Photosynthetic Oxygen Evolution Is Not Reversed at High Oxygen Pressures: Mechanistic Consequences for the Water-Oxidizing Complex

Abstract

We investigated the effects of elevated O(2) pressure on the production of O(2) by photosynthetic organisms in several species of plants, algae, and a cyanobacterium. Using a noninvasive fluorometry technique to monitor sequential turnover of the photosystem II (PSII) reaction center as a function of O(2) pressures, we showed that none of the reactions of water oxidation are affected by elevated O(2) pressures up to 50-fold greater than atmospheric conditions. Thus, the terminal step of O(2) release from the water oxidation complex (S(4) --> S(0) + O(2) + nH(+)) is not reversible in whole cells, leaves, or isolated thylakoid membranes containing PSII, in contrast to reports using detergent-extracted PSII complexes. This implies that there is no thermodynamically accessible intermediate that can be populated by preventing or reversing the O(2) release step with O(2) at atmospheric pressure. To assess the sensitivity of PSII charge recombination to O(2) pressure, we quantitatively modeled the consequences of two putative perturbations to the catalytic cycle of water oxidation within the framework of the Kok model. On the basis of the breadth of oxygenic phototrophs examined in this study, we conclude that O(2) accumulation in cells or the atmosphere does not suppress photosynthetic productivity through the reversal of water oxidation in contemporary phototrophs and would have been unlikely to influence the evolution of oxygenic photosynthesis.