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Intracellular symbiont Symbiodolus is vertically transmitted and widespread across insect orders
The ISME Journal ( IF 10.8 ) Pub Date : 2024-06-14 , DOI: 10.1093/ismejo/wrae099 Jürgen C Wierz 1 , Philipp Dirksen 1, 2 , Roy Kirsch 1 , Ronja Krüsemer 1 , Benjamin Weiss 1 , Yannick Pauchet 1 , Tobias Engl 1 , Martin Kaltenpoth 1
The ISME Journal ( IF 10.8 ) Pub Date : 2024-06-14 , DOI: 10.1093/ismejo/wrae099 Jürgen C Wierz 1 , Philipp Dirksen 1, 2 , Roy Kirsch 1 , Ronja Krüsemer 1 , Benjamin Weiss 1 , Yannick Pauchet 1 , Tobias Engl 1 , Martin Kaltenpoth 1
Affiliation
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 S. 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.
中文翻译:
细胞内共生体 Symbiodolus 在昆虫目中垂直传播并广泛传播
昆虫与细菌进行多种相互作用,这些相互作用可以沿着寄生-互利的连续体变化。然而,只有少数细菌类群通过宿主细胞进入、免疫逃避、种系向性、繁殖操纵的进化机制,和/或通过为宿主提供稳定共生的益处,成功地在多种昆虫中定殖。协会。在这里,我们报告了肠杆菌内共生菌(Symbiodolus,模式种 S. clandestinus)的发现,该菌广泛分布于至少六种昆虫目中,并且在宿主种群中普遍存在。几种鞘翅目和一种双翅目物种的荧光原位杂交揭示了 Symbiodolus 在所有宿主生命阶段和跨组织中的细胞内存在,在雌性卵巢中丰度很高,表明跨卵巢垂直传播。跨 16 个宿主分类单元的共生体基因组测序揭示了侵蚀和富含转座子的基因组的高度功能保守性。所有测序的 Symbiodolus 基因组都编码多个分泌系统,以及效应器和毒素-抗毒素系统,这可能促进宿主细胞进入并与宿主相互作用。然而,感染共生体的昆虫没有表现出明显的疾病迹象,细菌基因组编码的几种氨基酸和辅因子的生物合成途径表明,共生体也可能为宿主提供益处。宿主与共生体共生的缺乏为偶尔的水平传播提供了证据,因此共生体的成功很可能基于混合传播模式。 我们的发现揭示了一种迄今为止未被描述的广泛的昆虫内共生体,这可能为揭示共生建立和维持的分子基础提供了宝贵的机会。
更新日期:2024-06-14
中文翻译:
细胞内共生体 Symbiodolus 在昆虫目中垂直传播并广泛传播
昆虫与细菌进行多种相互作用,这些相互作用可以沿着寄生-互利的连续体变化。然而,只有少数细菌类群通过宿主细胞进入、免疫逃避、种系向性、繁殖操纵的进化机制,和/或通过为宿主提供稳定共生的益处,成功地在多种昆虫中定殖。协会。在这里,我们报告了肠杆菌内共生菌(Symbiodolus,模式种 S. clandestinus)的发现,该菌广泛分布于至少六种昆虫目中,并且在宿主种群中普遍存在。几种鞘翅目和一种双翅目物种的荧光原位杂交揭示了 Symbiodolus 在所有宿主生命阶段和跨组织中的细胞内存在,在雌性卵巢中丰度很高,表明跨卵巢垂直传播。跨 16 个宿主分类单元的共生体基因组测序揭示了侵蚀和富含转座子的基因组的高度功能保守性。所有测序的 Symbiodolus 基因组都编码多个分泌系统,以及效应器和毒素-抗毒素系统,这可能促进宿主细胞进入并与宿主相互作用。然而,感染共生体的昆虫没有表现出明显的疾病迹象,细菌基因组编码的几种氨基酸和辅因子的生物合成途径表明,共生体也可能为宿主提供益处。宿主与共生体共生的缺乏为偶尔的水平传播提供了证据,因此共生体的成功很可能基于混合传播模式。 我们的发现揭示了一种迄今为止未被描述的广泛的昆虫内共生体,这可能为揭示共生建立和维持的分子基础提供了宝贵的机会。