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.

Highlights

  • IntroductionIcefishes (suborder Notothenioidei; family Channichthyidae) are the only vertebrates that lack functional haemoglobin genes and red blood cells

  • Icefishes are the only vertebrates that lack functional haemoglobin genes and red blood cells

  • Concluding remarks Here, we report a high-quality genome assembly and linkage map, which together provide a chromonome for the Antarctic blackfin icefish

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Summary

Introduction

Icefishes (suborder Notothenioidei; family Channichthyidae) are the only vertebrates that lack functional haemoglobin genes and red blood cells. Antarctic icefishes inhabit the Earth’s coldest marine environment These remarkable animals are the only vertebrates that lack functional red blood cells and functional haemoglobin genes; they are ‘white blooded’[1,2]. Notothenioids, living in constant cold, evolved a substantially non-conventional heat-shock response[13,14] From these benthic ancestors, eight notothenioid taxa, including the icefishes, evolved to exploit the food-rich water column through increased buoyancy, which was achieved by reducing densely mineralized elements such as bones and scales[15,16,17] and increasing deposits of lipids[18]. To help investigate the genomic basis for these extreme evolutionary adaptations, we sequenced the genome of the blackfin icefish

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