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.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$259.00 per year
only $21.58 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Suga, M. et al. Native structure of photosystem II at 1.95 Å resolution viewed by femtosecond X-ray pulses. Nature 517, 99–103 (2015).
Nath, K. et al. Towards a critical understanding of the photosystem II repair mechanism and its regulation during stress conditions. FEBS Lett. 587, 3372–3381 (2013).
Kruse, O., Rupprecht, J., Mussgnug, J.H., Dismukes, G.C. & Hankamer, B. Photosynthesis: a blueprint for solar energy capture and biohydrogen production technologies. Photochem. Photobiol. Sci. 4, 957–970 (2005).
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).
Badura, A., Kothe, T., Schuhmann, W. & Rögner, M. Wiring photosynthetic enzymes to electrodes. Energy Environ. Sci. 4, 3263–3274 (2011).
Mersch, D. et al. Wiring of photosystem II to hydrogenase for photoelectrochemical water splitting. J. Am. Chem. Soc. 137, 8541–8549 (2015).
Kato, M., Cardona, T., Rutherford, A.W. & Reisner, E. Photoelectrochemical water oxidation with photosystem II integrated in a mesoporous indium-tin oxide electrode. J. Am. Chem. Soc. 134, 8332–8335 (2012).
Lai, Y.-H., Kato, M., Mersch, D. & Reisner, E. Comparison of photoelectrochemical water oxidation activity of a synthetic photocatalyst system with photosystem II. Faraday Discuss. 176, 199–211 (2014).
Yehezkeli, O. et al. Integrated photosystem II-based photo-bioelectrochemical cells. Nat. Commun. 3, 742 (2012).
Romero, E., van Stokkum, I.H.M., Novoderezhkin, V.I., Dekker, J.P. & van Grondelle, R. Two different charge separation pathways in photosystem II. Biochemistry 49, 4300–4307 (2010).
Romero, E. et al. Mixed exciton-charge-transfer states in photosystem II: Stark spectroscopy on site-directed mutants. Biophys. J. 103, 185–194 (2012).
Romero, E. et al. Quantum coherence in photosynthesis for efficient solar-energy conversion. Nat. Phys. 10, 676–682 (2014).
Renger, G. & Renger, T. Photosystem II: the machinery of photosynthetic water splitting. Photosynth. Res. 98, 53–80 (2008).
Ananyev, G. & Dismukes, G.C. How fast can photosystem II split water? Kinetic performance at high and low frequencies. Photosynth. Res. 84, 355–365 (2005).
Terasaki, N. et al. Photocurrent generation properties of Histag-photosystem II immobilized on nanostructured gold electrode. Thin Solid Films 516, 2553–2557 (2008).
Kato, M., Cardona, T., Rutherford, A.W. & Reisner, E. Covalent immobilization of oriented photosystem II on a nanostructured electrode for solar water oxidation. J. Am. Chem. Soc. 135, 10610–10613 (2013).
Badura, A. et al. Photo-induced electron transfer between photosystem 2 via cross-linked redox hydrogels. Electroanalysis 20, 1043–1047 (2008).
Cai, P. et al. Co-assembly of photosystem II/reduced graphene oxide multilayered biohybrid films for enhanced photocurrent. Nanoscale 7, 10908–10911 (2015).
Umena, Y., Kawakami, K., Shen, J.-R. & Kamiya, N. Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å. Nature 473, 55–60 (2011).
Barber, J., Morris, E. & Büchel, C. Revealing the structure of the photosystem II chlorophyll binding proteins, CP43 and CP47. Biochim. Biophys. Acta 1459, 239–247 (2000).
Tributsch, H. Reaction of excited chlorophyll molecules at electrodes and in photosynthesis. Photochem. Photobiol. 16, 261–269 (1972).
Kay, A., Humphry-Baker, R. & Graetzel, M. Artificial photosynthesis. 2. Investigations on the mechanism of photosensitization of nanocrystalline TiO2 solar cells by chlorophyll derivatives. J. Phys. Chem. 98, 952–959 (1994).
