Mitochondrial-Driven Bicarbonate Transport Supports Photosynthesis in a Marine Microalga

Abstract

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 CO2efflux using H13CO3 − stable isotope techniques. H13CO3 −pump-13CO2 leak activity of the CCM was unaffected by 10 μm3(3,4-dichlorophenyl)-1,1-dimethylurea, an inhibitor of chloroplast linear electron transport, although photosynthetic O2evolution 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.