Genomic diversity and biosynthetic capabilities of sponge-associated chlamydiae

Sponge microbiomes contribute to host health, nutrition, and defense through the production of secondary metabolites. Chlamydiae, a phylum of obligate intracellular bacteria ranging from animal pathogens to endosymbionts of microbial eukaryotes, are frequently found associated with sponges. However, sponge-associated chlamydial diversity has not yet been investigated at the genomic level and host interactions thus far remain unexplored. Here, we sequenced the microbiomes of three sponge species and found high, though variable, Chlamydiae relative abundances of up to 18.7% of bacteria. Using genome-resolved metagenomics 18 high-quality sponge-associated chlamydial genomes were reconstructed, covering four chlamydial families. Among these, Candidatus Sororchlamydiaceae shares a common ancestor with Chlamydiaceae animal pathogens, suggesting long-term co-evolution with animals. Based on gene content, sponge-associated chlamydiae resemble members from the same family more than sponge-associated chlamydiae of other families, and have greater metabolic versatility than known chlamydial animal pathogens. Sponge-associated chlamydiae are also enriched in genes for degrading diverse compounds found in sponges. Unexpectedly, we identified widespread genetic potential for secondary metabolite biosynthesis across Chlamydiae, which may represent an unexplored source of novel natural products. This finding suggests that Chlamydiae members may partake in defensive symbioses and that secondary metabolites play a wider role in mediating intracellular interactions. Furthermore, sponge-associated chlamydiae relatives were found in other marine invertebrates, pointing towards wider impacts of the Chlamydiae phylum on marine ecosystems.

Automated summary

Sponge microbiomes contribute to host health, nutrition, and defense through the production of secondary metabolites. This study investigated the genomic diversity of sponge-associated Chlamydiae, revealing potential long-term co-evolution with animals and greater metabolic versatility compared to known chlamydial animal pathogens. Sponge-associated chlamydiae were found to have genes for degrading compounds found in sponges and potential for secondary metabolite biosynthesis, suggesting their involvement in defensive symbioses and expanding the role of secondary metabolites in intracellular interactions. Additionally, sponge-associated chlamydiae relatives were found in other marine invertebrates, indicating broader impacts of the Chlamydiae phylum on marine ecosystems.