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

View ORCID ProfileFlorent Figon, Ilse Hurbain, View ORCID ProfileXavier Heiligenstein, View ORCID ProfileSylvain Trépout, View ORCID ProfileKadda Medjoubi, View ORCID ProfileAndrea Somogyi, View ORCID ProfileCédric Delevoye, Graça Raposo, View ORCID ProfileJérôme Casas
doi: https://doi.org/10.1101/2021.02.22.432296
Florent Figon
aInstitut de Recherche sur la Biologie de l’Insecte, UMR 7261, CNRS, Université de Tours, 37200 Tours, France
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  • For correspondence: florent.figon@univ-tours.fr jerome.casas@univ-tours.fr
Ilse Hurbain
bInstitut Curie, PSL Research University, CNRS, UMR 144, Structure and Membrane Compartments, 75005 Paris, France
cInstitut Curie, PSL Research University, CNRS, UMR 144, Cell and Tissue Imaging Facility (PICT-IBiSA), 75005 Paris, France
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Xavier Heiligenstein
dCryoCapCell, 80 rue du Général Leclerc, 94276 Le Kremlin-Bicêtre, France
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Sylvain Trépout
eInstitut Curie, INSERM U1196, CNRS, UMR 9187, Université Paris-Sud, Université Paris-Saclay, 91405 Orsay, France
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Kadda Medjoubi
fSynchrotron Soleil, Saint-Aubin, 91192 Gif-sur-Yvette, France
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Andrea Somogyi
fSynchrotron Soleil, Saint-Aubin, 91192 Gif-sur-Yvette, France
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  • ORCID record for Andrea Somogyi
Cédric Delevoye
bInstitut Curie, PSL Research University, CNRS, UMR 144, Structure and Membrane Compartments, 75005 Paris, France
cInstitut Curie, PSL Research University, CNRS, UMR 144, Cell and Tissue Imaging Facility (PICT-IBiSA), 75005 Paris, France
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Graça Raposo
bInstitut Curie, PSL Research University, CNRS, UMR 144, Structure and Membrane Compartments, 75005 Paris, France
cInstitut Curie, PSL Research University, CNRS, UMR 144, Cell and Tissue Imaging Facility (PICT-IBiSA), 75005 Paris, France
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Jérôme Casas
aInstitut de Recherche sur la Biologie de l’Insecte, UMR 7261, CNRS, Université de Tours, 37200 Tours, France
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  • For correspondence: florent.figon@univ-tours.fr jerome.casas@univ-tours.fr
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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.

Competing Interest Statement

The authors have declared no competing interest.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted February 22, 2021.
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Catabolism of lysosome-related organelles in color-changing spiders supports intracellular turnover of pigments
Florent Figon, Ilse Hurbain, Xavier Heiligenstein, Sylvain Trépout, Kadda Medjoubi, Andrea Somogyi, Cédric Delevoye, Graça Raposo, Jérôme Casas
bioRxiv 2021.02.22.432296; doi: https://doi.org/10.1101/2021.02.22.432296
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Catabolism of lysosome-related organelles in color-changing spiders supports intracellular turnover of pigments
Florent Figon, Ilse Hurbain, Xavier Heiligenstein, Sylvain Trépout, Kadda Medjoubi, Andrea Somogyi, Cédric Delevoye, Graça Raposo, Jérôme Casas
bioRxiv 2021.02.22.432296; doi: https://doi.org/10.1101/2021.02.22.432296

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