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Oxidation and reduction reactions of the water-oxidizing complex in photosystem II
Umeå University, Faculty of Science and Technology, Department of Chemistry.
2015 (English)Doctoral thesis, comprehensive summary (Other academic)Alternative title
Oxidations- och reduktionsreaktioner av det vattenoxiderande komplexet i fotosystem II (Swedish)
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 [en]
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: urn:nbn:se:umu:diva-111862ISBN: 978-91-7601-387-8 (print)OAI: oai:DiVA.org:umu-111862DiVA: diva2:873751
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
List of papers
1. Electrochemically produced hydrogen peroxide affects Joliot-type oxygen-evolution measurements of photosystem II
Open this publication in new window or tab >>Electrochemically produced hydrogen peroxide affects Joliot-type oxygen-evolution measurements of photosystem II
2014 (English)In: Biochimica et Biophysica Acta - Bioenergetics, ISSN 0005-2728, E-ISSN 1879-2650, Vol. 1837, no 9, 1411-1416 p.Article in journal (Refereed) Published
Abstract [en]

The main technique employed to characterize the efficiency of water-splitting in photosynthetic preparations in terms of miss and double hit parameters and for the determination of S-i (i = 2,3,0) state lifetimes is the measurement of flash-induced oxygen oscillation pattern on bare platinum (Joliot-type) electrodes. We demonstrate here that this technique is not innocent. Polarization of the electrode against an Ag/AgCl electrode leads to a time-dependent formation of hydrogen peroxide by two-electron reduction of dissolved oxygen continuously supplied by the flow buffer. While the miss and double hit parameters are almost unaffected by H2O2, a time dependent reduction of S-1 to S-1 occurs over a time period of 20 mm. The S-1 reduction can be largely prevented by adding catalase or by removing O-2 from the flow buffer with N-2. Importantly, we demonstrate that even at the shortest possible polarization times (40 s in our set up) the S-2 and S-0 decays are significantly accelerated by the side reaction with H2O2. The removal of hydrogen peroxide leads to unperturbed S-2 state data that reveal three instead of the traditionally reported two phases of decay. In addition, even under the best conditions (catalase + N-2; 40 s polarization) about 4% of S-1 state is observed in well dark-adapted samples, likely indicating limitations of the equal fit approach. This article is part of a Special Issue entitled: Photosynthesis Research for Sustainability: Keys to Produce Clean Energy.

Place, publisher, year, edition, pages
Elsevier, 2014
Keyword
photosystem II (PSII), oxygen evolving complex (OEC), water oxidation, manganese, hydrogen peroxide (H2O2)
National Category
Biochemistry and Molecular Biology
Identifiers
urn:nbn:se:umu:diva-94141 (URN)10.1016/j.bbabio.2014.01.013 (DOI)000341474300005 ()
Available from: 2014-10-08 Created: 2014-10-06 Last updated: 2017-12-05Bibliographically approved
2. Probing S-state advancements and recombination pathways in photosystem II with a global fit program for flash-induced oxygen evolution pattern
Open this publication in new window or tab >>Probing S-state advancements and recombination pathways in photosystem II with a global fit program for flash-induced oxygen evolution pattern
2016 (English)In: Biochimica et Biophysica Acta - Bioenergetics, ISSN 0005-2728, E-ISSN 1879-2650, Vol. 1857, no 6, 848-859 p.Article in journal (Refereed) Published
Abstract [en]

