The exchange of the fast substrate water in the S 2 state of photosystem II is limited by diffusion of bulk water through channels – implications for the water oxidation mechanism

de Lichtenberg, Casper; Kim, Christopher J.; Chernev, Petko; Debus, Richard J.; Messinger, Johannes

doi:10.1039/D1SC02265B

Title: The exchange of the fast substrate water in the S ₂ state of photosystem II is limited by diffusion of bulk water through channels – implications for the water oxidation mechanism

Journal Article · Wed Oct 06 00:00:00 EDT 2021 · Chemical Science

DOI:https://doi.org/10.1039/D1SC02265B· OSTI ID:1818794

^[1]; Kim, Christopher J. ^[2];

^[3];

^[2];

^[1]

Department of Chemistry, Umeå University, Linnaeus väg 6 (KBC huset), SE-901 87, Umeå, Sweden, Molecular Biomimetics, Department of Chemistry – Ångström Laboratory, Uppsala University, POB 523, SE-75120 Uppsala, Sweden
Department of Biochemistry, University of California, Riverside, California 92521, USA
Molecular Biomimetics, Department of Chemistry – Ångström Laboratory, Uppsala University, POB 523, SE-75120 Uppsala, Sweden

The molecular oxygen we breathe is produced from water-derived oxygen species bound to the Mn₄CaO₅ cluster in photosystem II (PSII). Present research points to the central oxo-bridge O5 as the ‘slow exchanging substrate water (W_s)’, while, in the S₂ state, the terminal water ligands W2 and W3 are both discussed as the ‘fast exchanging substrate water (W_f)’. A critical point for the assignment of W_f is whether or not its exchange with bulk water is limited by barriers in the channels leading to the Mn₄CaO₅ cluster. In this study, we measured the rates of H₂¹⁶O/H₂¹⁸O substrate water exchange in the S₂ and S₃ states of PSII core complexes from wild-type (WT) Synechocystis sp. PCC 6803, and from two mutants, D1-D61A and D1-E189Q, that are expected to alter water access via the Cl1/O4 channels and the O1 channel, respectively. We found that the exchange rates of W_f and W_s were unaffected by the E189Q mutation (O1 channel), but strongly perturbed by the D61A mutation (Cl1/O4 channel). It is concluded that all channels have restrictions limiting the isotopic equilibration of the inner water pool near the Mn₄CaO₅ cluster, and that D61 participates in one such barrier. In the D61A mutant this barrier is lowered so that W_f exchange occurs more rapidly. This finding removes the main argument against Ca-bound W3 as fast substrate water in the S₂ state, namely the indifference of the rate of W_f exchange towards Ca/Sr substitution.

View Journal Article

Cite

Export

Save

Research Organization:: Univ. of California, Riverside, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC); ÅForsk; Vetenskapsrådet

Grant/Contract Number:: SC0005291; 2016-051832020-03809

OSTI ID:: 1818794

Alternate ID(s):: OSTI ID: 1904513

Journal Information:: Chemical Science, Journal Name: Chemical Science Vol. 12 Journal Issue: 38; ISSN 2041-6520

Publisher:: Royal Society of Chemistry (RSC)Copyright Statement

Country of Publication:: United Kingdom

Language:: English

References (102)