Miyasaka, T., Watanabe, T., Fujishima, A. & Honda, K. Photoelectrochemical study of chlorophyll-a multilayers on SnO2 electrode. Photochem. Photobiol. 32, 217–222 (1980).
Barazzouk, S., Kamat, P.V. & Hotchandani, S. Photoinduced electron transfer between chlorophyll a and gold nanoparticles. J. Phys. Chem. B 109, 716–723 (2005).
Seely, G.R. The energetics of electron-transfer reactions of chlorophyll and other compounds. Photochem. Photobiol. 27, 639–654 (1978).
Wakerley, D.W. & Reisner, E. Oxygen-tolerant proton reduction catalysis: much O2 about nothing? Energy Environ. Sci. 8, 2283–2295 (2015).
Nakato, Y., Chiyoda, T. & Tsubomura, H. Experimental determination of ionization potentials of organic amines, β-carotene and chlorophyll a. Bull. Chem. Soc. Jpn. 47, 3001–3005 (1974).
Huang, Z. et al. Dye-controlled interfacial electron transfer for high-current indium tin oxide photocathodes. Angew. Chem. Int. Ed. Engl. 54, 6857–6861 (2015).
Krieger-Liszkay, A. Singlet oxygen production in photosynthesis. J. Exp. Bot. 56, 337–346 (2005).
Bielski, B.H.J., Cabelli, D.E., Arudi, R.L. & Ross, A.B. Reactivity of perhydroxyl/superoxide radicals in aqueous solution. J. Phys. Chem. 14, 1041–1100 (1985).
Adamiak, W. & Opallo, M. Electrochemical redox processes of fullerene C60 and decamethylferrocene dissolved in cast 1,2-dichlorobenzene film in contact with aqueous electrolyte. J. Electroanal. Chem. 643, 82–88 (2010).
El-Khouly, M.E., Araki, Y., Fujitsuka, M., Watanabe, A. & Ito, O. Photoinduced electron transfer between chlorophylls (a/b) and fullerenes (C60/C70) studied by laser flash photolysis. Photochem. Photobiol. 74, 22–30 (2001).
Yamakoshi, Y. et al. Active oxygen species generated from photoexcited fullerene (C60) as potential medicines: O2−· versus 1O2 . J. Am. Chem. Soc. 125, 12803–12809 (2003).
Allakhverdiev, S.I. et al. Redox potentials of primary electron acceptor quinone molecule (QA)− and conserved energetics of photosystem II in cyanobacteria with chlorophyll a and chlorophyll d. Proc. Natl. Acad. Sci. USA 108, 8054–8058 (2011).
Kato, Y., Nagao, R. & Noguchi, T. Redox potential of the terminal quinone electron acceptor QB in photosystem II reveals the mechanism of electron transfer regulation. Proc. Natl. Acad. Sci. USA 113, 620–625 (2016).
Shibamoto, T. et al. Species-dependence of the redox potential of the primary quinone electron acceptor QA in photosystem II verified by spectroelectrochemistry. FEBS Lett. 584, 1526–1530 (2010).
Léger, C. & Bertrand, P. Direct electrochemistry of redox enzymes as a tool for mechanistic studies. Chem. Rev. 108, 2379–2438 (2008).
Stevenson, G.P. et al. Theoretical analysis of the two-electron transfer reaction and experimental studies with surface-confined cytochrome c peroxidase using large-amplitude Fourier transformed AC voltammetry. Langmuir 28, 9864–9877 (2012).
Johnson, G.N., Rutherford, A.W. & Krieger, A. A change in the midpoint potential of the quinone QA in Photosystem II associated with photoactivation of oxygen evolution. Biochim. Biophys. Acta 1229, 202–207 (1995).
Shibamoto, T., Kato, Y., Sugiura, M. & Watanabe, T. Redox potential of the primary plastoquinone electron acceptor QA in photosystem II from Thermosynechococcus elongatus determined by spectroelectrochemistry. Biochemistry 48, 10682–10684 (2009).
