Asexual reproduction of Aurelia aurita depends on the presence of a balanced microbiome at polyp stage

Abstract The Cnidarian Aurelia aurita undergoes a complex life cycle alternating between the benthic polyp to the pelagic medusa. In absence of its natural microbiome, the asexual reproduction of this jellyfish is severely comprised, with limited strobilation and ephyrae release, whereas the recolonization of sterile polyps can restore this defect. Yet, the timing and molecular consequences of the microbiome during the strobilation process had not been investigated. Here, we demonstrate that a microbiota must be present at the polyp stage, before strobilation is initiated, to ensure normal asexual reproduction and a successful polyp-to-jellyfish transition. Addition of a microbiota at later stages of sterile animals failed to restore the defected process. Absence of a microbiome was accompanied with reduced transcription of developmental and strobilation genes. The transcription of strobilation genes was exclusively observed for native and recolonized polyps, pointing to the microbiome's impact on the strobilation process at the molecular level. Moreover, direct cell contact between the host and the bacteria was required for the generation of normal offspring. Overall, this study demonstrates that the timing of the host-microbe interaction in this developmental animal model is crucial, with the microbial impact being essential at the polyp stage, to ensure normal polyp-to-jellyfish transition.