Detection of the Water-Binding Sites of the Oxygen-Evolving Complex of Photosystem II Using W-Band ¹⁷ O Electron–Electron Double Resonance-Detected NMR Spectroscopy Rapatskiy, Leonid; Cox, Nicholas; Savitsky, Anton Journal of the American Chemical Society, Vol. 134, Issue 40 https://doi.org/10.1021/ja3053267	journal	September 2012
Untangling the sequence of events during the S ₂ → S ₃ transition in photosystem II and implications for the water oxidation mechanism Ibrahim, Mohamed; Fransson, Thomas; Chatterjee, Ruchira Proceedings of the National Academy of Sciences, Vol. 117, Issue 23 https://doi.org/10.1073/pnas.2000529117	journal	May 2020
Electronic–Level View of O–O Bond Formation in Nature’s Water Oxidizing Complex Corry, Thomas A.; O’Malley, Patrick J. The Journal of Physical Chemistry Letters, Vol. 11, Issue 10 https://doi.org/10.1021/acs.jpclett.0c00794	journal	May 2020
Capturing structural changes of the S ₁ to S ₂ transition of photosystem II using time-resolved serial femtosecond crystallography Li, Hongjie; Nakajima, Yoshiki; Nomura, Takashi IUCrJ, Vol. 8, Issue 3 https://doi.org/10.1107/S2052252521002177	journal	April 2021
Structures and Energetics for O ₂ Formation in Photosystem II Siegbahn, Per E. M. Accounts of Chemical Research, Vol. 42, Issue 12 https://doi.org/10.1021/ar900117k	journal	December 2009
Thermodynamics of the S ₂ -to-S ₃ state transition of the oxygen-evolving complex of photosystem II Amin, Muhamed; Kaur, Divya; Yang, Ke R. Physical Chemistry Chemical Physics, Vol. 21, Issue 37 https://doi.org/10.1039/C9CP02308A	journal	January 2019
Exploring the energetics of water permeation in photosystem II by multiple steered molecular dynamics simulations Vassiliev, Sergey; Zaraiskaya, Tatiana; Bruce, Doug Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1817, Issue 9 https://doi.org/10.1016/j.bbabio.2012.05.016	journal	September 2012
Evidence from FTIR Difference Spectroscopy That a Substrate H ₂ O Molecule for O ₂ Formation in Photosystem II Is Provided by the Ca Ion of the Catalytic Mn ₄ CaO ₅ Cluster Kim, Christopher J.; Debus, Richard J. Biochemistry, Vol. 56, Issue 20 https://doi.org/10.1021/acs.biochem.6b01278	journal	May 2017
Substrate water exchange in the S ₂ state of photosystem II is dependent on the conformation of the Mn ₄ Ca cluster de Lichtenberg, Casper; Messinger, Johannes Physical Chemistry Chemical Physics, Vol. 22, Issue 23 https://doi.org/10.1039/D0CP01380C	journal	January 2020
Redox-coupled substrate water reorganization in the active site of Photosystem II—The role of calcium in substrate water delivery Ugur, Ilke; Rutherford, A. William; Kaila, Ville R. I. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1857, Issue 6 https://doi.org/10.1016/j.bbabio.2016.01.015	journal	June 2016
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 Boussac, Alain; Rutherford, A. William; Sugiura, Miwa Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1847, Issue 6-7 https://doi.org/10.1016/j.bbabio.2015.03.006	journal	June 2015
Principles, Efficiency, and Blueprint Character of Solar-Energy Conversion in Photosynthetic Water Oxidation Dau, Holger; Zaharieva, Ivelina Accounts of Chemical Research, Vol. 42, Issue 12 https://doi.org/10.1021/ar900225y	journal	December 2009
Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å Umena, Yasufumi; Kawakami, Keisuke; Shen, Jian-Ren Nature, Vol. 473, Issue 7345 https://doi.org/10.1038/nature09913	journal	April 2011
Reflections on substrate water and dioxygen formation Cox, Nicholas; Messinger, Johannes Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1827, Issue 8-9 https://doi.org/10.1016/j.bbabio.2013.01.013	journal	August 2013
Theoretical reflections on the structural polymorphism of the oxygen-evolving complex in the S2 state and the correlations to substrate water exchange and water oxidation mechanism in photosynthesis Guo, Yu; Li, Hui; He, Lan-Lan Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1858, Issue 10 https://doi.org/10.1016/j.bbabio.2017.08.001	journal	October 2017
Effects of methanol on the S i -state transitions in photosynthetic water-splitting Nöring, Birgit; Shevela, Dmitriy; Renger, Gernot Photosynthesis Research, Vol. 98, Issue 1-3 https://doi.org/10.1007/s11120-008-9364-4	journal	September 2008
Where Water Is Oxidized to Dioxygen: Structure of the Photosynthetic Mn4Ca Cluster Yano, J.; Kern, J.; Sauer, K. Science, Vol. 314, Issue 5800 https://doi.org/10.1126/science.1128186	journal	November 2006
