Antarctica is almost the last place on Earth that you would expect to be teaming with life. Survival below zero should be impossible, especially for ectothermic creatures that depend on their environment for warmth. But for the enterprising icefishes, Antarctica represented bountiful evolutionary and ecological opportunities. The icefish lineage dominates the modern Southern Ocean and its members famously sport colourless blood, huge hearts and ample mitochondria, the cell's power packs. Charmed by these unusual fish, a multinational team led by H. William Detrich III of Northeastern University, USA, John H. Postlethwait of the University of Oregon, USA, and Hyun Park from the Korea Polar Research Institute and the University of Science and Technology, Korea, investigated the genetic building blocks of extreme evolutionary adaptation in icefish.
A single adult Chaenocephalus aceratus, angled from the Antarctic Peninsula, provided the raw genetic material to sequence 30,773 protein-coding genes. When comparing the new genome with those of other bony fish, the researchers found 373 gene families that were larger than expected, and 346 gene families that looked too small, revealing icefish-specific genetic quirks. Nearly 40% of these quirks appeared within the last 7 million years, coinciding with plummeting temperatures and rising oxygen levels in the ocean surrounding Antarctica. How did these 719 gene families relate to adaptation to the world's coldest marine environment?
Antifreeze glycoproteins prevent ice crystals from expanding and tearing tissues. Unsurprisingly, icefish have a respectable 23 genes for antifreeze glycoproteins and their evolutionary precursors, trypsinogen and trypsinogen-like proteases. Yet strangely, icefish embryos do not express antifreeze glycoproteins, raising the question of how these animals develop at sub-zero temperatures. The authors hypothesized that embryos rely on other glycoproteins, such as those in the zona pellucida layer around their eggs, to fulfil the antifreeze role; and the genome supported their hunch. Icefish have 131 zona pellucida genes, far more than the 16 to 35 genes found in other fishes.
Another piece of the icefish adaptation puzzle is their huge stock of mitochondria and polyunsaturated fats in their muscles, to counteract the effects of cold on the fish's metabolism and biological membranes. Mitochondria naturally produce small amounts of toxic molecules that can damage DNA, fats and other cell components. The high mitochondria and polyunsaturated fat content of icefish tissues makes them extra sensitive to oxidative stress, and this shows in their genes. Icefish expanded the gene families that prevent oxidative damage, including antioxidant proteins superoxide dismutase (icefish have three extra copies) and NAD(P)H-quinone dehydrogenase (there are 33 copies in icefish, compared with between 2 and 10 in other fish). Icefish are also the only vertebrates to double up on their 8-oxoguanine DNA glycosylase gene, which produces a protein that removes damaged pieces of DNA.
Beyond the challenges of living in the cold, making their homes so far south means icefish experience the summer ‘midnight sun’ and prolonged winter darkness. Day length guides the rhythm and expression of hundreds of genes through the circadian clock pathways. How do icefish keep time when the sun is so unreliable? Their genome suggests that they simply don't bother. The icefish genome is missing many (though not all) of the time-keeping ‘period’ and cryptochrome genes found in other fish. Apparently, such extreme fluctuations in day length made light-dependent timekeeping less useful and the genes disappeared from the genome.
Somehow, 10 to 14 million years ago, life found a way. Although we have known about the peculiarities of icefish since the earliest expeditions to the remote continent, we are just starting to understand the complex genetic machinery underlying their physiology. With over 30,000 genes to mine for interesting patterns, this new high-quality genome is only the tip of the iceberg in our understanding of adaptation to extreme environments.
