Photoperiod-dependent developmental reprogramming of the transcriptional response to seawater entry in Atlantic salmon (Salmo salar)

The developmental transition of juvenile salmon from a freshwater resident morph (parr) to a seawater (SW) migratory morph (smolt), known as smoltification, entails a reorganization of gill function to cope with the altered water environment. Recently, we used RNAseq to characterize the breadth of transcriptional change which takes place in the gill in the FW phase of smoltification. This highlighted the importance of extended exposure to short, winter-like photoperiods (SP) followed by a subsequent increase in photoperiod for completion of transcriptional reprogramming in FW and for efficient growth following transfer to SW. Here, we extend this analysis to examine the consequences of this photoperiodic history-dependent reprogramming for subsequent gill responses upon exposure to SW. We use RNAseq to analyse gill samples taken from fish raised on the photoperiod regimes we used previously and then challenged by SW exposure for 24-h. While fish held on constant light (LL) throughout were able to hypo-osmoregulate during a 24-h SW challenge, the associated gill transcriptional response was highly distinctive from that in fish which had experienced an 7 week period of exposure to SP followed by a return to LL (SPLL) and had consequently acquired the characteristics of fully developed smolts. Fish transferred from LL to SP, and then held on SP for the remainder of the study were unable to hypo-osmoregulate, and the associated gill transcriptional response to SW exposure featured many transcripts apparently regulated by the glucocorticoid stress axis and by the osmo-sensing transcription factor NFAT5. The importance of these pathways for the gill transcriptional response to SW exposure appears to diminish as a consequence of photoperiod mediated induction of the smolt phenotype, presumably reflecting preparatory developmetal changes taking place during this process.

Effects of freshwater hyperoxia and hypercapnia and their influences on subsequent seawater transfer in Atlantic salmon (Salmo salar) smolts

Atlantic salmon (Salmo salar) presmolts, smolts, and postsmolts compensate for a respiratory acidosis associated with 96 h of exposure to hyperoxia (100% O2; hO2), hypercapnia (2% CO2 and 98% air; hCO2), and combined hO2/hCO2 in freshwater (FW) by increasing strong ion difference, predominantly through a reduction in plasma [Cl-] (presumably via branchial Cl-/HCO3- exchange). In smolts, compensation during hO2 or hCO2 occurred within 24 h, whereas that in combined hO2/hCO2 was much slower, resulting in 33% mortality by 96 h. FW hO2 and combined hO2/hCO2 appeared to impair gill function, likely through oxidative cell damage. This resulted in reduced hypoosmoregulatory ability following subsequent transfer to seawater (SW), as indicated by changes in plasma ion levels, osmolality, and muscle water content, resulting in considerable mortalities. Interestingly, FW hCO2 appeared to enhance hypoosmoregulatory ability during subsequent SW transfer. Smolts are often transported from FW to a subsequent SW release site, and these data indicate that care should be taken to minimize the degree of hyperoxia experienced by the smolts. Hypercapnia, which results from metabolic CO2 production and inadequate water aeration, does not impair SW transfer, provided it does not occur in conjunction with hyperoxia.