Water in Photosystem II: Structural, functional and mechanistic considerations Linke, Katrin; Ho, Felix M. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1837, Issue 1 https://doi.org/10.1016/j.bbabio.2013.08.003	journal	January 2014
A five-coordinate Mn( iv ) intermediate in biological water oxidation: spectroscopic signature and a pivot mechanism for water binding Retegan, Marius; Krewald, Vera; Mamedov, Fikret Chemical Science, Vol. 7, Issue 1 https://doi.org/10.1039/C5SC03124A	journal	January 2016
Metal oxidation states in biological water splitting Krewald, Vera; Retegan, Marius; Cox, Nicholas Chemical Science, Vol. 6, Issue 3 https://doi.org/10.1039/C4SC03720K	journal	January 2015
Characterization of ammonia binding to the second coordination shell of the oxygen-evolving complex of photosystem II Mandal, Manoj; Askerka, Mikhail; Banerjee, Gourab Dalton Transactions, Vol. 46, Issue 46 https://doi.org/10.1039/C7DT03901H	journal	January 2017
18O-Water exchange in photosystem II: Substrate binding and intermediates of the water splitting cycle Hillier, W.; Wydrzynski, T. Coordination Chemistry Reviews, Vol. 252, Issue 3-4 https://doi.org/10.1016/j.ccr.2007.09.004	journal	February 2008
Proton and Water Transfer Pathways in the S ₂ → S ₃ Transition of the Water-Oxidizing Complex in Photosystem II: Time-Resolved Infrared Analysis of the Effects of D1-N298A Mutation and NO ₃ ^– Substitution Okamoto, Yasutada; Shimada, Yuichiro; Nagao, Ryo The Journal of Physical Chemistry B, Vol. 125, Issue 25 https://doi.org/10.1021/acs.jpcb.1c03386	journal	June 2021
Missing Pieces in the Puzzle of Biological Water Oxidation Pantazis, Dimitrios A. ACS Catalysis, Vol. 8, Issue 10 https://doi.org/10.1021/acscatal.8b01928	journal	September 2018
The manganese complex of photosystem II in its reaction cycle—Basic framework and possible realization at the atomic level Dau, H.; Haumann, M. Coordination Chemistry Reviews, Vol. 252, Issue 3-4 https://doi.org/10.1016/j.ccr.2007.09.001	journal	February 2008
The S ₂ to S ₃ transition for water oxidation in PSII (photosystem II), revisited Siegbahn, Per E. M. Physical Chemistry Chemical Physics, Vol. 20, Issue 35 https://doi.org/10.1039/C8CP03720E	journal	January 2018
On the functional significance of substrate accessibility in the photosynthetic water oxidation mechanism Wydrzynski, Tom; Hillier, Warwick; Messinger, Johannes Physiologia Plantarum, Vol. 96, Issue 2 https://doi.org/10.1111/j.1399-3054.1996.tb00224.x	journal	February 1996
Oxygenic photosynthesis: history, status and perspective Junge, Wolfgang Quarterly Reviews of Biophysics, Vol. 52 https://doi.org/10.1017/S0033583518000112	journal	January 2019
Origins of Water Molecules in the Photosystem II Crystal Structure Sakashita, Naoki; Watanabe, Hiroshi C.; Ikeda, Takuya Biochemistry, Vol. 56, Issue 24 https://doi.org/10.1021/acs.biochem.7b00220	journal	June 2017
Monitoring Water Reactions during the S-State Cycle of the Photosynthetic Water-Oxidizing Center: Detection of the DOD Bending Vibrations by Means of Fourier Transform Infrared Spectroscopy ^† Suzuki, Hiroyuki; Sugiura, Miwa; Noguchi, Takumi Biochemistry, Vol. 47, Issue 42 https://doi.org/10.1021/bi801580e	journal	October 2008
¹⁸ O Isotope Exchange Measurements Reveal that Calcium Is Involved in the Binding of One Substrate-Water Molecule to the Oxygen-Evolving Complex in Photosystem II Hendry, Garth; Wydrzynski, Tom Biochemistry, Vol. 42, Issue 20 https://doi.org/10.1021/bi034279i	journal	May 2003
Molecular Identification of a High-Spin Deprotonated Intermediate during the S ₂ to S ₃ Transition of Nature’s Water-Oxidizing Complex Corry, Thomas A.; O’Malley, Patrick J. Journal of the American Chemical Society, Vol. 142, Issue 23 https://doi.org/10.1021/jacs.0c01351	journal	May 2020
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 Kulik, Leonid V.; Epel, Boris; Lubitz, Wolfgang Journal of the American Chemical Society, Vol. 129, Issue 44 https://doi.org/10.1021/ja071487f	journal	November 2007
Orientational Jahn–Teller Isomerism in the Dark‐Stable State of Nature's Water Oxidase Drosou, Maria; Zahariou, Georgia; Pantazis, Dimitrios A. Angewandte Chemie International Edition https://doi.org/10.1002/anie.202103425	journal	May 2021
Pulse Electron Paramagnetic Resonance Studies of the Interaction of Methanol with the S ₂ State of the Mn ₄ O ₅ Ca Cluster of Photosystem II Oyala, Paul H.; Stich, Troy A.; Stull, Jamie A. Biochemistry, Vol. 53, Issue 50 https://doi.org/10.1021/bi501323h	journal	December 2014
