Centre for Microbiology and Environmental Systems Science, University of Vienna, Vienna, Austria.
Doctoral School in Microbiology and Environmental Science, University of Vienna, Vienna, Austria.
Microbiol Spectr. 2022 Dec 21;10(6):e0262722. doi: 10.1128/spectrum.02627-22. Epub 2022 Oct 27.
Free-living bacteria have evolved multiple times to become host-restricted endosymbionts. The transition from a free-living to a host-restricted lifestyle comes with a number of different genomic changes, including a massive loss of genes. In host-restricted endosymbionts, gene inactivation and genome reduction are facilitated by mobile genetic elements, mainly insertion sequences (ISs). ISs are small autonomous mobile elements, and one of, if not the most, abundant transposable elements in bacteria. Proliferation of ISs is common in some facultative endosymbionts, and is likely driven by the transmission bottlenecks, which increase the level of genetic drift. In this study, we present a manually curated genome annotation for a Cardinium endosymbiont of the dwarf spider Oedothorax gibbosus. Cardinium species are host-restricted endosymbionts that, similarly to Colbachia spp., include strains capable of manipulating host reproduction. Through the focus on mobile elements, the annotation revealed a rampant spread of ISs, extending earlier observations in other Cardinium genomes. We found that a large proportion of IS elements are pseudogenized, with many displaying evidence of recent inactivation. Most notably, we describe the lineage-specific emergence and spread of a novel IS-derived Miniature Inverted repeat Transposable Element (MITE), likely being actively maintained by intact copies of its parental IS982-family element. This study highlights the relevance of manual curation of these repeat-rich endosymbiont genomes for the discovery of novel MITEs, as well as the possible role these understudied elements might play in genome streamlining. Cardinium bacteria, a widespread symbiont lineage found across insects and nematodes, have been linked to reproductive manipulation of their hosts. However, the study of Cardinium has been hampered by the lack of comprehensive genomic resources. The high content of mobile genetic elements, namely, insertion sequences (ISs), has long complicated the analyses and proper annotations of these genomes. In this study, we present a manually curated annotation of the Cardinium symbiont of the spider Oedothorax gibbosus. Most notably, we describe a novel IS-like element found exclusively in this strain. We show that this mobile element likely evolved from a defective copy of its parental IS and then spread throughout the genome, contributing to the pseudogenization of several other mobile elements. We propose this element is likely being maintained by the intact copies of its parental IS element and that other similar elements in the genome could potentially follow this route.
自由生活的细菌多次进化成为宿主限制的内共生体。从自由生活到宿主限制的生活方式的转变伴随着许多不同的基因组变化,包括大量基因的丢失。在宿主限制的内共生体中,基因失活和基因组减少是由移动遗传元件,主要是插入序列(ISs)来促进的。ISs 是小型自主移动元件,是细菌中最丰富的转座元件之一。在一些兼性内共生体中,ISs 的增殖很常见,这可能是由遗传漂变的传递瓶颈驱动的。在这项研究中,我们提出了一个手动注释的 Cardinium 内共生体的基因组,该内共生体是 dwarf spider Oedothorax gibbosus 的内共生体。Cardinium 物种是宿主限制的内共生体,类似于 Colbachia spp.,包括能够操纵宿主繁殖的菌株。通过关注移动元件,注释揭示了 ISs 的猖獗传播,扩展了之前在其他 Cardinium 基因组中的观察结果。我们发现,很大一部分 IS 元件是假基因化的,许多元件显示出最近失活的证据。值得注意的是,我们描述了一种新型的由 IS 衍生的微型反向重复转座元件(MITE)的谱系特异性出现和传播,它可能由其亲本 IS982 家族元件的完整拷贝积极维持。这项研究强调了对这些富含重复序列的内共生体基因组进行手动注释的重要性,以发现新的 MITEs,以及这些研究较少的元件可能在基因组简化中发挥的作用。Cardinium 细菌是一种广泛存在于昆虫和线虫中的共生体谱系,与宿主的生殖操纵有关。然而,Cardinium 的研究受到缺乏全面基因组资源的阻碍。高含量的移动遗传元件,即插入序列(ISs),长期以来一直使这些基因组的分析和正确注释复杂化。在这项研究中,我们提出了对蜘蛛 Oedothorax gibbosus 的 Cardinium 共生体的手动注释。值得注意的是,我们描述了一种仅在该菌株中发现的新型 IS 样元件。我们表明,这种移动元件可能是从其亲本 IS 的缺陷拷贝进化而来的,然后在整个基因组中传播,导致其他几个移动元件的假基因化。我们提出,这个元件可能是由其亲本 IS 元件的完整拷贝维持的,而基因组中的其他类似元件可能会沿着这条路线发展。