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Project A5

Award-Winning Poster by Martin Bommer (project A5): Superstructure of Photosystem II published in Structure (Nov. 2014)

Award-Winning Poster by Martin Bommer (project A5): Superstructure of Photosystem II published in Structure (Nov. 2014) -- Click on picture to enlarge it!
Image Credit: M. Bommer

Structural basis of proton release in water oxidation by photosystem II: Crystallization, X-ray, and neutron diffraction analyses of chloride-modified and site-directed variants

Principal Investigators: Prof. Dr. Athina Zouni (HU), Prof. Dr. Holger Dobbek (HU)

In oxygenic photosynthesis, water is oxidized and dioxygen is formed at the Mn4Ca complex of photosystem II (PSII). The last ten years have seen a constant refinement of the structural details of PSII, which now provide a solid basis for further work on the underlying protonation dynamics. We want to focus on the coupling between electron and proton transfer during photosynthetic water oxidation. To achieve our aims we will combine conventional and room temperature femtosecond X-ray diffraction on chloride-modified PSII variants and site-directed mutants in a collaborative effort.



Chatterjee, R., Lasalle, L., Gul, S., Fuller, F.D., Young, I.D., Ibrahim, M., de Lichtenberg, C., Cheah, M.H., Zouni, A., Messinger, J., Yachandra, V.K., Kern, J., and Yano, J. (2019). Structural isomers of the S2 state in photosystem II: do they exist at room temperature and are they important for function? Physiol Plant. 166(1):60-72, doi: doi.org/10.1111/ppl.12947.

Fuller, F. D., Gul, S., Chatterjee, R., Burgie, E. S., Young, I. D., Lebrette, H., Srinivas, V., Brewster, A.S., Michels-Clark, T., Clinger, J. A., Andi, B., Ibrahim, M., Pastor, E., de Lichtenberg, C., Hussein, R., Pollock, C. J., Zhang, M., Stan, C. A., Kroll, T., Fransson, T., Weninger, C., Kubin, M., Aller, P., Lassalle, L., Brauer, P., Miller, M. D., Amin, M., Koroidov, S., Roessler, C. G., Allaire, M., Sierra, R. G., Docker, P. T., Glownia, J. M., Nelson, S., Koglin, J. E., Zhu, D., Chollet, M., Song, S., Lemke, H., Liang, M., Sokaras, D., Alonso-Mori, R., Zouni, A., Messinger, J., Bergmann, U., Boal, A. K., Bollinger Jr, J. M., Krebs, C., Hogbom, M., Phillips Jr, G. N., Vierstra, R. D., Sauter, N. K., Orville, A. M., Kern, J., Yachandra, V. K., and Yano, J. (2017). Drop-on-demand sample delivery for studying biocatalysts in action at X-ray free-electron lasers. Nature Meth. 4, 443-449; doi: 10.1038/nmeth.4195

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.

Hussein, R., Ibrahim, M., Chatterjee, R., Coates, L., Muh, F., Yachandra, V. K., Yano, J., Kern, J., Dobbek, H., Zouni, A. (2018). Optimizing Crystal Size of Photosystem II by Macroseeding: Toward Neutron Protein Crystallography. Cryst Growth Des 18, 85-94; doi: 10.1021/acs.cgd.7b00878

Kemmler, L., Ibrahim, M., Dobbek, H., Zouni, A., and Bondar, A.-N. (2019). Dynamic water bridging and proton transfer at a surface carboxylate cluster of photosystem II. Physical Chemistry Chemical Physics 21(45), 25449-25466, doi: 10.1039/C9CP03926k.

Kern, J., Chatterjee, R., Young, I. D., Fuller, F. D., Lassalle, L., Ibrahim, M., Gul, S., Fransson, T., Brewster, A. S., Alonso-Mori, R., Hussein, R., Zhang, M., Douthit, L., de Lichtenberg, C., Cheah, M. H., Shevela, D., Wersig, J., Seuffert, I., Sokaras, D., Pastor, E., Weninger, C., Kroll, T., Sierra, R. G., Aller, P., Butryn, A., Orville, A. M., Liang, M., Batyuk, A., Koglin, J. E., Carbajo, S., Boutet, S., Moriarty, N. W., Holton, J. M., Dobbek, H., Adams, P. D., Bergmann, U., Sauter, N. K., Zouni, A., Messinger, J., Yano, J., and Yachandra, V. K. (2018). Structures of the intermediates of Kok's photosynthetic water oxidation clock. Nature 563, 421-425; doi:10.1038/s41586-018-0681-2.

