Chromosome-level genome assembly of a deep-sea Venus flytrap sea anemone sheds light upon adaptations to an extremely oligotrophic environment.

The Venus flytrap sea anemone Actinoscyphia liui inhabits the nutrient-limited deep ocean in the tropical western Pacific. Compared with most other sea anemones, it has undergone a distinct modification of body shape similar to that of the botanic flytrap. However, the molecular mechanism by which such a peculiar sea anemone adapts to a deep-sea oligotrophic environment is unknown. Here, we report the chromosomal-level genome of A. liui constructed from PacBio and Hi-C data. The assembled genome is 522 Mb in size and exhibits a continuous scaffold N50 of 58.4 Mb. Different from most other sea anemones, which typically possess 14-18 chromosomes per haplotype, A. liui has only 11. The reduced number of chromosomes is associated with chromosome fusion, which likely represents an adaptive strategy to economize energy in oligotrophic deep-sea environments. Comparative analysis with other deep-sea sea anemones revealed adaptive evolution in genes related to cellular autophagy (TMBIM6, SESN1, SCOCB and RPTOR) and mitochondrial energy metabolism (MDH1B and KAD2), which may aid in A. liui coping with severe food scarcity. Meanwhile, the genome has undergone at least two rounds of expansion in gene families associated with fast synaptic transmission, facilitating rapid responses to water currents and prey. Positive selection was detected on putative phosphorylation sites of muscle contraction-related proteins, possibly further improving feeding efficiency. Overall, the present study provides insights into the molecular adaptation to deep-sea oligotrophic environments and sheds light upon potential effects of a novel morphology on the evolution of Cnidaria.