Tracking protonation dynamics in photosynthetic water oxidation in wild-type and mutated photosystem II

Principal Investigator: Prof. Dr. Holger Dau (FU)

Photosynthetic water oxidation and O₂-formation by plants, algae and cyanobacteria has shaped the biosphere and atmosphere. The goal of this project is to understand the pivotal role of protonation dynamics in the redox chemistry of photosynthetic water oxidation. In classical and novel biophysical experiments, the functionally relevant proton movements are tracked with microsecond resolution, with a focus on time-resolved infrared spectroscopy.

Publications

2021 - 2024

Dau, H. and Greife, P. (2023). Applicability of Transition State Theory to the (Proton-Coupled) Electron Transfer in Photosynthetic Water Oxidation with Emphasis on the Entropy of Activation. Inorganics, 11, 10. doi: 10.3390/inorganics11100389.

Dekmak, M.Y., Mäusle, S.M., Brandhorst, J., Simon, P.S. and Dau, H. (2024). Tracking the first electron transfer step at the donor side of oxygen-evolving photosystem II by time-resolved infrared spectroscopy. Photosynth Res. doi: 10.1007/s11120-023-01057-3.

Greife, P., Schönborn, M., Capone, M., Assunção, R., Narzi, D., Guidoni, L. and Dau, H. (2023). The electron–proton bottleneck of photosynthetic oxygen evolution. Nature. doi: 10.1038/s41586-023-06008-5.

Mäusle, S.M., Agarwala, N., Eichmann, V.G., Dau, H., Nürnberg, D.J. and Hastings, G. (2024). Nanosecond time-resolved infrared spectroscopy for the study of electron transfer in photosystem I. Photosynth Res, 159, 2-3: 229-239. doi:10.1007/s11120-023-01035-9.

Oliver, N., Avramov, A.P., Nürnberg, D.J., Dau, H. and Burnap, R.L. (2022). From manganese oxidation to water oxidation: assembly and evolution of the water-splitting complex in photosystem II. Photosynth Res, 152, 2: 107-133. doi: 10.1007/s11120-022-00912-z.

Viola, S., Roseby, W., Santabarbara, S., Nürnberg, D., Assuncao, R., Dau, H., Selles, J., Boussac, A., Fantuzzi, A. and Rutherford, A.W. (2022). Impact of energy limitations on function and resilience in long-wavelength Photosystem II. Elife, 11. doi: 10.7554/eLife.79890.

2017 - 2020

Assunção, R., Zaharieva, I., and Dau, H. (2019). Ammonia as a substrate-water analogue in photosynthetic water oxidation: Influence on activation barrier of the O2-formation step. Biochim. Biophys. Acta 1860, 533-540; doi: 10.1016/j.bbabio.2019.04.005.

Bommer, M., Coates, L., Dau, H., Zouni, A., and Dobbek, H. (2017). Protein crystallization and initial neutron diffraction studies of the photosystem II subunit PsbO. Acta Crystallogr F Struct Biol Commun 73, 525-531; doi: 10.1107/S2053230X17012171

Dau, H., Nürnberg, D. J., and Burnap, R. L. (2019). Local cycle of photosynthesis and quasi-aerobic respiration facilitated by manganese oxides – a hypothesis on the evolution of phototrophy. In: Bioenergetics: Oxygen Production and Reduction, eds. J. Barber, P. Nixon and A. V. Ruban, (World Scientific Publishers, Singapore), 367-391; doi: 10.1142/9789813276925_0018.

Chernev, P., Fischer, S., Hoffmann, J., Oliver, N., Assunção, R., Yu, B., Burnap, R., Zaharieva, I., Nürnberg, D., Haumann, M., Dau, H. (2020) Light-driven formation of manganese oxide by today's photosystem II supports evolutionarily ancient manganese-oxidizing photosynthesis. Nat commun, 11, 6110. doi: 10.1038/s41467-020-19852-0.

Gerland, L.M., Friedrich, D., Hopf, L., Donovan, E., Wallmann, A., Erdmann, N., Diehl, A., Bommer, M., Buzar, K., Ibrahim, M., Schmieder, P., Dobbek, H., Zouni, A., Bondar, A.-N., Dau, H., and Oschkinat, H. (2020). pH‐Dependent Protonation of Surface Carboxylates in PsbO Enables Local Buffering and Triggers Structural Changes. ChemBioChem 21, 1597-1604. doi: 10.1002/cbic.201900739.

Han, R., Rempfer, K., Zhang, M., Dobbek, H., Zouni, A., Dau, H., Luber, S. (2019). Investigating the Structure and Dynamics of Apo‑Photosystem II. ChemCatChem 11, 4072–4080; doi: 10.1002/cctc.201900351.