Kern, J., Müh, F., Zouni, A. (2019). Structural studies on tetrapyrrole containing proteins enabled by femtosecond X-ray pulses. In: Grimm B, Ed (2019). Metabolsm, structure and function of plant tetrapyrroles: Control mechanisms of chlorophyll biosynthesis and analysis of chlorophyll-binding proteins. Advances in Botanical Research, vol 91. pp. 33-67; doi: 10.1016/bs.abr.2019.04.003

Kielb, P., Utesch, T., Kozuch, J., Jeoung, J.-H., Dobbek, H., Mroginski, M.A., Hildebrandt, P., and Weidinger, I. (2017). Switchable Redox Chemistry of the Hexameric Tyrosine-Coordinated Heme Protein. Journal of Physical Chemistry B 121, 3955-3964; doi: 10.1021/acs.jpcb.7b01286

Müh, F., and Zouni, A. (2020). Structural basis of the light-harvesting in the photosystem II core complex. Protein Sci. 29(5):1090-1119; doi: 10.1002/pro.3841.

Riedel, M., Wersig, J., Ruff, A., Schuhmann, W., Zouni, A., and Lisdat, F. (2019). A Z‐scheme‐inspired photobioelectrochemical H2O/O2 cell with a 1 V open‐circuit voltage combining photosystem II and PbS quantum dots. Angewandte Chemie - International Edition 58, 801-805; doi: 10.1002/anie.201811172

Sidabras, J. W., Duan, J. Winkler, M., Happe, T., Hussein, R., Zouni, A., Suter, D., Schnegg, A., Lubitz, W., Reijerse, E. J. (2019). Extending electron paramagnetic resonance to nanoliter volume protein single crystals using a self-resonant microhelix. Sci. Adv 5, No 10; doi: 10.1126/sciadv.aay1394.

Sullivan, B., Archibald, R., Langan, P. S., Dobbek, H., Bommer, M., McFeeters, R. L., Coates, L., Wang, X., Gallmeier, F., Carpenter, J. M., Lynch, V., and Langan, P. (2018). Improving the accuracy and resolution of neutron crystallographic data by three-dimensional profile fitting of Bragg peaks in reciprocal space. Acta Crystallogr D Struct Biol 74, 1085-1095; doi: 10.1107/S2059798318013347

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 wateroxidizing Mn4CaO5- cluster in photosystem II. eLife 6; doi: 10.7554/eLife.26933

2013 - 2016

Alonso-Mori, R., Asa, K., Bergmann, U., Brewster, A.S., Chatterjee, R., Cooper, J.K., Frei, M., Fuller, F.D., Goggins, E., Gul, S., Fukuzawa, H., Iablonsky, D., Ibrahim, M., Katayamaj, T., Kroll, T., Kumagai, Y., McClure, B.A., Messinger, J., Motomura, K., Nagaya, K., Nishiyama, T., Saracini, C., Sato, Y., Sauter, N.K., Sokaras, D., Takanashi, T., Togashi, T., Ueda, K., Weare, W.W., Weng, T.-C., Yabashi, M., Yachandra, V.K., Young, I.D., Zouni, A., Kern, J.F. and Yano, J. (2016). Towards Characterization of Photo-Excited Electron Transfer and Catalysis in Natural and Artificial Systems Using XFELs. Faraday Discussions, The Royal Society of Chemistry 194, 621-638.

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.

Brecht, M., Skandary, S., Hellmich, J., Gloeckner, C., Konrad, A., Hussels, M., Meixner, A.J., Zouni, A., and Schlodder, E. (2014). Spectroscopic properties of photosystem II core complexes from Thermosynechococcus elongatus revealed by single-molecule experiments. Biochimica et Biophysica Acta (BBA) - Bioenergetics 1837, 773-781.

Glockner, C., Kern, J., Broser, M., Zouni, A., Yachandra, V., and Yano, J. (2013). Structural Changes of the Oxygen-evolving Complex in Photosystem II during the Catalytic Cycle. Journal of Biological Chemistry 288, 22607-22620.

Hellmich, J., Bommer, M., Burkhardt, A., Ibrahim, M., Kern, J., Meents, A., Müh, F., Dobbek, H., and Zouni, A. (2014). Native-like Photosystem II Superstructure at 2.44 Å Resolution through Detergent Extraction from the Protein Crystal. Structure 22, 1607-1615. [Link to news section.]

Ibrahim, M., Chatterjee, R., Hellmich, J., Tran, R., Bommer, M., Yachandra, V.K., Yano, J., Kern, J., and Zouni, A. (2015). Improvements in serial femtosecond crystallography of photosystem II by optimizing crystal uniformity using microseeding procedures. Structural Dynamics 2, 041705.

