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.

Chromosomal-Level Assembly of Antarctic Scaly Rockcod, Trematomus loennbergii Genome Using Long-Read Sequencing and Chromosome Conformation Capture (Hi-C) Technologies

Trematomus species (suborder Notothenioidei; family Nototheniidae) are widely distributed in the southern oceans near Antarctica. There are 11 recognized species in the genus Trematomus, and notothenioids are known to have high chromosomal diversity (2n = 24–58) because of relatively recent and rapid adaptive radiation. Herein, we report the chromosomal-level genome assembly of T. loennbergii, the first characterized genome representative of the genus Trematomus. The final genome assembly of T. loennbergii was obtained using a Pacific Biosciences long-read sequencing platform and high-throughput chromosome conformation capture technology. Twenty-three chromosomal-level scaffolds were assembled to 940 Mb in total size, with a longest contig size of 48.5 Mb and contig N50 length of 24.7 Mb. The genome contained 42.03% repeat sequences, and a total of 24,525 protein-coding genes were annotated. We produced a high-quality genome assembly of T. loennbergii. Our results provide a first reference genome for the genus Trematomus and will serve as a basis for studying the molecular taxonomy and evolution of Antarctic fish.

Antarctic Fish as a Global Pollution Sensor: Metals Biomonitoring in a Twelve-Year Period

Antarctica represents a unique natural laboratory for ecotoxicological studies as it is characterized by low internal pollutants emissions but high external contamination levels. Indeed, warm temperatures promote pollutant evaporation (low latitudes), while cool temperatures (high latitudes) promote its deposition from the atmosphere on land/water. Metals are the most important pollutants in ecosystems and represent a serious and global threat to aquatic and terrestrial organisms. Since 2000, the risks posed by metals have led many States to ratify protocols aimed at reducing their emissions. Endemic Antarctic organisms represent excellent bioindicators in order to evaluate the efficacy of global measures adopted to mitigate pollutants release into the environment. In this study (supported by PNRA18-00133), we estimated the metals contamination levels and the metallothionein-1 expression in liver samples of two Antarctic fish species, the icefish Chionodraco hamatus and the red-blooded Trematomus bernacchii, collected in the same area during 2002 and 2014. The chosen area is located in the Ross Sea, a unique area as it is also isolated from the rest of the Southern Ocean. The analysis of contamination trends throughout this period showed, in both species, a significant increase over time of metals bioaccumulation and metallothionein-1 expression. In addition, our result clearly indicated that the detoxifying ability of the two organisms analyzed greatly differs, probably due to haemoglobin presence/absence. Our work represents an important early step to obtain valuable information in conservation strategies for both Antarctic and non-Antarctic ecosystems.

A First Genome Survey and Genomic SSR Marker Analysis of Trematomus loennbergii Regan, 1913

Trematomus loennbergii Regan, 1913, is an evolutionarily important marine fish species distributed in the Antarctic Ocean. However, its genome has not been studied to date. In the present study, whole genome sequencing was performed using next-generation sequencing (NGS) technology to characterize its genome and develop genomic microsatellite markers. The 25-mer frequency distribution was estimated to be the best, and the genome size was predicted to be 815,042,992 bp. The heterozygosity, average rate of read duplication, and sequencing error rates were 0.536%, 0.724%, and 0.292%, respectively. These data were used to analyze microsatellite markers, and a total of 2,264,647 repeat motifs were identified. The most frequent repeat motif was di-nucleotide with 87.00% frequency, followed by tri-nucleotide (10.45%), tetra-nucleotide (1.94%), penta-nucleotide (0.34%), and hexa-nucleotide (0.27%). The AC repeat motif was the most abundant motif among di-nucleotides and among all repeat motifs. Among microsatellite markers, 181 markers were selected and PCR technology was used to validate several markers. A total of 15 markers produced only one band. In summary, these results provide a good basis for further studies, including evolutionary biology studies and population genetics of Antarctic fish species.

