Structural isomers of the S 2 state in photosystem II: do they exist at room temperature and are they important for function?
Abstract
In nature, an oxo‐bridged Mn 4 CaO 5 cluster embedded in photosystem II (PSII), a membrane‐bound multi‐subunit pigment protein complex, catalyzes the water oxidation reaction that is driven by light‐induced charge separations in the reaction center of PSII. The Mn 4 CaO 5 cluster accumulates four oxidizing equivalents to enable the four‐electron four‐proton catalysis of two water molecules to one dioxygen molecule and cycles through five intermediate S‐states, S 0 – S 4 in the Kok cycle. One important question related to the catalytic mechanism of the oxygen‐evolving complex (OEC) that remains is, whether structural isomers are present in some of the intermediate S‐states and if such equilibria are essential for the mechanism of the O‐O bond formation. Here we compare results from electron paramagnetic resonance (EPR) and X‐ray absorption spectroscopy (XAS) obtained at cryogenic temperatures for the S 2 state of PSII with structural data collected of the S 1 , S 2 and S 3 states by serial crystallography at neutral pH (∼6.5) using an X‐ray free electron laser at room temperature. While the cryogenic data show the presence of at least two structural forms of the S 2 state, the room temperature crystallography data can be well‐described bymore »
- Authors:
-
[1];
[1];
[3];
[1];
[1]
- Molecular Biophysics and Integrated Bioimaging Division Lawrence Berkeley National Laboratory Berkeley CA 94720 USA
- Institut für Biologie, Humboldt‐Universität zu Berlin Berlin D‐10099 Germany
- Department of Chemistry – Ångström Molecular Biomimetics, Uppsala University Uppsala 75237 Sweden, Institutionen för Kemi, Kemiskt Biologiskt Centrum, Umeå Universitet Umeå 90187 Sweden
- Department of Chemistry – Ångström Molecular Biomimetics, Uppsala University Uppsala 75237 Sweden
- Publication Date:
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1500133
- Grant/Contract Number:
- DE‐AC02‐76SF00515
- Resource Type:
- Publisher's Accepted Manuscript
- Journal Name:
- Physiologia Plantarum
- Additional Journal Information:
- Journal Name: Physiologia Plantarum Journal Volume: 166 Journal Issue: 1; Journal ID: ISSN 0031-9317
- Publisher:
- Wiley-Blackwell
- Country of Publication:
- Denmark
- Language:
- English
Citation Formats
Chatterjee, Ruchira, Lassalle, Louise, Gul, Sheraz, Fuller, Franklin D., Young, Iris D., Ibrahim, Mohamed, de Lichtenberg, Casper, Cheah, Mun Hon, Zouni, Athina, Messinger, Johannes, Yachandra, Vittal K., Kern, Jan, and Yano, Junko. Structural isomers of the S 2 state in photosystem II: do they exist at room temperature and are they important for function?. Denmark: N. p., 2019.
Web. doi:10.1111/ppl.12947.
Chatterjee, Ruchira, Lassalle, Louise, Gul, Sheraz, Fuller, Franklin D., Young, Iris D., Ibrahim, Mohamed, de Lichtenberg, Casper, Cheah, Mun Hon, Zouni, Athina, Messinger, Johannes, Yachandra, Vittal K., Kern, Jan, & Yano, Junko. Structural isomers of the S 2 state in photosystem II: do they exist at room temperature and are they important for function?. Denmark. https://doi.org/10.1111/ppl.12947
Chatterjee, Ruchira, Lassalle, Louise, Gul, Sheraz, Fuller, Franklin D., Young, Iris D., Ibrahim, Mohamed, de Lichtenberg, Casper, Cheah, Mun Hon, Zouni, Athina, Messinger, Johannes, Yachandra, Vittal K., Kern, Jan, and Yano, Junko. Fri .
"Structural isomers of the S 2 state in photosystem II: do they exist at room temperature and are they important for function?". Denmark. https://doi.org/10.1111/ppl.12947.
