A novel cell death process eliminates both bacteriocytes and their symbionts in the pea aphid/Buchnera symbiotic system - INRAE - Institut national de recherche pour l’agriculture, l’alimentation et l’environnement Accéder directement au contenu
Poster De Conférence Année : 2019

A novel cell death process eliminates both bacteriocytes and their symbionts in the pea aphid/Buchnera symbiotic system

Karen Gaget
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  • PersonId : 748250
  • IdHAL : gaget-karen

Résumé

Symbiosis is a key source of ecological and evolutionary diversification of eukaryotic organisms throughout the animal and plant kingdoms. In insects that are obligatorily dependent on intracellular bacterial symbionts, novel host cells, the bacteriocytes, have evolved for harboring beneficial microbial partners. These cells constitute a fascinating riddle in developmental cell biology, as their embryonic origin and the molecular mechanisms governing their development and organogenesis, as well as their elimination in response to host physiology, remain largely unsolved. Here we report the discovery of a hitherto unknown cell-death process involved in the degeneration of bacteriocytes in the pea aphid Acyrthosiphon pisum/Buchnera aphidicola symbiotic system, which emerged in recent years as a powerful model for studying symbiotic relationships. This new form of cell death is activated progressively throughout aphid adulthood and exhibits morphological features distinct from evolutionary-conserved pathways, including apoptosis- or autophagy-dependent cell deaths. By combining electron microscopy, immunohistochemistry, and molecular analyses, we demonstrated that the initial event of bacteriocyte cell death is the cytoplasmic accumulation of non-autophagic vacuoles, followed by a sequence of cellular stress responses including the formation of autophagosomes in intervacuolar spaces, swelling of bacteriocyte mitochondria, activation of reactive oxygen species, and Buchnera aphidicola endosymbiont degradation by the lysosomal system. This multistep cell-death process originates from the endoplasmic reticulum, an organelle exhibiting a unique reticular network organization in these cells, probably imposed by the presence of millions of Buchnera endosymbionts in each bacteriocyte. Our findings reveal novel mechanisms by which both bacteriocyte cell and symbiotic bacterial numbers are controlled to maintain organismal homeostasis. They also shed light on previously unknown consequences of persistent obligatory symbiotic bacteria on the cellular organization and functioning of bacteriocytes in their eukaryotic hosts.
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Dates et versions

hal-03513018 , version 1 (05-01-2022)

Identifiants

  • HAL Id : hal-03513018 , version 1

Citer

Mélanie Ribeiro Lopes, Pierre Simonet, Karen Gaget, Severine Balmand, Nicolas Parisot, et al.. A novel cell death process eliminates both bacteriocytes and their symbionts in the pea aphid/Buchnera symbiotic system. UK-France joint Meeting Aphid Special Interest Group – BAPOA, Apr 2019, Rothamsted, United Kingdom. ⟨hal-03513018⟩
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