Abstract
Redox polymer/protein biophotoelectrochemistry was used to analyse forward electron transfer of isolated PSII complexes with natural PsbA-variants. PsbA1- or PsbA3-PSII was embedded in a redox hydrogel that allows diffusion-free electron transfer to the electrode surface and thus measurement of an immediate photocurrent response. The initial photocurrent density of the electrode is up to ~2-fold higher with PsbA1-PSII under all tested light conditions, the most prominent under high-light [2,300 μmol(photon) m–2 s–1] illumination with 5 μA cm–2 for PsbA3-PSII and 9.5 μA cm–2 for PsbA1-PSII. This indicates more efficient electron transfer in low-light-adapted PsbA1-PSII. In contrast, the photocurrent decays faster in PsbA1-PSII under all tested light conditions, which suggests increased stability of high-light-adapted PsbA3-PSII. These results confirm and extend previous observations that PsbA3-PSII has increased P680+•/QA–• charge recombination and thus less efficient photon-to-charge conversion, whereas PsbA1-PSII is optimised for efficient electron transfer with limited stability.
Similar content being viewed by others
Abbreviations
- Chl:
-
chlorophyll
- Cyt:
-
cytochrome
- DCMU:
-
3-(3,4-dichlorophenyl)-1,1-dimethylurea
- LED:
-
light emitting diode
- MES:
-
2-(N-morpholino)ethanesulfonic acid
- P680:
-
reaction centre chlorophylls
- PEG-DGE:
-
poly(ethyleneglycol)diglycidylether
- PET:
-
photosynthetic electron transfer chain
- Phe:
-
pheophytin
- POs :
-
redox-hydrogel
- Q:
-
plastoquinone
- ROS:
-
reactive oxygen species
- β-DM:
-
N-dodecyl-β-D-maltoside
References
Badura A., Esper B., Ataka K. et al.: Light-driven water splitting for (bio-)hydrogen production. Photosystem 2 as the central part of a bioelectrochemical device.–Photochem. Photobiol. 82: 1385–1390, 2006.
Badura A., Guschin D., Esper B. et al.: Photo-induced electron transfer between Photosystem 2 via cross-linked redox hydrogels.–Electroanalysis 20: 1043–1047, 2008.
Baniulis D., Yamashita E., Zhang H. et al.: Structure-function of the cytochrome b6f complex.–Photochem. Photobiol. 84: 1349–1358, 2008.
Clarke A.K., Hurry V.M., Gustafsson P., Oquist G.: Two functionally distinct forms of the photosystem II reactioncenter protein D1 in the cyanobacterium Synechococcus sp. PCC 7942.–P. Natl. Acad. Sci. USA 90: 11985–11989, 1993.
Cox N., Messinger J.: Reflections on substrate water and dioxygen formation.–BBA-Bioenergetics 1827: 1020–1030, 2013.
Dau H., Zaharieva I.: Principles, efficiency, and blueprint character of solar-energy conversion in photosynthetic water oxidation.–Acc. Chem. Res. 42: 1861–1870, 2009
East G.A., del Valle M.A.: Easy-to-make Ag/AgCl reference electrode.–J. Chem. Educ. 77: 97, 2000.
Habermüller K., Ramanavicius A., Laurinavicius V., Schuhmann W.: An oxygen-insensitive reagentless glucose biosensor based on osmium-complex modified polypyrrole.–Electroanalysis 12: 1383–1389, 2000.
Hartmann V., Kothe T., Pöller S. et al.: Redox hydrogels with adjusted redox potential for improved efficiency in Z-scheme inspired biophotovoltaic cells.–Phys. Chem. Chem. Phys. 16: 11936–11941, 2014.
Holzwarth A.R., Müller M.G., Reus M. et al.: Kinetics and mechanism of electron transfer in intact photosystem II and in the isolated reaction center. Pheophytin is the primary electron acceptor.–P. Natl. Acad. Sci. USA 103: 6895–6900, 2006.
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, 2012a.
Kato Y., Shibamoto T., Yamamoto S. et al.: Influence of the PsbA1/PsbA3, Ca2+/Sr2+ and Cl-/Br-exchanges on the redox potential of the primary quinone QA in Photosystem II from Thermosynechococcus elongatus as revealed by spectroelectrochemistry.–BBA-Bioenergetics 1817: 1998–2004, 2012b.
Kós P.B., Deák Z., Cheregi O., Vass I.: Differential regulation of psbA and psbD gene expression, and the role of the different D1 protein copies in the cyanobacterium Thermosynechococcus elongatus BP-1.–Biochim. Biophys. Acta 1777: 74–83, 2008.
Kothe T., Plumeré N., Badura A. et al.: Combination of a photosystem 1-based photocathode and a photosystem 2-based photoanode to a Z-scheme mimic for biophotovoltaic applications.–Angew. Chem. Int. Edit. 52: 14233–14236, 2013.
Krieger-Liszkay A., Fufezan C., Trebst A.: Singlet oxygen production in photosystem II and related protection mechanism.–Photosynth. Res. 98: 551–564, 2008.
