Elucidation of the self-repair mechanism of the light-driven water oxidation in photosystem II (PSII): Crystallization of the Mn-depleted PSII and its structural/functional analysis

Photosystem II (PSII) of oxygenic photosynthesis has the unique capability of utilizing visible light to oxidize water at the Mn4CaO5-cluster (the water oxidizing complex, WOC). Important progress in elucidating the molecular structure of the WOC has been achieved in the last ten years involving protein crystallography on the cyanobacterial PSII core complex (PSIIcc) and X-ray absorption spectroscopy, providing a solid basis for the analysis of the molecular mechanisms of water oxidation that are still poorly understood. Our first research aim in this proposal is to improve the quality of our crystals of monomeric and dimeric PSIIcc to at least 2.0 Å resolution. These structural data will be combined with different spectroscopic measurements on single PSIIcc crystals (EPR, EXAFS, XAS) for understanding the catalytic process itself. The second central topic in our project is the elucidation of the self-repair mechanism of the light-driven water oxidation in PSIIcc that may be essential also in artificial water oxidation catalysts. For this reason our interest is the crystallization of PSIIcc with an assembly intermediate of the WOC as well as Mn-depleted PSIIcc. These structural data will give insight into structural changes accompanying the repair cycle.

Principal Investigators
Zouni, Athina PD Dr. (Details) (Honorary Chairs / Professors by Special Appointment / Part-Time Lecturers)

participating organizational facilities of the HU

Financer
DFG-Exzellenzinitiative: Cluster

Duration of Project
Start date: 11/2012
End date: 10/2017

Research Areas
Basic Research in Biology and Medicine, Biophysics, Life Sciences, Molecular Chemistry, Natural Sciences, Physical and Theoretical Chemistry, Physical Chemistry of Molecules, Interfaces and Liquids - Spectroscopy, Kinetics, Plant Biochemistry and Biophysics, Structural Biology

Research Areas
Erneuerbare Energien, Membran

Publications
Kern J, Alonso-Mori R, Tran R, Hattne J, Gildea R.G., Echols N, Glöckner C, Hellmich J, Laksmono H, Sierra R G, Lassalle-Kaiser B, Koroidov S, Lampe A, Han G, Gul S, DiFiore D, Milathianaki D, Fry A R, Miahnari A, Schafer D W, Messerschmidt M, Seibert M M, Jason Koglin E, Sokaras D, Weng T C, Sellberg J, Latimer M J, Grosse-Kunstleve R W, Zwart P H, White W H, Glatzel P, Adams P D, Bogan M J, Williams G j, Boutet S, Messinger J, Zouni A, Sauter N K, Yachandra V K, Bergmann U, Yano J, Simultaneous Femtosecond X-Ray Spectroscopy and Diffraction of Photosystem II at Room Temperature. Science 2013, 340, 491-495
http://www.sciencemag.org/content/340/6131/491.short

Glöckner C, Kern J, Broser M, Zouni A, Yachandra V, Junko Y, Structural Changes of the Oygen-evolving Complex in Photosystem II during the Catalytic Cycle, J. Biol. Chem. 2013, 288, 22607-22620
http://www.jbc.org/content/288/31/22607.short

Müh F., Zouni A., The nonheme iron in photosystem II, Photosynth Res (2013) 116: 295-414, DOI 10.1007/s11120-013-9926-y.
http://link.springer.com/article/10.1007/s11120-013-9926-y

Brose K., Zouni A., Müh F., Mroginski M.A., Maultzsch J., Simulations of the polarization-dependent Raman intensity of β-carotene in photosystem II crystals, Chemical Physics 2013, 418, 65-73
http://www.sciencedirect.com/science/article/pii/S0301010413001572

Kern, J., Tran, R., Alonso-Mori, R., Koroidov, S., Echols, N., Hattne, J., Ibrahim M., Gul, S, Laksmono, H., Sierra, R. G., Gildea, R. J., Han, G., Hellmich, J., Lassalle-Kaiser, B., Chatterjee, R., Brewster, A. S., Stan, C. A., Glöckner, C., Lampe, A., DiFiore, D., Milathianaki, D., Fry, A. R., Seibert, M. M., Koglin, J. E., Gallo, E., Uhlig, J., Sokaras, D., Weng, T.-C., Zwart, P. H., Skinner, D. E., Bogan, M. J., Messerschmidt, M., Glatzel, P., Williams, G. J., Boutet, S., Adams, P. D., Zouni, A., Messinger, J., Sauter, N. K., Bergmann, U., Yano, J., and Yachandra, V. K., Taking snapshots of photosynthetic water oxidation using femtosecond X-ray diffraction and spectroscopy Nat. Commun. 2014, 5, DOI: 10.1038/ncomms5371
http://www.nature.com/ncomms/2014/140709/ncomms5371/full/ncomms5371.html

