Abstract Background Sponge-associated bacteria play important roles in the physiology of their host, whose recruitment processes are crucial to maintain symbiotic associations. However, the acquisition of bacterial communities within freshwater sponges is still under explored. Spongilla lacustris is a model sponge widely distributed in European rivers and lakes, producing dormant cysts (named gemmules) for their asexual reproduction, before winter. Through an in vitro experiment, this study aims to describe the dynamics of bacterial communities and their transmission modes following the hatching of these gemmules. Results An overall change of bacterial β -diversity was observed through the ontology of the juvenile sponges. These temporal differences were potentially linked, first to the osculum acquisition and the development of a canal system, and then, the increasing colonization of the Chlorella -like photosymbionts. Gemmules hatching with a sterilized surface were found to have a more dispersed and less diverse microbiome, revealing the importance of gemmule epibacteria for the whole holobiont stability. These epibacteria were suggested to be vertically transmitted from the maternal tissues to the gemmule surface. Vertical transmission through the incorporation of bacterial communities inside of the gemmule, was also found as a dominant transmission mode, especially with the nitrogen fixers Terasakiellaceae . Finally, we showed that almost no ASVs were shared between the free-living community and the juveniles, suggesting that horizontal recruitment is unlikely to happen during the first stages of development. However, the free-living bacteria filtered are probably used as a source of nutrients, allowing an enrichment of copiotrophic bacteria already present within its microbiome. Conclusions This study brings new insight for a better understanding of the microbiome acquisition during the first stages of freshwater sponge development. We showed the importance of epibacterial communities on gemmules for the whole holobiont stability, and demonstrated the near absence of recruitment of free-living bacteria during the first stages.