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Title: One of the Substrate Waters for O2 Formation in Photosystem II Is Provided by the Water-Splitting Mn4CaO5 Cluster’s Ca2+ Ion

Journal Article · · Biochemistry

During the catalytic step immediately prior to O–O bond formation in Photosystem II, a water molecule deprotonates and moves next to the water-splitting Mn4CaO5 cluster’s O5 oxo bridge. Considerable evidence identifies O5 as one of the two substrate waters that ultimately form O2. The relocated oxygen, known as O6 or Ox, may be the second. It is currently debated whether O6 or Ox originates as the Mn-bound water denoted W2 or as the Ca2+-bound water denoted W3. To distinguish between these two possibilities, we analyzed the D–O–D bending mode of the water molecule that deprotonates/relocates to become O6/Ox. Here, we show that this D–O–D bending mode is not altered by the D1-S169A mutation. Previously, we showed that this D–O–D bending mode is altered substantially when Sr2+ is substituted for Ca2+. Because Sr2+/Ca2+ substitution alters this D–O–D bending mode but the D1-S169A mutation does not, we conclude that the water-derived oxygen that relocates and becomes O6/Ox derives from the Ca2+-bound W3. This conclusion provides an important constraint for proposed mechanisms of O–O bond formation in Photosystem II.

Research Organization:
Univ. of California, Riverside, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division
Grant/Contract Number:
SC0005291
OSTI ID:
1785444
Journal Information:
Biochemistry, Vol. 58, Issue 29; ISSN 0006-2960
Publisher:
American Chemical Society (ACS)Copyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 24 works
Citation information provided by
Web of Science

References (67)