Parasites of Three Closely Related Antarctic Fish Species (Teleostei: Nototheniinae) from Elephant Island

Background Studies of parasite communities and patterns in the Antarctic are an important knowledge base with the potential to track shifts in ecological relations and study the effects of climate change on host–parasite systems. Endemic Nototheniinae is the dominant fish group found in Antarctic marine habitats. Through their intermediate position within the food web, Nototheniinae link lower to higher trophic levels and thereby also form an important component of parasite life cycles. The study was set out to gain insight into the parasite fauna of Nototheniops larseni, N. nudifrons and Lepidonotothen squamifrons (Nototheniinae) from Elephant Island (Antarctica). Methods Sampling was conducted at three locations around Elephant Island during the ANT-XXVIII/4 expedition of the research vessel Polarstern. The parasite fauna of three Nototheniine species was analysed, and findings were compared to previous parasitological and ecological research collated from a literature review. Results All host species shared the parasites Neolebouria antarctica (Digenea), Corynosoma bullosum (Acanthocephala) and Pseudoterranova decipiens E (Nematoda). Other parasite taxa were exclusive to one host species in this study. Nototheniops nudifrons was infected by Ascarophis nototheniae (Nematoda), occasional infections of N. larseni with Echinorhynchus petrotschenkoi (Acanthocephala) and L. squamifrons with Elytrophalloides oatesi (Digenea) and larval tetraphyllidean Cestoda were detected. Conclusion All examined fish species’ parasites were predominantly euryxenous regarding their fish hosts. The infection of Lepidonotothen squamifrons with Lepidapedon garrardi (Digenea) and Nototheniops larseni with Echinorhynchus petrotschenkoi represent new host records. Despite the challenges and limited opportunities for fishing in remote areas, future studies should continue sampling on a more regular basis and include a larger number of fish species and sampling sites within different habitats.

Productivity and Change in Fish and Squid in the Southern Ocean

Southern Ocean ecosystems are globally important and vulnerable to global drivers of change, yet they remain challenging to study. Fish and squid make up a significant portion of the biomass within the Southern Ocean, filling key roles in food webs from forage to mid-trophic species and top predators. They comprise a diverse array of species uniquely adapted to the extreme habitats of the region. Adaptations such as antifreeze glycoproteins, lipid-retention, extended larval phases, delayed senescence, and energy-conserving life strategies equip Antarctic fish and squid to withstand the dark winters and yearlong subzero temperatures experienced in much of the Southern Ocean. In addition to krill exploitation, the comparatively high commercial value of Antarctic fish, particularly the lucrative toothfish, drives fisheries interests, which has included illegal fishing. Uncertainty about the population dynamics of target species and ecosystem structure and function more broadly has necessitated a precautionary, ecosystem approach to managing these stocks and enabling the recovery of depleted species. Fisheries currently remain the major local driver of change in Southern Ocean fish productivity, but global climate change presents an even greater challenge to assessing future changes. Parts of the Southern Ocean are experiencing ocean-warming, such as the West Antarctic Peninsula, while other areas, such as the Ross Sea shelf, have undergone cooling in recent years. These trends are expected to result in a redistribution of species based on their tolerances to different temperature regimes. Climate variability may impair the migratory response of these species to environmental change, while imposing increased pressures on recruitment. Fisheries and climate change, coupled with related local and global drivers such as pollution and sea ice change, have the potential to produce synergistic impacts that compound the risks to Antarctic fish and squid species. The uncertainty surrounding how different species will respond to these challenges, given their varying life histories, environmental dependencies, and resiliencies, necessitates regular assessment to inform conservation and management decisions. Urgent attention is needed to determine whether the current management strategies are suitably precautionary to achieve conservation objectives in light of the impending changes to the ecosystem.

Comparative Proteomic Analysis of Erythropoiesis Tissue Head Kidney Among three Antarctic Fish Species

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 4,672 identified proteins, in the Antarctic ice fish head kidney, 123 proteins were significantly up-regulated and 95 proteins were down-regulated. The functional grouping of differentially expressed proteins 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 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. 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.