Alcantara, K., Munge, B., Pendon, Z., Frank, H.A. & Rusling, J.F. Thin film voltammetry of spinach photosystem II. Proton-gated electron transfer involving the Mn4 cluster. J. Am. Chem. Soc. 128, 14930–14937 (2006).
Satoh, K., Oh-hashi, M., Kashino, Y. & Koike, H. Mechanism of electron flow through the QB site in photosystem II. 1. Kinetics of the reduction of electron acceptors at the QB and plastoquinone sites in photosystem II particles from the cyanobacterium Synechococcus vulcanus. Plant Cell Physiol. 36, 597–605 (1995).
Kashino, Y., Yamashita, M., Okamoto, Y., Koike, H. & Satoh, K. Mechanisms of electron flow through the QB site in photosystem II. 3. Effects of the presence of membrane structure on the redox reactions at the QB site. Plant Cell Physiol. 37, 976–982 (1996).
Pospisil, P. Molecular mechanisms of production and scavenging of reactive oxygen species by photosystem II. Biochim. Biophys. Acta 1817, 218–231 (2012).
Pospisil, P. Production of reactive oxygen species by photosystem II. Biochim. Biophys. Acta 1787, 1151–1160 (2009).
Vöpel, T. et al. Simultaneous measurements of photocurrents and H2O2 evolution from solvent exposed photosystem 2 complexes. Biointerphases 11, 019001 (2015).
Ishikita, H. & Knapp, E.-W. Redox potentials of chlorophylls and β-carotene in the antenna complexes of photosystem II. J. Am. Chem. Soc. 127, 1963–1968 (2005).
Sugiura, M. & Inoue, Y. Highly purified thermo-stable oxygen-evolving photosystem II core complex from the thermophilic cyanobacterium Synechococcus elongatus having His-tagged CP43. Plant Cell Physiol. 40, 1219–1231 (1999).
van Leeuwen, P.J., Nieveen, M.C., van de Meent, E.J., Dekker, J.P. & van Gorkom, H.J. Rapid and simple isolation of pure photosystem II core and reaction center particles from spinach. Photosynth. Res. 28, 149–153 (1991).
van Roon, H., van Breemen, J.F.L., de Weerd, F.L., Dekker, J.P. & Boekema, E.J. Solubilization of green plant thylakoid membranes with n-dodecyl-α,D-maltoside. Implications for the structural organization of the Photosystem II, Photosystem I, ATP synthase and cytochrome b6f complexes. Photosynth. Res. 64, 155–166 (2000).
Groot, M.-L. et al. Spectroscopic properties of the CP43 core antenna protein of photosystem II. Biophys. J. 77, 3328–3340 (1999).
Porra, R.J., Thompson, W.A. & Kriedemann, P.E. Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim. Biophys. Acta 975, 384–394 (1989).
Merry, S.A.P. et al. Modulation of quantum yield of primary radical pair formation in photosystem II by site-directed mutagenesis affecting radical cations and anions. Biochemistry 37, 17439–17447 (1998).
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.
Author information
Authors and Affiliations
Contributions
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.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Supplementary information
Supplementary Text and Figures
Supplementary Results and Supplementary Figures 1–17. (PDF 2429 kb)
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/nchembio.2192
This article is cited by
-
Photovoltaic activity of electrodes based on intact photosystem I electrodeposited on bare conducting glass
Photosynthesis Research (2020)
-
Advancing photosystem II photoelectrochemistry for semi-artificial photosynthesis
Nature Reviews Chemistry (2019)
-
Bias-free photoelectrochemical water splitting with photosystem II on a dye-sensitized photoanode wired to hydrogenase
Nature Energy (2018)
-
Light-induced formation of partially reduced oxygen species limits the lifetime of photosystem 1-based biocathodes
Nature Communications (2018)
-
Quantum design of photosynthesis for bio-inspired solar-energy conversion
Nature (2017)