Recent developments in biological water oxidation journal April 2016
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 journal December 2016
Missing Pieces in the Puzzle of Biological Water Oxidation journal September 2018
Water oxidation in photosystem II journal June 2019
Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å journal April 2011
Native structure of photosystem II at 1.95 Å resolution viewed by femtosecond X-ray pulses journal November 2014
Two Different Structures of the Oxygen-Evolving Complex in the Same Polypeptide Frameworks of Photosystem II journal January 2017
Structure of spinach photosystem II–LHCII supercomplex at 3.2 Å resolution journal May 2016
Subunit and chlorophyll organization of the plant photosystem II supercomplex journal June 2017
Structure and assembly mechanism of plant C 2 S 2 M 2 -type PSII-LHCII supercomplex journal August 2017
Structure, assembly and energy transfer of plant photosystem II supercomplex journal September 2018
Light-induced structural changes and the site of O=O bond formation in PSII caught by XFEL journal February 2017
Structures of the intermediates of Kok’s photosynthetic water oxidation clock journal November 2018
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 journal September 2012
Ammonia binding to the oxygen-evolving complex of photosystem II identifies the solvent-exchangeable oxygen bridge ( -oxo) of the manganese tetramer journal September 2013
Structure, ligands and substrate coordination of the oxygen-evolving complex of photosystem II in the S2 state: a combined EPR and DFT study journal January 2014
The First State in the Catalytic Cycle of the Water-Oxidizing Enzyme: Identification of a Water-Derived μ-Hydroxo Bridge journal October 2017
18O-Water exchange in photosystem II: Substrate binding and intermediates of the water splitting cycle journal February 2008
Reflections on substrate water and dioxygen formation journal August 2013
Substrate water exchange in photosystem II core complexes of the extremophilic red alga Cyanidioschyzon merolae journal August 2014
Computational Insights on Crystal Structures of the Oxygen-Evolving Complex of Photosystem II with Either Ca 2+ or Ca 2+ Substituted by Sr 2+ journal January 2015
Electronic structure of the oxygen-evolving complex in photosystem II prior to O-O bond formation journal August 2014
Two Interconvertible Structures that Explain the Spectroscopic Properties of the Oxygen-Evolving Complex of Photosystem II in the S 2 State journal August 2012
Theoretical illumination of water-inserted structures of the CaMn4O5 cluster in the S2 and S3 states of oxygen-evolving complex of photosystem II: full geometry optimizations by B3LYP hybrid density functional journal January 2012
Structural isomers of the S 2 state in photosystem II: do they exist at room temperature and are they important for function? journal March 2019
Structures and Energetics for O 2 Formation in Photosystem II journal December 2009
Water oxidation mechanism in photosystem II, including oxidations, proton release pathways, O―O bond formation and O2 release journal August 2013
Alternative mechanisms for O 2 release and O–O bond formation in the oxygen evolving complex of photosystem II journal January 2015
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
QM/MM study of the S2 to S3 transition reaction in the oxygen-evolving complex of photosystem II journal September 2015
Mechanism of Water Delivery to the Active Site of Photosystem II along the S 2 to S 3 Transition journal January 2016
Reorganization of Substrate Waters between the Closed and Open Cubane Conformers during the S 2 to S 3 Transition in the Oxygen Evolving Complex journal October 2015
A five-coordinate Mn( iv ) intermediate in biological water oxidation: spectroscopic signature and a pivot mechanism for water binding journal January 2016
Redox-coupled substrate water reorganization in the active site of Photosystem II—The role of calcium in substrate water delivery journal June 2016
Interaction of methanol with the oxygen-evolving complex: atomistic models, channel identification, species dependence, and mechanistic implications journal January 2016
The S 2 to S 3 transition for water oxidation in PSII (photosystem II), revisited journal January 2018
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 journal September 2015
S 3 State of the O 2 -Evolving Complex of Photosystem II: Insights from QM/MM, EXAFS, and Femtosecond X-ray Diffraction journal February 2016
Crystallographic Data Support the Carousel Mechanism of Water Supply to the Oxygen-Evolving Complex of Photosystem II journal September 2017
The open-cubane oxo–oxyl coupling mechanism dominates photosynthetic oxygen evolution: a comprehensive DFT investigation on O–O bond formation in the S 4 state journal January 2017
Theoretical Evaluation of Structural Models of the S 2 State in the Oxygen Evolving Complex of Photosystem II: Protonation States and Magnetic Interactions 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 journal September 2013
A Comparison of Experimental and Broken Symmetry Density Functional Theory (BS-DFT) Calculated Electron Paramagnetic Resonance (EPR) Parameters for Intermediates Involved in the S 2 to S 3 State Transition of Nature’s Oxygen Evolving Complex journal January 2018
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 journal October 2008
Evidence from FTIR Difference Spectroscopy That D1-Asp61 Influences the Water Reactions of the Oxygen-Evolving Mn 4 CaO 5 Cluster of Photosystem II journal April 2014
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 journal May 2017
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
D1-S169A Substitution of Photosystem II Perturbs Water Oxidation journal February 2019
Structure of Sr-substituted photosystem II at 2.1 A resolution and its implications in the mechanism of water oxidation journal February 2013
Characterization of the Sr 2+ - and Cd 2+ -Substituted Oxygen-Evolving Complex of Photosystem II by Quantum Mechanics/Molecular Mechanics Calculations journal September 2015
What does the Sr-substituted 2.1 Å resolution crystal structure of photosystem II reveal about the water oxidation mechanism? journal January 2014
Site-Directed Photosystem II Mutants with Perturbed Oxygen-Evolving Properties. 1. Instability or Inefficient Assembly of the Manganese Cluster In vivo journal May 1994
Flash-Induced FTIR Difference Spectra of the Water Oxidizing Complex in Moderately Hydrated Photosystem II Core Films:  Effect of Hydration Extent on S-State Transitions journal February 2002
Analysis of Flash-Induced FTIR Difference Spectra of the S-State Cycle in the Photosynthetic Water-Oxidizing Complex by Uniform 15 N and 13 C Isotope Labeling journal May 2003
Mid- to Low-Frequency Fourier Transform Infrared Spectra of S-State Cycle for Photosynthetic Water Oxidation in Synechocystis sp. PCC 6803 journal June 2004
Light-induced FTIR difference spectroscopy as a powerful tool toward understanding the molecular mechanism of photosynthetic oxygen evolution journal February 2007
Fourier transform infrared analysis of the photosynthetic oxygen-evolving center journal February 2008
Protein ligation of the photosynthetic oxygen-evolving center journal February 2008
Monitoring the reactions of photosynthetic water oxidation using infrared spectroscopy journal January 2013
FTIR studies of metal ligands, networks of hydrogen bonds, and water molecules near the active site Mn4CaO5 cluster in Photosystem II journal January 2015
Fourier transform infrared difference and time-resolved infrared detection of the electron and proton transfer dynamics in photosynthetic water oxidation journal January 2015
The low spin - high spin equilibrium in the S2-state of the water oxidizing enzyme journal May 2018
Monitoring the Reaction Process During the S 2 → S 3 Transition in Photosynthetic Water Oxidation Using Time-Resolved Infrared Spectroscopy journal January 2017
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
Sequential and Coupled Proton and Electron Transfer Events in the S 2 → S 3 Transition of Photosynthetic Water Oxidation Revealed by Time-Resolved X-ray Absorption Spectroscopy journal December 2016
S 0 -State Model of the Oxygen-Evolving Complex of Photosystem II journal October 2013
Metal oxidation states in biological water splitting journal January 2015