Molecular mechanisms of continuous light inhibition of Atlantic salmon parr–smolt transformation

Abstract

Atlantic salmon (Salmo salar) rely on changes in photoperiod for the synchronization of the developmental events constituting the parr–smolt transformation. In the absence of photoperiod cues, parr–smolt transformation is incomplete, and such ‘pseudo-smolts’ normally fail to adapt to seawater. The present study addresses the endocrine and molecular mechanisms controlling the development of hypo-osmoregulatory ability and how artificial photoperiod can disrupt these changes. Juvenile Atlantic salmon reared under constant light (LL) from first feeding, were separated into two groups, and exposed to either LL or simulated natural photoperiod (LDN) from October, eight months prior to the expected completion of smoltification. Juveniles reared on LL grew well, but failed to show the smolt-related reduction in condition factor in spring. Gill mRNA levels of Na+, K+–ATPase (NKA) isoform α1a decreased in LDN fish through completion of parr–smolt transformation, while levels remained unchanged in the LL group. In contrast, α1b expression increased 6-fold in the LDN group between February and May, again with no change in the LL group. Further, Na+, K+, 2Cl− co-transporter (NKCC) showed a transient increase in expression in smolts on LDN between February and May, while no changes in mRNA levels were seen in juveniles under LL. Consequently, gill NKA activity and NKA α and NKCC protein abundance were significantly lower in juveniles on LL than in smolts on LDN. LL fish in spring had lower circulating levels of thyroid hormones (THs), growth hormone (GH) and cortisol. Gill GH-receptor mRNA levels, determined by quantitative PCR, were less than 50% of controls. In contrast, circulating levels of IGF-1 and gill IGF-1 receptor expression, were comparable to controls. Our findings show that continuous light prevents the completion of parr–smolt transformation at a very basic level, disrupting the natural up-regulation of key elements of the endocrine system involved in the regulation of the parr–smolt transformation, and consequently inhibiting the smoltification-related increase in expression, abundance and activity of gill ion transport proteins.