@article{osti_1500133,
title = {Structural isomers of the S 2 state in photosystem II: do they exist at room temperature and are they important for function?},
author = {Chatterjee, Ruchira and Lassalle, Louise and Gul, Sheraz and Fuller, Franklin D. and Young, Iris D. and Ibrahim, Mohamed and de Lichtenberg, Casper and Cheah, Mun Hon and Zouni, Athina and Messinger, Johannes and Yachandra, Vittal K. and Kern, Jan and Yano, Junko},
abstractNote = {In nature, an oxo‐bridged Mn 4 CaO 5 cluster embedded in photosystem II (PSII), a membrane‐bound multi‐subunit pigment protein complex, catalyzes the water oxidation reaction that is driven by light‐induced charge separations in the reaction center of PSII. The Mn 4 CaO 5 cluster accumulates four oxidizing equivalents to enable the four‐electron four‐proton catalysis of two water molecules to one dioxygen molecule and cycles through five intermediate S‐states, S 0 – S 4 in the Kok cycle. One important question related to the catalytic mechanism of the oxygen‐evolving complex (OEC) that remains is, whether structural isomers are present in some of the intermediate S‐states and if such equilibria are essential for the mechanism of the O‐O bond formation. Here we compare results from electron paramagnetic resonance (EPR) and X‐ray absorption spectroscopy (XAS) obtained at cryogenic temperatures for the S 2 state of PSII with structural data collected of the S 1 , S 2 and S 3 states by serial crystallography at neutral pH (∼6.5) using an X‐ray free electron laser at room temperature. While the cryogenic data show the presence of at least two structural forms of the S 2 state, the room temperature crystallography data can be well‐described by just one S 2 structure. We discuss the deviating results and outline experimental strategies for clarifying this mechanistically important question.},
doi = {10.1111/ppl.12947},
journal = {Physiologia Plantarum},
number = 1,
volume = 166,
place = {Denmark},
year = {Fri Mar 15 00:00:00 EDT 2019},
month = {Fri Mar 15 00:00:00 EDT 2019}
}
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1111/ppl.12947
https://doi.org/10.1111/ppl.12947
Other availability
Search WorldCat to find libraries that may hold this journal
Cited by: 22 works
Citation information provided by
Web of Science
Web of Science
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
Water oxidation mechanism in photosystem II, including oxidations, proton release pathways, O―O bond formation and O2 release
journal, August 2013
- Siegbahn, Per E. M.
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1827, Issue 8-9
Electronic Structural Changes of Mn in the Oxygen-Evolving Complex of Photosystem II during the Catalytic Cycle
journal, April 2013
- Glatzel, Pieter; Schroeder, Henning; Pushkar, Yulia
- Inorganic Chemistry, Vol. 52, Issue 10
EPR studies of the oxygen-evolving enzyme of Photosystem II
journal, October 1984
- Zimmermann, J. L.; Rutherford, A. W.
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 767, Issue 1
Structural changes correlated with magnetic spin state isomorphism in the S 2 state of the Mn 4 CaO 5 cluster in the oxygen-evolving complex of photosystem II
journal, January 2016
- Chatterjee, Ruchira; Han, Guangye; Kern, Jan
- Chemical Science, Vol. 7, Issue 8
The low spin - high spin equilibrium in the S2-state of the water oxidizing enzyme
journal, May 2018
- Boussac, Alain; Ugur, Ilke; Marion, Antoine
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1859, Issue 5
Complete EPR Spectrum of the S 3 -State of the Oxygen-Evolving Photosystem II
journal, April 2009
- Boussac, Alain; Sugiura, Miwa; Rutherford, A. William
- Journal of the American Chemical Society, Vol. 131, Issue 14
Conversion of the Spin State of the Manganese Complex in Photosystem II Induced by Near-Infrared Light
journal, January 1996
- Boussac, Alain; Girerd, Jean-Jacques; Rutherford, A. William
- Biochemistry, Vol. 35, Issue 22
Mechanism of light induced water splitting in Photosystem II of oxygen evolving photosynthetic organisms
journal, August 2012
- Renger, Gernot
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1817, Issue 8
55Mn ESE-ENDOR of a Mixed Valence Mn(III)Mn(IV) Complex: Comparison with the Mn Cluster of the Photosynthetic Oxygen-Evolving Complex
journal, November 1995
- Randall, David W.; Sturgeon, Bradley E.; Ball, James A.
