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.

细菌细胞内共生（内共生）在自然界很普遍，并影响许多生物学过程。在全代谢共生昆虫中，变态需要彻底而突然的内部重组，这会限制共生体从幼虫向成虫的传播。为了评估共生过程在整个主要宿主组织重组过程中如何应对并潜在地进化，我们使用谷类象鼻虫Sitophilus oryzae和Sodalis pierantonius细菌之间的关联作为模型系统。沙门氏菌它们包含在专门的宿主细胞即细菌细胞内，该细胞又组成一个器官即细菌群。谷物象鼻虫需要从它们的内共生体中代谢输入，特别是在成人角质层合成过程中，当内共生体负荷急剧增加时。通过结合双重RNA测序分析和细胞成像，我们表明，幼虫菌群在变态的开始时解离，并释放细菌细胞，这些细菌细胞经历共生依赖的转录组变化，从而影响细胞运动性，细胞粘附和细胞骨架组织。值得注意的是，细菌细胞会变成纺锤形细胞并沿着中肠上皮迁移，从而将共生菌运送到中肠部位，未来的肠系膜盲肠将会发育。同时，内共生体感染假定的干细胞并进入其细胞核时，编码III型分泌系统和鞭毛器的内共生体基因被瞬时上调。被感染的细胞然后变成新分化的细菌细胞，并在成年人中形成多种新细菌。这些发现表明，全代谢昆虫中的共生重组依赖于同步的宿主共生体分子和细胞“编排”，并说明了一种适应性特征，可促进细菌组的繁殖，以满足新兴成年人的新陈代谢需求。