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Trapping Tyrosine Z: Exploring the Relay between Photochemistry and Water Oxidation in Photosystem II
Uppsala University, Disciplinary Domain of Science and Technology, Chemistry, Department of Chemistry - Ångström, Molecular Biomimetics.
2012 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Photosystem II is unique! It remains the only enzyme that can oxidize water using light as energy input. Water oxidation in photosystem II is catalyzed by the CaMn4 cluster. The electrons extracted from the CaMn4 cluster are transferred to P680+ via the tyrosine residue D1-Tyr161 (YZ). Favorable oxidation of YZ is coupled to a proton transfer along a hydrogen bond to the nearby D1-His190 residue, resulting in the neutral radical YZ. By illuminating photosystem II at cryogenic temperatures, YZ can be trapped in a stable state. Magnetic interaction between this radical and the CaMn4 cluster gives rise to a split electron paramagnetic resonance (EPR) signal with characteristics that depend on the oxidation state (S state) of the cluster.

The mechanism by which the split EPR signals are formed is different depending on the S state. In the S0 and S1 states, split signal induction proceeds via a P680+-centered mechanism, whereas in the S2 and S3 states, our results show that split induction stems from a Mn-centered mechanism. This S state-dependent pattern of split EPR signal induction can be correlated to the charge of the CaMn4 cluster in the S state in question and has prompted us to propose a general model for the induction mechanism across the different S states. At the heart of this model is the stability or otherwise of the YZ–(D1-His190)+ pair during cryogenic illumination. The model is closely related to the sequence of electron and proton transfers from the cluster during the S cycle.

Furthermore, the important hydrogen bond between YZ and D1-His190 has been investigated by following the split EPR signal formation in the different S states as a function of pH. All split EPR signals investigated decrease in intensity with a pKa of ~4-5. This pKa can be correlated to a titration event that disrupts the essential hydrogen bond, possibly by a direct protonation of D1-His190.  This has important consequences for the function of the CaMn4 cluster as this critical YZ–D1-His190 hydrogen bond steers a multitude of reactions at the cluster.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2012. , 74 p.
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 943
Keyword [en]
Photosystem II, Tyrosine Z, EPR, proton-coupled electron transfer, hydrogen bond, pH
National Category
Biochemistry and Molecular Biology Biophysics
Identifiers
URN: urn:nbn:se:uu:diva-173575ISBN: 978-91-554-8390-6 (print)OAI: oai:DiVA.org:uu-173575DiVA: diva2:524139
Public defence
2012-06-15, Polhemsalen, Ångströmlaboratoriet, Lägerhyddsvägen 1, Uppsala, 10:15 (English)
Opponent
Supervisors
Available from: 2012-05-25 Created: 2012-04-27 Last updated: 2012-08-01Bibliographically approved
List of papers
1. Two tyrosines that changed the world: Interfacing the oxidizing power of photochemistry to water splitting in photosystem II
Open this publication in new window or tab >>Two tyrosines that changed the world: Interfacing the oxidizing power of photochemistry to water splitting in photosystem II
2012 (English)In: Biochimica et Biophysica Acta - Bioenergetics, ISSN 0005-2728, E-ISSN 1879-2650, Vol. 1817, no 1, 76-87 p.Article, review/survey (Refereed) Published
Abstract [en]

Photosystem II (PSII), the thylakoid membrane enzyme which uses sunlight to oxidize water to molecular oxygen, holds many organic and inorganic redox cofactors participating in the electron transfer reactions. Among them, two tyrosine residues, Tyr-Z and Tyr-D are found on the oxidizing side of PSII. Both tyrosines demonstrate similar spectroscopic features while their kinetic characteristics are quite different. Tyr-Z, which is bound to the D1 core protein, acts as an intermediate in electron transfer between the primary donor, P(680) and the CaMn(4) cluster. In contrast, Tyr-D, which is bound to the D2 core protein, does not participate in linear electron transfer in PSII and stays fully oxidized during PSII function. The phenolic oxygens on both tyrosines form well-defined hydrogen bonds to nearby histidine residues, His(Z) and His(D) respectively. These hydrogen bonds allow swift and almost activation less movement of the proton between respective tyrosine and histidine. This proton movement is critical and the phenolic proton from the tyrosine is thought to toggle between the tyrosine and the histidine in the hydrogen bond. It is found towards the tyrosine when this is reduced and towards the histidine when the tyrosine is oxidized. The proton movement occurs at both room temperature and ultra low temperature and is sensitive to the pH. Essentially it has been found that when the pH is below the pK(a) for respective histidine the function of the tyrosine is slowed down or, at ultra low temperature, halted. This has important consequences for the function also of the CaMn(4) complex and the protonation reactions as the critical Tyr-His hydrogen bond also steer a multitude of reactions at the CaMn(4) cluster. This review deals with the discovery and functional assignments of the two tyrosines. The pH dependent phenomena involved in oxidation and reduction of respective tyrosine is covered in detail. This article is part of a Special Issue entitled: Photosystem II.