Relative stability of the S2 isomers of the oxygen evolving complex of photosystem II Kaur, Divya; Szejgis, Witold; Mao, Junjun Photosynthesis Research, Vol. 141, Issue 3 https://doi.org/10.1007/s11120-019-00637-6	journal	April 2019
Structural rearrangements preceding dioxygen formation by the water oxidation complex of photosystem II Bao, Han; Burnap, Robert L. Proceedings of the National Academy of Sciences, Vol. 112, Issue 45 https://doi.org/10.1073/pnas.1512008112	journal	October 2015
The O ₂ -Evolving Complex of Photosystem II: Recent Insights from Quantum Mechanics/Molecular Mechanics (QM/MM), Extended X-ray Absorption Fine Structure (EXAFS), and Femtosecond X-ray Crystallography Data Askerka, Mikhail; Brudvig, Gary W.; Batista, Victor S. Accounts of Chemical Research, Vol. 50, Issue 1 https://doi.org/10.1021/acs.accounts.6b00405	journal	December 2016
Current Understanding of the Mechanism of Water Oxidation in Photosystem II and Its Relation to XFEL Data Cox, Nicholas; Pantazis, Dimitrios A.; Lubitz, Wolfgang Annual Review of Biochemistry, Vol. 89, Issue 1 https://doi.org/10.1146/annurev-biochem-011520-104801	journal	June 2020
The D1-V185N mutation alters substrate water exchange by stabilizing alternative structures of the Mn4Ca-cluster in photosystem II de Lichtenberg, Casper; Avramov, Anton P.; Zhang, Minquan Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1862, Issue 1 https://doi.org/10.1016/j.bbabio.2020.148319	journal	January 2021
Identification of Oxidized Amino Acid Residues in the Vicinity of the Mn ₄ CaO ₅ Cluster of Photosystem II: Implications for the Identification of Oxygen Channels within the Photosystem Frankel, Laurie K.; Sallans, Larry; Limbach, Patrick A. Biochemistry, Vol. 51, Issue 32 https://doi.org/10.1021/bi300650n	journal	July 2012
Location of Methanol on the S ₂ State Mn Cluster in Photosystem II Studied by Proton Matrix Electron Nuclear Double Resonance Nagashima, Hiroki; Mino, Hiroyuki The Journal of Physical Chemistry Letters, Vol. 8, Issue 3 https://doi.org/10.1021/acs.jpclett.7b00110	journal	January 2017
Ammonia binding to the oxygen-evolving complex of photosystem II identifies the solvent-exchangeable oxygen bridge ( -oxo) of the manganese tetramer Perez Navarro, M.; Ames, W. M.; Nilsson, H. Proceedings of the National Academy of Sciences, Vol. 110, Issue 39 https://doi.org/10.1073/pnas.1304334110	journal	September 2013
Detection of one slowly exchanging substrate water molecule in the S3 state of photosystem II. Messinger, J.; Badger, M.; Wydrzynski, T. Proceedings of the National Academy of Sciences, Vol. 92, Issue 8 https://doi.org/10.1073/pnas.92.8.3209	journal	April 1995
Substrate–water exchange in photosystem II is arrested before dioxygen formation Nilsson, Håkan; Rappaport, Fabrice; Boussac, Alain Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms5305	journal	July 2014
Role of the O4 Channel in Photosynthetic Water Oxidation as Revealed by Fourier Transform Infrared Difference and Time-Resolved Infrared Analysis of the D1-S169A Mutant Shimada, Yuichiro; Kitajima-Ihara, Tomomi; Nagao, Ryo The Journal of Physical Chemistry B, Vol. 124, Issue 8 https://doi.org/10.1021/acs.jpcb.9b11946	journal	February 2020
Structures of the intermediates of Kok’s photosynthetic water oxidation clock Kern, Jan; Chatterjee, Ruchira; Young, Iris D. Nature, Vol. 563, Issue 7731 https://doi.org/10.1038/s41586-018-0681-2	journal	November 2018
On Ammonia Binding to the Oxygen-Evolving Complex of Photosystem II: A Quantum Chemical Study Schraut, Johannes; Kaupp, Martin Chemistry - A European Journal, Vol. 20, Issue 24 https://doi.org/10.1002/chem.201304464	journal	May 2014
VMD: Visual molecular dynamics Humphrey, William; Dalke, Andrew; Schulten, Klaus Journal of Molecular Graphics, Vol. 14, Issue 1 https://doi.org/10.1016/0263-7855(96)00018-5	journal	February 1996
Amino acid oxidation of the D1 and D2 proteins by oxygen radicals during photoinhibition of Photosystem II Kale, Ravindra; Hebert, Annette E.; Frankel, Laurie K. Proceedings of the National Academy of Sciences, Vol. 114, Issue 11 https://doi.org/10.1073/pnas.1618922114	journal	March 2017
The low spin - high spin equilibrium in the S2-state of the water oxidizing enzyme Boussac, Alain; Ugur, Ilke; Marion, Antoine Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1859, Issue 5 https://doi.org/10.1016/j.bbabio.2018.02.010	journal	May 2018
