A thylakoid-located carbonic anhydrase regulates CO2 uptake in the cyanobacterium Synechocystis sp. PCC 6803.

Carbonic anhydrases (CAs) are involved in CO2 uptake and conversion, a fundamental process in photosynthetic organisms. Nevertheless, the mechanism underlying the regulation of CO2 uptake and intracellular conversion in cyanobacteria is largely unknown. We report the characterization of a previously unrecognized thylakoid-located CA Slr0051 (EcaB) from the cyanobacterium Synechocystis sp. PCC 6803, which possesses CA activity to regulate CO2 uptake. Inactivation of ecaB stimulated CO2 hydration in the thylakoids, suppressed by the classical CA inhibitor acetazolamide. Absence of ecaB increased the reduced state of the photosynthetic electron transport system, lowered the rate of photosynthetic O2 evolution at high light (HL) and pH, and decreased the cellular affinity for extracellular inorganic carbon. Furthermore, EcaB was upregulated in cells grown at limiting CO2 concentration or HL in tandem with CupA. EcaB is mainly located in the thylakoid membranes where it interacts with CupA and CupB involved in CO2 uptake by converting it to bicarbonate. We propose that modulation of the EcaB level and activity in response to CO2 changes, illumination or pH reversibly regulates its conversion to HCO3 by the two CO2 -uptake systems (CupA, CupB), dissipating the excess HCO3- and alleviating photoinhibition, and thereby optimizes photosynthesis, especially under HL and alkaline conditions.