An undiscovered circadian clock to regulate phytoplankton photosynthesis

Abstract Circadian clocks exist in all types of organisms and coordinate key biological processes, e.g. photosynthesis in phytoplankton (microalgae) and land plants. We asked whether a circadian rhythm sustains in phytoplankton when living under constant illumination without environmental cues. Here, we report the first transcriptomic architecture of persistent oscillatory gene expression in the model marine diatom, Phaeodactylum tricornutum living under constant illumination and temperature without environmental cues. We show that cyclic expression of a considerable number of genes involved in light harvesting and carbon fixation sustained after 24 hours of constant illumination (free-running), which could pose additional constraints on cell growth under constant light conditions. Over long-term adaptation to constant illumination, the majority of the rhythmic genes identified under diel light conditions lose their oscillatory expression in the absence of external entrainers, and the genes potentially controlled by persistent circadian clocks are primarily involved in transcriptional regulation and cell division. We find constant illumination leads to an increased average expression of transcription factors and cell division genes, while genes involved in the Calvin-Benson cycle and pigment biosynthesis are kept at low expression levels, which plays a role in the down-regulation of photosynthetic efficiency. By manipulation of the dark rest period, we confirm a fine-tuned light/dark cycle could dramatically improve photosynthetic efficiency in microalgae. Our results unveil a novel persistent circadian rhythm on photosynthetic regulation in marine phytoplankton and provide critical insights into the interaction between environmental signals and inheritable internal circadian clocks in diatoms.