Hellmich J, Bommer M, Burkhardt A, Ibrahim M, Kern J, Meents A, Müh F, Dobbek H, Zouni A, Native-like Photosystem II Superstructure at 2.44 Å Resolution through Detergent Extraction from the Protein Crystal, Structure 2014, 22, 1607-1615
http://www.sciencedirect.com/science/article/pii/S0969212614003141

Tran R., Kern J., Hattne J., Kroidov S., Hellmich J., Alonso-Mori R., Sauter N.K., Bergmann U., Messinger J., Zouni A., Yano J., Yachandra V.K., The Mn4Ca photosynthetic water-oxidation catalyst studied by simultaneous X-ray spectroscopy and crystallography using an X-ray free-electron laser, Phil. Trans. R. Soc. B (2014): 2014369 20130324, DOI: 10.1098/rstb.2013.0324
http://rstb.royalsocietypublishing.org/content/369/1647/20130324.short

Brecht M, Skandary S., Hellmich J., Glöckner C., Konrad A., Hussels M., Meixner A. J., Zouni A., Schlodder E., Spectroscopic properties of photosystem II core complexes from Thermosynechococcus elongatus revealed by single-molecule experiments, Biochim Biophys Acta 2014, 1837, 773-781
http://www.sciencedirect.com/science/article/pii/S0005272814000358

Skandary S, Hussels M, Konrad A, Renger T, Müh F, Bommer M, Zouni A, Meixner A.J, and Brecht M, Variation of Exciton-Vibrational Coupling in Photosystem II Core Complexes from Thermosynechococcus elongatus As Revealed by Single-Molecule Spectroscopy, The Journal of Physical Chemistry B 02/2015; 119(11). DOI:10.1021/jp510631x
http://pubs.acs.org/doi/pdf/10.1021/jp510631x

Ibrahim M, Chatterjee R, Hellmich J, Tran R, Bommer M, Yachandra V.K, Yano J, Kern J and Zouni A, Improvements in serial femtosecond crystallography of photosystem II by optimizing crystal uniformity using microseeding procedures, Structural Dynamics 07/2015; 2(4):041705. DOI: 10.1063/1.4919741
http://scitation.aip.org/docserver/fulltext/aca/journal/sdy/2/4/1.4919741.pdf?expires=1450093182&id=id&accname=guest&checksum=672DFADEE075FB166A97D58C8E322C17

Müh F, DiFiore D, and Zouni A, Influence of poly(ethylene glycol) on the micelle formation of alkyl maltosides used in membrane protein crystallization, Physical Chemistry Chemical Physics 03/2015; 17(17). DOI: 10.1039/C5CP00431D
http://pubs.rsc.org/en/content/articlepdf/2015/cp/c5cp00431d

Sierra R.G, Gati C, Laksmono H, Han Dao E, 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, Concentric-flow electrokinetic injector enables serial crystallography of ribosome and photosystem II, Nature Methods.11/2015; DOI: 10.1038/nmeth.3667
http://www.nature.com/nmeth/journal/vaop/ncurrent/pdf/nmeth.3667.pdf

Baxter E.L, Aquila L, Alonso-Mori R, Barnes C.O, Bonagura C.A, Brehmer W, Brunger A.T, Calero G, Caradoc-Davies T.T, Chatterjee R, Degrado W.F, Fraser J.S, Ibrahim M, Kern J, Kobilka B.K, Kruse A.C, Larsson K.M, Lemke, H.T, Lyubimov A.Y, Manglik A, McPhillips S.E, Norgren E, Pang S.S, Soltis S.M, Song J, Thomaston J, Tsai Y, Weis W.I, Woldeyes R.A, Yachandra V, Yano J, Zouni A, and Cohen A.E, High-density grids for efficient data collection from multiple crystals, Acta Crystallographica Section D Structural Biology 01/2016; 72(1). DOI: 10.1107/S2059798315020847
https://www.ncbi.nlm.nih.gov/pubmed/26894529

