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Transcriptome Analysis Provides Insights Into the Adaptive Responses to Hypoxia of a Schizothoracine Fish (Gymnocypris eckloni).

ABSTRACT: The schizothoracine fish endemic to the Qinghai-Tibetan Plateau are comparatively well adapted to aquatic environments with low oxygen partial pressures. However, few studies have used transcriptomic profiling to investigate the adaptive responses of schizothoracine fish tissues to hypoxic stress. This study compared the transcriptomes of Gymnocypris eckloni subjected to 72 h of hypoxia (Dissolved oxygen, DO = 3.0 ± 0.1 mg/L) to those of G. eckloni under normoxia (DO = 8.4 ± 0.1 mg/L). To identify the potential genes and pathways activated in response to hypoxic stress, we collected muscle, liver, brain, heart, and blood samples from normoxic and hypoxic fish for RNA-Seq analysis. We annotated 337,481 gene fragments. Of these, 462 were differentially expressed in the hypoxic fish as compared to the normoxic fish. Under hypoxia, the transcriptomic profiles of the tissues differed, with muscle the most strongly affected by hypoxia. Our data indicated that G. eckloni underwent adaptive changes in gene expression in response to hypoxia. Several strategies used by G. eckloni to cope with hypoxia were similar to those used by other fish, including a switch from aerobic oxidation to anaerobic glycolysis and the suppression of major energy-requiring processes. However, G. eckloni used an additional distinct strategy to survive hypoxic environments: a strengthening of the antioxidant system and minimization of ischemic injury. Here, we identified several pathways and related genes involved in the hypoxic response of the schizothoracine fish. This study provides insights into the mechanisms used by schizothoracine fish to adapt to hypoxic environments.

SUBMITTER: Qi D

PROVIDER: S-EPMC6160557 | biostudies-literature | 2018

REPOSITORIES: biostudies-literature

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Transcriptome Analysis Provides Insights Into the Adaptive Responses to Hypoxia of a Schizothoracine Fish (Gymnocypris eckloni).

Qi Delin D Chao Yan Y Wu Rongrong R Xia Mingzhe M Chen Qichang Q Zheng Zhiqin Z

Frontiers in physiology 20180921

The schizothoracine fish endemic to the Qinghai-Tibetan Plateau are comparatively well adapted to aquatic environments with low oxygen partial pressures. However, few studies have used transcriptomic profiling to investigate the adaptive responses of schizothoracine fish tissues to hypoxic stress. This study compared the transcriptomes of Gymnocypris eckloni subjected to 72 h of hypoxia (Dissolved oxygen, DO = 3.0 ± 0.1 mg/L) to those of G. eckloni under normoxia (DO = 8.4 ± 0.1 mg ...[more]

PMID: 30298021

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Project description:BackgroundCopper was used for many years in aquaculture operations as an effective algaecide or a parasite treatment of fish. It is an essential nutrient with numerous functions in organisms, but is toxic at high concentrations. However, the toxicity of copper to fish remains unclear. In this study, we used the piebald naked carp, Gymnocypris eckloni, as a model. RNA-seq data from different tissues, including gills, kidney, and liver, were used to investigate the underlying mechanism of copper toxicology in G. eckloni.ResultsWe compared the transcriptomes from different tissues with different time durations of copper ion treatment. After 72 h copper ion treatment, the number of genes with different expression in gills and liver changed dramatically, but not in kidneys. In KEGG functional enrichment, the pattern of differentially expressed genes (DEGs) was also similar in the gills and liver. The most enriched pathway of DEGs was "Ribosome" in both tissues. Furthermore, we analyzed the expression levels of genes involved in oxidative stress response and protein synthesis using qPCR and RNA-seq data. Our results showed that several genes involved in oxidative stress response were up-regulated both in gills and liver. Up-regulation of these genes indicated that copper treatment caused oxidative stress, which is likely to result in ribosome damage. In addition, our results showed that the expression of Eef1b2, a transcription elongation factor, was decreased in the liver under oxidative stress, and the expression of translation initiation factors Eif4ebp1 and eIF2α, and elongation factor eEF2 was up-regulated. These results supported the idea that oxidative stress inhibits protein synthesis in cells.ConclusionsOur results indicate that copper exposure caused different responses in different tissues, since the gene expression patterns changed substantially either in the gills or liver, while the effect on the kidney was relatively weak. Furthermore, our results indicated that the expression pattern of the genes involved in the ribosome, which is a complex molecular machine orchestrating protein synthesis in the cell, together with translation initiation factor and elongation factors, were affected by copper exposure both in the gills and liver of piebald naked carp. This result leads us to speculate that the downregulation of global protein synthesis is an acute response strategy of fish to metal-induced oxidative stress. Moreover, we speculate that this strategy not only exists in the selective translation of proteins but also exists in the specific translation of functional proteins in tissues and cells.

