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Photosynthesis re-wired on the pico-second timescale

Nature volume 615, pages 836–840 (2023)Cite this article

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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.

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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.

Data availability

The data underlying all figures in the main text are publicly available from the University of Cambridge repository at https://doi.org/10.17863/CAM.92167.

Code availability

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

References

  1. Grattieri, M., Beaver, K., Gaffney, E. M., Dong, F. & Minteer, S. D. Advancing the fundamental understanding and practical applications of photo-bioelectrocatalysis. Chem. Commun. 56, 8553–8568 (2020).

    Article  CAS  Google Scholar 

  2. Zhang, J. Z. & Reisner, E. Advancing photosystem II photoelectrochemistry for semi-artificial photosynthesis. Nat. Rev. Chem. 4, 6–21 (2020).

    Article  CAS  Google Scholar 

  3. Fu, H.-Y. et al. Redesigning the QA binding site of Photosystem II allows reduction of exogenous quinones. Nat. Commun. 8, 15274 (2017).

    Article  PubMed  PubMed Central  ADS  Google Scholar 

  4. Jordan, P. et al. Three-dimensional structure of cyanobacterial photosystem I at 2.5 Å resolution. Nature 411, 909–917 (2001).

    Article  CAS  PubMed  ADS  Google Scholar 

  5. Shen, G., Boussiba, S. & Vermaas, W. F. J. Synechocystis sp PCC 6803 strains lacking photosystem I and phycobilisome function. Plant Cell 5, 1853 (2007).

    Google Scholar 

  6. Berera, R., van Grondelle, R. & Kennis, J. T. M. Ultrafast transient absorption spectroscopy: principles and application to photosynthetic systems. Photosynth. Res. 101, 105–118 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Harris, E. H. Chlamydomonas as a model organism. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52, 363–406 (2001).

    Article  CAS  PubMed  Google Scholar 

  8. Suda, S. et al. Taxonomic characterization of a marine Nannochloropsis species, N. oceanica sp. nov. (Eustigmatophyceae). Phycologia 41, 273–279 (2019).

  9. Park, S. et al. Chlorophyll–carotenoid excitation energy transfer and charge transfer in Nannochloropsis oceanica for the regulation of photosynthesis. Proc. Natl Acad. Sci. USA 116, 3385–3390 (2019).

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  10. Howe, C. J., Barbrook, A. C., Nisbet, R. E. R., Lockhart, P. J. & Larkum, A. W. D. The origin of plastids. Philos. Trans. R. Soc. B: Biol. Sci. 363, 2675–2685 (2008).

    Article  CAS  Google Scholar 

  11. Lea-Smith, D. J. et al. Hydrocarbons are essential for optimal cell size, division, and growth of cyanobacteria. Plant Physiol. 172, 1928–1940 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Fălămas, A., Porav, S. A. & Tosa, V. Investigations of the energy transfer in the phycobilisome antenna of Arthrospira platensis using femtosecond spectroscopy. Appl. Sci. 10, 4045 (2020).

  13. Kopczynski, M. et al. Ultrafast transient lens spectroscopy of various C40 carotenoids: lycopene, β-carotene, (3R,3′ R)-zeaxanthin, (3R,3′ R,6′ R)-lutein, echinenone, canthaxanthin, and astaxanthin. Phys. Chem. Chem. Phys. 7, 2793–2803 (2005).

    Article  CAS  PubMed  Google Scholar 

  14. Longatte, G. et al. Investigation of photocurrents resulting from a living unicellular algae suspension with quinones over time. Chem. Sci. 9, 8271–8281 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Evans, M. C. W. & Heathcote, P. Effects of glycerol on the redox properties of the electron acceptor complex in spinach Photosystem I particles. Biochim. Biophys. Acta Bioenerg. 590, 89–96 (1980).

    Article  CAS  Google Scholar 

  16. De Causmaecker, S., Douglass, J. S., Fantuzzi, A., Nitschke, W. & Rutherford, A. W. Energetics of the exchangeable quinone, QB, in Photosystem II. Proc. Natl Acad. Sci. USA 116, 19458–19463 (2019).

    Article  PubMed  PubMed Central  ADS  Google Scholar 

  17. Stirbet, A. Excitonic connectivity between photosysstem II units: what is it, and how to measure it? Photosynth. Res. 116, 189–214 (2013).

  18. Mirkovic, T. et al. Light absorption and energy transfer in the antenna complexes of photosynthetic organisms. Chem. Rev. 117, 249–293 (2017).

