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Background: The white-blooded Antarctic icefishes is a representative organism that survive under the stenothermal conditions of the Southern Ocean without the hemoglobin genes. To compensate for inefficient oxygen transport, distinct features such as increased heart size, greater blood volume, and reduced hematocrit density enhance the amount of dissolved oxygen and the velocity of blood flow. Results: Here, we investigated these unique characteristics by comparing high-quality genomic data between white-blooded and red-blooded fishes and identified the loss of FAAP20, which is implicated in anemia. Although the gene region containing FAAP20 is conserved in notothenioids as shown through collinear analysis, only remnants of FAAP20 persist in several icefish species. Additionally, we observed the loss of SOAT1, which plays a pivotal role in cholesterol metabolism, providing a clue for further investigations into the unique mitochondrial form of the icefish. Conclusions: The loss of FAAP20, which is known to reduce erythrocyte counts under stress conditions in mice and humans, may provide a clue to understanding the genomic characteristics related to oxygen supply, such as low hematocrit, in Antarctic icefishes. [ABSTRACT FROM AUTHOR]

Abstract Background The white-blooded Antarctic icefishes is a representative organism that survive under the stenothermal conditions of the Southern Ocean without the hemoglobin genes. To compensate for inefficient oxygen transport, distinct features such as increased heart size, greater blood volume, and reduced hematocrit density enhance the amount of dissolved oxygen and the velocity of blood flow. Results Here, we investigated these unique characteristics by comparing high-quality genomic data between white-blooded and red-blooded fishes and identified the loss of FAAP20, which is implicated in anemia. Although the gene region containing FAAP20 is conserved in notothenioids as shown through collinear analysis, only remnants of FAAP20 persist in several icefish species. Additionally, we observed the loss of SOAT1, which plays a pivotal role in cholesterol metabolism, providing a clue for further investigations into the unique mitochondrial form of the icefish. Conclusions The loss of FAAP20, which is known to reduce erythrocyte counts under stress conditions in mice and humans, may provide a clue to understanding the genomic characteristics related to oxygen supply, such as low hematocrit, in Antarctic icefishes.

Liver‐expressed antimicrobial peptide 2 (LEAP2) is a small peptide, which is consisted of signal peptide, pro‐peptide and the bioactive mature peptide. Mature LEAP2 is an antibacterial peptide with four highly conserved cysteines forming two intramolecular disulfide bonds. Chionodraco hamatus, an Antarctic notothenioid fish that lives in the coldest water, has white blood unlike most fish of the world. In this study, the LEAP2 coding sequence was cloned from C. hamatus, including a 29 amino acids signal peptide and mature peptide of 46 amino acids. High levels of LEAP2 mRNA were detected in the skin and liver. Mature peptide was obtained by chemical synthesis in vitro, displayed selective antimicrobial activities against Escherichia coli, Aeromonas hydrophila, Staphylococcus aureus and Streptococcus agalactiae. Liver‐expressed antimicrobial peptide 2 showed bactericidal activity by destroying the cell membrane integrity and robustly combined with bacterial genomic DNA. In addition, overexpression of the Tol‐LEAP2‐EGFP in zebrafish larva showed stronger antimicrobial activity in C. hamatus than in zebrafish, accompanied by lower bacterial load and expression of pro‐inflammatory factors. This is the first demonstration of the antimicrobial activity of LEAP2 from C. hamatus, which is of useful value in improving resistance to pathogens. [ABSTRACT FROM AUTHOR]

Antarctic icefish is the only known vertebrate species that lacks oxygen-carrying hemoglobin and functional erythrocytes. To reveal the unique hematopoietic process of icefish, we used an integrated approach including tandem mass tag (TMT) labeling and liquid chromatography–tandem mass spectrometry (LC–MS/MS) to quantify the dynamic changes in the head kidney whole proteome of a white-blooded icefish, Chionodraco hamatus, compared to those in two other red-blooded Antarctic fish, Trematomus bernacchii and Notothenia coriiceps. Of the 4672 identified proteins, in the Antarctic icefish head kidney, 123 proteins were significantly upregulated and 95 proteins were downregulated. The functional grouping of differentially expressed proteins (DEPs) based on KEGG pathway analysis shows that white blood fish and red blood fish have significant differences in erythropoiesis, heme biogenesis, leucocyte and platelet cell development. The proteins involved in the hematopoietic process in icefish showed a clear trend of downregulation of erythroid lineage marker proteins (β-Spectrin, hemoglobin, CTCF and tfr1a) and upregulation of lymphoid and megakaryocytic lineage marker proteins, including CD9, ITGB2, and mTOR, which suggests a shift in hematopoiesis in the icefish head kidney due to the loss of erythrocytes. Moreover, western blotting analysis showed that a significantly down expression level of CTCF protein was detected in the icefish head kidney, which was in line with the proteomics data. The results of the present study not only provide basic datasets for the head kidney proteins of Antarctic fishes, but also provide important references for studies on immunity and hematopoiesis in various species. [ABSTRACT FROM AUTHOR]

