Genome Evolution in the Cold: Antarctic Icefish Muscle Transcriptome Reveals Selective Duplications Increasing Mitochondrial Function

Abstract

Antarctic notothenioids radiated over millions of years in subzero waters, evolving peculiar features, such as antifreeze glycoproteins and absence of heat shock response. Icefish, family Channichthyidae, also lack oxygen-binding proteins and display extreme modifications, including high mitochondrial densities in aerobic tissues. A genomic expansion accompanying the evolution of these fish was reported, but paucity of genomic information limits the understanding of notothenioid cold adaptation. We reconstructed and annotated the first skeletal muscle transcriptome of the icefish Chionodraco hamatus providing a new resource for icefish genomics (http://compgen.bio.unipd.it/chamatusbase/, last accessed December 12, 2012). We exploited deep sequencing of this energy-dependent tissue to test the hypothesis of selective duplication of genes involved in mitochondrial function. We developed a bioinformatic approach to univocally assign C. hamatus transcripts to orthology groups extracted from phylogenetic trees of five model species. Chionodraco hamatus duplicates were recorded for each orthology group allowing the identification of duplicated genes specific to the icefish lineage. Significantly more duplicates were found in the icefish when transcriptome data were compared with whole-genome data of model species. Indeed, duplicated genes were significantly enriched in proteins with mitochondrial localization, involved in mitochondrial function and biogenesis. In cold conditions and without oxygen-carrying proteins, energy production is challenging. The combination of high mitochondrial densities and the maintenance of duplicated genes involved in mitochondrial biogenesis and aerobic respiration might confer a selective advantage by improving oxygen diffusion and energy supply to aerobic tissues. Our results provide new insights into the genomic basis of icefish cold adaptation.

De Novo Assembly and Analysis of the Testes Transcriptome from the Menhaden, Bervoortia tyrannus

“…By merging the Blast2GO annotations with the InterProScan results, 70,919 contigs out of 254,446 (27.87%) were assigned at least one GO term (Table 3). These results are comparable to other annotation efforts in non-model fish studies that utilized the de novo assembly approach [9,13,47,50]. Again, it should be taken into consideration that the limited number of publically available fish genomes inhibits the overall successful rate of annotating non-model fish [49].…”

“…Based on a phylogenetic tree analysis with the eleven publically available fish genomes on Ensembl, it was determined that zebrafish along with Mexican tetra were the closest related genera to menhaden. The BLASTX alignments for the menhaden against the zebrafish (42.56%) and Mexican tetra (41.34%) yielded analogous results with other non-model fish de novo transcriptome assembly studies signifying that the assemblies are reliable [9,12,13,47,48]. The low number of hits for both zebrafish and Mexican tetra could be due the presence of menhaden-specific contigs, as menhaden belong to separate clades in the phylogenetic tree ( Figure 2).…”

“…In this study, the percentage of matches for the menhaden was 46.23%. This percentage is comparable to other non-model fish de novo assemblies, further establishing the credibility of the assemblies [9,12,13,47,50]. It should be noted that the number of matches is affected by the amount of available sequence data, and there is a limited number of publically available fish genomes to contribute to the overall success of the annotation [49].…”

“…However, due to the scarcity of cDNA or EST sequences for menhaden, another alignment technique was performed for the validation. In this method, the contigs for the species of interest was aligned to its closest phylogenetic relative with a reference genome utilizing BLASTX [9]. Based on a phylogenetic tree analysis with the eleven publically available fish genomes on Ensembl, it was determined that zebrafish along with Mexican tetra were the closest related genera to menhaden.…”

“…The first is the reduction fishery that turns the menhaden into fish oil omega-3 supplements for example, and into fishmeal for livestock and aquaculture consumption [4,5]. The second is the bait fishery that uses the menhaden as bait for bluefish, crab, and lobster [6][7][8][9][10][11][12][13][14][15]. They have been rarely studied at the genetic level most likely due to the lack of genomic and transcriptome data.…”