Dual-transcriptomic on microdissected cells reveals functional specialisation of symbiont-bearing-cells and contrasted responses to standard diet and nutritional stress in the cereal weevil Sitophilus oryzae

Insects thriving on a nutritionally imbalanced diet often establish long-term relationships with intracellular symbiotic bacteria (endosymbionts), which complement their nutritional needs and improve their physiological performances. Endosymbionts are in host specialised cells, called the bacteriocytes, which in many insects group together to form a symbiotic organ, the bacteriome. The cereal weevil Sitophilus oryzae houses multiple bacteriomes at the adult mesenteric caeca. Using microscopic cell imaging, we revealed that bacteriomes consist of several cell types, including progenitor cells, peripheral bacteriocytes, central bacteriocytes and epithelial cells. By combining laser capture microdissection and dual RNA-sequencing, we showed that both host cell types and their associated endosymbionts express distinct transcriptional profiles. The comparison between peripheral bacteriocytes and midgut cells from insects artificially deprived from endosymbionts (aposymbiotic) unravelled cellular pathways modulated by the presence of endosymbionts. The cell-specific response to endosymbionts in peripheral bacteriocytes includes a boost of fatty-acid and amino-acid metabolisms. We found that central bacteriocytes overexpress transport and G-protein signalling-related genes when compared to peripheral bacteriocytes, indicating their potential involvement in nutrient exchange between the gut lumen and peripheral bacteriocytes. Diet composition strongly impacts host and endosymbiont gene expression and revealed a molecular trade-off among metabolic pathways. This study provides evidence on how endosymbionts interfere and enhance metabolic performances of insect bacteriocytes, and highlights key genes involved in the bacteriocyte differentiation and metabolic pathways.