A multinational team of researchers has successfully sequenced the genome of the Antarctic blackfin icefish (Chaenocephalus aceratus), opening a genetic window on fish that evolved over the last 77 million years to survive in extreme Antarctic temperatures.
The Antarctic blackfin icefish (Chaenocephalus aceratus). Image credit: Thomas Desvignes.
Antarctic icefishes are members of the family Channichthyidae.
These ‘white blooded’ creatures inhabit the Earth’s coldest marine environment and are the only vertebrates that lack functional red blood cells and functional hemoglobin genes.
Icefish blood carries oxygen solely in physical solution, resulting in an oxygen-carrying capacity per unit of blood volume of less than 10% of that in closely related red-blooded Antarctic notothenioid fishes.
The blackfin icefish, along with 5 other species among the 16 recognized species of icefishes, also lack oxygen-binding proteins called myoglobins.
Icefishes evolved mechanisms that appear to compensate for loss of these oxygen-binding proteins, including enormous hearts with increased stroke volume relative to body size, enhanced vascular systems, and changes in mitochondrial density and morphology.
“In a human, such traits would normally signal disease. These adaptations, however, help the fish survive,” said University of Oregon’s Professor John Postlethwait, co-lead author of the study.
“The icefishes are examples of what Charles Darwin called the ‘wrecks of ancient life.’ They diverged from the ancestors of stickleback, losing many of the features common to their ancestral forms as they evolved. Among genes that disappeared amid the months of night and months of sunlight in the polar region were those tied to circadian rhythms.”
“Ice fish populations first appeared at the end of the Pliocene after Antarctica’s surface temperatures dropped by 2.5 degrees Celsius. About 77 million years ago, they had diverged from the line of their common ancestors with the stickleback — and then developed phenotypes that were better adapted to the cold,” said co-author Professor Manfred Schartl, a researcher at the Julius Maximilians University of Würzburg and Texas A&M University.
To help investigate the genomic basis for these extreme evolutionary adaptations, Professor Postlethwait, Professor Schartl and their colleagues sequenced the genome of the blackfin icefish.
They collected blackfin icefish, which average about 12 inches (30.5 cm) in length, from various depths near King Sejong Station and the Western Bransfield Strait along the Antarctic Peninsula.
Along with genomic DNA taken from the female, RNA was extracted from 12 tissues — brain, eye, gill, heart, intestine, kidney, liver, muscle, ovary, skin, spleen and stomach — to help understand what genes each organ uses.
The scientists mapped 30,773 protein-coding genes and how they localize along chromosomes.
“Icefish and other notothenioid fishes experienced gene changes that produced antifreeze proteins to help them survive — an adaptation discovered in the 1970s. The completed mapping helps place this discovery into a genomic context,” they said.
The genome assembly and linkage map reveal remarkable stability of contents of the 24 chromosomes among bony fish, including medaka (Japanese rice fish), European sea bass and blackfin icefish spanning 110 million years, especially when compared with chromosome changes in mammals over the same time period.
The biggest divergence involved the genes of icefish and sea bass, suggesting changes in the cold.
“Our results show that the number of genes involved in the protection against ice damage, including the genes coding for anti-freeze glycoproteins, is strongly expanded in the icefish genome,” Professor Schartl said.
“Icefish evolved from fish that lived on the bottom and had no swim bladder, an organ that develops like our lungs but then loses the attachment to the pharynx and fills with gas. Most fish, except for bottom feeders, have one and it helps them maintain position in the water column,” Professor Postlethwait said.
“When most fish species became extinct around Antarctica as the waters cooled, icefishes evolved to occupy the Southern Ocean water column. One of the biggest challenges they faced was getting off the bottom without a swim bladder.”
“They likely limited the mineralization of their bones, the most dense part of our bodies, and accumulated lipids, which are lighter than water — think of olive oil that floats on the top of the water in a pan about to cook spaghetti.”
The results appear in the journal Nature Ecology & Evolution.
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Bo-Mi Kim et al. 2019. Antarctic blackfin icefish genome reveals adaptations to extreme environments. Nature Ecology & Evolution 3: 469-478; doi: 10.1038/s41559-019-0812-7
