Genome-resolved metagenomics reveals unexpected diversity and host range of Candidatus Lariskella (Rickettsiales: Midichloriaceae)

The intracellular endosymbiont Candidatus Lariskella (Alphaproteobacteria, Candidatus Midichloriaceae) has been found across a wide diversity of terrestrial arthropods, including ticks, true bugs, beetles, fleas, wasps and moths. Despite its prevalence, little is known about the biology of Ca. Lariskella, nor do we grasp the full extent of its host range. Here, we report the first known occurrence of Ca. Lariskella infecting a population of free-living marine nematodes (Enoplida, Thoracostomopsideae). This novel nematode-infecting Ca. Lariskella was found to be closely related to insect-infecting strains, despite the drastic shift in both host taxonomy and habitat. TEM and FISH microscopy showed Ca. Lariskella is localized within both the nematode somatic cells and developing oocytes, confirming its status as a nematode endosymbiont and strongly suggesting maternal transmission. This finding led us to reassess the host range of Ca. Lariskella. We screened the SRA database for Ca. Lariskella sequences and performed genome-resolved metagenomics on SRA entries positive for Ca. Lariskella. We recovered 16 novel Ca. Lariskella metagenome-assembled genomes from SRA entries, including from novel hosts such as ants and treehoppers. However, we did not encounter further instances of Ca. Lariskella within nematodes or marine invertebrates, which we attribute to the relatively poor sampling of these groups. Overall, our findings illustrate the ability of Ca. Lariskella to infect both arthropods and nematodes as well as hosts from both terrestrial and marine environments.