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

Significance Pigment–light interactions have shaped animal evolution, from vision to camouflage. How organisms cope with harmful photodegradative products while maintaining pigment-bearing cell integrity, from skin to light screening in eyes, remains mysterious. We studied color-changing crab spiders to unravel the intracellular mechanisms leading to within-cell formation and degradation of pigment organelles. We found that they belong to the widespread lysosome-related organelle family, like vertebrate melanosomes. The endolysosomal system allows reversible coloration in spiders by sustaining pigment turnover thanks to its fundamental anabolic and catabolic functions, a hypothesis first laid out for human eyes. Our findings imply that the ubiquitous endolysosomal system had been repurposed early in animal evolution to handle pigment–light interactions, providing phenotypic plasticity and cell function maintenance. 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.