  19. Ma, F., Romero, E., Jones, M. R., Novoderezhkin, V. I. & van Grondelle, R. Both electronic and vibrational coherences are involved in primary electron transfer in bacterial reaction center. Nat. Commun. 10, 933 (2019).

    Article  PubMed  PubMed Central  ADS  Google Scholar 

  20. Dods, R. et al. Ultrafast structural changes within a photosynthetic reaction centre. Nature 589, 310–314 (2021).

    Article  CAS  PubMed  ADS  Google Scholar 

  21. Trebst, A. The three-dimensional structure of the herbicide binding niche on the reaction center polypeptides of photosystem II. Z. Naturforsch. C J. Biosci. 42, 742–750 (1987).

    Article  CAS  Google Scholar 

  22. Longatte, G. et al. Evaluation of photosynthetic electrons derivation by exogenous redox mediators. Biophys. Chem. 205, 1–8 (2015).

    Article  CAS  PubMed  Google Scholar 

  23. O’Reilly, J. E. Oxidation-reduction potential of the ferro-ferricyanide system in buffer solutions. Biochim. Biophys. Acta Bioenerg. 292, 509–515 (1973).

    Article  Google Scholar 

  24. Durrant, J. R. et al. Subpicosecond equilibration of excitation energy in isolated photosystem II reaction centers. Proc. Natl Acad. Sci. USA 89, 11632–11636 (1992).

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  25. Groot, M. L. et al. Initial electron donor and acceptor in isolated Photosystem II reaction centers identified with femtosecond mid-IR spectroscopy. Proc. Natl Acad. Sci. USA 102, 13087–13092 (2005).

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  26. Klug, D. R., Durrant, J. R. & Barber, J. The entanglement of excitation energy transfer and electron transfer in the reaction centre of photosystem II. Philos. Trans. R. Soc. London, Ser. A 356, 449–464 (1998).

    Article  CAS  ADS  Google Scholar 

  27. Russo, M., Casazza, A. P., Cerullo, G., Santabarbara, S. & Maiuri, M. Ultrafast excited state dynamics in the monomeric and trimeric photosystem I core complex of Spirulina platensis probed by two-dimensional electronic spectroscopy. J. Chem. Phys. 156, 164202 (2022).

    Article  CAS  PubMed  ADS  Google Scholar 

  28. Slavov, C., Ballottari, M., Morosinotto, T., Bassi, R. & Holzwarth, A. R. Trap-limited charge separation kinetics in higher plant photosystem I complexes. Biophys. J. 94, 3601–3612 (2008).

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  29. Lee, Y., Gorka, M., Golbeck, J. H. & Anna, J. M. Ultrafast energy transfer involving the red chlorophylls of cyanobacterial photosystem I probed through two-dimensional electronic spectroscopy. J. Am. Chem. Soc. 140, 11631–11638 (2018).

    Article  CAS  PubMed  Google Scholar 

  30. Shelaev, I. V. et al. Femtosecond primary charge separation in Synechocystis sp. PCC 6803 photosystem I. Biochim. Biophys. Acta Bioenerg. 1797, 1410–1420 (2010).

    Article  CAS  Google Scholar 

  31. Weliwatte, N. S., Grattieri, M. & Minteer, S. D. Rational design of artificial redox-mediating systems toward upgrading photobioelectrocatalysis. Photochem. Photobiol. Sci. 20, 1333–1356 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Bennett, T. et al. Elucidating the role of methyl viologen as a scavenger of photoactivated electrons from photosystem I under aerobic and anaerobic conditions. Phys. Chem. Chem. Phys. 18, 8512–8521 (2016).

    Article  CAS  PubMed  Google Scholar 

  33. Wey, L. T. et al. The development of biophotovoltaic systems for power generation and biological analysis. Chem. Electro. Chem. 6, 5375–5386 (2019).

    CAS  PubMed  Google Scholar 

  34. Kato, M., Zhang, J. Z., Paul, N. & Reisner, E. Protein film photoelectrochemistry of the water oxidation enzyme photosystem II. Chem. Soc. Rev. 43, 6485–6497 (2014).

    Article  CAS  PubMed  Google Scholar 

  35. Lea-Smith, D. J., Bombelli, P., Vasudevan, R. & Howe, C. J. Photosynthetic, respiratory and extracellular electron transport pathways in cyanobacteria. Biochim. Biophys. Acta, Bioenerg. 1857, 247–255 (2016).

