Metabolic Flexibility Underpins Growth Capabilities of the Fastest Growing Alga

The factors rate-limiting growth of photosynthetic organisms under optimal conditions are controversial [1–8]. Adaptation to extreme environments is usually accompanied by reduced performance under optimal conditions [9, 10]. However, the green alga Chlorella ohadii, isolated from a harsh desert biological soil crust [11–17], does not obey this rule. In addition to resistance to photodamage [17, 18], it performs the fastest growth ever reported for photosynthetic eukaryotes. A multiphasic growth pattern (very fast growth [phase I], followed by growth retardation [phase II] and additional fast growth [phase III]) observed under constant illumination and temperature indicates synchronization of the algal population. Large physiological changes at transitions between growth phases suggest metabolic shifts. Indeed, metabolome analyses at points along the growth phases revealed large changes in the levels of many metabolites during growth with an overall rise during phase I and decline in phase II. Multivariate analysis of the metabolome data highlighted growth phase as the main factor contributing to observed metabolite variance. The analyses identified putrescine as the strongest predictive metabolite for growth phase and a putative growth regulator. Indeed, extracellular additions of polyamines strongly affected the growth rate in phase I and the growth arrest in phase II, with a marked effect on O2 exchange. Our data implicate polyamines as the signals harmonizing metabolic shifts and suggest that metabolic flexibility enables the immense growth capabilities of C. ohadii. The data provide a new dimension to current models focusing on growth-limiting processes in photosynthetic organisms where the anabolic and catabolic metabolisms must be strictly regulated. •Multiphasic growth is observed in the desert-inhabiting green alga Chlorella ohadii•Metabolic shifts mediate transition between growth phases•Polyamines serve as surveillance molecules coordinating metabolism and growth rate•Metabolic flexibility is key to unparalleled growth rate in this new model alga The processes which rate limit growth of photosynthetic organisms, where anabolic and catabolic metabolisms must be strictly regulated, are still controversial. Treves et al. show that metabolic flexibility in a desert green alga enables its unparalleled growth rate, providing a new dimension to current models, with polyamines playing a key role.