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