenses as part of the photoreceptor system in brittlestars. Nature 412, 819-822 (2001)

3. Parker, A. R., McPhedran, R. C., McKenzie, D. R., Botten, L. C. & Nicorovici, N. A. Photonic engineering: Aphrodite's iridescence. Nature 409, 36-37 (2001)

4. Vukusic, P. in Optical Interference Coatings (eds Kaiser, N. & Pulker, H. K.) 1-34 (Springer, New York, 2003)

5. Knight, J. C. & Russell, P. St. J. Photonic Crystal Fibers: New Ways to Guide Light. Science 296, 276-277 (2002)

Nature http://www.nature.com/nature

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CALCITIC MICROLENSES AS PART OF THE PHOTORECEPTOR SYSTEM IN BRITTLESTARS.

The following points are made by J. Aizenberg et al (Nature. 2001 412:783):

1) Photosensitivity in most echinoderms has been attributed to "diffuse" dermal receptors. The authors report that certain single calcite crystals used by brittlestars for skeletal construction are also a component of specialized photosensory organs, conceivably with the function of a compound eye.

2) The analysis of arm ossicles in Ophiocoma showed that in light-sensitive species, the periphery of the labyrinthic calcitic skeleton extends into a regular array of spherical microstructures that have a characteristic double-lens design. These structures are absent in light-indifferent species.

3) Photolithographic experiments in which a photoresist film was illuminated through the lens array showed selective exposure of the photoresist under the lens centers. These results provide experimental evidence that the microlenses are optical elements that guide and focus the light inside the tissue. The estimated focal distance (4-7 microns below the lenses) coincides with the location of nerve bundles -- the presumed primary photoreceptors.

4) The lens array is designed to minimize spherical aberration and birefringence and to detect light from a particular direction. The optical performance is further optimized by phototropic chromatophores that regulate the dose of illumination reaching the receptors. These structures represent an example of a multifunctional biomaterial that fulfills both mechanical and optical functions.

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