Deep-coverage spatiotemporal proteome of the picoeukaryote Ostreococcus tauri reveals differential effects of environmental and endogenous 24-hour rhythms

The cellular landscape changes dramatically over the course of a 24 h day. The proteome responds directly to daily environmental cycles and is additionally regulated by the circadian clock. To quantify the relative contribution of diurnal versus circadian regulation, we mapped proteome dynamics under light:dark cycles compared with constant light. Using Ostreococcus tauri, a prototypical eukaryotic cell, we achieved 85% coverage, which allowed an unprecedented insight into the identity of proteins that facilitate rhythmic cellular functions. The overlap between diurnally- and circadian-regulated proteins was modest and these proteins exhibited different phases of oscillation between the two conditions. Transcript oscillations were generally poorly predictive of protein oscillations, in which a far lower relative amplitude was observed. We observed coordination between the rhythmic regulation of organelle-encoded proteins with the nuclear-encoded proteins that are targeted to organelles. Rhythmic transmembrane proteins showed a different phase distribution compared with rhythmic soluble proteins, indicating the existence of a circadian regulatory process specific to the biogenesis and/or degradation of membrane proteins. Our observations argue that the cellular spatiotemporal proteome is shaped by a complex interaction between intrinsic and extrinsic regulatory factors through rhythmic regulation at the transcriptional as well as post-transcriptional, translational, and post-translational levels. Holly Kay, Ellen Grunewald, et al. provide an in-depth examination of the proteome in the eukaryotic green alga, Ostreococcus tauri, under circadian constant light or cycling diurnal light-dark conditions. They observe that there is little overlap between mRNA and protein expression rhythms, or the diurnal and circadian proteome, suggesting that the cellular spatiotemporal proteome is shaped through rhythmic regulation at multiple stages of transcription and translation.

Automated summary

The cellular landscape undergoes significant changes over a 24-hour period, with the proteome responding directly to daily environmental cycles and being regulated by the circadian clock. Research suggests that transcript oscillations are not strong predictors of protein oscillations, indicating that the cellular spatiotemporal proteome is shaped by rhythmic regulation at various stages of transcription and translation.