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

Abstract

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.

Tryptophan regulatesDrosophilazinc stores

“…S13 and S16 ). These findings suggest that the two Trp metabolites are likely involved in Zn binding in microenvironments of variable pH and metal ion content, which may arise during the maturation and turnover of the Zn storage granule ( 44 , 45 ).…”

Towards routine 3D characterization of intact mesoscale samples by multi-scale and multimodal scanning X-ray tomography

“…Recent developments in fast continuous scanning, data acquisition 1 – 4 , and the high flux obtained at modern synchrotron-based hard X-ray nanoprobes have opened routine access to scanning 2D multimodal imaging. Amongst the scanning techniques, the high analytical sensitivity of X-ray Fluorescence (XRF) imaging provides unique possibilities in several scientific fields to study the role and fate of trace elements 5 – 13 . However, the unambiguous interpretation of 2D elemental distribution maps is not always straightforward or feasible and is especially problematic in the case of thick, complex samples.…”

The Formation of Biogenic Guanine Crystals Closely Resembles Melanosome Morphogenesis

“…Bagnara et al, postulated that all vertebrate pigment organelles ('-somes') derive from a common 'primordial vesicle' 21 , originating from the endosomal pathway 19 . Furthermore, it was shown that many of these pigment granules are lysosome-related organelles (LRO) [22][23][24] . Despite their inclusion in .…”

“…Bagnara et al, postulated that all vertebrate pigment organelles ('-somes') derive from a common 'primordial vesicle' 21 , originating from the endosomal pathway 19 . Furthermore, it was shown that many of these pigment granules are lysosome-related organelles (LRO) [22][23][24] . Despite their inclusion in the LRO family, iridosomes differ from other pigments in that they generate structural colors from crystals, rather than absorptive colors from pigments.…”