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Competing charge transfer pathways at the photosystem II–electrode interface

Abstract

The integration of the water-oxidation enzyme photosystem II (PSII) into electrodes allows the electrons extracted from water oxidation to be harnessed for enzyme characterization and to drive novel endergonic reactions. However, PSII continues to underperform in integrated photoelectrochemical systems despite extensive optimization efforts. Here we carried out protein-film photoelectrochemistry using spinach and Thermosynechococcus elongatus PSII, and we identified a competing charge transfer pathway at the enzyme–electrode interface that short-circuits the known water-oxidation pathway. This undesirable pathway occurs as a result of photo-induced O2 reduction occurring at the chlorophyll pigments and is promoted by the embedment of PSII in an electron-conducting fullerene matrix, a common strategy for enzyme immobilization. Anaerobicity helps to recover the PSII photoresponse and unmasks the onset potentials relating to the QA/QB charge transfer process. These findings impart a fuller understanding of the charge transfer pathways within PSII and at photosystem–electrode interfaces, which will lead to more rational design of pigment-containing photoelectrodes in general.

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Figure 1: Energy/charge transfer pathways.
Figure 2: PSII photocathodic currents stem from protein-bound and isolated Chl a pigments.
Figure 3: O2 and the fullerene derivative C60-DMePyI are electron acceptors for photoexcited Chl a.
Figure 4: Onset potential.
Figure 5: Summary of the photoanodic and photocathodic charge transfer pathways within PSII and at the PSII–electrode interface.

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Acknowledgements

This work was supported by the UK Engineering and Physical Sciences Research Council (EP/H00338X/2 to E. Reisner; DTA PhD studentship to K.P.S.), the UK Biology and Biotechnological Sciences Research Council (BB/K010220/1 to E. Reisner), and a Marie Curie International Incoming Fellowship (PIIF-GA-2012-328085 RPSII to J.Z.Z.). N.P. was supported by the Winton Programme for the Physics of Sustainability. E. Romero. and R.v.G. were supported by the VU Amsterdam, the Laserlab-Europe Consortium, the Foundation of Chemical Sciences of NWO (TOP grant 700.58.305), the European Research Council (Advanced Investigator grant 267333, PHOTPROT), and EU FP7 project PAPETS (GA 323901). R.v.G. gratefully acknowledges an 'Academy Professor' grant from the Royal Netherlands Academy of Arts and Sciences. We also thank K. Brinkert and W.A. Rutherford (Imperial College London, London, UK) for samples of T. elongatus PSII, and H. van Roon for preparation of the spinach PSII samples. Lastly, we thank D.W. Wakerley and T.E. Rosser for valuable discussions.

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J.Z.Z. and E. Reisner conceived the research. J.Z.Z. performed all experiments and wrote the manuscript. K.P.S. provided the ITO electrodes. E. Romero and R.v.G. provided the spinach PSII. J.Z.Z., N.P., E. Romero and E. Reisner added to the discussion and contributed to the preparation of the manuscript. E. Reisner supervised the work.

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Correspondence to Erwin Reisner.

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Zhang, J., Sokol, K., Paul, N. et al. Competing charge transfer pathways at the photosystem II–electrode interface. Nat Chem Biol 12, 1046–1052 (2016). https://doi.org/10.1038/nchembio.2192

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