Dynamic pigmentary and structural coloration within cephalopod chromatophore organs

Abstract

Chromatophore organs in cephalopod skin are known to produce ultra-fast changes in appearance for camouflage and communication. Light-scattering pigment granules within chromatocytes have been presumed to be the sole source of coloration in these complex organs. We report the discovery of structural coloration emanating in precise register with expanded pigmented chromatocytes. Concurrently, using an annotated squid chromatophore proteome together with microscopy, we identify a likely biochemical component of this reflective coloration as reflectin proteins distributed in sheath cells that envelop each chromatocyte. Additionally, within the chromatocytes, where the pigment resides in nanostructured granules, we find the lens protein Ω- crystallin interfacing tightly with pigment molecules. These findings offer fresh perspectives on the intricate biophotonic interplay between pigmentary and structural coloration elements tightly co-located within the same dynamic flexible organ - a feature that may help inspire the development of new classes of engineered materials that change color and pattern.

Cephalopod-inspired optical engineering of human cells

“…First, our work introduces the concept of directly engineering the optical properties, i.e. refractive index, and extent of light scattering, for living human cells via the incorporation of reflectin-based structures and, therefore, lays the groundwork for the development of mammalian cells and organoids with other sophisticated cephalopod-inspired optical functionalities, such as stimuliresponsive dynamic iridescence or mechanically reconfigurable coloration 26,50 . Second, the unexpected observation that reflectinbased structure arrangements not only readily self-assemble but also maintain their high refractive indices within the foreign biological environment of human cells suggests that common paradigms, e.g.…”

“…Second, the unexpected observation that reflectinbased structure arrangements not only readily self-assemble but also maintain their high refractive indices within the foreign biological environment of human cells suggests that common paradigms, e.g. sequence motifs, may underpin the structures and functions of reflectin-based architectures within the proteins' diverse native biological environments, which include chromatophore sheath cells 50 , iridophores [25][26][27][28] , and leucophores [17][18][19][20] . Third, given that such native cephalopod skin cells remain quite challenging to culture, the reported designer mammalian cells may constitute appropriate surrogate model frameworks for making further discoveries with regard to the properties of reflectins and the molecular and cellular biology of molluscs.…”

Structure, self-assembly, and properties of a truncated reflectin variant

“…Analogously, folded membranes containing distributed reflectin-based particle arrangements within sheath cells lead to the mechanically actuated iridescence of squid chromatophore organs, as shown in Fig. 1 C ( 15 , 16 , 21 , 22 ). Moreover, in vitro, films processed from squid reflectins not only exhibit proton conductivities on par with some state-of-the-art artificial materials ( 23 – 27 ) but also support the growth of murine and human neural stem cells ( 28 , 29 ).…”

“…Within this context, unique structural proteins known as reflectins have recently attracted substantial attention because of their key roles in the fascinating color-changing capabilities of cephalopods, such as the squid shown in Fig. 1 A , and have furthermore demonstrated their utility for unconventional biophotonic and bioelectronic technologies ( 11 – 40 ). For example, in vivo, Bragg stack-like ultrastructures from reflectin-based high refractive index lamellae (membrane-enclosed platelets) are responsible for the angle-dependent narrowband reflectance (iridescence) of squid iridophores, as shown in Fig.…”

Electronic coupling in the reduced state lies at the origin of color changes of ommochromes

“…Second, it has long been known that absorbance spectra of ommochromes are red-shifted in insects eyes compared to in vitro ( [6,48,49]). We propose that properties of the matrix in which ommochromes are deposited and that alter their absorbance, such as proteins [49,50] and metals [51,52], do so by modulating the electrophilicity and the conjugation of ommochrome EWAs, leading ultimately to their bathochromic behaviors uniquely observed in vivo.…”