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. 2019 Mar;3(3):469-478.
doi: 10.1038/s41559-019-0812-7. Epub 2019 Feb 25.

Antarctic blackfin icefish genome reveals adaptations to extreme environments

Bo-Mi Kim  1 , Angel Amores  2 , Seunghyun Kang  1 , Do-Hwan Ahn  1 , Jin-Hyoung Kim  1 , Il-Chan Kim  3 , Jun Hyuck Lee  1   4 , Sung Gu Lee  1   4 , Hyoungseok Lee  1   4 , Jungeun Lee  1   4 , Han-Woo Kim  1   4 , Thomas Desvignes  2 , Peter Batzel  2 , Jason Sydes  2 , Tom Titus  2 , Catherine A Wilson  2 , Julian M Catchen  5 , Wesley C Warren  6 , Manfred Schartl  7   8   9 , H William Detrich 3rd  10 , John H Postlethwait  11 , Hyun Park  12   13
Affiliations

Antarctic blackfin icefish genome reveals adaptations to extreme environments

Bo-Mi Kim et al. Nat Ecol Evol. 2019 Mar.

Abstract

Icefishes (suborder Notothenioidei; family Channichthyidae) are the only vertebrates that lack functional haemoglobin genes and red blood cells. Here, we report a high-quality genome assembly and linkage map for the Antarctic blackfin icefish Chaenocephalus aceratus, highlighting evolved genomic features for its unique physiology. Phylogenomic analysis revealed that Antarctic fish of the teleost suborder Notothenioidei, including icefishes, diverged from the stickleback lineage about 77 million years ago and subsequently evolved cold-adapted phenotypes as the Southern Ocean cooled to sub-zero temperatures. Our results show that genes involved in protection from ice damage, including genes encoding antifreeze glycoprotein and zona pellucida proteins, are highly expanded in the icefish genome. Furthermore, genes that encode enzymes that help to control cellular redox state, including members of the sod3 and nqo1 gene families, are expanded, probably as evolutionary adaptations to the relatively high concentration of oxygen dissolved in cold Antarctic waters. In contrast, some crucial regulators of circadian homeostasis (cry and per genes) are absent from the icefish genome, suggesting compromised control of biological rhythms in the polar light environment. The availability of the icefish genome sequence will accelerate our understanding of adaptation to extreme Antarctic environments.

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Figures

Fig. 1 |
Fig. 1 |. Chromosome stability of blackfin icefish with respect to teleost outgroups.
a, Gene content in icefish chromosomes supports a one-to-one correspondence between icefish and medaka chromosomes. Each line represents orthologous genes in icefish and medaka, colour-coded by icefish chromosome. The few lines that cross linkage groups (LGs) probably represent paralogues. b, A comparison of orthologous gene orders in icefish LG12 (Cac12) and medaka LG12 (Ola12) illustrates icefish-specific chromosome inversions and transpositions (see text). Each line represents orthologous genes in the icefish and medaka chromosome, colour-coded by icefish genomic scaffold. Conserved syntenic blocks are labelled 1–8. c, Comparison of orthologous gene order in Cac12 and European sea bass LG19 (Dla19). Conserved syntenic blocks are labelled 1–8. d, Comparison of orthologous gene order between sea bass Dla19 and medaka Ola12 reveals that most chromosome rearrangements occurred after the divergence of the icefish lineage from the sea bass lineage. M, megabase position along the chromosome.
Fig. 2 |
Fig. 2 |. Comparative analysis of the C. aceratus genome assembly.
a, Phylogenetic tree and gene family gain-and-loss analysis, including the number of gained gene families (+) and lost gene families (−). Blue numbers specify divergence times between lineages. The red dotted line indicates the appearance of Antarctic ice sheets (35 Ma), which allowed the circum-Antarctic current to form after the opening of the Drake Passage. Subsequent cooling of the Southern Ocean drove local extinction of most fish taxa and adaptive radiation of the Antarctic notothenioid suborder. E, Eocene; M, Miocene; O, Oligocene; P, Palaeocene. b, Inferring icefish population history by PSMC analysis. The left y axis represents the demographic history of C. aceratus (red line). During the Plio-Pleistocene (3–0.9 Ma), which is shaded blue, Antarctic sea-surface temperatures dropped by around 2.5 °C, judged by a proxy for marine palaeo-temperature changes based on oxygen isotope ratios, (right y axis). Concomitant decreases in marine temperatures (black line) probably allowed the cold-adapted C. aceratus populations to increase in size. The green shading represents the mid-Pleistocene transition, during which temperature fluctuations were large. g, generation time; μ, mutation rate.
Fig. 3 |
Fig. 3 |. Conserved syntenies for expanded gene clusters identified in the blackfin icefish genome.
a, AFGP and trypsinogen gene loci. The pink-shaded area indicates the trypsinogen gene locus. kbp, kilobase pair. b, Zona pellucida c5 (zpc5) locus. c, sod3 gene cluster. Genomic neighbourhoods are shown within representative sequenced teleost genomes. Each arrow indicates a complete gene orientated in the (5′ → 3′) direction. d. Phylogenetic analysis of vertebrate sod3 genes. Divergence times were calculated by applying the mutation rate formula μ = D/2t = 3.28 × 10−9. Ca, C. aceratus (icefish); Dr, D. rerio (zebrafish); Ga, G. aculeatus (stickleback); Nc, N. coriiceps (bullhead notothen); Ol, O. latipes (medaka); Pf, P. Formosa (Amazon molly); Tr, T. rubripes (fugu); Xm, X. maculatus (platyfish).
Fig. 4 |
Fig. 4 |. Genomic evidence supporting gene loss events for blackfin icefish circadian rhythm-related genes.
a,b, Genomic structures and syntenic comparisons of the period genes per2a (a) and per3 (b). c,d, Cryptochrome gene clusters for the cry1ab (c) and cry2 (d) are shown within representative sequenced teleost genomes.
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