Transcriptomic sequencing reveals dynamic shifts in nutrient utilization and energy metabolism during embryonic and larval development of the purple sea urchin Heliocidaris crassispina

Abstract Background Heliocidaris crassispina is an economically important sea urchin in the Northwest Pacific, yet large-scale aquaculture is constrained by high mortality during early development. This limitation is largely attributable to the poor understanding of gene expression patterns across these critical stages. Therefore, a stage-resolved developmental transcriptomic profile from fertilization to the settled juvenile is needed to clarify the molecular basis of early developmental transitions and to support improved hatchery management and stage-appropriate feeding. Results We described a complete developmental profile of H. crassispina from fertilization to the settled juvenile and established transcriptomes for 14 consecutive developmental stages. Beginning with the two-arm pluteus stage, H. crassispina undergoes rapid growth, paralleling a marked rise in mortality that continues through metamorphosis until the juvenile settles. Based on global gene expression patterns, development was divided into four periods. Period-I spanned the fertilized egg to 32-cell stages, Period-II covered two late-cleavage stages (LC1–LC2), Period-III extended from blastula to two-arm pluteus, and Period-IV extended from the four-arm pluteus to the settled juvenile stages. GO and KEGG analyses indicated a stepwise transition in gene expression programs across developmental periods, consistent with the morphological and physiological changes observed. Weighted gene co-expression network analysis (WGCNA) identified ten modules whose expression profiles correlated significantly with specific developmental periods, indicating development is regulated by a coordinated, module-level transcriptional program. Analysis of digestive enzyme and energy metabolism genes showed that early embryos rely on endogenous reserves, whereas feeding larvae progressively establish exogenous digestive capacity, accompanied by stage-dependent fluctuations and a late-stage rise in glycolysis and TCA cycle gene expression, suggesting a metabolic transition associated with exogenous feeding and settlement. Conclusion This study established transcriptomes for 14 consecutive stages of H. crassispina from fertilization to the settled juvenile and, together with growth and survival, resolved four transcriptomic periods. Functional enrichment and WGCNA indicated coordinated, period-specific programs that track major morphological and physiological transitions. Digestive enzyme and energy metabolism genes showed a clear shift from reliance on endogenous reserves in embryos to the progressive establishment of exogenous digestive capacity in feeding larvae, accompanied by late-stage upregulation of glycolysis and TCA cycle genes around settlement. These insights support stage-specific feeding and hatchery management to reduce mortality.