- Journal of the American Chemical Society, Vol. 117, Issue 47
Generalized approximate spin projection calculations of effective exchange integrals of the CaMn 4 O 5 cluster in the S 1 and S 3 states of the oxygen evolving complex of photosystem II
journal, January 2014
- Isobe, H.; Shoji, M.; Yamanaka, S.
- Phys. Chem. Chem. Phys., Vol. 16, Issue 24
Oxygen-evolving complex of photosystem II: correlating structure with spectroscopy
journal, January 2014
- Pokhrel, Ravi; Brudvig, Gary W.
- Physical Chemistry Chemical Physics, Vol. 16, Issue 24
Taking snapshots of photosynthetic water oxidation using femtosecond X-ray diffraction and spectroscopy
journal, July 2014
- Kern, Jan; Tran, Rosalie; Alonso-Mori, Roberto
- Nature Communications, Vol. 5, Issue 1
Electron transfer pathways from the S 2 -states to the S 3 -states either after a Ca 2+ /Sr 2+ or a Cl − /I − exchange in Photosystem II from Thermosynechococcus elongatus
journal, June 2015
- Boussac, Alain; Rutherford, A. William; Sugiura, Miwa
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1847, Issue 6-7
Redox-coupled substrate water reorganization in the active site of Photosystem II—The role of calcium in substrate water delivery
journal, June 2016
- Ugur, Ilke; Rutherford, A. William; Kaila, Ville R. I.
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1857, Issue 6
Reflections on substrate water and dioxygen formation
journal, August 2013
- Cox, Nicholas; Messinger, Johannes
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1827, Issue 8-9
Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å
journal, April 2011
- Umena, Yasufumi; Kawakami, Keisuke; Shen, Jian-Ren
- Nature, Vol. 473, Issue 7345
EPR/ENDOR characterization of the physical and electronic structure of the OEC Mn cluster
journal, January 2001
- Peloquin, Jeffrey M.; Britt, R. David
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1503, Issue 1-2
Structural changes in the Mn4Ca cluster and the mechanism of photosynthetic water splitting
journal, February 2008
- Pushkar, Y.; Yano, J.; Sauer, K.
- Proceedings of the National Academy of Sciences, Vol. 105, Issue 6
Drop-on-demand sample delivery for studying biocatalysts in action at X-ray free-electron lasers
journal, February 2017
- Fuller, Franklin D.; Gul, Sheraz; Chatterjee, Ruchira
- Nature Methods, Vol. 14, Issue 4
A five-coordinate Mn( iv ) intermediate in biological water oxidation: spectroscopic signature and a pivot mechanism for water binding
journal, January 2016
- Retegan, Marius; Krewald, Vera; Mamedov, Fikret
- Chemical Science, Vol. 7, Issue 1
Structural and Oxidation State Changes of the Photosystem II Manganese Complex in Four Transitions of the Water Oxidation Cycle (S 0 → S 1 , S 1 → S 2 , S 2 → S 3 , and S 3,4 → S 0 ) Characterized by X-ray Absorption Spectroscopy at 20 K and Room Temperature †
journal, February 2005
- Haumann, M.; Müller, C.; Liebisch, P.
- Biochemistry, Vol. 44, Issue 6
Simultaneous Femtosecond X-ray Spectroscopy and Diffraction of Photosystem II at Room Temperature
journal, February 2013
- Kern, J.; Alonso-Mori, R.; Tran, R.
