Department of Insect Symbiosis, Max Planck Institute for Chemical Ecology, 07745 Jena, Germany.
Department of Evolutionary Ecology, Institute of Organismic and Molecular Evolution, Johannes Gutenberg University, 55128 Mainz, Germany.
ISME J. 2024 Jan 8;18(1). doi: 10.1093/ismejo/wrae099.
Insects engage in manifold interactions with bacteria that can shift along the parasitism-mutualism continuum. However, only a small number of bacterial taxa managed to successfully colonize a wide diversity of insects, by evolving mechanisms for host-cell entry, immune evasion, germline tropism, reproductive manipulation, and/or by providing benefits to the host that stabilize the symbiotic association. Here, we report on the discovery of an Enterobacterales endosymbiont (Symbiodolus, type species Symbiodolus clandestinus) that is widespread across at least six insect orders and occurs at high prevalence within host populations. Fluorescence in situ hybridization in several Coleopteran and one Dipteran species revealed Symbiodolus' intracellular presence in all host life stages and across tissues, with a high abundance in female ovaries, indicating transovarial vertical transmission. Symbiont genome sequencing across 16 host taxa revealed a high degree of functional conservation in the eroding and transposon-rich genomes. All sequenced Symbiodolus genomes encode for multiple secretion systems, alongside effectors and toxin-antitoxin systems, which likely facilitate host-cell entry and interactions with the host. However, Symbiodolus-infected insects show no obvious signs of disease, and biosynthetic pathways for several amino acids and cofactors encoded by the bacterial genomes suggest that the symbionts may also be able to provide benefits to the hosts. A lack of host-symbiont cospeciation provides evidence for occasional horizontal transmission, so Symbiodolus' success is likely based on a mixed transmission mode. Our findings uncover a hitherto undescribed and widespread insect endosymbiont that may present valuable opportunities to unravel the molecular underpinnings of symbiosis establishment and maintenance.
昆虫与细菌之间存在多种相互作用,这些相互作用沿着寄生-共生连续体发生变化。然而,只有少数细菌类群通过进化出宿主细胞进入、免疫逃避、生殖细胞趋向性、生殖操纵和/或为宿主提供稳定共生关系的益处等机制,成功地在广泛的昆虫多样性中定植。在这里,我们报告了一种肠杆菌内共生体(Symbiodolus,模式种 Symbiodolus clandestinus)的发现,该共生体广泛存在于至少六个昆虫目,并且在宿主种群中普遍存在。在几种鞘翅目和一种双翅目物种中的荧光原位杂交显示,Symbiodolus 存在于所有宿主生命阶段和组织中,在雌性卵巢中丰度较高,表明经卵垂直传播。对 16 个宿主类群的共生体基因组测序揭示了在侵蚀和转座子丰富的基因组中具有高度的功能保守性。所有测序的 Symbiodolus 基因组都编码了多个分泌系统,以及效应子和毒素-抗毒素系统,这可能有助于宿主细胞进入和与宿主相互作用。然而,感染 Symbiodolus 的昆虫没有明显的疾病迹象,并且细菌基因组编码的几种氨基酸和辅酶的生物合成途径表明,共生体也可能为宿主提供益处。宿主-共生体的非共进化提供了偶尔水平传播的证据,因此 Symbiodolus 的成功可能基于混合传播模式。我们的发现揭示了一种迄今未被描述的广泛存在的昆虫内共生体,它可能为揭示共生体建立和维持的分子基础提供有价值的机会。