Single-cell transcriptomic analyses reveal the cellular and genetic basis of aquatic locomotion in scyphozoan jellyfish

Scyphozoan jellyfish (Cnidaria, Medusozoa) exhibit a unique metagenesis from the sessile polyp stage to the motile medusa stage, representing one of the earliest known animal taxa to develop the primitive striated muscle and central nervous system. The emergence of a predominant medusa in scyphozoans is an evolutionary innovation in neuromuscular control of aquatic locomotion (swimming). However, the molecular and cellular process of the transition from sessile to motile remain unclear. Here, we present a comprehensive multi-stage cell atlas for 74,944 cells that cover all six typical life stages, namely, planula, polyp, early strobila, advanced strobila, ephyra, and medusa, in the scyphozoan jellyfish Aurelia coerulea. We uncovered seven broad cell groups and discovered previously unrecognised cell types in scyphozoans and characterised the cellular and genetic basis of neuromuscular development during successive strobilation. Notably, we identified key functional cell types, including striated muscle and mechanosensory cells, which control swimming in scyphozoan medusa. Moreover, numerous transcriptional regulatory factors (including KLF8, OTX2 and SOX4) involved in neuromuscular genesis were revealed. Overall, our study provides the first cell atlas in true jellyfish spanning typical life cycle stages and new insights into the cellular and genetic basis of aquatic locomotion. Our study may facilitate future understanding of the biological characteristics of jellyfish blooms linked to global climate change and human activities.