- Science, Vol. 340, Issue 6131
Role of a Water Network around the Mn 4 CaO 5 Cluster in Photosynthetic Water Oxidation: A Fourier Transform Infrared Spectroscopy and Quantum Mechanics/Molecular Mechanics Calculation Study
journal, January 2016
- Nakamura, Shin; Ota, Kai; Shibuya, Yuichi
- Biochemistry, Vol. 55, Issue 3
Effect of Near-Infrared Light on the S 2 -State of the Manganese Complex of Photosystem II from Synechococcus elongatus †
journal, June 1998
- Boussac, Alain; Kuhl, Helena; Un, Sun
- Biochemistry, Vol. 37, Issue 25
Metal oxidation states in biological water splitting
journal, January 2015
- Krewald, Vera; Retegan, Marius; Cox, Nicholas
- Chemical Science, Vol. 6, Issue 3
FTIR detection of water reactions in the oxygen-evolving centre of photosystem II
journal, October 2007
- Noguchi, Takumi
- Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 363, Issue 1494
Structural Changes of the Oxygen-evolving Complex in Photosystem II during the Catalytic Cycle
journal, June 2013
- Glöckner, Carina; Kern, Jan; Broser, Matthias
- Journal of Biological Chemistry, Vol. 288, Issue 31
Chemical Equilibrium Models for the S 3 State of the Oxygen-Evolving Complex of Photosystem II
journal, November 2015
- Isobe, Hiroshi; Shoji, Mitsuo; Shen, Jian-Ren
- Inorganic Chemistry, Vol. 55, Issue 2
Strong Coupling between the Hydrogen Bonding Environment and Redox Chemistry during the S 2 to S 3 Transition in the Oxygen-Evolving Complex of Photosystem II
journal, April 2015
- Isobe, Hiroshi; Shoji, Mitsuo; Shen, Jian-Ren
- The Journal of Physical Chemistry B, Vol. 119, Issue 43
The manganese complex of photosystem II in its reaction cycle—Basic framework and possible realization at the atomic level
journal, February 2008
- Dau, H.; Haumann, M.
- Coordination Chemistry Reviews, Vol. 252, Issue 3-4
The first tyrosyl radical intermediate formed in the S2–S3 transition of photosystem II
journal, January 2014
- Retegan, Marius; Cox, Nicholas; Lubitz, Wolfgang
- Physical Chemistry Chemical Physics, Vol. 16, Issue 24
The effect of temperature on the formation and decay of the multiline EPR signal species associated with photosynthetic oxygen evolution
journal, June 1983
- Brudvig, Gary W.; Casey, John L.; Sauer, Kenneth
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 723, Issue 3
Electron paramagnetic resonance properties of the S2 state of the oxygen-evolving complex of photosystem II
journal, August 1986
- Zimmermann, J. L.; Rutherford, A. W.
- Biochemistry, Vol. 25, Issue 16
Effect of Ca 2+ /Sr 2+ Substitution on the Electronic Structure of the Oxygen-Evolving Complex of Photosystem II: A Combined Multifrequency EPR, 55 Mn-ENDOR, and DFT Study of the S 2 State
journal, March 2011
- Cox, Nicholas; Rapatskiy, Leonid; Su, Ji-Hu
- Journal of the American Chemical Society, Vol. 133, Issue 10
Biological Water Oxidation
journal, March 2013
- Cox, Nicholas; Pantazis, Dimitrios A.; Neese, Frank
- Accounts of Chemical Research, Vol. 46, Issue 7
The S 2 State of the Oxygen-Evolving Complex of Photosystem II Explored by QM/MM Dynamics: Spin Surfaces and Metastable States Suggest a Reaction Path Towards the S 3 State
journal, September 2013
- Bovi, Daniele; Narzi, Daniele; Guidoni, Leonardo
- Angewandte Chemie International Edition, Vol. 52, Issue 45
Structure of photosystem II and substrate binding at room temperature
journal, November 2016
- Young, Iris D.; Ibrahim, Mohamed; Chatterjee, Ruchira
- Nature, Vol. 540, Issue 7633
The S3 state of photosystem II: differences between the structure of the manganese complex in the S2 and S3 states determined by x-ray absorption spectroscopy
journal, January 1990
- Guiles, R. D.; Zimmermann, J. L.; McDermott, Ann E.
- Biochemistry, Vol. 29, Issue 2
55 Mn ENDOR of the S 2 -State Multiline EPR Signal of Photosystem II: Implications on the Structure of the Tetranuclear Mn Cluster
journal, November 2000
- Peloquin, Jeffrey M.; Campbell, Kristy A.; Randall, David W.
