Coexistence of both gyroid chiralities in individual butterfly wing scales of Callophrys rubi

Abstract

The wing scales of the Green Hairstreak butterfly Callophrys rubi consist of crystalline domains with sizes of a few micrometers, which exhibit a congenitally handed porous chitin microstructure identified as the chiral triply periodic single-gyroid structure. Here, the chirality and crystallographic texture of these domains are investigated by means of electron tomography. The tomograms unambiguously reveal the coexistence of the two enantiomeric forms of opposite handedness: the left-and right-handed gyroids. These two enantiomers appear with nonequal probabilities, implying that molecularly chiral constituents of the biological formation process presumably invoke a chiral symmetry break, resulting in a preferred enantiomeric form of the gyroid structure. Assuming validity of the formation model proposed by Ghiradella H (1989) J Morphol 202(1): 69-88 and Saranathan V, et al. (2010) Proc Natl Acad Sci USA 107(26):11676-11681, where the two enantiomeric labyrinthine domains of the gyroid are connected to the extracellular and intra-SER spaces, our findings imply that the structural chirality of the single gyroid is, however, not caused by the molecular chirality of chitin. Furthermore, the wing scales are found to be highly textured, with a substantial fraction of domains exhibiting the <001> directions of the gyroid crystal aligned parallel to the scale surface normal. Both findings are needed to completely understand the photonic purpose of the single gyroid in gyroid-forming butterflies. More importantly, they show the level of control that morphogenesis exerts over secondary features of biological nanostructures, such as chirality or crystallographic texture, providing inspiration for biomimetic replication strategies for synthetic self-assembly mechanisms.electron tomography | chirality | crystallographic texture | photonic crystal | butterfly wing scales A lthough the formation of chiral structures is fascinating, their occurrence can often be rationalized by simple energy or free energy considerations without a need to resort to their possible biological origin. For example, handed structures are observed in the simplest models of phyllotaxis (1) and self-assembly of biological fibers (2). In such models, there is no energetic distinction between and hence, a balance of the two enantiomers [that is, the right-handed (RH) and left-handed (LH) versions of the chiral structure]. Chiral symmetry breaking, the process by which one enantiomer occurs exclusively or with prevalence, is commonly observed in biological materials on a range of scales from molecular dimensions and the structure of DNA to the macroscopic size of snails (3). The dominance of one enantiomer is driven by the presence of a force or molecular building block that favors one enantiomer over the other; constituent chiral molecules (4), genetically controlled molecular pathways (3), and biological generation of torque (5) are possible causes.Here, we investigate the chiral symmetry breaking of the singlegyroid structure, a complex network-lik...

Highly sensitive, reproducible and uniform SERS substrates with a high density of three-dimensionally distributed hotspots: gyroid-structured Au periodic metallic materials

“…[28][29][30][31][32][33][34] The gyroid-structured scales stack in a tiled manner on the ventral wings of C. rubi. Randomly oriented domains exist inside the scales, as shown in the optical image of a single gyroid scale ( Figure 2a) and also demonstrated in the SEM and TEM images (Figures 2b-d).…”

Fabrication of Photonic Bandgap Materials by Shifting Double Frameworks

“…The double‐diamond (Figure a,c), double‐gyroid (Figure e,g), and double‐primitive structures are the most commonly observed. Nevertheless, the biological structures discovered in the exoskeleton of beetles and weevils and the wing scales of butterfly only consist of one set of the frameworks …”

“…Nevertheless, the biological structures discovered in the exoskeleton of beetles and weevils and the wing scales of butterfly only consist of one set of the frameworks. [19,20,[22][23][24][25][26] It is worth noting that the single-framework feature of these biological structures is crucial to their photonic properties. Unfortunately,t heir outstanding optical performance was not reflectedi nb icontinuous structures with double frameworks.…”

“…The gyroid surface contains two sets of threefold connected chiral labyrinths with opposite chirality, in which the screw axes run through the labyrinths along different directions (space group Ia d ). Similarly, the single‐gyroid structure was discovered in the scales of butterfly wings of some papilionids and lycaenids (Figure f) . The single‐gyroid structure contains no inversion centers or mirror planes, exhibiting inherent chirality that is different from other materials (space group I 4 1 32).…”

“…Similarly,t he single-gyroid structure was discovered in the scales of butterfly wings of some papilionids and lycaenids ( Figure 1f). [8,20,[22][23][24][25][26] The single-gyroid structure contains no inversion centers or mirrorp lanes, exhibiting inherent chirality that is different from other materials (space group I4 1 32). Compared to the single-diamond, the single-gyroid structure also showsacomplete band gap feature nearly as good as the single-diamonds tructure, [27] whereas the single-gyroid structure exhibits the unique chiralf eature of polarization-dependento pticalr esponse and negative refractionst ot he recent prediction of Weyl points and line nodes.…”