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.
Highlights
Salmonid species are evolutionarily adapted to pristine habitats with cold water and are characterized with high oxygen requirements and sensitivity to oxygen deficiency (Davis, 1975; Metcalfe et al, 1995; Remen et al, 2013)
There is a constantly growing interest regarding the effects of hypoxia on the development, performance, and robustness of Atlantic salmon, which is associated with the expanding use of recirculation aquaculture systems (RAS) in commercial aquaculture and expected climate change leading to an increase of water temperature in the sea
The expression profiles of immune and stress genes in the lymphatic organs and gill were overall similar the numbers and composition of differentially expressed genes (DEG) varied (Figures 2, 3)
Summary
Salmonid species are evolutionarily adapted to pristine habitats with cold water and are characterized with high oxygen requirements and sensitivity to oxygen deficiency (Davis, 1975; Metcalfe et al, 1995; Remen et al, 2013). There is a constantly growing interest regarding the effects of hypoxia on the development, performance, and robustness of Atlantic salmon, which is associated with the expanding use of RAS in commercial aquaculture and expected climate change leading to an increase of water temperature in the sea. Many recent publications have addressed direct and remote consequences of low oxygen levels on Atlantic salmon with the observed effects ranging from complete recovery to significant changes. Cyclic hypoxia over 23 days with DO levels of 70% and below significantly reduced feed intake in postsmolts (Remen et al, 2012), and a 120 day exposure to low oxygen levels in large (1.5–2 kg) post-smolts showed a significant reduction in growth performance, and gene expression of liver tissue indicated clear effects of hypoxia on metabolic and protein catabolic pathways (Olsvik et al, 2013). Exposure to hypoxia from fertilization until start feeding did not appear to influence tolerance to hypoxia later in life (Wood et al, 2019, 2020)
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