Comparative transcriptomics sheds new light on peculiar cold adaptation strategies in the gills of Cryonotothenioidea

Cryonotothenioidea represent one of the most striking cases of evolutionary adaptations to an extreme environment known in vertebrates. The icefish Chionodraco hamatus, the main target species of this study, lacks hemoglobin and displays a unique cardio-circulatory system and a series of unique morphological and physiological peculiarities that enabled this species to survive and thrive in the sub-zero temperatures of coastal Antarctic waters. However, our knowledge of the genetic and molecular bases of these adaptations is still limited. Here we provide the first large scale comparative analysis between the transcriptional profiles of C. hamatus, five red-blooded Cryonotothenioidea, the sub-Antarctic notothenioid fish Eleginops maclovinus and seven temperate teleost species. This analysis targeted the gills, the main surface of contact with the external environment, and a tissue of primary importance in fish for gaseous exchange and its role in the fish immunity. We identified a set of genes consistently up-regulated in Cryonotothenioidea, which were surprisingly shared by red- and white-blooded species and revealed several previously unreported alterations which may have contributed to the evolutionary success of this fish lineage in Antarctica. In particular, we detected an increased activity of carbonic anhydrases, paired with an upregulation of the molecular machinery involved in the Golgi to endoplasmic reticulum retrograde transport, consistent with high secretory activity, and molecular signatures of cobalamin deficiency. We discuss the possible biological implications of this condition with respect to hematological alterations and the heavy parasitic loads typically observed in all Cryonotothenioidea.