Roessler CG, Agarwal R, Allaire M, Alonso-Mori R, Andi B, Bachega JF, Bommer M, Brewster AS, Browne MC, Chatterjee R, Cho E, Cohen AE, Cowan M, Datwani S, Davidson VL, Defever J, Eaton B, Ellson R, Feng Y, Ghislain LP, Glownia JM, Han G, Hattne J, Hellmich J, Héroux A, Ibrahim M, Kern J, Kuczewski A, Lemke HT, Liu P, Majlof L, McClintock WM, Myers S, Nelsen S, Olechno J, Orville AM, Sauter NK, Soares AS, Soltis SM, Song H, Stearns RG, Tran R, Tsai Y, Uervirojnangkoorn M, Wilmot CM, Yachandra V, Yano J, Yukl ET, Zhu D, Zouni A. Acoustic Injectors for Drop-On-Demand Serial Femtosecond Crystallography. Structure. 2016 Apr 5;24(4):631-40. doi: 10.1016/j.str.2016.02.007. Epub 2016 Mar 17.
http://www.sciencedirect.com/science/article/pii/S0969212616000526

Alonso-Mori R, Asa K, Bergmann U, Brewster AS, Chatterjee R, Cooper JK, Frei HM, Fuller FD, Goggins E, Gul S, Fukuzawa H, Iablonskyi D, Ibrahim M, Katayama T, Kroll T, Kumagai Y, McClure BA, Messinger J, Motomura K, Nagaya K, Nishiyama T, Saracini C, Sato Y, Sauter NK, Sokaras D, Takanashi T, Togashi T, Ueda K, Weare WW, Weng TC, Yabashi M, Yachandra VK, Young ID, Zouni A, Kern JF, Yano J. Towards characterization of photo-excited electron transfer and catalysis in natural and artificial systems using XFELs. Faraday Discuss. 2016 Dec 16;194:621-638. doi: 10.1039/c6fd00084c.
https://www.ncbi.nlm.nih.gov/pubmed/27711803

Young ID, Ibrahim M, Chatterjee R, Gul S, Koroidov S, Brewster AS, Tran R, Alonso-Mori R, Kroll T, Michels-Clark T, Laksmono H, Sierra RG, Stan CA, Hussein R, Zhang M, Douthit L, Kubin M, de Lichtenberg C, Pham LV, Nilsson H, Cheah MH, Shevela D, Saracini C, Bean MA, Seuffert I, Sokaras D, Weng TC. Pastor E,…, Zouni A, Messinger J, Bergmann U, Sauter NK, Kern J, Yanchandra VK, Junko Yano. Structure of photosystem II and substrate binding at room temperature. Nature 540, 453–457 (15 December 2016) doi:10.1038/nature20161
http://www.nature.com/nature/journal/v540/n7633/full/nature20161.html

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,…,Zouni A, Johannes Messinger, Uwe Bergmann,…,Orville A.M, Kern J, Yachandra V.K & Yano J. Drop-on-demand sample delivery for studying biocatalysts in action at X-ray free-electron lasers. Nature Methods 14, 443–449 (2017) doi:10.1038/nmeth.4195 Published online: 27 February 2017
https://www.nature.com/articles/nmeth.4195

Skandary S, Müh F, Ashraf I, Ibrahim M, Metzger M, Zouni A, Meixner AJ, and Brecht M. Role of missing carotenoid in reducing the fluorescence of single monomeric photosystem II core complexes. Phys Chem Chem Phys. 2017 May 24;19(20):13189-13194. doi: 10.1039/c6cp07748j.
http://pubs.rsc.org/-/content/articlelanding/2017/cp/c6cp07748j/unauth#!divAbstract

Zhang M, Bommer M, Chatterjee R, Hussein R, Yano J, Dau H, Kern J, Dobbek H, Zouni A. Structural insights into the light-driven auto-assembly process of the water-oxidizing Mn4CaO5-cluster in photosystem II. Elife. 2017 Jul 18;6. pii: e26933. doi 10.7554/eLife.26933
https://elifesciences.org/articles/26933

Last updated on 2020-16-03 at 23:17