One to host them all: genomics of the diverse bacterial endosymbionts of the spiderOedothorax gibbosus

Abstract

AbstractBacterial endosymbionts of the groupsWolbachia, CardiniumandRickettsiaceaeare well-known for their diverse effects on their arthropod hosts, ranging from mutualistic relationships to reproductive phenotypes. Here, we analyzed a unique system in which the dwarf spiderOedothorax gibbosusis co-infected with up to five different endosymbionts affiliated withWolbachia, ‘CandidatusTisiphia’ (formerly Torix groupRickettsia), Cardinium,andRhabdochlamydia.Using short-read genome sequencing data, we show that the endosymbionts are heterogeneously distributed amongO. gibbosuspopulations and are frequently found co-infecting spider individuals. To study this intricate host-endosymbiont system on a genome resolved level, we used long-read sequencing to reconstruct closed genomes of theWolbachia, ‘Ca.Tisiphia’ andCardiniumendosymbionts. We provide insights in the ecology and evolution of the endosymbionts and shed light on the interactions with their spider host. We detected high quantities of transposable elements in all endosymbiont genomes and provide evidence that ancestors of theCardinium, ‘Ca.Tisiphia’ andWolbachiaendosymbionts have co-infected the same hosts in the past. Our findings contribute to broadening our knowledge about endosymbionts infecting one of the largest animal phyla on earth and show the usefulness of transposable elements as an evolutionary “contact-tracing” tool.Data summaryAll supporting data, code and protocols have been provided within the article or through supplementary data files. Seven supplementary figures and seven supplementary tables are available with the online version of this article. Sequencing data used in this study was generated and previously published by Hendrickxet al.,2021. Genome assemblies generated in this study have been deposited under the project PRJEB52003 at DDBJ/ENA/GenBank. The MAG ofR. oedothoracisOV001 was deposited at DDBJ/ENA/GenBank under the sample SAMN28026840. The genome of‘CandidatusRhabdochlamydia oedothoracis W744×776’ was previously published by Halteret al.,2022 and is available at DDBJ/ENA/GenBank (accession:CP075587-CP075588). The collection of genomes and proteomes, all files for phylogenetic analyses including gene alignments, concatenated alignments, and tree files, and original output files of the HGT and SNP predictions used in this study are available at zenodo (https://doi.org/10.5281/zenodo.6362846).