Weak influence of light and time of day on transcriptional response to SAV3 infection in Atlantic salmon (Salmo salar) smolts

Abstract

Seventeen percent of aquaculture Atlantic salmon in Norway die after transfer from freshwater to seawater facilities, many from infectious disease. The degree to which these deaths are attributable to unseen weakness in smolt preparation is therefore an important concern. Strong evidence in mammals and supporting evidence in other teleosts show that the light environment shapes the immune response via entrainment of the circadian clock. These data are alarming as most smoltification protocols use constant light, which does not entrain the circadian clock and is associated with negative survival outcomes to disease challenge in other species. The goal of our study was to establish how different light environments affected the anti-viral immunity of Atlantic salmon smolts. To achieve this goal, we measured the transcriptional response of select type I and type II interferons and major histocompatibility complexes in the heart and head kidney following an intraperitoneal SAV3 viral challenge delivered under different lighting conditions. We began with two hypotheses. First, that compared with a regular light-dark cycle (LP), constant light (LL) would have a weaker resistance to viral challenge in Atlantic salmon smolts. Second, that Atlantic salmon smolts kept in a regular light-dark cycle would have altered immune sensitivity between the light and dark phases. To test our first hypothesis we photostimulated smoltification in parr through exposure to either LP or LL conditions for 6 weeks then challenged them by SAV3 infection. LP and LL groups showed indistinguishable measurements in classical smolt characteristics and comparable levels of SAV3 mRNA in the heart after 8 and 14 days post infection. They also showed comparable transcriptional responses of select type I interferons (IFNa, IFNb, IFNc) and both class I and class II major histocompatibility complexes (MHC I and MHC II) in both heart and head kidney tissue. IFN{gamma} induction in the heart, however, was marked higher in the LL compared to the LP group. While this data suggests a heightened sensitivity or better immune response of the LL group to viral challenge, the consistent induction of MHC II, a key target gene of IFN{gamma} signaling, to SAV3 infection in both LL and LP groups indicates that photoperiod may only have a minor impact on interferon regulation, rather than a more general influence on the viral immune response. To test our second hypothesis, we compared the transcriptomic response in the heart to SAV3 infection delivered either at the mid-light or mid-dark phase in the LP group. Both mid-light and mid-dark groups showed an upregulation of immune related genes and down-regulation of structural genes of mitochondria, but an analysis of the interaction between infection and time of day identified no differentially regulated genes. Overall, our data suggest that, unlike mammals, daily timing of viral infection may not play a major role in the immune response of Atlantic salmon. HighlightsO_LIAtlantic salmon smolts die in large numbers following sea-water transfer in aquaculture C_LIO_LIEvidence in other species suggest that the light environment used in aquaculture contributes to these deaths C_LIO_LIWe find that IFN{gamma} and MHC I induction to a SAV3 infection in the heart is affected by photoperiod C_LIO_LIRNAseq analysis of hearts collected 14 days after PBS or SAV3 treatment, showed no statistical difference in SAV3-mediated gene induction between the light or dark phase. C_LIO_LIOur data suggests that, unlike in mammals, the viral immune response in Atlantic salmon is not affected by the time of day of infection. C_LI