The genome of the deep-sea anemone Actinernus sp. contains a mega-array of ANTP-class homeobox genes

Members of the phylum Cnidaria include sea anemones, corals and jellyfish, and have successfully colonized both marine and freshwater habitats throughout the world. The 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 sp., which was 1.39 Gbp in length and contained 44 970 gene models including 14 806 tRNA genes and 30 164 protein-coding genes. Analyses of homeobox genes revealed the longest chromosome hosts a mega-array of Hox cluster, HoxL, NK cluster and NKL homeobox genes; until now, such an array has only been hypothesized to have existed in ancient ancestral genomes. In addition to this striking arrangement of homeobox genes, analyses 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. Also, compared with other sea anemones, circadian rhythm genes were lost in Actinernus sp., which likely reflects adaptation to living in the dark. This high-quality genome of a deep-sea cnidarian thus reveals some of the likely molecular adaptations of this ecologically important group of metazoans to the extreme deep-sea environment. It also deepens our understanding of the evolution of genome content and organization of animals in general and cnidarians in particular, specifically from the viewpoint of key developmental control genes like the homeobox-encoding genes, where we find an array of genes that until now has only been hypothesized to have existed in the ancient ancestor that pre-dated both the cnidarians and bilaterians.

刺胞动物门（Cnidaria）类群涵盖海葵、珊瑚与水母，已成功定殖全球范围内的海洋与淡水生境。由于缺乏基因组学数据，学界对刺胞动物如何适应黑暗、高压的深海极端生境的认知一直受限。本研究报道了首个染色体水平的深海刺胞动物基因组，来自海葵类群Actinernus sp.（未定种），其基因组总长1.39 Gbp，共包含44970个基因模型，其中包括14806个转运RNA（tRNA）基因与30164个蛋白质编码基因。对同源框基因（homeobox genes）的分析显示，最长染色体携带了Hox基因簇、HoxL、NK基因簇与NKL同源框基因的巨型阵列；截至目前，此类阵列仅被假设存在于远古祖先基因组中。除上述同源框基因的独特排布外，微小RNA（microRNAs）分析揭示了刺胞动物特有的基因组分，该组分在这类动物的嵌套演化支中呈现显著差异，这大概率反映了其所在基因调控网络的渐进式演化。此外，与其他海葵相比，Actinernus sp.（未定种）缺失了昼夜节律基因，这很可能反映了其对黑暗生境的适应性演化。因此，这一深海刺胞动物的高质量基因组，揭示了这类生态重要后生动物类群适应极端深海环境的部分潜在分子机制。同时，本研究也加深了学界对动物（尤其是刺胞动物）基因组内容与组织形式演化的认知，特别是从同源框编码基因这类关键发育调控基因的视角：我们发现的基因阵列此前仅被假设存在于刺胞动物与两侧对称动物（bilaterians）分化前的远古共同祖先中。