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The genomic basis for colonizing the freezing Southern Ocean revealed by Antarctic toothfish and Patagonia robalo genomes.

GigaScience 2019 January 32
The Southern Ocean is the coldest ocean on Earth but a hotspot of evolution. The bottom-dwelling Eocene ancestor of Antarctic notothenioid fishes survived polar marine glaciation and underwent adaptive radiation forming >120 species that fill all water column niches today. Genome-wide changes enabling physiological adaptations and rapid expansion of the Antarctic Notothenioids remain poorly understood. To advance our understanding, we sequenced and compared two notothenioid genomes-the cold-adapted and neutrally buoyant Antarctic toothfish Dissostichus mawsoni, and the basal Patagonian robalo (also known as the Patagonian blenny) Eleginops maclovinus representing the temperate ancestor. We detected >200 protein gene families that had expanded and thousands of genes that had evolved faster in the toothfish, with diverse cold-relevant functions including stress response, lipid metabolism, protein homeostasis and freeze resistance. Besides AFGP, an eggshell protein had functionally diversified to aid in cellular freezing resistance. Genomic and transcriptomic comparisons revealed proliferation of Selcys-tRNA genes and broad transcriptional upregulation across anti-oxidative selenoproteins, signifying their prominent role in mitigating oxidative stress in the oxygen-rich Southern Ocean. We found expansion of transposable elements, temporally correlated to Antarctic notothenioid diversification. Additionally, the toothfish exhibited remarkable shifts in genetic programs towards enhanced fat cell differentiation and lipid storage, and promotion of chondrogenesis while inhibiting osteogenesis in bone development, collectively contributing to achieving neutral buoyancy and pelagicism. Our study revealed a comprehensive landscape of evolutionary changes essential for Antarctic notothenioid cold adaptation and ecological expansion. The two genomes are valuable resources for further exploration of mechanisms underlying the spectacular notothenioid radiation in the coldest marine environment.

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