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The advent of CO2 biomitigation with microalgae re-fuelled the interest to CO2-tolerant microalgae. The rare extremely CO2-tolerant microalgae known so far are free-living species. Assuming that symbiotic microalgae are naturally tolerant to CO2 (due to their animal host respiration, especially during polar night), we studied the chlorophyte Desmodesmus sp. 3Dp86E-1 isolated from the hydroid Dynamena pumila (White Sea). As far as we know, this is the first report on high CO2-tolerance of symbiotic chlorophytes. We studied the effects of CO2 (atmospheric–100 vol.%; 1 v/v/min) in bubbling gas mixture on the growth, photosynthetic performance (chlorophyll PAM fluorometry, O2 evolution rate), pigments (HPLC) and fatty acid (GC/MS) in the microalga under batch (9 days) or semi-continuous cultivation conditions at PAR irradiances ranging from limiting to saturating (40–240 µE/m2/s). The Desmodesmus thrived even at extremely high CO2 (up to 100%) levels maintaining the favorable pH (~8) of the medium. The gas mixture containing 20% CO2 was chosen for the routine experiments as more relevant to biomitigation of CO2 from flue gases. Under 20% CO2 and in the absence of light limitation, the Desmodesmus displayed higher biomass accumulation and correspondingly higher photosynthetic performance and CO2 assimilation rates in comparison with the cultures grown at the atmospheric CO2 level. No adverse changes in the cell ultrastructure were found at the elevated CO2; cell compartments serving as carbon sinks displayed a moderate increase. Collectively, Desmodesmus sp. 3Dp86E-1 is a promising candidate for biomitigation of CO2. Its high CO2 tolerance is obviously achieved via robust pH homeostasis, rapid acclimation of the photosynthetic apparatus (increase of cyclic electron transport around PSI), the capability of swift CCM (carbon concentrating mechanisms) shutdown, and channelling the excessively fixed carbon to structural components. Generally, symbiotic microalgae deserve close attention as a promising source of highly CO2-tolerant isolates for biomitigation applications.