Xenobiotic metabolism and its physiological consequences in high-Antarctic Notothenioid fishes

The Antarctic ecosystem is progressively exposed to anthropogenic contaminants, such as polycyclic aromatic hydrocarbons (PAHs). So far, it is largely unknown if PAHs leave a mark in the physiology of high-Antarctic fish. We approached this issue via two avenues: first, we examined the functional response of the aryl hydrocarbon receptor (Ahr), which is a molecular initiating event of many toxic effects of PAHs in biota. Chionodraco hamatus and Trematomus loennbergii served as representatives for high-Antarctic Notothenioids, and Atlantic cod, Gadus morhua as non-polar reference species. We sequenced and cloned the Ahr ligand binding domain (LBD) of the Notothenioids and deployed a GAL4-based luciferase reporter gene assay expressing the Ahr LBD. Benzo[a]pyrene (BaP), beta-naphthoflavone and chrysene were used as ligands for the reporter gene assay. Second, we investigated the energetic costs of Ahr activation in isolated liver cells of the Notothenioids during acute, non-cytotoxic BaP exposure. In the reporter assay, the Ahr LBD of Atlantic cod and the Antarctic Notothenioids were activated by the ligands tested herein. In the in vitro assays with isolated liver cells of high-Antarctic Notothenioids, BaP exposure had no effect on overall respiration, but caused shifts in the respiration dedicated to protein synthesis. Thus, our study demonstrated that high-Antarctic fish possess a functional Ahr that can be ligand-activated in a concentration-dependent manner by environmental contaminants. This is associated with altered cost for cellular protein synthesis. Future studies have to show if the toxicant-induced activation of the Ahr pathway may lead to altered organism performance of Antarctic fish.

Not Frozen in the Ice: large and Dynamic Rearrangements in the Mitochondrial Genomes of the Antarctic Fish

The vertebrate mitochondrial genomes generally present a typical gene order. Exceptions are uncommon and important to study the genetic mechanisms of gene order rearrangements and their consequences on phylogenetic output and mitochondrial function. Antarctic notothenioid fish carry some peculiar rearrangements of the mitochondrial gene order. In this first systematic study of 28 species, we analysed known and undescribed mitochondrial genome rearrangements for a total of eight different gene orders within the notothenioid fish. Our reconstructions suggest that transpositions, duplications and inversion of multiple genes are the most likely mechanisms of rearrangement in notothenioid mitochondrial genomes. In Trematominae, we documented an extremely rare inversion of a large genomic segment of 5300 bp that partially affected the gene compositional bias but not the phylogenetic output. The genomic region delimited by nad5 and trnF, close to the area of the Control Region, was identified as the hot spot of variation in Antarctic fish mitochondrial genomes. Analysing the sequence of several intergenic spacers and mapping the arrangements on a newly generated phylogeny showed that the entire history of the Antarctic notothenioids is characterized by multiple, relatively rapid, events of disruption of the gene order. We hypothesised that a pre-existing genomic flexibility of the ancestor of the Antarctic notothenioids may have generated a precondition for gene order rearrangement, and the pressure of purifying selection could have worked for a rapid restoration of the mitochondrial functionality and compactness after each event of rearrangement.

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

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 genome sequence of the channel bull blenny, Cottoperca gobio (Günther, 1861)

We present a genome assembly for Cottoperca gobio (channel bull blenny, (Günther, 1861)); Chordata; Actinopterygii (ray-finned fishes), a temperate water outgroup for Antarctic Notothenioids. The size of the genome assembly is 609 megabases, with the majority of the assembly scaffolded into 24 chromosomal pseudomolecules. Gene annotation on Ensembl of this assembly has identified 21,662 coding genes.

PhylSim: A New Phylogenetic Tool for Modeling Trait Evolution and Speciation

ABSTRACTWe present a new software tool in R, the PhylSim package, which allows the user to simulate trait evolution on a phylogeny, while varying the speciation rate and evolutionary model over the course of the simulation. In particular, the user can specify any number of regimes, with a different speciation rate for each regime, or set the speciation rate to vary when the value of a trait exceeds a certain threshold. The evolutionary model can also be varied as many times as necessary over the course of the simulation, to account for traits tending toward different optima at different periods in evolutionary history. We illustrate the use of the package with an example, a simulation of the adaptive radiation of Antarctic notothenioids in the Southern Ocean.

Maximum cardiac performance of Antarctic fishes that lack haemoglobin and myoglobin: exploring the effect of warming on nature’s natural knockouts

Antarctic notothenioids, some of which lack myoglobin (Mb) and/or haemoglobin (Hb), are considered extremely stenothermal, which raises conservation concerns since Polar regions are warming at unprecedented rates. Without reliable estimates of maximum cardiac output ($\dot{Q}$), it is impossible to assess their physiological scope in response to warming seas. Therefore, we compared cardiac performance of two icefish species, Chionodraco rastrospinosus (Hb−Mb+) and Chaenocephalus aceratus (Hb−Mb−), with a related notothenioid, Notothenia coriiceps (Hb+Mb+) using an in situ perfused heart preparation. The maximum $\dot{Q}$, heart rate (fH), maximum cardiac work (WC) and relative ventricular mass of N. coriiceps at 1°C were comparable to temperate-water teleosts, and acute warming to 4°C increased fH and WC, as expected. In contrast, icefish hearts accommodated a higher maximum stroke volume (VS) and maximum $\dot{Q}$ at 1°C, but their unusually large hearts had a lower fH and maximum afterload tolerance than N. coriiceps at 1°C. Furthermore, maximum VS, maximum $\dot{Q}$ and fH were all significantly higher for the Hb−Mb+ condition compared with the Hb−Mb− condition, a potential selective advantage when coping with environmental warming. Like N. coriiceps, both icefish species increased fH at 4°C. Acutely warming C. aceratus increased maximum $\dot{Q}$, while C. rastrospinosus (like N. coriiceps) held at 4°C for 1 week maintained maximum $\dot{Q}$ when tested at 4°C. These experiments involving short-term warming should be followed up with long-term acclimation studies, since the maximum cardiac performance of these three Antarctic species studied seem to be tolerant of temperatures in excess of predictions associated with global warming.