Elucidation of the photo-assembly mechanism of the light-driven water oxidizing complex in photosystem II
Oxygen photosynthesis in green plants, algae and cyanobacteria is catalyzed by the two large membrane protein complexes Photosystem I (PSI) and Photosystem II (PSII). Both complexes contain a reaction center (RC) that conducts a light-driven charge transfer across the thylakoid membrane, forming a radical pair P+A- of an oxidized primary donor P and a reduced acceptor A in picoseconds. These rapid photochemical events are accompanied by protein relaxation. The strong oxidant P+ is able to abstract electrons from water in the water-oxidizing complex (WOC), a protein-bound Mn4CaO5 cluster. The WOC passes through five intermediate states (referred to as S-states S0 to S4) corresponding to the successive abstraction of four electrons from H2O. In this way, the four-electron reaction 2 H2O O2 + 4e- + 4 H+ is coupled to the one-electron reaction in the RC. The conventional synchrotron X-ray crystallography used to determine the structure of the dimeric PSII core complex (dPSIIcc) of cyanobacteria causes radiation damage to the WOC. Although the most recent dPSIIcc structure at 1.95 Å resolution at cryogenic temperature using XFEL provided a radiation-damage-free view of the S1 state, measurements at room temperature (RT) are required to determine the dynamic mechanism of water oxidation in PSII.
Despite the recent progress in the structure elucidation and mechanistic PSII research in general, the mechanism of the light-driven assembly of the Mn4CaO5 cluster has remained elusive. Very recently, we obtained a crystal structure of PSII fully depleted of the Mn4CaO5 cluster at 2.55 Å resolution. This structure can serve as a basis for understanding the mechanism of WOC assembly/disassembly in PSII.
The understanding of the dynamic water oxidation reaction in PSII under physiological conditions is a crucial prerequisite for the design of artificial water-oxidizing catalysts. Furthermore, a systematic investigation of the photo-assembly of the Mn4CaO5 clusters into the apo (fully Mn4CaO5 depleted) – PSII single crystals are planned. The dynamic light-induced structure of the Mn4CaO5 cluster in PSII is to be decoded. This would provide important information for the synthesis of artificial water-splitting catalysts.
Zouni, Athina PD Dr. (Details) (Honorary Chairs / Professors by Special Appointment / Part-Time Lecturers)
Further project members
Participating external organisations
Financer
DFG Excellence Initiative Cluster
Duration of project
Start date: 11/2017
End date: 12/2018
Research Areas
Basic Research in Biology and Medicine, Biophysics, Life Sciences, Molecular Chemistry, Natural Sciences, Physical Chemistry, Physical Chemistry of Molecules, Liquids and Interfaces, Biophysical Chemistry, Plant Biochemistry and Biophysics, Structural Biology
Research Areas
Erneuerbare Energien, Membran
Publications
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
Kern J, Chatterjee R, Young ID, FD Fuller, Lassalle L, Ibrahim M, Gul S, Fransson T; Brewster AS, Alonso-Mori R, Hussein R, Zhang M, Douthit L, de Lichtenberg C, Cheah MH, Shevela D, Wersig J, Seuffert I, Sokaras D, Pastor E, Weninger Cl, Kroll T, … , Dobbek H, Adams PD, Bergmann U, Sauter NK, Zouni A, Messinger J, Yano J and Yachandra VK. Structures of the intermediates of Kok’s photosynthetic water oxidation clock. Nature volume 563, pages 421–425 (2018).
https://www.nature.com/articles/s41586-018-0681-2
Kölsch A, Hejazi M, Stieger KR, Feifel SC, Kern JF, Müh F, Lisdat F, Lokstein H, Zouni A. Insights into the binding behavior of native and non-native cytochromes to Photosystem I from Thermosynechococcus elongates. J Biol Chem. 2018 Jun 8;293(23):9090-9100. doi: 10.1074/jbc.RA117.000953. Epub 2018 Apr 25