    Article  CAS  Google Scholar 

  36. Kurashov, V. et al. Critical evaluation of electron transfer kinetics in P700–FA/FB, P700–FX, and P700–A1 Photosystem I core complexes in liquid and in trehalose glass. Biochim. Biophys. Acta Bioenerg. 1859, 1288–1301 (2018).

    Article  CAS  PubMed  Google Scholar 

  37. Setif, P. Q. Y. & Bottin, H. Laser flash absorption spectroscopy study of ferredoxin reduction by photosystem I: spectral and kinetic evidence for the existence of several photosystem I-ferredoxin complexes. Biochemistry 34, 9059–9070 (1995).

    Article  CAS  PubMed  Google Scholar 

  38. Young, I. D. et al. Structure of photosystem II and substrate binding at room temperature. Nature 540, 453–457 (2016).

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  39. Stanier, R. Y., Kunisawa, R., Mandel, M. & Cohen-Bazire, G. Purification and properties of unicellular blue-green algae (order Chroococcales). Bacteriol. Rev. 35, 171–205 (1971).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Lea-Smith, D. J. et al. Thylakoid terminal oxidases are essential for the cyanobacterium Synechocystis sp. PCC 6803 to survive rapidly changing light intensities. Plant Physiol. 162, 484–495 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Lea-Smith, D. J. et al. Phycobilisome-deficient strains of Synechocystis sp PCC 6803 have reduced size and require carbon-limiting conditions to exhibit enhanced productivity. Plant Physiol. 165, 705–714 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Zhang, J. Z. et al. Photoelectrochemistry of photosystem II in vitro vs in vivo. J. Am. Chem. Soc. 140, 6–9 (2018).

    Article  CAS  PubMed  Google Scholar 

  43. Mersch, D. et al. Wiring of photosystem II to hydrogenase for photoelectrochemical water splitting. J. Am. Chem. Soc. 137, 8541–8549 (2015).

    Article  CAS  PubMed  Google Scholar 

  44. El-Mohsnawy, E. et al. Structure and function of intact photosystem 1 monomers from the cyanobacterium Thermosynechococcus elongatus. Biochemistry 49, 4740–4751 (2010).

    Article  CAS  PubMed  Google Scholar 

  45. Paul, N. Intermolecular Photophysics of Photosystem II Core Complexes at Protein-Nanomaterial Interfaces. PhD thesis, Univ. Cambridge (2015).

  46. Longatte, G., Rappaport, F., Wollman, F.-A., Guille-Collignon, M. & Lemaître, F. Mechanism and analyses for extracting photosynthetic electrons using exogenous quinones–what makes a good extraction pathway? Photochem. Photobiol. Sci. 15, 969–979 (2016).

    Article  CAS  PubMed  Google Scholar 

  47. Pandya, R., MacQueen, R. W., Rao, A. & Davies, N. J. L. K. Simple and robust panchromatic light harvesting antennacomposites via FRET engineering in solid state host matrices. J. Phys. Chem. C. 122, 22330–22338 (2018).

    Article  CAS  Google Scholar 

  48. Hinrichsen, T. F. et al. Long-lived and disorder-free charge transfer states enable endothermic charge separation in efficient non-fullerene organic solar cells. Nat Commun. 11, 5617 (2020).

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  49. Wey, L. T. et al. A biophotoelectrochemical approach to unravelling the role of cyanobacterial cell structures in exoelectrogenesis. Electrochim. Acta 395, 139214 (2021).

    Article  CAS  Google Scholar 

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Acknowledgements

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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Author notes

  1. These authors contributed equally: Tomi K. Baikie, Laura T. Wey

Authors and Affiliations

  1. Cavendish Laboratory, University of Cambridge, Cambridge, UK

    Tomi K. Baikie, Richard H. Friend, Christoph Schnedermann & Akshay Rao

  2. Department of Biochemistry, University of Cambridge, Cambridge, UK

    Laura T. Wey, Joshua M. Lawrence & Christopher J. Howe

  3. Department of Life Technologies, University of Turku, Turku, Finland

    Laura T. Wey

  4. Yusuf Hamied Department of Chemistry, University of Cambridge, Cambridge, UK

    Joshua M. Lawrence, Erwin Reisner & Jenny Z. Zhang

  5. Plant Biochemistry, Ruhr University Bochum, Bochum, Germany

    Hitesh Medipally & Marc M. Nowaczyk

  6. Department of Biochemistry, University of Rostock, Rostock, Germany

    Marc M. Nowaczyk

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Contributions

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.

Corresponding authors

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). https://doi.org/10.1038/s41586-023-05763-9

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