María Conejero

Background: Animal development is frequently supported by microbial symbionts that contribute to host nutrition, metabolism, and physiology. While the functional importance of microbiomes in adult hosts is increasingly recognized, the role of symbiotic microbes during gametogenesis and embryogenesis remains poorly understood, particularly in early-diverging metazoans. Sponges represent an ideal system to investigate these processes due to their dense and diverse microbial communities. Here, we examined host-symbiont dynamics across the reproductive cycle of the marine sponge Halichondria panicea to assess how microbial communities contribute to reproduction and early development. Results: Specimens were collected monthly from February to July and classified by reproductive stage using histological analyses. We combined ultrastructural imaging, dual RNA sequencing of host and symbionts, 16S rRNA gene amplicon sequencing, and quantitative PCR to characterize microbial and transcriptional dynamics throughout reproduction. Pronounced shifts in both host gene expression and microbial community composition occurred during early embryogenesis, particularly in May. Transmission electron microscopy revealed nurse cells phagocytosing bacterial aggregates in close proximity to late oocytes, presumably converting them into yolk precursors. This coincided with a significant decline in the abundance of the dominant obligate symbiont, Candidatus Halichondribacter symbioticus. Host transcriptomic analyses showed upregulation of immune and phagocytic pathways, including pattern recognition receptors, lectins, and vesicle trafficking components, specifically in females undergoing embryogenesis in May. Concurrently, symbiont gene expression profiles indicated responses to acidic conditions, consistent with exposure to phagosomal environments. Conclusions: Our results are consistent with intracellular digestion of microbial symbionts during early embryogenesis, potentially to supplement the nutritional requirements of embryogenesis. These findings reveal symbiont phagocytosis as a previously underappreciated nutritional strategy during animal development and highlight the dynamic functional integration of microbiomes into reproductive physiology in basal metazoans.

Ribbon worms (Nemertea) are a less-known group of invertebrates, specially challenging for taxonomic studies due to the scarcity of external morphological features. As a consequence, the number of known nemertean species might represent just a small fraction of the true diversity of the phylum. The present study increases the number of known ribbon worm species with the description of the accordion worm Pararosa vigarae sp. nov., a new genus and species of Heternonemertea from the northwest coast of Spain. We performed molecular phylogenetic analyses based on partial sequences of 16S rRNA, 18S rRNA, 28S rRNA, cytochrome c oxidase subunit I ( COI ) and histone H3 gene markers that indicated the newly identified specimens represent a new genus and species of heteronemertean in the family Lineidae. We also provide morphological data and images illustrating its unique behaviour, contracting its body into a series of rings similar to an accordion. Our results increase our knowledge on the diversity of an important but often overlooked invertebrate phylum and emphasize the need to combine morphological and molecular data to discover new ribbon worm species and better evaluate the true diversity of the phylum.

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 sponge’s 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.