Mechanism of light induced water splitting in Photosystem II of oxygen evolving photosynthetic organisms Renger, Gernot Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1817, Issue 8 https://doi.org/10.1016/j.bbabio.2012.02.005	journal	August 2012
Photosynthetic Apparatus of Pea Thylakoid Membranes: Response to Growth Light Intensity Lee, Wen-Jane; Whitmarsh, John Plant Physiology, Vol. 89, Issue 3 https://doi.org/10.1104/pp.89.3.932	journal	March 1989
Assessment of the manganese cluster’s oxidation state via photoactivation of photosystem II microcrystals Cheah, Mun Hon; Zhang, Miao; Shevela, Dmitry Proceedings of the National Academy of Sciences, Vol. 117, Issue 1 https://doi.org/10.1073/pnas.1915879117	journal	December 2019
Early Binding of Substrate Oxygen Is Responsible for a Spectroscopically Distinct S ₂ State in Photosystem II Pushkar, Yulia; K. Ravari, Alireza; Jensen, Scott C. The Journal of Physical Chemistry Letters, Vol. 10, Issue 17 https://doi.org/10.1021/acs.jpclett.9b01255	journal	August 2019
NH ₃ Binding to the S ₂ State of the O ₂ -Evolving Complex of Photosystem II: Analogue to H ₂ O Binding during the S ₂ → S ₃ Transition Askerka, Mikhail; Vinyard, David J.; Brudvig, Gary W. Biochemistry, Vol. 54, Issue 38 https://doi.org/10.1021/acs.biochem.5b00974	journal	September 2015
Proton Isomers Rationalize the High- and Low-Spin Forms of the S ₂ State Intermediate in the Water-Oxidizing Reaction of Photosystem II Corry, Thomas A.; O’Malley, Patrick J. The Journal of Physical Chemistry Letters, Vol. 10, Issue 17 https://doi.org/10.1021/acs.jpclett.9b01372	journal	August 2019
Redox Isomerism in the S ₃ State of the Oxygen‐Evolving Complex Resolved by Coupled Cluster Theory Drosou, Maria; Pantazis, Dimitrios A. Chemistry – A European Journal, Vol. 27, Issue 50 https://doi.org/10.1002/chem.202101567	journal	August 2021
Production of reactive oxygen species in chloride- and calcium-depleted photosystem II and their involvement in photoinhibition Arató, András; Bondarava, Natallia; Krieger-Liszkay, Anja Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1608, Issue 2-3 https://doi.org/10.1016/j.bbabio.2003.12.003	journal	February 2004
Isotopic composition of photosynthetic O ₂ flash yields in the presence of H ₂ ¹⁸ O and HC ¹⁸ O ⁻ ₃ Radmer, Richard; Ollinger, Otto FEBS Letters, Vol. 110, Issue 1 https://doi.org/10.1016/0014-5793(80)80022-6	journal	January 1980
Evaluation of different mechanistic proposals for water oxidation in photosynthesis on the basis of Mn4OxCa structures for the catalytic site and spectroscopic data Messinger, Johannes Physical Chemistry Chemical Physics, Vol. 6, Issue 20 https://doi.org/10.1039/b406437b	journal	January 2004
Glutamate 189 of the D1 Polypeptide Modulates the Magnetic and Redox Properties of the Manganese Cluster and Tyrosine Y _Z in Photosystem II ^† Debus, Richard J.; Campbell, Kristy A.; Pham, Donna P. Biochemistry, Vol. 39, Issue 21 https://doi.org/10.1021/bi992749w	journal	May 2000
Substrate water exchange in photosystem II core complexes of the extremophilic red alga Cyanidioschyzon merolae Nilsson, Håkan; Krupnik, Tomasz; Kargul, Joanna Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1837, Issue 8 https://doi.org/10.1016/j.bbabio.2014.04.001	journal	August 2014
Investigation of substrate water interactions at the high-affinity Mn site in the photosystem II oxygen-evolving complex Singh, Sonita; Debus, Richard J.; Wydrzynski, Tom Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 363, Issue 1494 https://doi.org/10.1098/rstb.2007.2219	journal	October 2007
Large-scale QM/MM calculations of the CaMn ₄ O ₅ cluster in the S ₃ state of the oxygen evolving complex of photosystem II. Comparison between water-inserted and no water-inserted structures Shoji, Mitsuo; Isobe, Hiroshi; Nakajima, Takahito Faraday Discussions, Vol. 198 https://doi.org/10.1039/C6FD00230G	journal	January 2017
FTIR detection of water reactions in the oxygen-evolving centre of photosystem II Noguchi, Takumi Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 363, Issue 1494 https://doi.org/10.1098/rstb.2007.2214	journal	October 2007
OO Bond Formation in the S4 State of the Oxygen-Evolving Complex in Photosystem II Siegbahn, Per E. M. Chemistry - A European Journal, Vol. 12, Issue 36 https://doi.org/10.1002/chem.200600774	journal	December 2006
