Transcriptomic adaptations of Cryonotothenioidea to the antarctic environment and response to heat stress

Antarctic fishes adopted a wide set of adaptations that allow them to thrive in the extreme antarctic environment. For example due to the high solubility of gases in cold waters some Channichthydae such as Chionodraco hamatus have completely lost hemoglobin and gasses are simply dissolved in their colorless blood. Although other adaptations, such as an increased activity of carbonic anhydrase activity in gills, have been previously described from a biochemical point of view, these have not been investigated from a genomic perspective. Here we explore cold adaptations of Cryonotothenioidea at a transcriptomic level in a multi-species comparison. Moreover we investigate the transcriptomic response of Trematomus bernacchii to a slight heat stress. Whole transcriptome sequencing data from 14 fish species were collected from NCBI or generated de novo. A bioinformatic approach based on gene expression anlalysis was used to identify peculiar transcriptomic features of antarctic species compared with species living in temperate environments, and to assess the response of Trematomus bernacchii to a +1.5°C environmental heat stress in 3 different tissues (brain, gill, muscle) of a 6H, 7D and 20D duration. We identified 130 upregulated genes in the gills of Cryonotothenioidea, including two carbonic anhydrases displaying high gill-specificity. Moreover molecular signatures of cobalamin deficiency, which could be linked with the high parasite loads found in these species, were observed. The heat stress experiment revealed gills as most sensible tissue in the 7 days time period and the brain as the most sensible tissue after 20 days of exposure to the exprimental conditions, with protein metabolism, vescicular transport, coagulation and cytoskeleton assembly being the most impacted processes. Comparatively, the gills and muscle tissues displayed an earlier and weaker transcriptomic response. Interestingly, several HSPs were regulated in response to stress resulting both from heat and stabling. This study allowed us to identify peculiar transcriptomic markers of cold adaptation in Cryonotothenioidea and to understand which may be their likely response to rising ocean temperature in a global warming scenario.