Journal Article

Spatial and morphological reorganization of endosymbiosis during metamorphosis accommodates adult metabolic requirements in a weevil

ANR-13-BSV7-0016,IMetSym,Contrôles immunitaire et métabolique dans les symbioses intracellulaires d'insectes, Institut de Génomique Fonctionnelle de Lyon (IGFL) ; École normale supérieure de Lyon (ENS de Lyon) ; Université de Lyon-Université de Lyon-Université Claude Bernard Lyon 1 (UCBL) ; Université de Lyon-Centre National de la Recherche Scientifique (CNRS)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Vincent-Monégat, Carole, Zaidman-Rémy, Anna, Galvao Ferrarini, Mariana, Parisot, Nicolas, Heddi, Abdelaziz, Hughes, Sandrine, Balmand, Severine, Gillet, Benjamin, Maire, Justin, Vallier, Agnès

2020

Overview

Bacterial intracellular symbiosis (endosymbiosis) is widespread in nature and impacts many biological processes. In holometabolous symbiotic insects, metamorphosis entails a complete and abrupt internal reorganization that creates a constraint for endosymbiont transmission from larvae to adults. To assess how endosymbiosis copes—and potentially evolves—throughout this major host-tissue reorganization, we used the association between the cereal weevil Sitophilus oryzae and the bacterium Sodalis pierantonius as a model system. S. pierantonius are contained inside specialized host cells, the bacteriocytes, that group into an organ, the bacteriome. Cereal weevils require metabolic inputs from their endosymbiont, particularly during adult cuticle synthesis, when endosymbiont load increases dramatically. By combining dual RNA-sequencing analyses and cell imaging, we show that the larval bacteriome dissociates at the onset of metamorphosis and releases bacteriocytes that undergo endosymbiosis-dependent transcriptomic changes affecting cell motility, cell adhesion, and cytoskeleton organization. Remarkably, bacteriocytes turn into spindle cells and migrate along the midgut epithelium, thereby conveying endosymbionts to midgut sites where future mesenteric caeca will develop. Concomitantly, endosymbiont genes encoding a type III secretion system and a flagellum apparatus are transiently up-regulated while endosymbionts infect putative stem cells and enter their nuclei. Infected cells then turn into new differentiated bacteriocytes and form multiple new bacteriomes in adults. These findings show that endosymbiosis reorganization in a holometabolous insect relies on a synchronized host–symbiont molecular and cellular “choreography” and illustrates an adaptive feature that promotes bacteriome multiplication to match increased metabolic requirements in emerging adults.

• Publisher: National Academy of Sciences,HAL CCSD
• Subject: Adults / Animals / Bacterial Physiological Phenomena / Biological activity / Biological Evolution / Biological Sciences / Cell adhesion / Cell adhesion & migration / Cell differentiation / Cell migration / Cytoskeleton / Digestive System - microbiology / Endophytes - genetics / Endophytes - isolation & purification / Endophytes - physiology / Endosymbionts / Enterobacteriaceae - genetics / Enterobacteriaceae - isolation & purification / Enterobacteriaceae - physiology / Epithelium / Evolution / Female / Flagella / Gene sequencing / Insects / Larva - growth & development / Larva - microbiology / Larva - physiology / Larvae / Life Sciences / Male / Metabolism / Metamorphosis / Metamorphosis, Biological / Midgut / Multiplication / Nuclei (cytology) / Ribonucleic acid / RNA / Stem cells / Symbiosis / Transcriptomics / Weevils - growth & development / Weevils - microbiology / Weevils - physiology
• ISBN: 0005617900000