Ancestors of the Antarctic icefishes (family Channichthyidae) were benthic and had no swim bladder, making it energetically expensive to rise from the ocean floor. To exploit the water column, benthopelagic icefishes were hypothesized to have evolved a skeleton with "reduced bone," which gross anatomical data supported. Here, we tested the hypothesis that changes to icefish bones also occurred below the level of gross anatomy. Histology and micro‐CT imaging of representative craniofacial bones (i.e., ceratohyal, frontal, dentary, and articular) of extant Antarctic fish species specifically evaluated two features that might cause the appearance of "reduced bone": bone microstructure (e.g., bone volume fraction and structure linear density) and bone mineral density (BMD, or mass of mineral per volume of bone). Measures of bone microstructure were not consistently different in bones from the icefishes Chaenocephalus aceratus and Champsocephalus gunnari, compared to the related benthic notothenioids Notothenia coriiceps and Gobionotothen gibberifrons. Some quantitative measures, such as bone volume fraction and structure linear density, were significantly increased in some icefish bones compared to homologous bones of non‐icefish. However, such differences were rare, and no microstructural measures were consistently different in icefishes across all bones and species analyzed. Furthermore, BMD was similar among homologous bones of icefish and non‐icefish Antarctic notothenioids. In summary, "reduced bone" in icefishes was not due to systemic changes in bone microstructure or BMD, raising the prospect that "reduced bone" in icefish occurs only at the gross anatomic level (i.e., smaller or fewer bones). Given that icefishes exhibit delayed skeletal development compared to non‐icefish Antarctic fishes, combining these phenotypic data with genomic data might clarify genetic changes driving skeletal heterochrony. [ABSTRACT FROM AUTHOR]

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The Antarctic icefish, a family (Channichthyidae) of teleosts within the perciform suborder Notothenioidei, are the only known vertebrates without oxygen-transporting haemoglobins and that are largely devoid of circulating erythrocytes. To elucidate the evo-devo mechanisms underpinning the suppressed erythropoiesis in the icefish, we conducted comparative studies on the transcriptomes and micro RNAomes of the primary haematopoietic tissues between an icefish ( Chionodraco hamatus) and two red-blooded notothenioids ( Trematomus bernacchii and Gymnodraco acuticeps). We identified substantial remodelling of the haematopoietic programs in the icefish through which erythropoiesis is selectively suppressed. Experimental verification showed that erythropoietic suppression in the icefish may be attributable to the upregulation of TGF-β signalling, which coincides with reductions in multiple transcription factors essential for erythropoiesis and the upregulation of hundreds of micro RNAs, the majority (> 80%) of which potentially target erythropoiesis regulating factors. Of the six micro RNAs selected for verification, three mi RNAs (miR-152, miR-1388 and miR-16b) demonstrated suppressive functions on GATA1 and ALAS2, which are two factors important for erythroid differentiation, resulting in reduced numbers of erythroids in microinjected zebra fish embryos. Codon substitution analyses of the genes of the TGF-β superfamily revealed signs of positive selection in TGF -β 1 and endoglin in the lineages leading to Antarctic notothenioids. Both genes are previously known to function in erythropoietic suppression. These findings implied a general trend of erythropoietic suppression in the cold-adapted notothenioid lineages through evolutionary modulation of the multi-functional TGF-β signalling pathway. This trend is more pronounced in the haemoglobin-less icefish, which may pre-emptively hinder the otherwise defective erythroids from production. [ABSTRACT FROM AUTHOR]

