Plant Physiol, September 2002, Vol. 130, pp. 284-291

Mitochondrial-Driven Bicarbonate Transport Supports Photosynthesis in a Marine Microalga¹

Department of Biology, York University, 4700 Keele Street, Toronto, Ontario, Canada M3J 1P3 (I.E.H., B.C.); and Department of Botany, University of Toronto, 3359 Mississauga Road, Mississauga, Ontario, Canada L5L 1C6 (I.E.H., G.S.E.)

The CO₂-concentrating mechanism (CCM) of the marine eustigmatophycean microalga Nannochloropsis gaditana consists of an active HCO₃ transport system and an internal carbonic anhydrase to facilitate accumulation and conversion of HCO₃ to CO₂ for photosynthetic fixation. Aqueous inlet mass spectrometry revealed that a portion of the CO₂ generated within the cells leaked to the medium, resulting in a significant rise in the extracellular CO₂ concentration to a level above its chemical equilibrium that was diagnostic for active HCO₃ transport. The transient rise in extracellular CO₂ occurred in the light and the dark and was resolved from concurrent respiratory CO₂ efflux using H¹³CO₃ stable isotope techniques. H¹³CO₃ pump-¹³CO₂ leak activity of the CCM was unaffected by 10 µM 3(3,4-dichlorophenyl)-1,1-dimethylurea, an inhibitor of chloroplast linear electron transport, although photosynthetic O₂ evolution was reduced by 90%. However, low concentrations of cyanide, azide, and rotenone along with anoxia significantly reduced or abolished ¹³CO₂ efflux in the dark and light. These results indicate that H¹³CO₃ transport was supported by mitochondrial energy production in contrast to other algae and cyanobacteria in which it is supported by photosynthetic electron transport. This is the first report of a direct role for mitochondria in the energization and functioning of the CCM in a photosynthetic organism.