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

Abstract

Background The Southern Ocean is the coldest ocean on Earth but a hot spot 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 the rapid expansion of the Antarctic notothenioids remain poorly understood. Results We sequenced and compared 2 notothenioid genomes—the cold-adapted and neutrally buoyant Antarctic toothfish Dissostichus mawsoni and the basal Patagonian robalo 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 antifreeze glycoprotein, an eggshell protein had functionally diversified to aid in cellular freezing resistance. Genomic and transcriptomic comparisons revealed proliferation of selcys–transfer RNA 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 the achievement of neutral buoyancy and pelagicism. Conclusions Our study revealed a comprehensive landscape of evolutionary changes essential for Antarctic notothenioid cold adaptation and ecological expansion. The 2 genomes are valuable resources for further exploration of mechanisms underlying the spectacular notothenioid radiation in the coldest marine environment.

De novo Assembly and Characterization of Patagonian Toothfish Transcriptome and Develop of EST-SSR Markers for Population Genetics

“…Generally the frequency of SSRs with different motifs and sizes are not distributed homogeneously in metazoans. Preceding studies have showed that dinucleotides, followed by trinucleotides, are the most frequent EST-SSR types in teleost, including members of the family Nototheniidae and that dinucleotides motif AC/GT is the one the most frequent motif (Chistiakov et al, 2006;Papetti et al, 2016;Chen et al, 2019). Our results confirm these findings, revealing that of the total of EST-SSR type discovered, 53.67% corresponded to dinucleotides and that within and that the SSR repeat motif AC/GT was the more representative (77.46%).…”

Not Frozen in the Ice: Large and Dynamic Rearrangements in the Mitochondrial Genomes of the Antarctic Fish

“…These include the ability to synthesize antifreeze glycoproteins (AFGP) and antifreeze-potentiating proteins (AFPP) (for a review see Duman 2015 ). The ecological hallmark of the notothenioid’s radiation is an evolutionary adaptation of morphology and physiology for life in the water column ( Eastman 2005 ), sometimes referred to as pelagization, and is enabled by a combination of lack of swim bladder, lipid deposition, and reduced skeletal mineralization that allows reductions in density and alterations in buoyancy ( Eastman 2005 ; Chen et al 2019 ). Pelagization is most strongly evident in the species of the subfamilies Pleuragramminae and Dissostichinae, all of which show adaptations towards neutral buoyancy ( Eastman and DeVries 1989 ; Eastman 1993 ; Near et al 2003 , 2007 ).…”

“…The ecological diversification of Antarctic notothenioids and the selective pressure of the cold have also elicited remarkable changes in the structure and gene content of cryonotothenioid nuclear genomes. These modifications range from extensive cold-specific gene duplications and functional diversification (e.g., the AFGP family and duplicated Zona Pellucida [ZP] genes to aid in cellular freezing resistance), to the expansion of transposable elements and high frequency of nuclear chromosomal rearrangements ( Pisano and Ozouf-Costaz 2000 ; Chen et al 2008 , 2019 ; Coppe et al 2013 ; Cao et al 2016 ; Bargelloni et al 2019 ; Auvinet et al 2020 ).…”

Chromosomal assembly of the Antarctic toothfish (<i>Dissostichus mawsoni</i>) genome using third-generation DNA sequencing and Hi-C technology

“…Recently, de novo assembly of the Antarctic toothfish genome and extensive transcriptomic characterization using short-read Illumina data have been reported ( Chen et al, 2019 ), though the genome was fragmented into many scaffolds due to sequencing by synthesis technology. The development of third-generation single-molecule sequencing technology has enabled the production of long-read sequences and the discovery of the features of previously unavailable DNA regions.…”

“…A draft D. mawsoni genome was previously generated using Illumina short-read sequencing ( Chen et al, 2019 ). However, since several gaps prevailed in the draft genome set and there was no information about the linkage group, it was difficult to compare the structure of the Antarctic toothfish genome at the chromosomal scale.…”