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Cephalopods produce dynamic colors and skin patterns for communication and camouflage via stratified networks of neuronally actuated yellow, red, and brown chromatophore organs, each filled with thousands of pigment granules. While compositional analysis of chromatophore granules in Doryteuthis pealeii reveals the pigments as ommochromes, the ultrastructural features of the granules and their effects on bulk coloration have not been explored. To investigate this, we isolated granules from specific colored chromatophores and imaged them using multiple modalities. The brown granules are largest with smooth surface coatings. Red granules are intermediate in size with irregular surface textures, and yellow granules are smallest, with rough, porous surfaces. Many of the granules contain sub-granular features that also vary in presentation with color. Correlated light and electron microscopy reveal that differences in hue of individual granules are similarly associated with size, shape, and texture, suggesting that granules may be structurally adapted to modify the dominant visible colors presented within the chromatophores. These findings suggest that granule ultrastructure, not just chemical composition, may be significant in producing the range of colors presented in cephalopod chromatophores.

Chromatophores provide an excellent model to study organelle transport as they specialize in the translocation of pigment granules in response to defined environmental signals. Our previous study revealed low-intensity light-induced xanthosomes aggregation is directly mediated by Opsin 3 in xanthophores of large yellow croaker ( Larimichthys crocea ). Herein, we report an incidental observation of prolonged (more than 40 min) high-intensity white light (HIWL) (10,000 lux, 3.86 mW/cm 2 ) exposure induce xanthosomes dispersion. After dispersion by HIWL exposure, the xanthosomes remains the ability to aggregate under low-intensity light conditions. Both light-emitting diode (LED) sources at different wavelengths (blue light, λ max  = 480 nm; red light, λ max  = 686 nm) with identical brightness (10,000 lux) but varying absolute irradiance levels (3.86–22.2 mW/cm 2 ) can induce xanthosome dispersion. Ex vivo illumination and pharmacological experiments on xanthophores revealed that HIWL-induced xanthosomes dispersion is irrelevant to signaling pathways typically associated with xanthosome movement, but mediated by microtubule depolymerization, which is due to extraordinary high level of intracellular Ca 2+ released from IP 3 R calcium channel in endoplasmic reticulum. Interestingly, such a mechanism was also presented in HeLa and HEK293T cells exposed to HIWL. In summary, our results expand our understanding of the impact of high-intensity light on intracellular organelle transport and cytoskeleton.

Few animals provide a readout that is as objective of their perceptual state as camouflaging cephalopods. Their skin display system includes an extensive array of pigment cells (chromatophores), each expandable by radial muscles controlled by motor neurons. If one could track the individual expansion states of the chromatophores, one would obtain a quantitative description—and potentially even a neural description by proxy—of the perceptual state of the animal in real time. Here we present the use of computational and analytical methods to achieve this in behaving animals, quantifying the states of tens of thousands of chromatophores at sixty frames per second, at single-cell resolution, and over weeks. We infer a statistical hierarchy of motor control, reveal an underlying low-dimensional structure to pattern dynamics and uncover rules that govern the development of skin patterns. This approach provides an objective description of complex perceptual behaviour, and a powerful means to uncover the organizational principles that underlie the function, dynamics and morphogenesis of neural systems. Tracking analyses of tens of thousands of individual chromatophores in freely behaving cephalopods enable studies of behaviour and development at cellular resolution.

Many chameleons, and panther chameleons in particular, have the remarkable ability to exhibit complex and rapid colour changes during social interactions such as male contests or courtship. It is generally interpreted that these changes are due to dispersion/aggregation of pigment-containing organelles within dermal chromatophores. Here, combining microscopy, photometric videography and photonic band-gap modelling, we show that chameleons shift colour through active tuning of a lattice of guanine nanocrystals within a superficial thick layer of dermal iridophores. In addition, we show that a deeper population of iridophores with larger crystals reflects a substantial proportion of sunlight especially in the near-infrared range. The organization of iridophores into two superposed layers constitutes an evolutionary novelty for chameleons, which allows some species to combine efficient camouflage with spectacular display, while potentially providing passive thermal protection. Colour change in many vertebrates originates from pigment dispersion or aggregation. Here, Teyssier et al . show that chameleons rapidly shift colour through a physical mechanism involving a lattice of nanocrystals in dermal iridophores, a second and deeper iridophore layer strongly reflects near-infrared light.

Cephalopod chromatophores are small dermal neuromuscular organs, each consisting of a pigment-containing cell and 10–20 surrounding radial muscles. Their expansions and contractions, controlled and coordinated by the brain, are used to modify the animal’s appearance during camouflaging and signaling. Building up on tools developed by this lab, we propose a flexible computational pipeline to track and analyze chromatophore dynamics from high-resolution videos of behaving cephalopods. This suite of functions, which we call CHROMAS, segments and classifies individual chromatophores, compensates for animal movements and skin deformations, thus enabling precise and parallel measurements of chromatophore dynamics and long-term tracking over development. A high-resolution tool for the analysis of chromatophore deformations during behavior reveals details of their motor control and thus, their likely innervation. When applied to many chromatophores simultaneously and combined with statistical and clustering tools, this analysis reveals the complex and distributed nature of the chromatophore motor units. We apply CHROMAS to the skins of the bobtail squid Euprymna berryi and the European cuttlefish Sepia officinalis , illustrating its performance with species with widely different chromatophore densities and patterning behaviors. More generally, CHROMAS offers many flexible and easily reconfigured tools to quantify the dynamics of pixelated biological patterns.

