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Absence of a substrate water ‘flip’ during the S2 → S3 transition of the oxygen-evolving complex in photosystem II
Umeå University, Faculty of Science and Technology, Department of Chemistry. (Johannes Messinger)
Umeå University, Faculty of Science and Technology, Department of Chemistry. (Johannes Messinger)
Department of Plant Molecular Physiology, Faculty of Biology, University of Warsaw, Poland. (Joanna Kargul)
Department of Plant Molecular Physiology, Faculty of Biology, University of Warsaw, Poland. (Joanna Kargul)
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(English)Manuscript (preprint) (Other academic)
Abstract [en]

After a sequential storage of four oxidizing equivalents created by light-induced charge separations in the reaction center of PSII the oxygen-evolving complex (OEC) in photosystem II (PSII) catalyzes the fast oxidation of two bound substrate water molecules into molecular oxygen and protons.  The oxidation states of the OEC are known as the S0, S1, S2, S3, and S4 states and involve MnIII to MnIV oxidation state changes of the Mn4CaO5 cluster. The binding of the two substrate water molecules to the manganese cluster in the S0 to S3 states is reversible and their exchange with 18O-labelled bulk water can be observed by time-resolved H218O/H216O-exchange membrane inlet mass spectrometry. One fast and one slowly exchanging substrate water were identified in both the S2 and S3 states, indicating that the two substrates are ligated in different ways. The easy interconversion of two structural forms of the Mn4CaO5 cluster in the S2 state and the possibility that only one of these forms can be oxidized to the S3 state open up the question whether the identities of the fast (Wf) and slow (Ws) exchanging substrate waters are identical in both states or if they reverse. In this study, we measured the substrate water exchange rates in the S2 and S3 states of Cyanidioschyzon merolae thylakoids. We  then probed the possible interchange of the fast (Wf) and slow (Ws) substrate water molecules by inducing the S2 → S3 transition after the completion of the fast water exchange (Wf) in the S2 state. The results proved that Wf (S2) is identical to Wf (S3) and that Ws (S2) = Ws (S3). Consequences for the mechanism of water oxidation in PSII are discussed.

Keyword [en]
Photosystem II (PSII), thylakoids, substrate water, Cyanidioschyzon merolae, MIMS, FIOP
National Category
Physical Chemistry
Identifiers
URN: urn:nbn:se:umu:diva-111861OAI: oai:DiVA.org:umu-111861DiVA: diva2:873745
Available from: 2015-11-24 Created: 2015-11-24 Last updated: 2015-11-26
In thesis
1. Oxidation and reduction reactions of the water-oxidizing complex in photosystem II
Open this publication in new window or tab >>Oxidation and reduction reactions of the water-oxidizing complex in photosystem II
2015 (English)Doctoral thesis, comprehensive summary (Other academic)
Alternative title[sv]
Oxidations- och reduktionsreaktioner av det vattenoxiderande komplexet i fotosystem II
Abstract [en]

The oxygen that we breathe and food that we eat are products of the natural photosynthesis. Molecular oxygen is crucial for life on Earth owing to its role in the glycolysis and citric acid pathways that yield in aerobic organisms the energy-rich ATP molecules. Photosynthetic water oxidation, which produces molecular oxygen from water and sunlight, is performed by higher plants, algae and cyanobacteria. Within the molecular structure of a plant cell, photosynthesis is performed by a specific intracellular organelle – the chloroplast. Chloroplasts contain a membrane system, the thylakoid membrane, which comprises lipids, quinones and a very high content of protein complexes. The unique photosynthetic oxidation of water into molecular oxygen, protons and electrons is performed by the Mn4CaO5 cluster in photosystem II (PSII) complex. Understanding the mechanism of water oxidation by Mn4CaO5 cluster is one of the great challenges in science nowadays. When the mechanism of this process is fully understood, artificial photosynthetic systems can be designed that have high efficiencies of solar energy conversion by imitating the fundamental principle of natural system. These systems can be used in future for generation of fuels from sunlight.

 

In this thesis, the efficiency of water-splitting process in natural photosynthetic preparations was studied by measuring the flash-induced oxygen evolution pattern (FIOP). The overall aim is to achieve a deeper understanding of oxygen evolving mechanism of the Mn4O5Ca cluster via developing a complete kinetic and energetic model of the light-induced redox reactions within PSII complex. On the way to reach this goal, the hydrogen peroxide that is electrochemically generated on surface of Pt-cathode was discovered. The chemical effect of electrochemically produced H2O2 that can interfere in the oxygen evolution pathway or change the observed FIOP data was demonstrated. Therefore, in order to record the clean FIOP data that are further characterized by global fitting program (GFP), H2O2 has to be abolished by catalase addition and by purging the flow buffer of the Joliot-type electrode with nitrogen gas.   

 

After FIOPs free of H2O2-induced effects were achieved, these clean data were then applied to a global fitting approach (GFP) in order to (i) result a comprehensive figure of all S-state decays whose kinetic rates were simultaneously analyzed in a high reliability and consistency, (ii) the dependence of miss parameter on S-state transitions and the oxidation state of tyrosine D (YD) can be tested, (iii) how dependent of all S-state re-combinations (to S1 state) on the various pH/pD values can be also determined in case of using Cyanidioschyzon merolae (C. merolae) thylakoids. Our data support previous suggestions that the S0 → S1 and S1 → S2 transitions involve low or no misses, while high misses occur in the S2 → S3 transition or the S3 → S0 transition. Moreover, the appearance of very slow S2 decay was clearly observed by using the GFP analysis, while there are no evidences of very slow S3 decay were recorded under all circumstances. The unknown electron donor for the very slow S2 decay which can be one of the substances of PSII-protective branch (i.e. cytochrome b559, carotenoid or ChlZ) will be determined in further researches.

Place, publisher, year, edition, pages
Umeå: Umeå University, 2015. 57 p.
Keyword
Photosystem II (PSII), oxidation, reduction, flash induced oxygen evolution pattern (FIOP), water, oxygen, global fitting program (GFP), thylakoids
National Category
Chemical Sciences
Research subject
Physical Chemistry
Identifiers
urn:nbn:se:umu:diva-111862 (URN)978-91-7601-387-8 (ISBN)
Public defence
2015-12-18, KB3B1, KBC huset, Umeå, 13:00 (English)
Opponent
Supervisors
Available from: 2015-11-27 Created: 2015-11-24 Last updated: 2015-11-26Bibliographically approved

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