The Mehler reaction site is the Phylloquinone within Photosystem I

Abstract

Photosynthesis is a vital process, responsible for fixing carbon dioxide, and producing most of the organic matter on the planet. However, photosynthesis has some inherent limitations in utilizing solar energy. Up to a third of the energy absorbed is lost in the reduction of O2 to produce the superoxide radical (O2*-), which occurs principally within photosystem I (PSI) via the Mehler reaction. Strikingly, the precise location as well as the evolutionary role of the reaction have long been a matter of debate. For decades, O2 reduction was assumed to take place solely in the distal iron-sulfur clusters of PSI rather than within the two asymmetrical cofactor branches. Here we demonstrate that under high irradiance, O2 photoreduction by PSI takes place at the phylloquinone of one of the branches (the A-branch). This conclusion derives from the light dependency of the O2 photoreduction rate constant, and from the high rates of O2 photoreduction in PSI complexes lacking iron-sulfur clusters and in a mutant PSI, in which the lifetime of this phyllosemiquinone state is extended 100-fold. On these grounds, we suggest that the Mehler reaction serves as a release valve, functioning only when needed, under conditions where both the distal iron-sulfur clusters of PSI and the mobile ferredoxin pool are over reduced. SIGNIFICANCE STATEMENTPhotosynthesis is the process responsible for the oxygenation of the ancient anoxic atmosphere, and the transformation of inorganic carbon to most of the organic matter on Earth. However, it is less commonly appreciated that the appearance of oxygen in the atmosphere led to the unavoidable opposite process in which oxygen is consumed, thereby producing deleterious oxygen radicals such as the superoxide radical. For almost half a decade, the location of the main site of superoxide radical production in chloroplasts has been a matter of debate. We now provide conclusive evidence that it is located in the phylloquinones(s) within photosystem I.