Project description:Erythropoietin (EPO) is a glycoprotein hormone that plays a principal regulatory role in erythropoiesis and initiates cell homeostatic responses to environmental challenges. The Qinghai-Tibet Plateau is a natural laboratory for hypoxia adaptation. Gymnocypris dobula is a highly specialized plateau schizothoracine fish that is restricted to?>?4500 m high-altitude freshwater rivers and ponds in the Qinghai-Tibet Plateau. The role of EPO in the adaptation of schizothoracine fish to hypoxia is unknown.The EPO and EPO receptor genes from G. dobula and four other schizothoracine fish from various altitudinal habitats were characterized. Schizothoracine EPOs are predicted to possess 2-3 N-glycosylation (NGS) sites, 4-5 casein kinase II phosphorylation (CK2) sites, 1-2 protein kinase C (PKC) phosphorylation sites, and four conserved cysteine residues within four helical domains, with variations in the numbers of NGS and CK2 sites in G. dobula. PAML analysis indicated a d N/d S value (?)?=?1.112 in the G. dobula lineage, and a few amino acids potentially under lineage-specific positive selection were detected within the G. dobula EPO. Similarly, EPO receptors of the two high-altitude schizothoracines (G. dobula and Ptychobarbus kaznakovi), were found to be statistically on the border of positive selection using the branch-site model (P-value?=?0.096), and some amino acids located in the ligand-binding domain and the fibronectin type III domain were identified as potentially positive selection sites. Tissue EPO expression profiling based on transcriptome sequencing of three schizothoracines (G. dobula, Schizothorax nukiangensis Tsao, and Schizothorax prenanti) showed significant upregulation of EPO expression in the brain and less significantly in the gill of G. dobula. The elevated expression together with the rapid evolution of the EPO gene in G. dobula suggested a possible role for EPO in adaptation to hypoxia. To test this hypothesis, Gd-EPO and Sp-EPO were cloned into an expression vector and transfected into the cultured cell line 293 T. Significantly higher cell viability was observed in cells transfected with Gd-EPO than cells harboring Sp-EPO when challenged by hypoxia.The deduced EPO proteins of the schizothoracine fish contain characteristic structures and important domains similar to EPOs from other taxa. The presence of potentially positive selection sites in both EPO and EPOR in G. dobula suggest possible adaptive evolution in the ligand-receptor binding activity of the EPO signaling cascade in G. dobula. Functional study indicated that the EPO from high-altitude schizothoracine species demonstrated features of hypoxic adaptation by reducing toxic effects or improving cell survival when expressed in cultured cells, providing evidence of molecular adaptation to hypoxic conditions in the Qinghai-Tibet Plateau.

Dataset Information

Transcriptome Analysis Provides Insights Into the Adaptive Responses to Hypoxia of a Schizothoracine Fish (Gymnocypris eckloni).

Publications

Transcriptome Analysis Provides Insights Into the Adaptive Responses to Hypoxia of a Schizothoracine Fish (<i>Gymnocypris eckloni</i>).

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