Kern, J., Alonso-Mori, R., Tran, R., Hattne, J., Gildea, R.J., Echols, N., Gloeckner, C., Hellmich, J., Laksmono, H., Sierra, R.G., et al. (2013). Simultaneous Femtosecond X-ray Spectroscopy and Diffraction of Photosystem II at Room Temperature. Science 340, 491-495.

Kern, J., Tran, R., Alonso-Mori, R., Koroidov, S., Echols, N., Hattne, J., Ibrahim, M., Gul, S., Laksmono, H., Sierra, R.G., et al. (2014). Taking snapshots of photosynthetic water oxidation using femtosecond X-ray diffraction and spectroscopy. Nature Communications 5, 4371.

Müh, F., DiFiore, D., and Zouni, A. (2015). The influence of poly(ethylene glycol) on the micelle formation of alkyl maltosides used in membrane protein crystallization. Physical Chemistry Chemical Physics 17, 11678-11691.

Müh, F., and Zouni, A. (2016). Cytochrome b559 in photosystem II. In: William A. Cramer, Toivo Kallas (ed.) Cytochrome Complexes: Evolution, Structures, Energy Transduction, and Signaling. Volume 41 of the series Advances in Photosynthesis and Respiration, 143-175.

Müh, F., and Zouni, A. (2013). The nonheme iron in photosystem II. Photosynthesis Research 116, 295-314.

Sierra, R.G., Gati, C., Laksmono, H., Dao, E.H., Gul, S., Fuller, F., Kern, J., Chatterjee, R., Ibrahim, M., Brewster, A.S., Young, I.D., Michels-Clark, T., Aquila, A., Liang, M., Hunter, M.S., Koglin, J.E., Boutet, S., Junco, E.A., Hayes, B., Bogan, M.J., Hampton, C.Y., Puglisi, E.V., Sauter, N.K., Stan, C.A., Zouni, A., Yano, J., Yachandra, V.K., Soltis, S.M., Puglisi, J.D., and DeMirci, H. (2016). Concentric-flow electrokinetic injector enables serial crystallography of ribosome and photosystem II. Nat. Methods 13, 59-62.

Skandary, S., Hussels, M., Konrad, A., Renger, T., Müh, F., Bommer, M., Zouni, A., Meixner, A.J., and Brecht, M. (2015). Variation of Exciton-Vibrational Coupling in Photosystem II Core Complexes from Thermosynechococcus elongatus As Revealed by Single-Molecule Spectroscopy. Journal of Physical Chemistry B 119, 4203-4210.

Tran, R., Kern, J., Hattne, J., Koroidov, S., Hellmich, J., Alonso-Mori, R., Sauter, N.K., Bergmann, U., Messinger, J., Zouni, A., et al. (2014). The Mn4Ca photosynthetic water-oxidation catalyst studied by simultaneous X-ray spectroscopy and crystallography using an X-ray free-electron laser. Philosophical Transactions of the Royal Society B-Biological Sciences 369, 20130324.

Young, I.D., Ibrahim, M., Chatterjee, R., Gul, S., Fuller, F.D., Koroidov, S., Brewster, A.S., Tran, R., Alonso-Mori, R., Kroll, T., Michels-Clark, T., Laksmono, H., Sierra, R.G., Stan, C.A., Hussein, R., Zhang, M., Douthit, L., Kubin, M., de Lichtenberg, C., Vo Pham, L., Nilsson, H., Hon Cheah, M., Shevela, D., Saracini, C., Bean, M.A., Seuffert, I., Sokaras, D., Weng, T.-C., Pastor, E., Weninger, C., Fransson, T., Lassalle, L., Bräuer, P., Aller, P., Docker, P.T., Andi, B., Orville, A.M., Glownia, J.M., Nelson, S., Sikorski, M., Zhu, D., Hunter, M.S., Lane, T.J., Aquila, A., Koglin, J.E., Robinson, J., Liang, M., Boutet, S., Lyubimov, A.Y., Uervirojnangkoorn, M., Moriarty, N.W., Liebschner, D., Afonine, P.V., Waterman, D.G., Evans, G., Wernet, P., Dobbek, H., Weis, W.I., Brunger, A.T., Zwart, P.H., Adams, P.D., Zouni, A., Messinger, J., Bergmann, U., Sauter, N.K., Kern, J., Yachandra, V.K., and Yano, J. (2016). Structure of photosystem II and substrate binding at room temperature. Nature 540, 453-457.