Circadian clock helps cyanobacteria manage energy in coastal and high latitude ocean

The circadian clock coordinates cellular functions over the diel cycle in many organisms. The molecular mechanisms of the cyanobacterial clock are well characterized, but its ecological role remains a mystery. We present an agent-based model of Synechococcus (harboring a self-sustained, bona fide circadian clock) that explicitly represents genes (e.g., kaiABC), transcripts, proteins, and metabolites. The model is calibrated to data from laboratory experiments with wild type and no-clock mutant strains, and it successfully reproduces the main observed patterns of glycogen metabolism. Comparison of wild type and no-clock mutant strains suggests a main benefit of the clock is due to energy management. For example, it inhibits glycogen synthesis early in the day when it is not needed and energy is better used for making the photosynthesis apparatus. To explore the ecological role of the clock, we integrate the model into a dynamic, three-dimensional global circulation model that includes light variability due to seasonal and diel incident radiation and vertical extinction. Model output is compared with field data, including in situ gene transcript levels. We simulate cyanobaceria with and without a circadian clock, which allows us to quantify the fitness benefit of the clock. Interestingly, the benefit is weakest in the low latitude open ocean, where Prochlorococcus (lacking a self-sustained clock) dominates. However, our attempt to experimentally validate this testable prediction failed. Our study provides insights into the role of the clock and an example for how models can be used to integrate across multiple levels of biological organization.