Phagocytosis of microbial symbionts supports embryonic nutrition in the sponge Halichondria panicea

Abstract Animals associate with microbial symbionts that play crucial roles in their nutrition and development, yet their function during gametogenesis and embryogenesis remains poorly understood. Here, we investigate host–symbiont dynamics throughout the reproductive cycle of the marine sponge Halichondria panicea. Specimens were collected monthly from February to July and classified by reproductive stage through microscopic analysis. We combined ultrastructural imaging, host and symbiont transcriptomics (“dual RNASeq”), 16S rRNA amplicon sequencing, and quantitative PCR to characterize changes between reproductive stages for each month. Our results revealed transcriptomic and microbial community shifts throughout the reproductive period, being particularly relevant during early embryogenesis in May. Ultrastructural observations showed nurse cells phagocytosing bacterial aggregations near late oocytes, presumably converting them into yolk precursors. These findings coincided with a significant decline in the abundance of the obligate symbiont Candidatus Halichondribacter symbioticus. We further revealed the upregulation of phagocytic and immune pathways, including pattern recognition receptors, lectins, and vesicle trafficking genes, specifically in females undergoing embryogenesis in May. Simultaneously, microbial gene expression profiles displayed significant shifts, including responses to acidic pH, consistent with adaptation to phagosome environments. Together, these results suggest that H. panicea digests its symbiotic community during early embryogenesis, presumably to meet the increased nutritional demands. These findings expand our understanding of how symbionts may impact early animal development.