Composition of Bacterial Communities Associated with Aurelia aurita Changes with Compartment, Life Stage, and Population

Abstract

The scyphozoan Aurelia aurita is recognized as a key player in marine ecosystems and a driver of ecosystem change. It is thus intensely studied to address ecological questions, although its associations with microorganisms remain so far undescribed. In the present study, the microbiota associated with A. aurita was visualized with fluorescence in situ hybridization (FISH) analysis, and community structure was analyzed with respect to different life stages, compartments, and populations of A. aurita by 16S rRNA gene amplicon sequencing. We demonstrate that the composition of the A. aurita microbiota is generally highly distinct from the composition of communities present in ambient water. Comparison of microbial communities from different developmental stages reveals evidence for life stage-specific community patterns. Significant restructuring of the microbiota during strobilation from benthic polyp to planktonic life stages is present, arguing for a restructuring during the course of metamorphosis. Furthermore, the microbiota present in different compartments of the adult medusa (exumbrella mucus and gastric cavity) display significant differences, indicating body part-specific colonization. A novel Mycoplasma strain was identified in both compartment-specific microbiota and is most likely present inside the epithelium as indicated by FISH analysis of polyps, indicating potential endosymbiosis. Finally, comparison of polyps of different populations kept under the same controlled laboratory conditions in the same ambient water showed population-specific community patterns, most likely due the genetic background of the host. In conclusion, the presented data indicate that the associated microbiota of A. aurita may play important functional roles, e.g., during the life cycle.

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

“…Besides the Simkania ‐like organisms, our metagenomic data revealed the presence of at least three additional major components. Similar to that observed in A. aurita (Weiland‐Bräuer et al ., ), we could detect in one metagenome the presence of a member of the Mollicutes , loosely affiliated to the Mycoplasma genus in sufficient abundance to bin a 74% complete genome. The A. aurita mycoplasma affiliated with a different branch than the C. tuberculata bin based on initial comparison of short sequences (data not shown).…”

“…These findings, together with the high abundance of the Tenacibaculum ‐like bacteria associated to the mesogleal axis of the gastric filaments, could be responsible for the digestion of ingested planktonic copepods and bacteria, which ultimately would be a source of carbon and energy for the jellyfish organs through the connected mesogleal tissues. One striking finding is that the Simkania ‐like and the Tenacibaculum ‐like phylotypes described here were also detected in other marine invertebrates as corals, gorgonian and sponges of the Mediterranean (Rubio‐Portillo et al ., unpublished), as well as in a recent survey of 'global sponge microbiome' (Thomas et al ., ) that together, with the presence of mycoplasmas and spiroplasmas in other jellyfishes (Daniels and Breitbart, ; Vega‐Orellana, ; Weiland‐Bräuer et al ., ), molluscs (Duperron et al ., ) corals (Kimes et al ., ), point to a common 'metamicrobiome' of some marine invertebrates.…”

Niche-Specific Impact of a Symbiotic Function on the Persistence of Microbial Symbionts within a Natural Host

“…For instance, when microbial communities isolated from diverse habitats are transplanted into gnotobiotic mice, the resulting composition closely resembles that normally found in the mouse cecum (5). Body part-specific microbiota have also been observed in nonmammalian systems, such as that of the jellyfish Aurelia aurita, which shows significant differences in microbial composition between the gastric cavity and exumbrellar mucus (6). These studies suggest that hosts select certain biogeographical landscapes for their associated microbiota.…”

“…For instance, polyps of the freshwater cnidarian Hydra initially assemble a microbial consortium of high diversity that becomes attenuated over time as the animals mature (32). Analysis of compositions at different life stages of the moonlight jelly fish Aurelia aurita revealed stage-specific microbiota (6). The microbiota of the asexual polyp stage differed significantly from the microbiota seen in the subsequent development stages that led to the formation of individuals in the free-living, sexual medusa stage.…”

Functions of the Microbiota for the Physiology of Animal Metaorganisms

“…This process is regarded as a respiratory carbon sink for the food web, but it may also function to maintain a host-specific microbial community. Indeed, jellyfish harbor a species-specific microbial community that changes with developmental transitions [62]. Also in basal marine metazoans, bacteria control major developmental transitions, for example settlement and metamorphosis in jellyfish [63] or settlement in corals via secreted tetrabromopyrroles by Pseudoalteromonas strains [64].…”