Ecology and evolution of chlamydial symbionts of arthropods

Abstract

The phylum Chlamydiae consists of obligate intracellular bacteria including major human pathogens and diverse environmental representatives. Here we investigated the Rhabdochlamydiaceae, which is predicted to be the largest and most diverse chlamydial family, with the few described members known to infect arthropod hosts. Using published 16S rRNA gene sequence data we identified at least 388 genus-level lineages containing about 14 051 putative species within this family. We show that rhabdochlamydiae are mainly found in freshwater and soil environments, suggesting the existence of diverse, yet unknown hosts. Next, we used a comprehensive genome dataset including metagenome assembled genomes classified as members of the family Rhabdochlamydiaceae, and we added novel complete genome sequences of Rhabdochlamydia porcellionis infecting the woodlouse Porcellio scaber, and of 'Candidatus R. oedothoracis' associated with the linyphiid dwarf spider Oedothorax gibbosus. Comparative analysis of basic genome features and gene content with reference genomes of well-studied chlamydial families with known host ranges, namely Parachlamydiaceae (protist hosts) and Chlamydiaceae (human and other vertebrate hosts) suggested distinct niches for members of the Rhabdochlamydiaceae. We propose that members of the family represent intermediate stages of adaptation of chlamydiae from protists to vertebrate hosts. Within the genus Rhabdochlamydia, pronounced genome size reduction could be observed (1.49-1.93 Mb). The abundance and genomic distribution of transposases suggests transposable element expansion and subsequent gene inactivation as a mechanism of genome streamlining during adaptation to new hosts. This type of genome reduction has never been described before for any member of the phylum Chlamydiae. This study provides new insights into the molecular ecology, genomic diversity, and evolution of representatives of one of the most divergent chlamydial families.

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

“…Such assembly challenges in metagenomic data highlights the importance of available complete genome sequences especially for groups known to include many transposable elements. Our comparative analysis further confirmed the involvement of transposable elements in genome rearrangements and genome evolution in Rhabdochlamydia oedothoracis as suggested earlier [39], as the location of transposase genes tend to correspond to breakages in synteny between the two genomes (Figure 2C).…”

“…Unlike other Rhabdochlamydia , the genome of ‘ Ca. R. oedothoracis’ contains a large number of transposable elements making up about 23% of the genome and leading to the hypothesis that its genome is currently undergoing genome size reduction [39]. Here, we compare the published genome of ‘ Ca.…”

“…For the endosymbionts of O. gibbosus we could identify different secretion systems that are well described for the respective clade. R. oedothoracis encodes, like all known members of the phylum Chlamydiae, a complete type III secretion system [22, 39, 70]. The genome of Cardinium sp.…”

“…ISs are mobile elements that can spread within a genome independent of cellular replication and are known to be major drivers of bacterial genome evolution and diversification [82]. They are involved in genome size reduction by inactivation of genes under relaxed selection [83], as suggested for Rhabdochlamydia [39]. ISs can also move between genomes of different species by means of horizontal gene transfer (HGT) and thereby mediate the exchange of genetic material across species [82].…”

“…The genome of the Rhabdochlamydia symbiont of O. gibbosus was previously described by Halter et al, 2022. It revealed a high similarity to its closest relatives R. porcellionis and 'Ca. R. helvetica', infecting crustacean and arachnid hosts, respectively [23,24].…”