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Multi-Omics Sequencing Provides Insights Into Age-Dependent Susceptibility of Grass Carp (Ctenopharyngodon idellus) to Reovirus.

ABSTRACT: Grass carp (Ctenopharyngodon idellus) is an important aquaculture species in China that is affected by serious diseases, especially hemorrhagic disease caused by grass carp reovirus (GCRV). Grass carp have previously shown age-dependent susceptibility to GCRV, however, the mechanism by which this occurs remains poorly understood. Therefore, we performed transcriptome and metabolome sequencing on five-month-old (FMO) and three-year-old (TYO) grass carp to identify the potential mechanism. Viral challenge experiments showed that FMO fish were susceptible, whereas TYO fish were resistant to GCRV. RNA-seq showed that the genes involved in immune response, antigen presentation, and phagocytosis were significantly upregulated in TYO fish before the GCRV infection and at the early stage of infection. Metabolome sequencing showed that most metabolites were upregulated in TYO fish and downregulated in FMO fish after virus infection. Intragroup analysis showed that arachidonic acid metabolism was the most significantly upregulated pathway in TYO fish, whereas choline metabolism in cancer and glycerophospholispid metabolism were significantly downregulated in FMO fish after virus infection. Intergroup comparison revealed that metabolites from carbohydrate, amino acid, glycerophospholipid, and nucleotide metabolism were upregulated in TYO fish when compared with FMO fish. Moreover, the significantly differentially expressed metabolites showed antiviral effects both in vivo and in vitro. Based on these results, we concluded that the immune system and host biosynthesis and metabolism, can explain the age-dependent viral susceptibility in grass carp.

SUBMITTER: He L

PROVIDER: S-EPMC8247658 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundMyxovirus resistance (Mx) proteins are crucial effectors of the innate antiviral response against a wide range of viruses, mediated by the type I interferon (IFN-I) signaling pathway. However, the antiviral activity of Mx proteins is diverse and complicated in different species.Methodology/principal findingsIn the current study, two novel Mx genes (CiMx1 and CiMx3) were identified in grass carp (Ctenopharyngodon idella). CiMx1 and CiMx3 proteins exhibit high sequence identity (92.1%), and low identity with CiMx2 (49.2% and 49.5%, respectively) from the GenBank database. The predicted three-dimensional (3D) structures are distinct among the three isoforms. mRNA instability motifs also display significant differences in the three genes. The spatial and temporal expression profiles of three C. idella Mx genes and the IFN-I gene were investigated by real-time fluorescence quantitative RT-PCR (qRT-PCR) following infection with grass carp reovirus (GCRV) in vivo and in vitro. The results demonstrated that all the four genes were implicated in the anti-GCRV immune response, that mRNA expression of Mx genes might be independent of IFN-I, and that CIK cells are suitable for antiviral studies. By comparing expression patterns following GCRV challenge or poly(I:C) treatment, it was observed that GCRV blocks mRNA expression of the four genes. To determine the functions of Mx genes, three CiMx cDNAs were cloned into expression vectors and utilized for transfection of CIK cells. The protection conferred by each recombinant CiMx protein against GCRV infection was evaluated. Antiviral activity against GCRV was demonstrated by reduced cytopathic effect, lower virus titer and lower levels of expressed viral transcripts. The transcription of IFN-I gene was also monitored.Conclusions/significanceThe results indicate all three Mx genes can suppress replication of grass carp reovirus and over-expression of Mx genes mediate feedback inhibition of the IFN-I gene.

Project description:BackgroundThe ultrahigh density intensive farming model of grass carp (Ctenopharyngodon idellus) may elicit growth inhibition, decrease flesh quality, and increase disease susceptibility of fish. The degradation in quality and excessive fat accumulation in cultured C. idellus have long been attributed to possible alterations in the lipid metabolism of fish muscle tissues as a result of overnutrition from artificial diets. To investigate the effects of different diets on fish muscle quality, a large-scale metabolomics study was performed on 250 tails of C. idellus.FindingsThe experimental fish were divided into four groups based on sex and diet-female artificial feed (FAF), female grass feed, male artificial feed (MAF), and male grass feed (MGF). After a 113-day rearing period, the artificial feed (AF) group showed a significantly higher total mass of muscle fat (P < 0.01), with the FAF group being the highest. Metabolomics profiling based on liquid chromatography-mass spectrometry revealed distinctive patterns of clustering according to the four groups. Overall, artificial feeding was associated with higher concentrations of docosapentaenoic acid, dihomo-gamma-linolenic acid, and arachidonic acid, whereas grass feeding was associated with elevated n-3 unsaturated fatty acids (UFAs) such as eicosapentaenoic acid, alpha-linolenic acid, and gamma-linolenic acid. Artificial feeding also resulted in significant increased docosahexaenoic acid in MAF muscle than in MGF fish, whereas there was no significance in the comparison of female samples. Metabolic pathway analyses using both targeted and untargeted approaches consistently revealed that arachidonic acid metabolism and steroid hormone biosynthesis pathways were significantly different between AF and grass fed groups.ConclusionsOur results suggest that grass is a better source of dietary fatty acid and protein when compared to artificial feed. Grass feeding could effectively lower triglycerides in serum, reduce fat accumulation, and alter lipid compositions in fish muscle by increasing the concentrations of n-3 UFAs, leading to better nutrition and health.

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Multi-Omics Sequencing Provides Insights Into Age-Dependent Susceptibility of Grass Carp (Ctenopharyngodon idellus) to Reovirus.

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