Photosynthesis re-wired on the pico-second timescale

Tomi K. Baikie, Laura T. Wey, Joshua M. Lawrence, Hitesh Medipally, Erwin Reisner, Marc M. Nowaczyk, Richard H. Friend, Christopher J. Howe (), Christoph Schnedermann (), Akshay Rao () and Jenny Z. Zhang ()
Additional contact information
Tomi K. Baikie: University of Cambridge
Laura T. Wey: University of Cambridge
Joshua M. Lawrence: University of Cambridge
Hitesh Medipally: Ruhr University Bochum
Erwin Reisner: University of Cambridge
Marc M. Nowaczyk: Ruhr University Bochum
Richard H. Friend: University of Cambridge
Christopher J. Howe: University of Cambridge
Christoph Schnedermann: University of Cambridge
Akshay Rao: University of Cambridge
Jenny Z. Zhang: University of Cambridge

Nature, 2023, vol. 615, issue 7954, 836-840

Abstract: Abstract Photosystems II and I (PSII, PSI) are the reaction centre-containing complexes driving the light reactions of photosynthesis; PSII performs light-driven water oxidation and PSI further photo-energizes harvested electrons. The impressive efficiencies of the photosystems have motivated extensive biological, artificial and biohybrid approaches to ‘re-wire’ photosynthesis for higher biomass-conversion efficiencies and new reaction pathways, such as H2 evolution or CO2 fixation1,2. Previous approaches focused on charge extraction at terminal electron acceptors of the photosystems3. Electron extraction at earlier steps, perhaps immediately from photoexcited reaction centres, would enable greater thermodynamic gains; however, this was believed impossible with reaction centres buried at least 4 nm within the photosystems4,5. Here, we demonstrate, using in vivo ultrafast transient absorption (TA) spectroscopy, extraction of electrons directly from photoexcited PSI and PSII at early points (several picoseconds post-photo-excitation) with live cyanobacterial cells or isolated photosystems, and exogenous electron mediators such as 2,6-dichloro-1,4-benzoquinone (DCBQ) and methyl viologen. We postulate that these mediators oxidize peripheral chlorophyll pigments participating in highly delocalized charge-transfer states after initial photo-excitation. Our results challenge previous models that the photoexcited reaction centres are insulated within the photosystem protein scaffold, opening new avenues to study and re-wire photosynthesis for biotechnologies and semi-artificial photosynthesis.

Date: 2023
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DOI: 10.1038/s41586-023-05763-9

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