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Photosynthesis re-wired on the pico-second timescale


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.

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Fig. 1: Exogenous electron mediator acts on the pico-second timescale in living cells.
Fig. 2: Action of quinone electron mediators on wild-type cells.
Fig. 3: Action of DCBQ on cells genetically modified to have only one type of photosystem.

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Data availability

The data underlying all figures in the main text are publicly available from the University of Cambridge repository at

Code availability

All code used in this work is available from the corresponding authors upon reasonable request.


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We acknowledge W. Vermaas (Arizona State University, USA) for the gift of the photosystem-less mutants used in this study and W. Rutherford (Imperial College London) for the gift of isolated PSII as well as valuable discussions on this project. We thank X. Chen for provision of porous electrodes. We acknowledge F. Lemaitre (École Normale Supérieure, France) and P. Rich (University College of London, UK) for helpful discussions about exogenous benzoquinones and photosynthetic microorganisms. We thank K. Redding for helpful discussions on photoexcited states of reaction centre proteins. C.S. and T.K.B. thank V. Gray for insightful discussion at the start of the project. We acknowledge N. Paul for his PhD work, which contributed ideas to this study. T.K.B. gives thanks to the Centre for Doctoral Training in New and Sustainable Photovoltaics (grant no. EP/L01551X/2) and the NanoDTC (grant no. EP/L015978/1) for financial support. L.T.W. acknowledges financial support from the Cambridge Trust. C.S. acknowledges financial support by the Royal Commission of the Exhibition of 1851. We acknowledge financial support by the BBSRC (grant no. BB/R011923/1 to J.Z.Z.), the EPSRC (grant no. EP/M006360/1) and the Winton Program for the Physics of Sustainability as well as from the Deutsche Forschungsgemeinschaft within the framework of the Research Training Group 2341 ‘MiCon’. This project has received funding from the European Research Council under the European Union’s Horizon 2020 research and innovation programme (grant agreement nos. 758826, 764920 and 682833).

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Authors and Affiliations



T.K.B. and L.T.W. contributed equally to the work and initially developed the application of ultrafast techniques to exame cyanobacteria. C.S. and A.R. supervised the spectroscopy, C.J.H. supervised the cell work, J.Z.Z. developed the research question. T.K.B. performed the TA and TCSPC experiments and the analysis, and prepared the figures. L.T.W. chose and prepared the samples for TA and TCSPC, performed the photo-electrochemistry, oxygen evolution, cytotoxicity and microscopy experiments, and did protein crystal structure analysis. J.M.L. prepared samples for the MV2+ study. H.M. prepared isolated PSI. T.K.B., L.T.W., M.M.N., R.H.F., E.R., C.S., J.Z.Z., C.J.H. and A.R. contributed to discussions, analysis and writing of the manuscript.

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Correspondence to Christopher J. Howe, Christoph Schnedermann, Akshay Rao or Jenny Z. Zhang.

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Baikie, T.K., Wey, L.T., Lawrence, J.M. et al. Photosynthesis re-wired on the pico-second timescale. Nature 615, 836–840 (2023).

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