Two-way cooperation in a single symbiotic organ: the developmental chronicle of a multi-partner insect endosymbiosis - Archive ouverte HAL
Communication Dans Un Congrès Année : 2024

Two-way cooperation in a single symbiotic organ: the developmental chronicle of a multi-partner insect endosymbiosis

Thierry Hance

Résumé

Dependence on multiple nutritional endosymbionts forming a metabolic unit has repeatedly evolved in insect taxa that feed on nutritionally unbalanced diets. Typically, the different endosymbionts coexisting in the same host are affected to distinct types of bacteriocytes forming the symbiotic organ (the bacteriome). This compartmentalization allows symbiont populations to be finely tuned according to the host's nutritional requirements during development. However, the mechanisms underlying the coordination of partners in these multi-symbiotic systems are unknown. To unveil these mechanisms, we performed cell imaging, qPCR and dual-RNA seq approaches on the cereal aphid Sipha maydis, which has evolved a nutritional dependence on the symbiotic unit Buchnera aphidicola-Serratia symbiotica. The two symbionts are rapidly internalized in distinct types of bacteriocytes during embryogenesis, forming a horseshoe-shaped bacteriome. This consists of an assembly of syncytial bacteriocytes containing Serratia, embedded between uninucleate bacteriocytes containing Buchnera, which tend to dissociate from each other as the aphid ages. Surprisingly, while the infection dynamics of the two nutritional symbionts are strictly parallel during the nymphal stages, they tend to diverge during the reproductive phase, with a decrease in Buchnera populations and an increase in Serratia populations until the death of the host. This suggests that the metabolic complementation of the two symbionts tends to relax with host development, and that their populations are not controlled in the same way. Dual RNA-seq analyses of bacteriocyte clusters collected at different developmental stages show that control of both symbionts involves a range of genes related to metabolism, development and virulence. Our study also reveals the existence of new cell types systematically associated with bacteriocyte clusters. In conclusion, our study highlights some of the developmental mechanisms governing cooperative intracellular life between anatomically integrated nutritional symbionts and provides a comprehensive base map for examining the evolutionary developmental biology of insect multi-symbiotic systems.
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Dates et versions

hal-04753845 , version 1 (25-10-2024)

Identifiants

  • HAL Id : hal-04753845 , version 1

Citer

François Renoz, Karen Gaget, Hubert Charles, Mélanie Ribeiro Lopes, Nicolas Parisot, et al.. Two-way cooperation in a single symbiotic organ: the developmental chronicle of a multi-partner insect endosymbiosis. 3rd Joint Congress on Evolutionary Biology, Jul 2024, Montreal, Canada. ⟨hal-04753845⟩
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