The identification of loci under selection (outliers) is a major challenge in evolutionary biology, being critical to comprehend evolutionary processes leading to population differentiation and speciation, and for conservation purposes, also in light of recent climate change. However, detection of selected loci can be difficult when populations are weakly differentiated. This is the case of marine fish populations, often characterized by high levels of gene flow and connectivity, and particularly of fish living in the Antarctic marine environment, characterized by a complex and strong circulating system promoting individual dispersal all around the continent. With the final aim of identifying outlier loci putatively under selection in the Chionodraco genus, we used 21 microsatellites, including both genomic (Type II) and EST-linked loci (Type I), to investigate the genetic differentiation among the three recently derived Chionodraco species that are endemic to the freezing Antarctic waters. Neutrality tests were applied in interspecific comparisons in order to identify candidate loci showing high levels of genetic differentiation, which might reveal imprints of past selection. Three outlier loci were identified, detecting a higher differentiation between species than did neutral loci. Outliers showed sequence similarity to a calmodulin gene, to an antifreeze glycoprotein/trypsinogen-like protease gene and to nonannotated fish mRNAs. Selective pressures acting on outlier loci identified in this study might reflect past evolutionary processes, which led to species divergence and local adaptation in the Chionodraco genus. Used loci will provide a valuable tool for future population genetic studies in Antarctic notothenioids. [ABSTRACT FROM AUTHOR]

ntarctic icefishes (Family: Channichthyidae) are the only adult vertebrate that do not express the circulatory oxygen-binding protein, hemoglobin. Six species of icefishes, including Dacodraco hunteri, also do not express myoglobin (Mb), an oxygen-binding protein found in ventricular tissue of Antarctic notothenioids. Sequence of the Mb gene from D. hunteri contains a duplicated TATA box in the promoter region of the Mb gene that is absent in Chionodraco rastrospinosus, an icefish species known to express Mb. The 15-base pair insertion in D. hunteri is identical to the duplicated TATA box that is thought to be directly responsible for preventing transcription of the Mb gene in C. aceratus, another icefish species that lacks Mb expression. Sequencing of the Mb promoter from the remaining channichthyid species revealed the duplicated TATA box in 14 of 16 icefish species, including 8 species known to express Mb. Based on the presence of the duplicated TATA box in promoters of both Mb-expressing and Mb-lacking species, loss of Mb expression in D. hunteri and C. aceratus is either independent of the duplicated TATA box, or the duplicated TATA box requires presence or absence of a distant regulatory element to prevent transcription. [ABSTRACT FROM AUTHOR]

The Antarctic icefishes (Family Channichthyidae) provide excellent examples of unique traits that can arise in a chronically cold and isolated environment. Their loss of hemoglobin (Hb) expression, and in some cases, loss of myoglobin (Mb) expression, has taught us much about the function of these proteins. Although absences of the proteins are fixed traits in icefishes, the losses do not appear to be of adaptive value. Contrary to some suggestions, loss of Hb has led to higher energetic costs for circulating blood, and losses of Mb have reduced cardiac performance. Moreover, losses of Hb and Mb have resulted in extensive modifications to the cardiovascular system to ensure adequate oxygen delivery to working muscles. Recent studies suggest that losses of Hb and Mb, and their associated nitric oxide (NO)-oxygenase activities, may have accelerated the development and evolution of these cardiovascular modifications. The high levels of NO that should occur in the absence of Hb and Mb have been shown in other animal groups to lead to an increase in tissue vascularization, an increase in the lumenal diameter of blood vessels, and an increase in mitochondrial densities. These characteristics are all hallmark traits of Antarctic icefishes. Homeostatic feedback mechanisms thus may have accelerated evolution of the pronounced cardiovascular traits of Antarctic icefishes. [ABSTRACT FROM AUTHOR]

We previously observed that Antarctic fish genes contain intron sequences of high A+T content (60–70% average A+T) which are in stark contrast with adjacent protein coding-sequences. Here, we report that this disparity in intron/exon base composition is a common feature among teleosts. We analyzed 483 teleost genomic DNA sequences, containing 2583 introns, from 80 teleost genera that populate polar, temperate, or tropical habitats. Eighty-nine percent of teleost introns display an A+T content between 50–84% A+T with a mean of 60% A+T. In contrast, only 37% of teleost exons have an A+T content greater-than 50% with a mean of 48% A+T. A comparison to homologous mammalian genes showed a striking difference; in this case, introns and exons have similar base compositions, averaging 45–47% A+T. This indicates that most teleost genes exhibit a large difference in base composition between their introns and exons. There was no correlation of teleost intron A+T content to intron length or habitat temperature range. Thus, teleost intron sequences tend to show the common feature of being much higher in A+T content then neighboring exons. [ABSTRACT FROM AUTHOR]