Nonvisual light regulation of biological rhythm and life history transformation

Biological rhythms are largely controlled by changes in light throughout the day and throughout the year. The organism uses these rhythms to synchronize biological processes to the time of the day or periods of the year. Atlantic salmon is a good model for studying how light regulates biological rhythms, especially seasonal rhythms since its life history is largely regulated by season, e.g. smoltification and reproduction. Melatonin, which is secreted from the pineal organ, is the central hormone that regulates both circadian and seasonal rhythms. In fish, the pineal organ is directly photoreceptive, but little is known about the photoreceptive mechanisms that regulate melatonin production. In this project, the photoreceptive capacity of the eye and pineal organ of Atlantic salmon is mapped. The results of the project show that the pineal organ's ability to perceive light is based on several extraretinal photoreceptors, some of which indicate that the organ can perceive several parts of the light spectrum. Smoltification is the physiological changes that adapt the salmon to seawater from freshwater and many studies have shown that this process is regulated by photoperiod (from a short day (winter) to a long day (spring)). In this project, photoreceptors that regulate smoltification are mapped, both through histological analyses of the pineal organ and gene editing. Verifying the photoreceptor system that regulates the melatonin level and smoltification, gives insight into how light regulates seasonally driven biological processes.

The Earth rotation and orbit around the sun, produce two fundamental light rhythmicity, a daily and annual oscillation, that have shaped the biology. Much is known with regards to circadian regulation, however, there is a significant lack of information with relation to annual biological rhythms. Nonetheless, in recent decades, there has been major advancements in our understanding of how some photoperiodic circannual rhythms are integrated into the endocrine system of mammals and birds; yet similar mechanisms in fishes have yet to be elucidated. Melatonin is the main hormonal output of the pineal organ and is involved in the control of daily rhythms; however, the activation of the pineal nonvisual sensor, and the daily and circannual entrainment of melatonin production are far less studied. We propose to functionally characterise the master circadian mediator of light in the pineal organ, exo-rhodopsin (exo-rod), by using innovative gene-editing (CRISPR-Cas9) techniques, to verify its physiological role in melatonin regulation and control of the life history transition of Atlantic salmon smoltification. This transformation is highly regulated by the photoperiod and can easily be induced synchronously at the parr stage by photo period. The ability to induce a seasonally-driven biological process provides a unique opportunity to investigate the molecular pathways that regulate this event. Advanced spectral activation (LEDs) will be employed to characterise the spectral environment regulating the melatonin pathway. Investigation of exo-rod, together with all 11 visual pigments in the retina, is critical in interpreting the spectral profile that drives circadian and circannual (melatonin) rhythms. This knowledge will be used to create a light environment that triggers nocturnal melatonin production and regulate circannual smoltification. Defining the spectral environment that decouples melatonin rhythms and vision is relevant for diminishing effects of light pollution.