A subpopulation of aquaculture salmon are characterized by abnormal swimming behavior, growth stunting and anorexia, as well as chronically elevated cortisol and brain serotonergic levels. This profile is associated with a depression-like state (DLS) and these fish are unable to respond to further stressors. Whereas the underlying causes behind this phenomenon remain elusive, the physiological profile strongly suggests that chronic stress plays a significant role in this phenomenon. We subjected Atlantic salmon to a chronic stress regime consisting of incremental increases in environmental CO2 concentrations during the freshwater phase for 68 days. Plasma corticosteroids, brain stem, hypothalamic and telencephalic serotonin concentrations and telencephalic whole transcriptome expression were then assessed under basal and acute stress conditions. We found that fish exposed to increased CO2 were characterized by a long-term increase in cortisol, cortisol+cortisone and serotonin (5-HT) signaling in the brain stem. Furthermore, in response to an acute confinement stressor, the CO2-treated fish increased their levels of cortisol and cortisol+cortisone, and decreased their cortisone/cortisol ratio. But unlike the control fish, they were unable to also respond to confinement by increased 5-HT signaling in the brain stem. In terms of their transcriptional response, post-stress gene regulation in CO2-treated fish was the opposite of that observed in control fish. We believe this profile is an example of allostatic overload, characterized by the inability to cope with stress. This profile is associated with DLS, suggesting that chronic stress may be an important factor leading to the development of the DLS phenotype in salmon.

Author contributions

Conceptualization: Ø.Ø., T.S.K., E.H.; Data curation: M.A.V., I.B.J.; Formal analysis: M.A.V., J.A.; Funding acquisition: O.F., J.A., Ø.Ø., J.N., I.B.J., T.S.K., E.H.; Investigation: M.A.V., O.F., J.N.; Methodology: M.A.V., J.A., J.N.; Project administration: T.S.K., E.H.; Resources: O.F., J.A., I.B.J.; Validation: M.A.V.; Writing – original draft: M.A.V.; Writing – review & editing: O.F., J.A., Ø.Ø., J.N., I.B.J., T.S.K., E.H.

Funding

This study was financed by the Norges Forskningsråd grant no. 267788/E40.

Data and resource availability

All relevant data can be found within the article and its supplementary information. The data for the RNAseq fastq files can be accessed at the Sequence Read Archive with accession number: PRJNA1271312 (http://www.ncbi.nlm.nih.gov/bioproject/1271312).

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