Cotylorhiza tuberculata is an important scyphozoan
jellyfish producing population blooms in the Mediterranean
probably due to pelagic ecosystem’s decay.
Its gastric cavity can serve as a simple model of
microbial–animal digestive associations, yet poorly
characterized. Using state-of-the-art metagenomic
population binning and catalyzed reporter deposition
fluorescence in situ hybridization (CARD-FISH), we
show that only four novel clonal phylotypes were
consistently associated with multiple jellyfish adults.
Two affiliated close to Spiroplasma and Mycoplasma
genera, one to chlamydial ‘Candidatus Syngnamydia’,
and one to bacteroidetal Tenacibaculum, and
were at least one order of magnitude more abundant
than any other bacteria detected. Metabolic modelling
predicted an aerobic heterotrophic lifestyle for the
chlamydia, which were found intracellularly in
Onychodromopsis-like ciliates. The Spiroplasma-like
organism was predicted to be an anaerobic fermenter
associated to some jellyfish cells, whereas the
Tenacibaculum-like as free-living aerobic heterotroph,
densely colonizing the mesogleal axis inside
the gastric filaments. The association between the
jellyfish and its reduced microbiome was close and
temporally stable, and possibly related to food digestion
and protection from pathogens. Based on the
genomic and microscopic data, we propose three
candidate taxa: ‘Candidatus Syngnamydia medusae’,
‘Candidatus Medusoplasma mediterranei’ and ‘Candidatus
Tenacibaculum medusae’.