Keyword
Photosystem II, Water oxidation, Tyrosine Z, Tyrosine D
National Category
Medical and Health Sciences
Identifiers
urn:nbn:se:uu:diva-168512 (URN)10.1016/j.bbabio.2011.03.016 (DOI)000298823000007 ()
Available from: 2012-02-13 Created: 2012-02-13 Last updated: 2017-12-07Bibliographically approved
2. Visible light induction of an EPR split signal in photosystem II in the S2 state reveals the importance of charges in the oxygen evolving center during catalysis: a unifying model
Open this publication in new window or tab >>Visible light induction of an EPR split signal in photosystem II in the S2 state reveals the importance of charges in the oxygen evolving center during catalysis: a unifying model
2012 (English)In: Biochemistry, ISSN 0006-2960, E-ISSN 1520-4995, Vol. 51, no 10, 2054-2064 p.Article in journal (Refereed) Published
Abstract [en]

Cryogenic illumination of Photosystem II (PSII) can lead to the trapping of the metastable radical Y-z(center dot), the radical form of the redox-active tyrosine residue D1-Tyr161 (known as Y-z). Magnetic interaction between this radical and the CaMn4 cluster of PSII gives rise to so-called split electron paramagnetic resonance (EPR) signals with characteristics that are dependent on the S state. We report here the observation and characterization of a split EPR signal that can be directly induced from PSII centers in the S-2 state through visible light illumination at 10 K. We further show that the induction of this split signal takes place via a Mn-centered mechanism, in the same way as when using near-infrared light illumination [Koulougliotis, D., et al. (2003) Biochemistry 42, 3045-3053]. On the basis of interpretations of these results, and in combination with literature data for other split signals induced under a variety of conditions (temperature and light quality), we propose a unified model for the mechanisms of split signal induction across the four S states (S-0, S-1, S-2, and S-3). At the heart of this model is the stability or instability of the Y-z(center dot)(D1-His190)(+) pair that would be formed during cryogenic oxidation of Y-Z. Furthermore, the model is closely related to the sequence of transfers of protons and electrons from the CaMn4, cluster during the S cycle and further demonstrates the utility of the split signals in probing the immediate environment of the oxygen-evolving center in PSII.

National Category
Biophysics Biochemistry and Molecular Biology
Identifiers
urn:nbn:se:uu:diva-173573 (URN)10.1021/bi2015794 (DOI)000301398000004 ()22352968 (PubMedID)
Available from: 2012-04-27 Created: 2012-04-27 Last updated: 2017-12-07Bibliographically approved
3. Split EPR Signal Induction from the S2 State of the Oxygen Evolving Complex in Photosystem II is Steered by the Substrate Water Analogue Methanol
Open this publication in new window or tab >>Split EPR Signal Induction from the S2 State of the Oxygen Evolving Complex in Photosystem II is Steered by the Substrate Water Analogue Methanol
Show others...
(English)Manuscript (preprint) (Other academic)
National Category
Biochemistry and Molecular Biology Biophysics
Identifiers
urn:nbn:se:uu:diva-173574 (URN)
Available from: 2012-04-27 Created: 2012-04-27 Last updated: 2012-12-20
4. Effects of pH on the S3 State of the Oxygen Evolving Complex in Photosystem II Probed by EPR Split Signal Induction
Open this publication in new window or tab >>Effects of pH on the S3 State of the Oxygen Evolving Complex in Photosystem II Probed by EPR Split Signal Induction
2010 (English)In: Biochemistry, ISSN 0006-2960, E-ISSN 1520-4995, Vol. 49, no 45, 9800-9808 p.Article in journal (Refereed) Published
Abstract [en]