The oxygen-evolving complex (OEC) in photosystem II catalyzes the oxidation of water to molecular oxygen. Four decades ago, measurements of flash-induced oxygen evolution have shown that the OEC steps through oxidation states S0, S1, S2, S3 and S4 before O2 is released and the S0 state is reformed. The light-induced transitions between these states involve misses and double hits. While it is widely accepted that the miss parameter is S state dependent and may be further modulated by the oxidation state of the acceptor side, the traditional way of analyzing each flash-induced oxygen evolution pattern (FIOP) individually did not allow using enough free parameters to thoroughly test this proposal. Furthermore, this approach does not allow assessing whether the presently known recombination processes in photosystem II fully explain all measured oxygen yields during Si state lifetime measurements. Here we present a global fit program that simultaneously fits all flash-induced oxygen yields of a standard FIOP (2 Hz flash frequency) and of 11–18 FIOPs each obtained while probing the S0, S2 and S3 state lifetimes in spinach thylakoids at neutral pH. This comprehensive data treatment demonstrates the presence of a very slow phase of S2 decay, in addition to the commonly discussed fast and slow reduction of S2 by YD and QB, respectively. 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 or S3 → S0 transitions.

Keyword
Photosynthesis, Photosystem 2 (PSII), Oxygen (O2) evolution, Water oxidation, Kok model, Flash induced oxygen evolution pattern (FIOP)
National Category
Physical Chemistry
Research subject
Physical Chemistry
Identifiers
urn:nbn:se:umu:diva-111855 (URN)10.1016/j.bbabio.2016.03.013 (DOI)000376700000024 ()
Note

Originally published in manuscript form with title Probing S-state advancements and recombination pathways in photosystem II with a global fit program for flash-induced oxygen evolution yields

Available from: 2015-11-24 Created: 2015-11-24 Last updated: 2017-12-01Bibliographically approved
3. Effects of pH and H/D-exchange on Si-state lifetimes and miss parameters of photosystem II in the extremophilic red alga Cyanidioschyzon merolae
Open this publication in new window or tab >>Effects of pH and H/D-exchange on Si-state lifetimes and miss parameters of photosystem II in the extremophilic red alga Cyanidioschyzon merolae
(English)Manuscript (preprint) (Other academic)
Abstract [en]

The extremophilic red alga Cyanidioschyzon merolae (C. merolae) grows in hot springs at very low pH (0.2-4.0) and moderately high temperature (40-56oC). PSII in C. merolae is structurally similar to that of cyanobacteria, but the OEC is protected by the four extrinsic proteins PsbV, PsdU, PsbO and PsbQ’, but the redox potential of QA/QA- is significantly less negative in C. merolae (Em = - 104 mV) than in both T. elongatus (Em = -140 mV) and spinach (Em = - 163 mV). Since this significantly different QA/QA- redox potential is bound to affect the internal redox equilibria, we study here the efficiency of Si state transitions and the stability of the S2, S3 and S0 states as a function of pH and H/D exchange via global analysis of flash-induced oxygen evolution patterns. We demonstrate that despite the highly acidic growing conditions, photosystem II in thylakoids isolated from C. merolae behaves very similar to spinach and T. elongatus. The data indicate that the redox potential of QA/QA- plays only a minor role for the miss parameter and the S-state lifetimes, and strongly support the idea that the S2 → S3 transition is the least efficient step during the oxidation of water to molecular oxygen in photosystem II.

Keyword
Cyanidioschyzon merolae, H/D exchange, flash induced oxygen evolution pattern (FIOP), global fitting program (GFP), photosystem II (PSII), thylakoid
National Category
Physical Chemistry
Research subject
Physical Chemistry
Identifiers
urn:nbn:se:umu:diva-111860 (URN)
Available from: 2015-11-24 Created: 2015-11-24 Last updated: 2015-11-26
4. Absence of a substrate water ‘flip’ during the S2 → S3 transition of the oxygen-evolving complex in photosystem II
Open this publication in new window or tab >>Absence of a substrate water ‘flip’ during the S2 → S3 transition of the oxygen-evolving complex in photosystem II
Show others...
(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
Photosystem II (PSII), thylakoids, substrate water, Cyanidioschyzon merolae, MIMS, FIOP
National Category
Physical Chemistry
Identifiers
urn:nbn:se:umu:diva-111861 (URN)
Available from: 2015-11-24 Created: 2015-11-24 Last updated: 2015-11-26

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