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

Pigment organelles of vertebrates belong to the lysosome-related organelle (LRO) family, of which melanin-producing melanosomes are the prototypes. While their anabolism has been extensively unraveled through the study of melanosomes in skin melanocytes, their catabolism remains poorly known. Here, we tap into the unique ability of crab spiders to reversibly change body coloration to examine the catabolism of their pigment organelles. By combining ultrastructural and metal analyses on high-pressure frozen integuments, we first assess whether pigment organelles of crab spiders belong to the LRO family and second, how their catabolism is intracellularly processed. Using scanning transmission electron microscopy, electron tomography, and nanoscale Synchrotron-based scanning X-ray fluorescence, we show that pigment organelles possess ultrastructural and chemical hallmarks of LROs, including intraluminal vesicles and metal deposits, similar to melanosomes. Monitoring ultrastructural changes during bleaching suggests that the catabolism of pigment organelles involves the degradation and removal of their intraluminal content, possibly through lysosomal mechanisms. In contrast to skin melanosomes, anabolism and catabolism of pigments proceed within the same cell without requiring either cell death or secretion/phagocytosis. Our work hence provides support for the hypothesis that the endolysosomal system is fully functionalized for within-cell turnover of pigments, leading to functional maintenance under adverse conditions and phenotypic plasticity. First formulated for eye melanosomes in the context of human vision, the hypothesis of intracellular turnover of pigments gets unprecedented strong support from pigment organelles of spiders.

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The Integrative Biology of Pigment Organelles, a Quantum Chemical Approach

Figon

Casas

2021

Integrative and Comparative Biology

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Coloration is a complex phenotypic trait involving both physical and chemical processes at a multiscale level, from molecules to tissues. Pigments, whose main property is to absorb specific wavelengths of visible light, are usually deposited in specialized organelles or complex matrices comprising proteins, metals, ions and redox compounds, among others. By modulating electronic properties and stability, interactions between pigments and these molecular actors can lead to color tuning. Furthermore, pigments are not only important for visual effects but also provide other critical functions, such as detoxification and antiradical activity. Hence, integrative studies of pigment organelles are required to understand how pigments interact with their cellular environment. In this review, we show how quantum chemistry, a computational method that models the molecular and optical properties of pigments, has provided key insights into the mechanisms by which pigment properties, from color to reactivity, are modulated by their organellar environment. These results allow to rationalize and to predict the way pigments behave in supramolecular complexes, up to the complete modelling of pigment organelles. We also discuss the main limitations of quantum chemistry, emphasizing the need for carrying experimental work with identical vigor. We finally suggest that taking into account the ecology of pigments (i.e. how they interact with these various other cellular components and at higher organizational levels) will lead to a greater understanding of how and why animals are vividly and variably colored, two fundamental questions in organismal biology.

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

Cited by 3 publications

References 51 publications

Unstability of cinnabarinic acid, an endogenous metabolite of tryptophan, under situations mimicking physiological conditions

Unstability of cinnabarinic acid, an endogenous metabolite of tryptophan, under situations mimicking physiological conditions

Catabolism of lysosome-related organelles in color-changing spiders supports intracellular turnover of pigments

The Integrative Biology of Pigment Organelles, a Quantum Chemical Approach

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