The construction of energetically autonomous artificial protocells is one of the most ambitious goals in bottom-up synthetic biology. Here, we show an efficient manner to build adenosine 5′- triphosphate (ATP) synthesizing hybrid multicompartment protocells. Bacterial chromatophores from Rhodobacter sphaeroides accomplish the photophosphorylation of adenosine 5′-diphosphate (ADP) to ATP, functioning as nanosized photosynthetic organellae when encapsulated inside artificial giant phospholipid vesicles (ATP production rate up to ∼100 ATP·s−1 per ATP synthase). The chromatophore morphology and the orientation of the photophosphorylation proteins were characterized by cryo-electron microscopy (cryo-EM) and time-resolved spectroscopy. The freshly synthesized ATP has been employed for sustaining the transcription of a DNA gene, following the RNA biosynthesis inside individual vesicles by confocal microscopy. The hybrid multicompartment approach here proposed is very promising for the construction of full-fledged artificial protocells because it relies on easy-to-obtain and ready-to-use chromatophores, paving the way for artificial simplified-autotroph protocells (ASAPs).

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. Chromatophores in cephalopod skin are known for fast changes in coloration due to light-scattering pigment granules. Here, authors demonstrate structural coloration facilitated by reflectin in sheath cells and offer insights into the interplay between structural and pigmentary coloration elements.

Animal body color is generated primarily by neural crest-derived pigment cells in the skin. Mammals and birds have only melanocytes on the surface of their bodies; however, fish have a variety of pigment cell types or chromatophores, including melanophores, xanthophores, and iridophores. The medaka has a unique chromatophore type called the leucophore. The genetic basis of chromatophore diversity remains poorly understood. Here, we report that three loci in medaka, namely, leucophore free (lf), lf-2 , and white leucophore (wl), which affect leucophore and xanthophore differentiation, encode solute carrier family 2, member 15b (slc2a15b), paired box gene 7a (pax7a), and solute carrier family 2 facilitated glucose transporter, member 11b (slc2a11b), respectively. Because lf-2 , a loss-of-function mutant for pax7a , causes defects in the formation of xanthophore and leucophore precursor cells, pax7a is critical for the development of the chromatophores. This genetic evidence implies that leucophores are similar to xanthophores, although it was previously thought that leucophores were related to iridophores, as these chromatophores have purine-dependent light reflection. Our identification of slc2a15b and slc2a11b as genes critical for the differentiation of leucophores and xanthophores in medaka led to a further finding that the existence of these two genes in the genome coincides with the presence of xanthophores in nonmammalian vertebrates: birds have yellow-pigmented irises with xanthophore-like intracellular organelles. Our findings provide clues for revealing diverse evolutionary mechanisms of pigment cell formation in animals.

Eukaryotic photosynthetic organelles, plastids, are the powerhouses of many aquatic and terrestrial ecosystems. The canonical plastid in algae and plants originated >1 Ga and therefore offers limited insights into the initial stages of organelle evolution. To address this issue, we focus here on the photosynthetic amoeba Paulinella micropora strain KR01 (hereafter, KR01) that underwent a more recent (∼124 Ma) primary endosymbiosis, resulting in a photosynthetic organelle termed the chromatophore. Analysis of genomic and transcriptomic data resulted in a high-quality draft assembly of size 707 Mb and 32,361 predicted gene models. A total of 291 chromatophore-targeted proteins were predicted in silico, 208 of which comprise the ancestral organelle proteome in photosynthetic Paulinella species with functions, among others, in nucleotide metabolism and oxidative stress response. Gene coexpression analysis identified networks containing known high light stress response genes as well as a variety of genes of unknown function (“dark” genes). We characterized diurnally rhythmic genes in this species and found that over 49% are dark. It was recently hypothesized that large double-stranded DNA viruses may have driven gene transfer to the nucleus in Paulinella and facilitated endosymbiosis. Our analyses do not support this idea, but rather suggest that these viruses in the KR01 and closely related P. micropora MYN1 genomes resulted from a more recent invasion.

Skin color patterns are ubiquitous in nature, impact social behavior, predator avoidance, and protection from ultraviolet irradiation. A leading model system for vertebrate skin patterning is the zebrafish; its alternating blue stripes and yellow interstripes depend on light-reflecting cells called iridophores. It was suggested that the zebrafish’s color pattern arises from a single type of iridophore migrating differentially to stripes and interstripes. However, here we find that iridophores do not migrate between stripes and interstripes but instead differentiate and proliferate in-place, based on their micro-environment. RNA-sequencing analysis further reveals that stripe and interstripe iridophores have different transcriptomic states, while cryogenic-scanning-electron-microscopy and micro-X-ray diffraction identify different crystal-arrays architectures, indicating that stripe and interstripe iridophores are different cell types. Based on these results, we present an alternative model of skin patterning in zebrafish in which distinct iridophore crystallotypes containing specialized, physiologically responsive, organelles arise in stripe and interstripe by in-situ differentiation. The skin of zebrafish is patterned by alternating blue stripes and yellow interstripes which arises from guanine crystal-containing cells called iridophores that reflect light. Here the authors track iridophores and see that they do not migrate between stripes and interstripes, but instead differentiate and proliferate in place based on their micro-environment.