The unparalleled performance of Chlorella ohadii under irradiances of twice-full sun light underlines that we lack essential information on how the photosynthetic machinery operates and what sets its upper functional limit. Rather than succumbing to photodamage, C. ohadii undergoes major structural and compositional changes pointing to unique features of PSII function, and exhibiting highly efficient utilization of reductants downstream of the photosynthetic reaction centers. This remarkable resistance allowed us to investigate, for the first time, the systems response of photosynthesis and growth to extreme illumination in a metabolically active cell. Using redox proteomics, transcriptomics, metabolomics and lipidomics, we explored the cellular mechanisms underlying inorganic carbon concentration, excess redox dissipation, protein S-glutathionylation, lipid and starch accumulation and increased thylakoid stacking. Frequently, the response in C. ohadii deviated from those reported in model species, reflecting its life history in desert sand crusts. It exhibited a readily available metabolic capacity to utilize a sudden excess of reducing power to support growth and reserve formation. Redox regulation played a pivotal role in this very rapid acclimation process. Comparative global and case-specific analyses, provided insights into the potential evolutionary role of effective reductant utilization in the extreme resistance of C. ohadii to photoinhibition.