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

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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. Video Abstract.

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