Transcriptome atlas of Phascolosoma esculenta tissues: analysis of tissue-specific functions and gametogenesis-related genes

Abstract

Phascolosoma esculenta , a commercially and ecologically significant sipunculan worm, lacks comprehensive molecular data regarding its tissue-specific functions and reproductive mechanisms. In this study, we constructed the first multi-tissue transcriptome atlas of P. esculenta , encompassing the coelomic fluid (male and female), intestine, nephridia, body wall, and retractor muscle. De novo assembly yielded 321,910 transcripts and 148,188 unigenes, with 46,489 differentially expressed genes (DEGs) identified across tissues. Functional enrichment analysis revealed distinct molecular signatures adapted to specific physiological roles. The intestine was enriched in digestion and absorption pathways; the nephridia showed high expression of genes involved in ion transport, detoxification, and osmoregulation; the body wall exhibited enrichment in protease inhibitors and Wnt signaling, suggesting roles in defense and regeneration; and the retractor muscle was dominated by ion channel and calcium signaling pathways. Notably, comparative analysis of the coelomic fluid, the site of gametogenesis in sipunculans, uncovered key molecular drivers of reproduction. Male coelomic fluid was characterized by the upregulation of microtubule motor proteins (kinesins and dyneins), oxidative phosphorylation, and autophagy-related genes, suggesting their potential involvement in spermatid development. Female coelomic fluid showed significant enrichment in ribosome biogenesis, spliceosome, cell cycle, and DNA repair pathways, highlighting mechanisms essential for oocyte growth and genomic integrity. This study provides a valuable genomic resource for Sipuncula and offers novel molecular insights into organ specialization and the potential regulatory mechanisms underlying gametogenesis in marine invertebrates.