Cold Adaptation in Antarctic Notothenioids: Comparative Transcriptomics Reveals Novel Insights in the Peculiar Role of Gills and Highlights Signatures of Cobalamin Deficiency

Abstract

Far from being devoid of life, Antarctic waters are home to Cryonotothenioidea, which represent one of the fascinating cases of evolutionary adaptation to extreme environmental conditions in vertebrates. Thanks to a series of unique morphological and physiological peculiarities, which include the paradigmatic case of loss of hemoglobin in the family Channichthyidae, these fish survive and thrive at sub-zero temperatures. While some of the distinctive features of such adaptations have been known for decades, our knowledge of their genetic and molecular bases is still limited. We generated a reference de novo assembly of the icefish Chionodraco hamatus transcriptome and used this resource for a large-scale comparative analysis among five red-blooded Cryonotothenioidea, the sub-Antarctic notothenioid Eleginops maclovinus and seven temperate teleost species. Our investigation targeted the gills, a tissue of primary importance for gaseous exchange, osmoregulation, ammonia excretion, and its role in fish immunity. One hundred and twenty genes were identified as significantly up-regulated in Antarctic species and surprisingly shared by red- and white-blooded notothenioids, unveiling several previously unreported molecular players that might have contributed to the evolutionary success of Cryonotothenioidea in Antarctica. In particular, we detected cobalamin deficiency signatures and discussed the possible biological implications of this condition concerning hematological alterations and the heavy parasitic loads typically observed in all Cryonotothenioidea.

The Antarctic Scallop Adamussium colbecki Is Unable to Transcriptomically Respond to Captivity and Moderate Thermal Stress

“…To ensure a reliable calculation of gene expression levels, we carefully evaluated the presence of contamination from exogenous sequences not belonging to the target species. In particular, we detected the presence of contamination from the notothenioids T. bernacchii and C. hamatus which were being studied at the MZS during the XXV PNRA expedition [28], concurrently with the collection and dissection of the biological samples used for the assembly of the transcriptome of A. colbecki. Moreover, traces of P. pseudoroscoffensis, a coccolithophore that was being studied in our laboratory in the same period the reads were prepared for sequencing, were also detected.…”

Comparative Transcriptomic Analysis Reveals Adaptive Traits in Antarctic Scallop Adamussium colbecki

“…Although different approaches may be used to mitigate this issue, a set of genes or transcripts unequivocally identified as orthologs can be used as a reference for read mapping. This strategy was initially suggested by early comparative studies conducted on microarray data [36] and has been consistently used in recent times for the analysis of RNA-seq data [37][38][39][40].…”

“…Taking into account this limitation, our analysis allowed the detection of alterations of the expression of genes constitutively expressed in all A. colbecki tested tissues, but it might have missed other equally important molecular adaptations involving inducible genes, or those exclusively expressed during embryogenesis. Moreover, molecular adaptations to cold may also involve gene gain, gene loss, and gene duplication processes (like those observed in Antarctic notothenioid fishes [62]), which we could not investigate due to the focus placed on the identification of single-copy orthologs following the strategy that is most commonly used to carry out comparative transcriptomic studies [36][37][38][39][40]63]. Such a fine-scale analysis will be only possible when a high-quality annotated genome assembly will be released for this species.…”

Gene Expression Profiling of Trematomus bernacchii in Response to Thermal and Stabling Stress

“…Antarctic notothenioid fishes are physiologically adapted to life in subzero water temperatures thanks to the acquisition of several striking unique morphological and physiological traits compared to their closest extant relatives living in temperate waters. Such adaptations include the ability to produce antifreeze glycoproteins that prevent the growth of ice crystals in body fluids (hypotonic compared with seawater) [13,14], the loss of an inducible Heat Shock response [15][16][17], the partial or complete loss of expression of adult hemoglobin [18,19] and modifications in gas exchange functionality in gills [20,21].…”