Feedforward non-Michaelis–Menten mechanism for CO2 uptake by Rubisco: Contribution of carbonic anhydrases and photorespiration to optimization of photosynthetic carbon assimilation

Rubisco, the most abundant protein serving as the primary engine generating organic biomass on Earth, is characterized by a low catalytic constant (in higher plants approx. 3 s−1) and low specificity for CO2 leading to photorespiration. We analyze here why this enzyme evolved as the main carbon fixation engine. The high concentration of Rubisco exceeding the concentration of its substrate CO2 by 2–3 orders of magnitude makes application of Michaelis–Menten kinetics invalid and requires alternative kinetic approaches to describe photosynthetic CO2 assimilation. Efficient operation of Rubisco is supported by a strong flux of CO2 to the chloroplast stroma provided by fast equilibration of bicarbonate and CO2 and forwarding the latter to Rubisco reaction centers. The main part of this feedforward mechanism is a thylakoidal carbonic anhydrase associated with photosystem II and pumping CO2 from the thylakoid lumen in coordination with the rate of electron transport, water splitting and proton gradient across the thylakoid membrane. This steady flux of CO2 limits photosynthesis at saturating CO2 concentrations. At low ambient CO2 and correspondingly limited capacity of the bicarbonate pool in the stroma, its depletion at the sites of Rubisco is relieved by utilizing O2 instead of CO2, i.e. by photorespiration, a process which supplies CO2 back to Rubisco and buffers the redox state and energy level in the chloroplast. Thus, the regulation of Rubisco function aims to keep steady non-equilibrium levels of CO2, NADPH/NADP and ATP/ADP in the chloroplast stroma and to optimize the condition of homeostatic photosynthetic flux of matter and energy.