Photoperiodic history modulates the response of the saccus vasculosus transcriptome to seawater exposure in Atlantic salmon

Atlantic salmon (Salmo salar) move from fresh- to seawater environments following a seasonally timed preparative transition called smoltification, which takes place under photoperiodic control in the freshwater environment. In masu salmon (Oncorhynchus masou), coordination of photoperiodic sexual maturation is proposed to involve in a fish-specific circumventricular organ, the saccus vasculosus (SV), through its intrinsic opsin-based light sensitivity, thyrotrophin secretion and modulation of deiodinase activity (TSH-DIO cascade). The saccus vasculosus is a highly vascularized structure located on the ventral side of the hypothalamus and its interface between the blood and cerebrospinal fluid also hints at a role in ionic balance of the cerebrospinal fluid (CSF). Both the potential photoperiodic and ionic functions of the SV led us to perform transcriptome analysis of the SV in smoltification in Atlantic salmon. Specifically, we compared transcriptomes of SVs collected from freshwater fish following exposure to an 8-week stimulated winter photoperiod followed by 8-week simulated summer photoperiod, or a 16-week simulated winter photoperiod control and from both photoperiod treatments after 24 h exposure to seawater. Our data show that SV response to seawater exposure is highly dependent on photoperiodic history and identifies ependymin as a major secretory output of the SV, consistent with a role in control of CSF composition. Conversely, we could not detect crucial elements of the opsin-TSH-DIO cascade suggesting that the photoperiodic history-dependence of the SV to seawater exposure is unlikely to stem from SV-intrinsic responses to photoperiod.