The electrons extracted from the CaMn4 cluster during water oxidation in photosystem II are transferred to P-680(+) via the redox-active tyrosine D1-Tyr161 (Y-z). Upon Y-z oxidation a proton moves in a hydrogen bond toward D1-His190 (His(z)). The deprotonation and reprotonation mechanism of Y-z-OH/Y-z-O is of key importance for the catalytic turnover of photosystem II. By light illumination at liquid helium temperatures (similar to 5 K) Y-z can be oxidized to its neutral radical, Y-z(center dot). This can be followed by the induction of a split EPR signal from Y-z(center dot) in a magnetic interaction with the CaMn4 cluster, offering a way to probe for Y-z oxidation in active photosystem II. In the S-3 state, light in the near-infrared region induces the split S-3 EPR signal, S-2'Y-z(center dot). Here we report on the pH dependence for the induction of S-2'Y-z(center dot) between pH 4.0 and pH 8.7. At acidic pH the split S-3 EPR signal decreases with the apparent pK(a) (pK(app)) similar to 4.1. This can be correlated to a titration event that disrupts the essential H-bond in the Y-z-His(z) motif. At alkaline pH, the split S-3 EPR signal decreases with the pK(app) similar to 7.5. The analysis of this pH dependence is complicated by the presence of an alkaline-induced split EPR signal (pK(app) similar to 8.3) promoted by a change in the redox potential of Y-z. Our results allow dissection of the proton-coupled electron transfer reactions in the S-3 state and provide further evidence that the radical involved in the split EPR signals is indeed Y-z(center dot).

Place, publisher, year, edition, pages
Easton: American Chemical Society (ACS), 2010
National Category
Chemical Sciences
Identifiers
urn:nbn:se:uu:diva-135370 (URN)10.1021/bi101364t (DOI)000283833800016 ()
Available from: 2010-12-06 Created: 2010-12-06 Last updated: 2017-12-11Bibliographically approved
5. The S0 state of the water oxidizing complex in photosystem II: pH dependence of the EPR Split signal, induction and mechanistic implications
Open this publication in new window or tab >>The S0 state of the water oxidizing complex in photosystem II: pH dependence of the EPR Split signal, induction and mechanistic implications
2009 (English)In: Biochemistry, ISSN 0006-2960, E-ISSN 1520-4995, Vol. 48, no 40, 9393-9404 p.Article in journal (Refereed) Published
Abstract [en]

Water oxidation in photosystem II is catalyzed by the CaMn4 cluster.   The electrons extracted from the CaMn4 cluster are transferred to   P-680(+) via the redox-active tyrosine residue D1-Tyr161 (Y-Z). The   oxidation of Y-Z is coupled to a deprotonation creating the neutral   radical Y-Z(center dot). Light-induced oxidation of Y-Z is possible   down to extreme temperatures. This call be observed as a split EPR   signal from Y-Z(center dot) in a magnetic interaction with the CaMn4   cluster, offering a way to probe for Y-Z oxidation in active PSII. Here   we have used the split S-0 EPR signal to study the mechanism of Y-Z   oxidation at 5 K in the S-0 state. The state of the hydrogen bond   between Y-Z and its proposed hydrogen bond partner D1-His190 is   investigated by varying the pH. The split S-0 EPR signal was induced by   illumination at 5 K between pH 3.9 and pH 9.0. Maximum signal intensity   was observed between pH 6 and pH 7. On both the acidic and alkaline   sides the signal intensity decreased with the apparent pK(a)s (pK(app))   similar to 4.8 and similar to 7.9, respectively. The illumination   protocol used to induce the split S-0 EPR signal also induces a mixed   radical signal in the g similar to 2 region. One part of this signal   decays with similar kinetics as the split S-0 EPR signal (similar to 3   min, at 5 K) and is easily distinguished from a stable radical   originating from Car/Chi. We suggest that this fast-decaying radical   originates from Y-Z(center dot). The pH dependence of the light-induced   fast-decaying radical was measured in the same pH range. as for the   split S-0 EPR signal. The pK(app) for the light-induced fast-decaying   radical was identical at acidic pH (similar to 4.8). At alkaline pH the   behavior was more complex. Between pH 6.6 and pH 7.7 the signal   decreased with pK(app) similar to 7.2. However, above pH 7.7 the   induction of the radical species was pH independent. We compare our   results with the pH dependence of the split S-1 EPR signal induced at 5   K and the S-0 -> S-1 and S-1 -> S-2 transitions at room temperature.   The result allows mechanistic conclusions concerning differences   between the hydrogen bond pattern around Y-Z in the S-0 and S-1 states.

Place, publisher, year, edition, pages
Easton: American Chemical Society (ACS), 2009
National Category
Chemical Sciences
Identifiers
urn:nbn:se:uu:diva-99342 (URN)10.1021/bi901177w (DOI)000270459100010 ()
Available from: 2009-03-12 Created: 2009-03-12 Last updated: 2017-12-13Bibliographically approved

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