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, 107 (26), 11676-81

Structure, Function, and Self-Assembly of Single Network Gyroid (I4132) Photonic Crystals in Butterfly Wing Scales

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Structure, Function, and Self-Assembly of Single Network Gyroid (I4132) Photonic Crystals in Butterfly Wing Scales

Vinodkumar Saranathan et al. Proc Natl Acad Sci U S A.

Abstract

Complex three-dimensional biophotonic nanostructures produce the vivid structural colors of many butterfly wing scales, but their exact nanoscale organization is uncertain. We used small angle X-ray scattering (SAXS) on single scales to characterize the 3D photonic nanostructures of five butterfly species from two families (Papilionidae, Lycaenidae). We identify these chitin and air nanostructures as single network gyroid (I4(1)32) photonic crystals. We describe their optical function from SAXS data and photonic band-gap modeling. Butterflies apparently grow these gyroid nanostructures by exploiting the self-organizing physical dynamics of biological lipid-bilayer membranes. These butterfly photonic nanostructures initially develop within scale cells as a core-shell double gyroid (Ia3d), as seen in block-copolymer systems, with a pentacontinuous volume comprised of extracellular space, cell plasma membrane, cellular cytoplasm, smooth endoplasmic reticulum (SER) membrane, and intra-SER lumen. This double gyroid nanostructure is subsequently transformed into a single gyroid network through the deposition of chitin in the extracellular space and the degeneration of the rest of the cell. The butterflies develop the thermodynamically favored double gyroid precursors as a route to the optically more efficient single gyroid nanostructures. Current approaches to photonic crystal engineering also aim to produce single gyroid motifs. The biologically derived photonic nanostructures characterized here may offer a convenient template for producing optical devices based on biomimicry or direct dielectric infiltration.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
Anatomy of the structural color-producing nanostructure in lycaenid and papilionid butterflies. (A) Light micrograph of the ventral wing cover scales of Callophrys (formerly Mitoura) gryneus (Lycaenidae). The opalescent highlights are produced by randomly oriented crystallite domains. (Scale bar: 100 μm.) (B) SEM image of the dorsal surface of a C. gryneus scale showing disjoint crystallites beneath windows created by a network of parallel, longitudinal ridges and slender, spaced cross-ribs. (Inset) Simulated SEM (111) projection from a thick slab of a level set single gyroid nanostructure. (Scale bar: 2.5 μm.) (C) TEM image of the C. gryneus nanostructure showing a distinctive motif, uniquely characteristic of the (310) plane of the gyroid morphology. (Inset) A matching simulated (310) TEM section of a level set single gyroid model. (Scale bar: 200 nm.) (D) Light micrograph of the dorsal wing cover scales of the Parides sesostris (Papilionidae). (Scale bar: 100 μm.) (E) SEM image of the lateral surface of the wing scale nanostructure of P. sesostris showing fused polycrystalline domains beneath columnar windows created by a network of ridges and spaced cross-ribs. The fractured face features a square lattice of air holes in chitin. (Inset) Simulated SEM (100) projection from a thick slab of a level set single gyroid nanostructure. (Scale bar: 2 μm.) (F) TEM image of the P. sesostris nanostructure showing a distinctive motif, uniquely characteristic of the (211) plane of the gyroid morphology. (Inset) A matching simulated (211) TEM section of a level set single gyroid model. (Scale bar: 2 μm.) c, chitin; a, air void.
Fig. 2.
Fig. 2.
Representative 2D SAXS patterns (original image 1340 × 1300 pixels) for (A) Teinopalpus imperialis, (B) Parides sesostris, (C) Callophrys (Mitoura) gryneus, and (D) Cyanophrys herodotus. The false color scale corresponds to the logarithm of the X-ray scattering intensity. The radii of the concentric circles are given by the peak scattering wave vector (qmax) times the moduli of the assigned hkl indices, where h, k, and l are integers allowed by the single gyroid (I4132) symmetry space group (IUCr International Tables for Crystallography).
Fig. 3.
Fig. 3.
Normalized azimuthally averaged X-ray scattering profiles (Intensity I/Imax vs. scattering wave vector q/qmax) calculated from the respective 2D SAXS patterns for Teinopalpus imperialis, Parides sesostris, Callophrys (Mitoura) gryneus, Callophrys dumetorum, and Cyanophrys herodotus. The vertical lines correspond to the expected Bragg peak positional ratios for the single gyroid crystallographic space group (I4132). The numbers above the lines are squares of the moduli of the Miller indices (hkl) for the allowed reflections. The calculated, normalized structure factors for a single gyroid (I4132) level set model for C. herodotus, with 29% dielectric volume fraction and a lattice constant of 331 nm, is also shown alongside for comparison (yellow diamonds). (Also see Fig. S3).
Fig. 4.
Fig. 4.
Predicted reflectance (black line) from azimuthal average of SAXS patterns versus measured optical reflectance (blue line) for (A) Teinopalpus imperialis, (B) Parides sesostris, (C) Callophrys (Mitoura) gryneus, and (D) Cyanophrys herodotus. The SAXS predicted reflectance follows from Bragg’s law and is given by mapping the X-ray scattering intensity from scattering wave vector to wavelength space by choosing a value of 1.16 for the average refractive index, nav, which corresponds to a chitin volume fraction of 0.25. See text for details.
Fig. 5.
Fig. 5.
Development of butterfly wing scale photonic nanostructure. (A) TEM cross-section of a ventral wing scale cell from a 9-day-old C. gryneus pupa (from refs.  and 21), depicts the complex infolding of the plasma membrane and SER membrane. The developing nanostructure shows the diagnostic motif of two concentric rings roughly in a triangular lattice (compare with Fig.5B). Yellow and red boxes highlight areas revealing different sections through the (110) plane of a polarized (ABCB′A′) pentacontinuous core-shell double gyroid (color insets). (Scale bar: 1 μm.) (Inset) Colored model of a core-shell double gyroid of ABCB′A′ form: A (red) is the extracellular space, B (black) is the plasma membrane, C (white) is the cytoplasmic intracellular space, B' (blue) is the SER membrane, and A' (yellow) is the intra-SER space. [Reprinted with permission from ref. .) (B) OsO4-stained (110) TEM section of an ABC triblock copolymer with core-shell double gyroid morphology. (Scale bar: 200 nm.) (Reprinted with permission from ref. . Copyright 2005, John Wiley and Sons.) (C) Three-dimensional model of development of photonic butterfly wing scale cell. (I) Unit-cell volume rendering of the core-shell double gyroid model structure of the form ABCB′A′. Color of each component from inset in A. (II) Single gyroid composed of cell plasma membrane (black) surrounding extracellular space (red). (III) As the scale cell dies, the cellular cytoplasm and membranes (BCB′A′ blocks of the core-shell double gyroid) are replaced with air leaving behind a single gyroid core-shell network of chitin (red) in air.

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