For the past 10–15 million years, the Southern ocean has experienced sub-freezing temperatures. The fishes of the Southern ocean are dominated by a single suborder, the notothenioids, which evolved to survive at–1.86°C. The extreme cold that these fish endure has driven a number of unique adaptations such as the production of antifreeze proteins, the constitutive expression of inducible heat shock proteins, and the loss of hemoproteins in some cases. However, our current knowledge of the cold-adapted phenotype and the genomic alterations that support it has remained limited by a lack of genomic-scale information. In their recent paper in PNAS,Zuozhou Chen and colleagues from the Chinese Academy of Sciences and the University of Illinois explore, for the first time, the genomics of cold adaptation in this amazing group of fish.

The team generated a library of 33,560 DNA sequences based on genes that are expressed in brain, liver, ovary and head kidney of the Antarctic toothfish Dissostichus mawsoni. They eventually distilled the library down to 13,000 unique sequences, of which 6208 appear to encode known or predicted proteins that can be classified into 3114 non-redundant gene families. Many of the most abundant transcripts identified in these tissues are involved in mediating the cellular stress response or have previously been identified as important for surviving cold stress. These results suggest a shift in the transcriptome of Antarctic fish towards an elevated and sustained stress response under normal living conditions. By comparing the gene frequencies in the D. mawsoni DNA libraries with those available for five different species of tropical or temperate fish, the authors were able to identify 189 gene families that are differentially expressed in D. mawsoni compared with the other species of fish including families involved in protein homeostasis and scavenging of reactive oxygen species,which are critical for cold adaptation.

The team also explored the genomes of three species of Antarctic fish(D. mawsoni, Pagothenia borchgrevinki and Chaenocephalus aceratus) for alterations that may explain the observed changes in the transcriptomes. The team compared the genomes of the three Antarctic species with those of two closely related fish from non-Antarctic waters(Bovichtus variegatus or Eleginops maclovinus). They discovered 118 duplicated or newly acquired genes and only 12 genes that appear to have contracted in the Antarctic species compared with the related temperate species. Most of the duplicated genes have a known function in other organisms, which suggests an augmentation of existing gene function as a major part of the process of adaption to sub-freezing temperatures. Of particular interest are the 17 duplication events of the long interspersed nuclear element (LINE) genes, which facilitate the rearrangement of eukaryotic genomes through retrotransposition events. The authors speculate that this may help to explain the observed expansion of the genome in the notothenioid lineage.

This paper reveals the genomic changes that may underlie adaptation to sub-freezing temperatures in the Antarctic notothenioid fish. In general, an upregulation in gene expression and concomitant genome expansions of a rather modest number of gene families appear to be an important part of cold adaptation, and are consistent with known principles of metabolic compensation in response to cold acclimation. While this study certainly raises more questions than it answers, it does provide a framework for future investigations of cold adaptation in vertebrates.

Chen, Z., Cheng, C.-H. C., Zhang, J., Cao, L., Chen, L., Zhou,L., Jin, Y., Ye, H., Deng, C., Dai, Z., Xu, Q., Hu, P., Sun, S. and Shen,Y. (
). Transcriptomic and genomic evolution under constant cold in Antarctic notothenioid fish.