The low diverse gastric microbiome of the jellyfish Cotylorhiza tuberculata is dominated by four novel taxa

Abstract

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'.

Predominance of deterministic microbial community dynamics in salterns exposed to different light intensities

“…Microbial cell counts were carried out using DAPI, FISH and CARD-FISH methodology. All samples were immediately fixed with formaldehyde and processed for the fluorescence microscope counts as previously reported (Viver et al, 2017). Additional details on the experiments' methods are described in Supplementary Materials and Methods.…”

The defensive Spiroplasma

“…Spiroplasma are broadly distributed among invertebrate hosts, often crustaceans, spiders, and insects; they are estimated to occur in about 7% of all terrestrial arthropods 6 . Interestingly, highly divergent Spiroplasma strains have recently been found associated with marine and deep-sea invertebrates, including jellyfish and sea cucumbers, and the biology of these lineages is essentially unknown 7,8 . Spiroplasma exhibits great variation in transmission mode, tissue tropism, and fitness effects, ranging from gut commensals, to insect-vectored plant pathogens, to symbionts that are highly efficiently maternally transmitted.…”

Bacteria associated with jellyfish during bloom and post-bloom periods

“…As a niche, the jellyfish ‘gut’ could somehow impose strict requirements of bacteria to survive. Studies on Cotylorhiza tuberculata showed possible intracellular symbiotic bacteria within organs of the gastral cavity (gastric filaments), with possible involvement in the digestion process [26]. The dominance of Betaproteobacteria in medusa gastral cavity detected within our study is somehow surprising, since they are more characteristic for organic aggregates in limnetic ecosystems [89].…”

“…Most of the bacteria were suggested to have an intracellular lifestyle and established a cooperative relationship with their host. In addition, a new candidate bacterial taxa were proposed [23,26].…”