Stable association of a chlamydial symbiont with the freshwater predator hydra suggests broad host potential.

Abstract

Symbiotic associations between microorganisms often involve eukaryotes partnering with microbes for nutrient exchange, protection, and resource acquisition. Bacterial lineages like the Chlamydiota have evolved entirely symbiotic lifestyles, exploiting their eukaryotic hosts for energy, diverse metabolites, and shelter. The study of environmental chlamydiae-outside the well-studied vertebrate host range-has revealed diverging interactions on the mutualism-parasitism spectrum. This highlights their potentially important roles in host-microbe interactions underscoring the relevance of obtaining isolates from diverse environments and hosts. Here, we describe an isolate of a chlamydial symbiont of the freshwater cnidarian Hydra. The symbiont could be isolated and stably maintained in insect cell lines and represents a member of the recently described family-level lineage Chlamydiae Clade III for which we propose the name Endochlamydiaceae. Fluorescence and electron microscopy reveal the symbiont morphology and its endodermal location. Comparative genomics shows the isolate, named Endochlamydia hydrae, encodes a conserved set of genes involved in host invasion, communication, and pathogenicity. Instead of displaying unique genomic adaptations to its animal host, E. hydrae shows signs consistent with ongoing genome reorganisation and streamlining, suggesting a more recent host shift. Screening for closely related 16S rRNA gene sequences in public environmental microbiomes also indicates a broader host range. Moreover, exploration of environmental Hydra oligactis populations revealed they might serve as host for a wider spectrum of chlamydial species. This study highlights the evolutionary success of chlamydiae and their genomic toolkit to infect a wide range of hosts and their ecological significance by interacting with diverse organisms.