Mäusle, S.M., Abzaliyeva, A., Greife, P., Simon, P.S., Perez, R., Zilliges, Y., and Dau, H. (2020). Activation energies for two steps in the S₂ → S₃ transition of photosynthetic water oxidation from time-resolved single-frequency infrared spectroscopy. J Chem Phys, 153, 215101. doi: 10.1063/5.0027995.

Schuth, N., Liang, Z., Schonborn, M., Kussicke, A., Assuncao, R., Zaharieva, I., Zilliges, Y., and Dau, H. (2017). Inhibitory and Non-Inhibitory NH₃ Binding at the Water-Oxidizing Manganese Complex of Photosystem II Suggests Possible Sites and a Rearrangement Mode of Substrate Water Molecules. Biochemistry 56, 6240-6256; doi: 10.1021/acs.biochem.7b00743.

Schuth, N., Zaharieva, I., Chernev, P., Berggren, G., Anderlund, M., Styring, S., Dau, H., and Haumann, M. (2018). Kalpha X-ray Emission Spectroscopy on the Photosynthetic Oxygen-Evolving Complex Supports Manganese Oxidation and Water Binding in the S₃ State. Inorg Chem 57,10424-10430; doi: 10.1021/acs.inorgchem.8b01674.

Zaharieva, I., and Dau, H. (2019). Energetics and kinetics of S-state transitions monitored by delayed chlorophyll fluorescence. Frontiers in Plant Science Vol. 10, Article 386, doi: 10.3389/fpls.2019.00386.

Zhang, M., Bommer, M., Chatterjee, R., Hussein, R., Yano, J., Dau, H., Kern, J., Dobbek, H., and Zouni, A. (2017). Structural insights into the light-driven auto-assembly process of the water-oxidizing Mn₄CaO₅-cluster in photosystem II. eLife 6; doi: 10.7554/eLife.26933.

2014 - 2016

Bommer, M., Bondar, A.-N., Zouni, A., Dobbek, H., and Dau, H. (2016). Crystallographic and computational analysis of the barrel part of the PsbO protein of photosystem II - carboxylate-water clusters as putative proton transfer relays and structural switches. Biochemistry 55, 4626-4635.

Chernev, P., Zaharieva, I., Rossini, E., Galstyan, A., Dau, H., and Knapp, E.-W. (2016). Merging structural information from X-ray crystallography, quantum chemistry and EXAFS spectra: The oxygen-evolving complex in PSII. Journal of Physical Chemistry B 120, 10899-10922.

Damrow, R., Maldener, I., and Zilliges, Y. (2016). The Multiple Functions of Common Microbial Carbon Polymers, Glycogen and PHB, during Stress Responses in the Non-Diazotrophic Cyanobacterium Synechocystis sp. PCC 6803. Frontiers in  Microbiology 7, 966.

Karge, O., Bondar, A.-N., and Dau, H. (2014). Cationic screening of charged surface groups (carboxylates) affects electron transfer steps in photosystem-II water oxidation and quinone reduction. Biochimica et Biophysica Acta (BBA) - Bioenergetics 1837, 1625-1634.

Klauss, A., Haumann, M., and Dau, H. (2015). Seven steps of alternating electron and proton transfer in photosystem II water oxidation traced by time-resolved photothermal beam deflection at improved sensitivity. J Phys Chem B 119, 2677-2689.

Zaharieva, I., Chernev, P., Berggren, G., Anderlund, M., Styring, S., Dau, H., and Haumann, M. (2016). Room-temperature energy-sampling K-beta X-ray emission spectroscopy of the Mn₄Ca complex of photosynthesis reveals three manganese-centered oxidation steps and suggests a coordination change prior to O₂ formation. Biochemistry 55, 4197-4211.

Zaharieva, I., Dau, H., and Haumann, M. (2016). Sequential and Coupled Proton and Electron Transfer Events in the S2 --> S3 Transition of Photosynthetic Water Oxidation Revealed by Time-Resolved X-ray Absorption Spectroscopy. Biochemistry 55, 6996-7004.

Zaharieva, I., González-Flores, D., Asfari, B., Pasquini, C., Mohammadi, M.R., Klingan, K., Zizak, I., Loos, S., Chernev, P., and Dau, H. (2016). Water oxidation catalysis – role of redox and structural dynamics in biological photosynthesis and inorganic manganese oxides. Energy Environ Sci 9, 2433-2443.

Zhang, C., Chen, C., Dong, H., Shen, J.-R., Dau, H., and Zhao, J. (2015). A synthetic Mn4Ca-cluster mimicking the oxygen-evolving center of photosynthesis. Science 348, 690-693.

Zilliges, Y. and Dau, H. (2016). Unexpected capacity for organic carbon assimilation by Thermosynechococcus elongatus, a crucial photosynthetic model organism. FEBS Letters 590, 962-970.