Krieger-Liszkay A., Rutherford A.W.: Influence of herbicide binding on the redox potential of the quinone acceptor in photosystem II: Relevance to photodamage and phytotoxicity.–Biochemistry 37: 17339–17344, 1998.
Kuhl H., Kruip J., Seidler A. et al.: Towards structural determination of the water-splitting enzyme. Purification, crystallization, and preliminary crystallographic studies of photosystem II from a thermophilic cyanobacterium.–J. Biol. Chem. 275: 20652–20659, 2000.
Nixon P.J., Michoux F., Yu J. et al.: Recent advances in understanding the assembly and repair of photosystem II.–Ann. Bot.-London 106: 1–16, 2010.
Ogami S., Boussac A., Sugiura M.: Deactivation processes in PsbA1-Photosystem II and PsbA3-Photosystem II under photoinhibitory conditions in the cyanobacterium Thermosynechococcus elongatus.–Biochim. Biophys. Acta 1817: 1322–1330, 20
Sander J., Nowaczyk M., Buchta J. et al.: Functional characterization and quantification of the alternative PsbA copies in Thermosynechococcus elongatus and their role in photoprotection.–J. Biol. Chem. 285: 29851–29856, 2010.
Schaefer M.R., Golden S.S.: Differential expression of members of a cyanobacterial psbA gene family in response to light.–J. Bacteriol. 171: 3973–3981, 1989.
Sicora C.I., Appleton S.E., Brown C.M. et al.: Cyanobacterial psbA families in Anabaena and Synechocystis encode trace, constitutive and UVB-induced D1 isoforms.–BBABioenergetics 1757: 47–56, 2006.
Sokol K.P., Mersch D., Hartmann V. et al.: Rational wiring of photosystem II to hierarchical indium tin oxide electrodes using redox polymers.–Energ. Environ. Sci. 9: 3698–3709, 2016.
Sugiura M., Azami C., Koyama K. et al.: Modification of the pheophytin redox potential in Thermosynechococcus elongatus Photosystem II with PsbA3 as D1.–BBA-Bioenergetics 1837: 139–148, 2014.
Sugiura M., Boussac A.: Some Photosystem II properties depending on the D1 protein variants in Thermosynechococcus elongatus.–BBA-Bioenergetics 1837: 1427–1434, 20
Sugiura M., Kato Y., Takahashi R. et al.: Energetics in photosystem II from Thermosynechococcus elongatus with a D1 protein encoded by either the psbA1 or psbA3 gene.–Biochim. Biophys. Acta 1797: 1491–1499, 2010.
Sugiura M., Ogami S., Kusumi M. et al.: Environment of TyrZ in photosystem II from Thermosynechococcus elongatus in which PsbA2 is the D1 protein.–J. Biol. Chem. 287: 13336–13347, 2012.
Tichý M., Lupı́nková L., Sicora C. et al.: Synechocystis 6803 mutants expressing distinct forms of the Photosystem II D1 protein from Synechococcus 7942. Relationship between the psbA coding region and sensitivity to visible and UV-B radiation.–BBA-Bioenergetics 1605: 55–66, 2003.
Trammell S.A., Wang L., Zullo J.M. et al.: Orientated binding of photosynthetic reaction centers on gold using Ni-NTA selfassembled monolayers.–Biosens. Bioelectron. 19: 1649–1655, 2004.
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.
Vinyard D.J., Gimpel J., Ananyev G.M. et al.: Natural variants of photosystem II subunit D1 tune photochemical fitness to solar intensity.–J. Biol. Chem. 288: 5451–5462, 2013.
Vinyard D.J., Gimpel J., Ananyev G.M. et al.: Engineered Photosystem II reaction centers optimize photochemistry versus photoprotection at different solar intensities.–J. Am. Chem. Soc. 136: 4048–4055, 2014.
Vöpel T., Ning Saw E., Hartmann V. et al.: Simultaneous measurements of photocurrents and H2O2 evolution from solvent exposed photosystem 2 complexes.–Biointerphases 11: 19001, 2015.
Yehezkeli O., Tel-Vered R., Michaeli D. et al.: Photosystem I (PSI)/Photosystem II (PSII)-based photo-bioelectrochemical cells revealing directional generation of photocurrents.–Small 9: 2970–2978, 2013.
Yehezkeli O., Tel-Vered R., Wasserman J. et al.: Integrated photosystem II-based photo-bioelectrochemical cells.–Nat. Commun. 3: 742, 2012.
Author information
Authors and Affiliations
Corresponding author
Additional information
Acknowledgements: We thank Claudia König and Melanie Völkel for excellent technical assistance. This work was financially supported by the Deutsch–Israelische Projektkooperation (DIP) in the framework of the project “Nanoengineered Optobioelectronics with Biomaterials and Bioinspired Assemblies” and by the Cluster of Excellence RESOLV (EXC 1069) funded by the Deutsche Forschungsgemeinschaft.
Electronic supplementary material
Rights and permissions
About this article
Cite this article
Hartmann, V., Ruff, A., Schuhmann, W. et al. Analysis of photosystem II electron transfer with natural PsbA-variants by redox polymer/protein biophotoelectrochemistry. Photosynthetica 56, 229–235 (2018). https://doi.org/10.1007/s11099-018-0775-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11099-018-0775-y