Microbiome transmission through the ontogeny of the marine sponge Crambe crambe

Abstract

Abstract Background Poriferans (sponges) are highly adaptable organisms that can thrive in diverse marine and freshwater environments due, in part, to their close associations with microbial communities. This sponge microbiome can be acquired from the surrounding environment (horizontal acquisition) or transferred to offspring during the reproductive process through a variety of mechanisms (vertical transfer), typically resulting in the presence of symbiotic microbes throughout all stages of sponge development. How and to what extent the different components of the microbiome are transferred to the developmental stages remain poorly understood. Here, we assess the microbiome composition of a common, low-microbial-abundance, Atlantic-Mediterranean sponge, Crambe crambe, along its ontogeny, including adult individuals, brooded larvae, lecithotrophic free-swimming larvae, newly settled juveniles still lacking osculum, and juveniles with a functional osculum for filter feeding. Results Using 16S rRNA gene analysis, we detected distinct microbiome compositions in each ontogenetic stage, with variations in the presence, relative abundances and diversity of microbial species. However, one particular dominant symbiont from the Gammaproteobacteria class was consistently present throughout all stages, suggesting its vertical transmission from parents to offspring. This symbiont fluctuated in relative abundance across developmental stages, with pronounced prevalence in lecithotrophic stages, constituting over 70% of the microbiome. A significant shift in microbial composition occurred as juveniles developed filter-feeding capacity, coinciding with osculum formation, marking the restoration of the adult microbiome. Microbial diversity peaked during filter-feeding stages, contrasting with lower diversity during lecithotrophic stages before filter feeding initiation. Furthermore, individual specific transmission patterns were detected, with greater similarity between larvae and their respective parents compared to conspecific parents. Conclusions These findings highlight the vertical transmission of a dominant symbiont, possibly playing a metabolic role during non-filtering developmental stages of C. crambe. The increased microbiome diversity during filter-feeding stages likely reflects enhanced interaction with environmental microbes, promoting horizontal transmission. Conversely, lower microbiome diversity in lecithotrophic stages, prior to filter feeding, suggests incomplete symbiont transfer or potential symbiont digestion. This research provides novel information on the dynamics of the microbiome during sponge development, on the symbiont acquisition strategies at each developmental stage, and on the potential importance of symbionts during larval development.