Distribution of Inorganic Carbon Among its Component Species in Cyanobacteria: Do Cyanobacteria in fact Actively Accumulate Inorganic Carbon?

A mathematical model is presented, which describes the distribution of inorganic carbon (Ci) between the species CaCO3, CaHCO3+, CO32−, HCO3−and CO2in the cytosol of a high CO2- requiring mutant of the cyanobacteriumSynechocystisPCC 6803, which lacks carboxysomes. The model assumes that entry and efflux of Ci occurs via a CO32−transport and diffusion of CO2. HCO3−is considered as impermeable. Intracellular Ci is distributed among the species according to the cytoplasmic pH and the calcium concentration. Former models considered entry of HCO3−, and not CO32−, and the intracellular interactions of calcium with CO32−and their implications for the Ci accumulating mechanism were not considered. del predicts that in the presence of 10−3–10−2M calcium, at low and moderate external inorganic carbon concentrations, CaCO3is the main cytoplasmic Ci species, whereas in its absence HCO3−is the main Ci species. Due to sequestration of CO32−by calcium and low permeability of the cells to CO2, the CO2, concentration is low and no net photosynthesis is observed. Photosynthesis is predicted to occur only at external Ci concentrations higher than 1 mM, where the CO32−transport is saturated and the main source of Ci is diffusion of CO2. This converts the mutant to a CO2user with a high photosynthetic Km(CO2), unlike the wild type which utilizes external CO32−as a substrate for photosynthesis at low external concentration. questration of CO32−by Ca2+efficiently reduced the Co32−and the CO2accumulation ratio in comparison with that of total Ci resulting in an inward CO2gradient and reduced CO32−gradient over a wide range of external Ci concentrations. This raises doubts as to whether the transport of Ci as such is an active transport. mulation predicts that in cases where the affinity of the uptake mechanism for CO32−is higher than that measured for this mutant and the accumulation ratio for Ci is consequently higher, the predicted accumulation ratio for the transported species CO32−remains low. Taking the permeability of the cells to gases to be as low as previously measured, the simulation predicts that O2may be accumulated in the cytoplasm up to saturation at CO2saturated photosynthesis rates. This results in a high rate of photorespiration and competitive inhibition of CO2fixation. of CO32−, accumulation of charged Ci species, Ci utilization and efflux of carbon stimulates ions movements required to compensate the charges of CO32−, HCO3−and CaHCO3+. del predicts accumulation of cations up to 50 mEq × 1−1or exclusion of the same amount of anions required to electroneutralize the accumulation of charged Ci species in the absence of calcium and up to 28 mEq × liter−1in the presence of 20 mM calcium. The steady-state CO32−dependent flux of electroneutralizing ions was found to be equal to the steady-state rate of Ci utilization and efflux (photosynthesis, photorespiratory CO2evolution and CO2leakage) multiplied by the valency of CO32−. The interconversion of Ci species resulting from Ci utilization and dissipation of Ci involves H+liberation in the hydration reaction and the dissociation of HCO3−to CO32−or H+consumption in the conversion of CO32−to HCO3−and dehydration of the latter. The H+production and the CO32−dependent transport of positive ions are interrelated and are non-monotonously altered in anti-parallel fashion as a function of the external Ci concentration. The presence of calcium reduces the magnitude of both these fluxes.