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      Development of Atlantic Salmon (Salmo salar L.) Under Hypoxic Conditions Induced Sustained Changes in Expression of Immune Genes and Reduced Resistance to Moritella viscosa

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          Abstract

          Atlantic salmon is characterized with high sensitivity to low dissolved oxygen (DO) levels. Hypoxia can affect diverse biological processes with consequences that can be manifested immediately or with delay. Effects of hypoxia on the immune system and the resistance to a bacterial pathogen were investigated. Two groups were reared at, respectively, normal (NO, 80–100%) and low (LO, 60%) levels of DO over 10 months after which both groups were reared at NO. Smoltification was initiated after 13 months by a winter signal for 6 weeks, followed by constant light for 6 weeks. Samples were collected at the start and end of the constant light period. Expression of 92 immune and stress genes was analyzed in the gill, head kidney, and spleen using a Biomark HD. Most of differentially expressed genes showed higher levels in LO fish compared to NO fish; many immune genes were downregulated during smoltification and these changes were stronger in NO fish. A notable exception was pro-inflammatory genes upregulated in gill of NO fish. Further, salmon were challenged with Moritella viscosa, the causative agent of winter ulcer. Mortality was registered from 5 days post infection (dpi) to the end of trial at 36 dpi. Survival was consistently higher in NO than LO fish, reaching a maximum difference of 18% at 21–23 dpi that reduced to 10% at the end. Analyses with a genome-wide microarray at 36 dpi showed strong responses to the pathogen in gill and spleen. Notable features were the stimulation of eicosanoid metabolism, suggesting an important role of lipid mediators of inflammation, and the downregulation of chemokines. Many immune effectors were activated, including multiple lectins and acute phase proteins, enzymes producing free radicals, and matrix metalloproteinases. The transcriptomic changes induced with a bacterial challenge were similar in NO and LO. After the challenge, interferons a and g and panel of genes of innate antiviral immunity showed higher expression in LO, especially in the gill. The results from the present study suggest that chronic hypoxia in early life stimulated immune genes and attenuated their downregulation associated with smoltification. However, these changes did not improve protection against a bacterial pathogen of major concern in salmon aquaculture.

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          Most cited references44

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          Metabolic rate, social status and life-history strategies in Atlantic salmon

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            Minimal Dissolved Oxygen Requirements of Aquatic Life with Emphasis on Canadian Species: a Review

            John Davis (1975)
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              Hypoxia causes transgenerational impairments in reproduction of fish

              Hypoxia is amongst the most widespread and pressing problems in aquatic environments. Here we demonstrate that fish (Oryzias melastigma) exposed to hypoxia show reproductive impairments (retarded gonad development, decrease in sperm count and sperm motility) in F1 and F2 generations despite these progenies (and their germ cells) having never been exposed to hypoxia. We further show that the observed transgenerational reproductive impairments are associated with a differential methylation pattern of specific genes in sperm of both F0 and F2 coupled with relevant transcriptomic and proteomic alterations, which may impair spermatogenesis. The discovered transgenerational and epigenetic effects suggest that hypoxia might pose a dramatic and long-lasting threat to the sustainability of fish populations. Because the genes regulating spermatogenesis and epigenetic modifications are highly conserved among vertebrates, these results may also shed light on the potential transgenerational effects of hypoxia on other vertebrates, including humans.
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                Author and article information

                Journal
                Frontiers in Ecology and Evolution
                Front. Ecol. Evol.
                Frontiers Media SA
                2296-701X
                August 2 2021
                August 2 2021
                : 9
                Article
                10.3389/fevo.2021.722218
                f1ccd982-c53a-4484-b855-197ce3554ee4
                © 2021

                Free to read

                https://creativecommons.org/licenses/by/4.0/

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