Inverted-region electron transfer as a mechanism for enhancing photosynthetic solar energy conversion efficiency

In all photosynthetic organisms, light energy is used to drive electrons from a donor chlorophyll species via a series of acceptors across a biological membrane. These light-induced electron-transfer processes display a remarkably high quantum efficiency, indicating a near-complete inhibition of unproductive charge recombination reactions. It has been suggested that unproductive charge recombination could be inhibited if the reaction occurs in the so-called inverted region. However, inverted-region electron transfer has never been demonstrated in any native photosynthetic system. Here we demonstrate that the unproductive charge recombination in native photosystem I photosynthetic reaction centers does occur in the inverted region, at both room and cryogenic temperatures. Computational modeling of light-induced electron-transfer processes in photosystem I demonstrate a marked decrease in photosynthetic quantum efficiency, from 98% to below 72%, if the unproductive charge recombination process does not occur in the inverted region. Inverted-region electron transfer is therefore demonstrated to be an important mechanism contributing to efficient solar energy conversion in photosystem I. Inverted-region electron transfer does not appear to be an important mechanism in other photosystems; it is likely because of the highly reducing nature of photosystem I, and the energetic requirements placed on the pigments to operate in such a regime, that the inverted-region electron transfer mechanism becomes important.