Proton transport facilitating water-oxidation: the role of second sphere ligands surrounding the catalytic metal cluster Bao, Han; Dilbeck, Preston L.; Burnap, Robert L. Photosynthesis Research, Vol. 116, Issue 2-3 https://doi.org/10.1007/s11120-013-9907-1	journal	August 2013
Ammonia Binds to the Dangler Manganese of the Photosystem II Oxygen-Evolving Complex Oyala, Paul H.; Stich, Troy A.; Debus, Richard J. Journal of the American Chemical Society, Vol. 137, Issue 27 https://doi.org/10.1021/jacs.5b04768	journal	July 2015
One of the Substrate Waters for O ₂ Formation in Photosystem II Is Provided by the Water-Splitting Mn ₄ CaO ₅ Cluster’s Ca ²⁺ Ion Kim, Christopher J.; Debus, Richard J. Biochemistry, Vol. 58, Issue 29 https://doi.org/10.1021/acs.biochem.9b00418	journal	June 2019
Architecture of the Photosynthetic Oxygen-Evolving Center Ferreira, K. N. Science, Vol. 303, Issue 5665 https://doi.org/10.1126/science.1093087	journal	March 2004
Molecular Structure of the S ₂ State with a g = 5 Signal in the Oxygen Evolving Complex of Photosystem II Taguchi, Shota; Noguchi, Takumi; Mino, Hiroyuki The Journal of Physical Chemistry B, Vol. 124, Issue 27 https://doi.org/10.1021/acs.jpcb.0c02913	journal	June 2020
Temperature dependence of the high-spin S2 to S3 transition in Photosystem II: Mechanistic consequences Boussac, Alain Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1860, Issue 6 https://doi.org/10.1016/j.bbabio.2019.05.001	journal	June 2019
Mono-manganese mechanism of the photosytem II water splitting reaction by a unique Mn4Ca cluster Kusunoki, Masami Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1767, Issue 6 https://doi.org/10.1016/j.bbabio.2007.03.012	journal	June 2007
Theoretical Evaluation of Structural Models of the S ₂ State in the Oxygen Evolving Complex of Photosystem II: Protonation States and Magnetic Interactions Ames, William; Pantazis, Dimitrios A.; Krewald, Vera Journal of the American Chemical Society, Vol. 133, Issue 49 https://doi.org/10.1021/ja2041805	journal	December 2011
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 Bovi, Daniele; Narzi, Daniele; Guidoni, Leonardo Angewandte Chemie International Edition, Vol. 52, Issue 45 https://doi.org/10.1002/anie.201306667	journal	September 2013
Extended protein/water H-bond networks in photosynthetic water oxidation Bondar, Ana-Nicoleta; Dau, Holger Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1817, Issue 8 https://doi.org/10.1016/j.bbabio.2012.03.031	journal	August 2012
Investigation of a Pathway for Water Delivery in Photosystem II Protein by Molecular Dynamics Simulation Ogata, Koji; Hatakeyama, Makoto; Sakamoto, Yuki The Journal of Physical Chemistry B, Vol. 123, Issue 30 https://doi.org/10.1021/acs.jpcb.9b04838	journal	July 2019
Mechanism of Methanol Inhibition of Photosynthetic Water Oxidation As Studied by Fourier Transform Infrared Difference and Time-Resolved Infrared Spectroscopies Yata, Haruna; Noguchi, Takumi Biochemistry, Vol. 57, Issue 32 https://doi.org/10.1021/acs.biochem.8b00596	journal	July 2018
The Mn Cluster in the S ₀ State of the Oxygen-Evolving Complex of Photosystem II Studied by EXAFS Spectroscopy: Are There Three Di-μ-oxo-bridged Mn ₂ Moieties in the Tetranuclear Mn Complex? Robblee, John H.; Messinger, Johannes; Cinco, Roehl M. Journal of the American Chemical Society, Vol. 124, Issue 25 https://doi.org/10.1021/ja011621a	journal	June 2002
Structure-based mechanism of photosynthetic water oxidation McEvoy, James P.; Brudvig, Gary W. Physical Chemistry Chemical Physics, Vol. 6, Issue 20 https://doi.org/10.1039/b407500e	journal	January 2004
Differences in the Active Site of Water Oxidation among Photosynthetic Organisms Retegan, Marius; Pantazis, Dimitrios A. Journal of the American Chemical Society, Vol. 139, Issue 41 https://doi.org/10.1021/jacs.7b06351	journal	September 2017
The First State in the Catalytic Cycle of the Water-Oxidizing Enzyme: Identification of a Water-Derived μ-Hydroxo Bridge Lohmiller, Thomas; Krewald, Vera; Sedoud, Arezki Journal of the American Chemical Society, Vol. 139, Issue 41 https://doi.org/10.1021/jacs.7b05263	journal	October 2017
QM/MM study of the S2 to S3 transition reaction in the oxygen-evolving complex of photosystem II Shoji, Mitsuo; Isobe, Hiroshi; Yamaguchi, Kizashi Chemical Physics Letters, Vol. 636 https://doi.org/10.1016/j.cplett.2015.07.039	journal	September 2015