- Journal of the American Chemical Society, Vol. 122, Issue 44
EPR-detectable magnetically interacting manganese ions in the photosynthetic oxygen-evolving system after continuous illumination
journal, February 1982
- Hansson, Örjan; Andréasson, Lars-Erik
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 679, Issue 2
Impact of D1-V185 on the Water Molecules That Facilitate O 2 Formation by the Catalytic Mn 4 CaO 5 Cluster in Photosystem II
journal, June 2018
- Kim, Christopher J.; Bao, Han; Burnap, Robert L.
- Biochemistry, Vol. 57, Issue 29
Electronic Structure of the Mn 4 O x Ca Cluster in the S 0 and S 2 States of the Oxygen-Evolving Complex of Photosystem II Based on Pulse 55 Mn-ENDOR and EPR Spectroscopy
journal, November 2007
- Kulik, Leonid V.; Epel, Boris; Lubitz, Wolfgang
- Journal of the American Chemical Society, Vol. 129, Issue 44
Fourier transform infrared difference and time-resolved infrared detection of the electron and proton transfer dynamics in photosynthetic water oxidation
journal, January 2015
- Noguchi, Takumi
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1847, Issue 1
Magnetic properties of manganese in the photosynthetic oxygen-evolving complex
journal, May 1985
- De Paula, Julio C.; Brudvig, Gary W.
- Journal of the American Chemical Society, Vol. 107, Issue 9
Mn 4 Ca Cluster in Photosynthesis: Where and How Water is Oxidized to Dioxygen
journal, March 2014
- Yano, Junko; Yachandra, Vittal
- Chemical Reviews, Vol. 114, Issue 8
Nature of the inhibition of the oxygen-evolving enzyme of photosystem II induced by sodium chloride washing and reversed by the addition of calcium(2+) or strontium(2+)
journal, May 1988
- Boussac, A.; Rutherford, A. W.
- Biochemistry, Vol. 27, Issue 9
QM/MM study of the S2 to S3 transition reaction in the oxygen-evolving complex of photosystem II
journal, September 2015
- Shoji, Mitsuo; Isobe, Hiroshi; Yamaguchi, Kizashi
- Chemical Physics Letters, Vol. 636
Light-induced structural changes and the site of O=O bond formation in PSII caught by XFEL
journal, February 2017
- Suga, Michihiro; Akita, Fusamichi; Sugahara, Michihiro
- Nature, Vol. 543, Issue 7643
The manganese and calcium ions of photosynthetic oxygen evolution
journal, October 1992
- Debus, Richard J.
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1102, Issue 3
Monitoring the Reaction Process During the S 2 → S 3 Transition in Photosynthetic Water Oxidation Using Time-Resolved Infrared Spectroscopy
journal, January 2017
- Sakamoto, Hiroki; Shimizu, Tatsuki; Nagao, Ryo
- Journal of the American Chemical Society, Vol. 139, Issue 5
EPR detection of a cryogenically photogenerated intermediate in photosynthetic oxygen evolution
journal, October 1984
- Casey, John L.; Sauer, Kenneth
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 767, Issue 1
Q-Band EPR of the S2 State of Photosystem II Confirms an S=5/2 Origin of the X-Band g=4.1 Signal
journal, October 2004
- Haddy, Alice; Lakshmi, K. V.; Brudvig, Gary W.
- Biophysical Journal, Vol. 87, Issue 4
Two Interconvertible Structures that Explain the Spectroscopic Properties of the Oxygen-Evolving Complex of Photosystem II in the S 2 State
journal, August 2012
- Pantazis, Dimitrios A.; Ames, William; Cox, Nicholas
- Angewandte Chemie International Edition, Vol. 51, Issue 39
EPR spectroscopy of the manganese cluster of photosystem II
journal, June 2007
- Haddy, Alice
- Photosynthesis Research, Vol. 92, Issue 3
Seven Steps of Alternating Electron and Proton Transfer in Photosystem II Water Oxidation Traced by Time-Resolved Photothermal Beam Deflection at Improved Sensitivity
journal, August 2014
- Klauss, André; Haumann, Michael; Dau, Holger
- The Journal of Physical Chemistry B, Vol. 119, Issue 6
Alternating electron and proton transfer steps in photosynthetic water oxidation
journal, September 2012
- Klauss, A.; Haumann, M.; Dau, H.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 40
Spin State as a Marker for the Structural Evolution of Nature’s Water-Splitting Catalyst
journal, November 2015
- Krewald, Vera; Retegan, Marius; Neese, Frank
- Inorganic Chemistry, Vol. 55, Issue 2
On the guiding principles for understanding of geometrical structures of the CaMn 4 O 5 cluster in oxygen-evolving complex of photosystem II. Proposal of estimation formula of structural deformations via the Jahn–Teller effects
journal, February 2017
- Yamaguchi, K.; Shoji, M.; Isobe, H.
