Environmental and Circadian Regulation Combine to Shape the Rhythmic Selenoproteome

Abstract

The circadian clock orchestrates an organism’s endogenous processes with environmental 24 h cycles. Redox homeostasis and the circadian clock regulate one another to negate the potential effects of our planet’s light/dark cycle on the generation of reactive oxygen species (ROS) and attain homeostasis. Selenoproteins are an important class of redox-related enzymes that have a selenocys-teine residue in the active site. This study reports functional understanding of how environmental and endogenous circadian rhythms integrate to shape the selenoproteome in a model eukaryotic cell. We mined quantitative proteomic data for the 24 selenoproteins of the picoeukaryote Ostreococcus tauri across time series, under environmentally rhythmic entrained conditions of light/dark (LD) cycles, compared to constant circadian conditions of constant light (LL). We found an overrepresentation of selenoproteins among rhythmic proteins under LL, but an underrepresentation under LD conditions. Rhythmic selenoproteins under LL that reach peak abundance later in the day showed a greater relative amplitude of oscillations than those that peak early in the day. Under LD, amplitude did not correlate with peak phase; however, we identified high-amplitude selenium uptake rhythms under LD but not LL conditions. Selenium deprivation induced strong qualitative defects in clock gene expression under LD but not LL conditions. Overall, the clear conclusion is that the circadian and environmental cycles exert differential effects on the selenoproteome, and that the combination of the two enables homeostasis. Selenoproteins may therefore play an important role in the cellular response to reactive oxygen species that form as a consequence of the transitions between light and dark.