Summary
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’.