Photosynthesis re-wired on the pico-second timescale

Photosystems II and I (PSII and PSI) are the reaction centre complexes that drive the light reactions of photosynthesis. PSII performs light-driven water oxidation (quantum efficiencies and catalysis rates of up to 80% and 1000 $e^{-}\text{s}^{-1}$, respectively) and PSI further photo-energises the harvested electrons (quantum efficiencies of ~100%). The impressive performance of the light harvesting components of photosynthesis has motivated extensive biological, artificial and biohybrid approaches to re-wire photosynthesis to enable higher efficiencies and new reaction pathways, such as H2 evolution or alternative CO2 fixation. To date these approaches have focussed on charge extraction at the terminal electron quinones of PSII and terminal iron-sulfur clusters of PSI. Ideally electron extraction would be possible immediately from the photoexcited reaction centres to enable the greatest thermodynamic gains. However, this was believed to be impossible because the reaction centres are buried around 4 nm within PSII and 5 nm within PSI from the cytoplasmic face. Here, we demonstrate using in vivo ultrafast transient absorption (TA) spectroscopy that it is possible to extract electrons directly from photoexcited PSI and PSII, using both live cyanobacterial cells and isolated photosystems, with the exogenous electron mediator 2,6-dichloro1,4-benzoquinone (DCBQ). We postulate that DCBQ can oxidise peripheral chlorophyll pigments participating in highly delocalised charge transfer (CT) states after initial photoexcitation. Our results open new avenues to study and re-wire photosynthesis for bioenergy and semi-artificial photosynthesis.