Central Transcriptional Regulator Controls Growth and Carbon Storage under High Light Stress in Photosynthetic Microalgae Model Strains

Carbon capture efficiency and storage are some of the primary drivers of photosynthetic productivity and by extension crop yield. To elucidate the mechanisms governing yield phenotypes and carbon allocation regulatory elements, we selected two microalgae strains as simplified models of photosynthetic crops. The Picochlorum celeri TG2 isolate is one of the fastest growing (specific growth rate) algae and in this work is juxtaposed to a closely related, slower growing, isolate, TG1, of the same species with less than 2% genomic divergence. Through the application of comprehensive systems biology light-stress response study, we observed a stark difference in carbon assimilation and storage rates, with the slower growing isolate accumulating almost three times the amount of starch compared to the fast-growing isolate. We characterized the carbon storage rates and allocation dynamics, with metabolic bottlenecks, and transport rates of intermediates underlying the variations in growth and composition in high light using instationary 13C-fluxomics experiments. High light stress analysis of transcriptomic dynamics during acclimation of the strains from low to high light identified widespread response with up to 73% the annotated gene set significantly differentially expressed after only 1 hour. Broad transcriptional regulatory control was inferred by a rapid depletion of a global diel-responsive transcription factor closely related to a circadian-regulator in plants, as the single most distinct transcription factor. Transferring this factor to the slower variant increased yield, specific growth rate, and carbohydrate accumulation of the selected engineered strain, providing further evidence for a coordinating regulatory mechanism for this complex phenotype.