Adaptations to the deep-sea alongside presence of a mega-array of homeobox genes in the genome of the cnidarian Actinernus

Members of the phylum Cnidaria include sea anemones, corals, and jellyfishes, and have successfully colonised both marine and freshwater habitats throughout the world. Understanding of how cnidarians adapt to extreme environments such as the dark, high-pressure deep-sea habitat has been hindered by the lack of genomic information. Here we report the first chromosome-level deep-sea cnidarian genome, of the anemone Actinernus. Analyses of homeobox genes revealed the longest chromosome hosts a mega-array of Hox cluster, HoxL, ParaHox, NK cluster, and NKL homeobox genes; until now, such an array has only been hypothesized to have existed in ancient ancestral genomes. Analysis of microRNAs revealed cnidarian-specific complements that are distinctive for nested clades of these animals, presumably reflecting the progressive evolution of the gene regulatory networks in which they are embedded. Compared to other sea anemones, circadian rhythm genes were lost in Actinernus, which likely reflects adaptation to living in the dark. This high-quality genome of a deep-sea cnidarian deepens our understanding of the evolution of genome content and organization of animals in general and cnidarians in particular and reveals some of the molecular adaptations of this ecologically important group of metazoans to the extreme deep-sea environment.