- Molecular Physics, Vol. 115, Issue 5
Pathway for Mn-cluster oxidation by tyrosine-Z in the S2 state of photosystem II
journal, June 2014
- Narzi, D.; Bovi, D.; Guidoni, L.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 24
Electronic structure of the oxygen-evolving complex in photosystem II prior to O-O bond formation
journal, August 2014
- Cox, N.; Retegan, M.; Neese, F.
- Science, Vol. 345, Issue 6198
COOPERATION OF CHARGES IN PHOTOSYNTHETIC O 2 EVOLUTION–I. A LINEAR FOUR STEP MECHANISM
journal, June 1970
- Kok, Bessel; Forbush, Bliss; McGLOIN, Marion
- Photochemistry and Photobiology, Vol. 11, Issue 6
X-ray Emission Spectroscopy as an in Situ Diagnostic Tool for X-ray Crystallography of Metalloproteins Using an X-ray Free-Electron Laser
journal, April 2018
- Fransson, Thomas; Chatterjee, Ruchira; Fuller, Franklin D.
- Biochemistry, Vol. 57, Issue 31
Correlation between Structure and Magnetic Spin State of the Manganese Cluster in the Oxygen-Evolving Complex of Photosystem II in the S2 State: Determination by X-ray Absorption Spectroscopy
journal, April 1994
- Liang, Wenchuan; Latimer, Matthew J.; Dau, Holger
- Biochemistry, Vol. 33, Issue 16
Intermediates of a polynuclear manganese center involved in photosynthetic oxidation of water
journal, January 1981
- Dismukes, G. C.; Siderer, Y.
- Proceedings of the National Academy of Sciences, Vol. 78, Issue 1
Protein ligation of the photosynthetic oxygen-evolving center
journal, February 2008
- Debus, R.
- Coordination Chemistry Reviews, Vol. 252, Issue 3-4
Binding of amines to the oxygen-evolving center of photosystem II
journal, October 1986
- Beck, Warren F.; Brudvig, Gary W.
- Biochemistry, Vol. 25, Issue 21
High-Spin States ( S ≥ 5 / 2 ) of the Photosystem II Manganese Complex
journal, March 1998
- Boussac, Alain; Un, Sun; Horner, Olivier
- Biochemistry, Vol. 37, Issue 12
Towards a spin coupling model for the Mn4 cluster in Photosystem II
journal, June 2005
- Charlot, Marie-France; Boussac, Alain; Blondin, Geneviève
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1708, Issue 1
The Electronic Structure of Mn in Oxides, Coordination Complexes, and the Oxygen-Evolving Complex of Photosystem II Studied by Resonant Inelastic X-ray Scattering
journal, August 2004
- Glatzel, Pieter; Bergmann, Uwe; Yano, Junko
- Journal of the American Chemical Society, Vol. 126, Issue 32
The Origin of the Multiline and g = 4.1 Electron Paramagnetic Resonance Signals from the Oxygen-Evolving System of Photosystem II
journal, May 1987
- Hansson, Örjan; Aasa, Roland; Vännga˙rd, Tore
- Biophysical Journal, Vol. 51, Issue 5
Structures of the intermediates of Kok’s photosynthetic water oxidation clock
journal, November 2018
- Kern, Jan; Chatterjee, Ruchira; Young, Iris D.
- Nature, Vol. 563, Issue 7731