The archaeal class Nitrososphaeria is a key player of the reproductive microbiome in sponges during gametogenesis

Sponge-associated microbes play fundamental roles in regulating their hosts physiology, yet their contribution to sexual reproduction has been largely overlooked. Most studies have concentrated on the proportion of the microbiome transmitted from parents to offspring, providing little evidence of the putative microbial functions during gametogenesis in sponges. Here, we use 16S rRNA gene analysis to assess whether the microbial composition of five gonochoristic sponge species differs between reproductive and non-reproductive individuals and correlate these changes with their gametogenic stages. In sponges with mature oocytes, reproductive status did not influence either beta or alpha microbial diversity. Interestingly, in two of the studied species, Geodia macandrewii and Petrosia ficiformis, which presented oocytes at the previtellogenic stage, significant microbial composition changes were detected between reproductive and non-reproductive individuals. These disparities were primarily driven by differentially abundant taxa affiliated with the Nitrososphaeria archaeal class in both species. We speculate that the previtellogenic stages are more energetically demanding, leading to microbial changes due to the phagocytosis of microbes to meet nutritional demands during this period. Supporting our hypothesis, we observed significant transcriptomic differences in G. macandrewii, mainly associated with the immune system, indicating potential changes in the sponges recognition system. Overall, we provide the first insights into the possible roles of sponge microbiomes during reproductive periods, potentially uncovering critical interactions that support reproductive success.