Light-induced structural changes and the site of O=O bond formation in PSII caught by XFEL Suga, Michihiro; Akita, Fusamichi; Sugahara, Michihiro Nature, Vol. 543, Issue 7643 https://doi.org/10.1038/nature21400	journal	February 2017
An oxyl/oxo mechanism for oxygen-oxygen coupling in PSII revealed by an x-ray free-electron laser Suga, Michihiro; Akita, Fusamichi; Yamashita, Keitaro Science, Vol. 366, Issue 6463 https://doi.org/10.1126/science.aax6998	journal	October 2019
Substrate Water Exchange for the Oxygen Evolving Complex in PSII in the S ₁ , S ₂ , and S ₃ States Siegbahn, Per E. M. Journal of the American Chemical Society, Vol. 135, Issue 25 https://doi.org/10.1021/ja401517e	journal	June 2013
Interaction of methanol with the oxygen-evolving complex: atomistic models, channel identification, species dependence, and mechanistic implications Retegan, Marius; Pantazis, Dimitrios A. Chemical Science, Vol. 7, Issue 10 https://doi.org/10.1039/C6SC02340A	journal	January 2016
A proposal for water oxidation in photosystem II Pecoraro, V. L.; Baldwin, M. J.; Caudle, M. T. Pure and Applied Chemistry, Vol. 70, Issue 4 https://doi.org/10.1351/pac199870040925	journal	January 1998
Reactive oxygen species leave a damage trail that reveals water channels in Photosystem II Weisz, Daniel A.; Gross, Michael L.; Pakrasi, Himadri B. Science Advances, Vol. 3, Issue 11 https://doi.org/10.1126/sciadv.aao3013	journal	November 2017
Two Interconvertible Structures that Explain the Spectroscopic Properties of the Oxygen-Evolving Complex of Photosystem II in the S ₂ State Pantazis, Dimitrios A.; Ames, William; Cox, Nicholas Angewandte Chemie International Edition, Vol. 51, Issue 39 https://doi.org/10.1002/anie.201204705	journal	August 2012
S ₃ State of the O ₂ -Evolving Complex of Photosystem II: Insights from QM/MM, EXAFS, and Femtosecond X-ray Diffraction Askerka, Mikhail; Wang, Jimin; Vinyard, David J. Biochemistry, Vol. 55, Issue 7 https://doi.org/10.1021/acs.biochem.6b00041	journal	February 2016
Proton-Coupled Electron Transfer During the S-State Transitions of the Oxygen-Evolving Complex of Photosystem II Amin, Muhamed; Vogt, Leslie; Szejgis, Witold The Journal of Physical Chemistry B, Vol. 119, Issue 24 https://doi.org/10.1021/jp510948e	journal	December 2014
Why nature chose the Mn ₄ CaO ₅ cluster as water-splitting catalyst in photosystem II: a new hypothesis for the mechanism of O–O bond formation Zhang, Biaobiao; Sun, Licheng Dalton Transactions, Vol. 47, Issue 41 https://doi.org/10.1039/C8DT01931B	journal	January 2018
Electronic structure of the oxygen-evolving complex in photosystem II prior to O-O bond formation Cox, N.; Retegan, M.; Neese, F. Science, Vol. 345, Issue 6198 https://doi.org/10.1126/science.1254910	journal	August 2014
COOPERATION OF CHARGES IN PHOTOSYNTHETIC O ₂ EVOLUTION–I. A LINEAR FOUR STEP MECHANISM Kok, Bessel; Forbush, Bliss; McGLOIN, Marion Photochemistry and Photobiology, Vol. 11, Issue 6 https://doi.org/10.1111/j.1751-1097.1970.tb06017.x	journal	June 1970
Inorganic and Bioinorganic Solvent Exchange Mechanisms Helm, Lothar; Merbach, André E. Chemical Reviews, Vol. 105, Issue 6 https://doi.org/10.1021/cr030726o	journal	June 2005
Five-coordinate Mn ^IV intermediate in the activation of nature’s water splitting cofactor Chrysina, Maria; Heyno, Eiri; Kutin, Yury Proceedings of the National Academy of Sciences, Vol. 116, Issue 34 https://doi.org/10.1073/pnas.1817526116	journal	August 2019
The D1-D61N Mutation in Synechocystis sp. PCC 6803 Allows the Observation of pH-Sensitive Intermediates in the Formation and Release of O ₂ from Photosystem II Dilbeck, Preston L.; Hwang, Hong Jin; Zaharieva, Ivelina Biochemistry, Vol. 51, Issue 6 https://doi.org/10.1021/bi201659f	journal	February 2012
Evidence from FTIR Difference Spectroscopy That D1-Asp61 Influences the Water Reactions of the Oxygen-Evolving Mn ₄ CaO ₅ Cluster of Photosystem II Debus, Richard J. Biochemistry, Vol. 53, Issue 18 https://doi.org/10.1021/bi500309f	journal	April 2014
Photosynthetic O2 Formation Tracked by Time-Resolved X-ray Experiments Haumann, M. Science, Vol. 310, Issue 5750 https://doi.org/10.1126/science.1117551	journal	November 2005
Oxygenic Photosystem II: The Mutation D1−D61N in Synechocystis sp. PCC 6803 Retards S-State Transitions without Affecting Electron Transfer from Y _Z to P ₆₈₀ ⁺ ^† Hundelt, Monika; Hays, Anna-Maria A.; Debus, Richard J. Biochemistry, Vol. 37, Issue 41 https://doi.org/10.1021/bi981164j	journal	October 1998

Similar Records

D1-S169A Substitution of Photosystem II Perturbs Water Oxidation

Journal Article · Fri Feb 01 00:00:00 EST 2019 · Biochemistry · OSTI ID:1818794

Ghosh, Ipsita; Banerjee, Gourab; Kim, Christopher J.; +4 more

Impact of D1-V185 on the Water Molecules That Facilitate O₂ Formation by the Catalytic Mn₄CaO₅ Cluster in Photosystem II

Journal Article · Tue Jun 26 00:00:00 EDT 2018 · Biochemistry · OSTI ID:1818794

Kim, Christopher J.; Bao, Han; Burnap, Robert L.; +1 more

Evolutionary diversity of proton and water channels on the oxidizing side of photosystem II and their relevance to function

Journal Article · Fri Jun 02 00:00:00 EDT 2023 · Photosynthesis Research · OSTI ID:1818794

Hussein, Rana; Ibrahim, Mohamed; Bhowmick, Asmit; +9 more

Related Subjects

37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY

Title: The exchange of the fast substrate water in the S 2 state of photosystem II is limited by diffusion of bulk water through channels – implications for the water oxidation mechanism

Citation Formats

References (102)

Similar Records

Related Subjects

Title: The exchange of the fast substrate water in the S ₂ state of photosystem II is limited by diffusion of bulk water through channels – implications for the water oxidation mechanism