Rapid Evolution of the Photosystem II Electronic Structure during Water Splitting

Davis, Katherine M.; Sullivan, Brendan T.; Palenik, Mark C.; Yan, Lifen; Purohit, Vatsal; Robison, Gregory; Kosheleva, Irina; Henning, Robert W.; Seidler, Gerald T.; Pushkar, Yulia

doi:10.1103/PhysRevX.8.041014

Title: Rapid Evolution of the Photosystem II Electronic Structure during Water Splitting

Journal Article · Mon Oct 01 00:00:00 EDT 2018 · Physical Review. X

DOI:https://doi.org/10.1103/PhysRevX.8.041014· OSTI ID:1480343

Davis, Katherine M.; Sullivan, Brendan T.; Palenik, Mark C.; Yan, Lifen; Purohit, Vatsal; Robison, Gregory; Kosheleva, Irina; Henning, Robert W.; Seidler, Gerald T.; Pushkar, Yulia

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Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Sponsoring Organization:: National Science Foundation (NSF)

OSTI ID:: 1480343

Journal Information:: Physical Review. X, Vol. 8, Issue 4; ISSN 2160-3308

Publisher:: American Physical Society

Country of Publication:: United States

Language:: ENGLISH

References (50)

Water oxidation mechanism in photosystem II, including oxidations, proton release pathways, O―O bond formation and O2 release Siegbahn, Per E. M. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1827, Issue 8-9 https://doi.org/10.1016/j.bbabio.2012.10.006	journal	August 2013
Probing the 3d Spin Momentum with X-ray Emission Spectroscopy: The Case of Molecular-Spin Transitions Vankó, György; Neisius, Thomas; Molnár, Gábor The Journal of Physical Chemistry B, Vol. 110, Issue 24 https://doi.org/10.1021/jp0615961	journal	June 2006
Reaction kinetics for positive charge accumulation on the water side of choloplast photosystem II T. Babcock, Gerald; E. Blankenship, Robert; Sauer, Kenneth FEBS Letters, Vol. 61, Issue 2 https://doi.org/10.1016/0014-5793(76)81058-7	journal	January 1976
Kα X-ray Emission Spectroscopy on the Photosynthetic Oxygen-Evolving Complex Supports Manganese Oxidation and Water Binding in the S ₃ State Schuth, Nils; Zaharieva, Ivelina; Chernev, Petko Inorganic Chemistry, Vol. 57, Issue 16 https://doi.org/10.1021/acs.inorgchem.8b01674	journal	April 2018
Absence of Mn-Centered Oxidation in the S₂ → S₃ Transition: Implications for the Mechanism of Photosynthetic Water Oxidation Messinger, Johannes; Robblee, John H.; Bergmann, Uwe Journal of the American Chemical Society, Vol. 123, Issue 32 https://doi.org/10.1021/ja004307+	journal	July 2001
Possible mechanisms of water splitting reaction based on proton and electron release pathways revealed for CaMn4O5 cluster of PSII refined to 1.9 Å X-ray resolution Saito, T.; Yamanaka, S.; Kanda, K. International Journal of Quantum Chemistry, Vol. 112, Issue 1 https://doi.org/10.1002/qua.23218	journal	August 2011
Cyanobacterial photosystem II at 2.9-Å resolution and the role of quinones, lipids, channels and chloride Guskov, Albert; Kern, Jan; Gabdulkhakov, Azat Nature Structural & Molecular Biology, Vol. 16, Issue 3 https://doi.org/10.1038/nsmb.1559	journal	February 2009
X-ray Detection of the Period-Four Cycling of the Manganese Cluster in Photosynthetic Water Oxidizing Enzyme Ono, T. -a.; Noguchi, T.; Inoue, Y. Science, Vol. 258, Issue 5086 https://doi.org/10.1126/science.258.5086.1335	journal	November 1992
High resolution 1s core hole X-ray spectroscopy in 3d transition metal complexes—electronic and structural information Glatzel, Pieter; Bergmann, Uwe Coordination Chemistry Reviews, Vol. 249, Issue 1-2 https://doi.org/10.1016/j.ccr.2004.04.011	journal	January 2005
Taking snapshots of photosynthetic water oxidation using femtosecond X-ray diffraction and spectroscopy Kern, Jan; Tran, Rosalie; Alonso-Mori, Roberto Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms5371	journal	July 2014
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
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 Zaharieva, Ivelina; Dau, Holger; Haumann, Michael Biochemistry, Vol. 55, Issue 50 https://doi.org/10.1021/acs.biochem.6b01078	journal	December 2016
Photosynthetic water oxidation at elevated dioxygen partial pressure monitored by time-resolved X-ray absorption measurements Haumann, M.; Grundmeier, A.; Zaharieva, I. Proceedings of the National Academy of Sciences, Vol. 105, Issue 45 https://doi.org/10.1073/pnas.0802596105	journal	November 2008
Model of the Oxygen Evolving Complex Which Is Highly Predisposed to O–O Bond Formation Pushkar, Yulia; Davis, Katherine M.; Palenik, Mark C. The Journal of Physical Chemistry Letters, Vol. 9, Issue 12 https://doi.org/10.1021/acs.jpclett.8b00800	journal	June 2018
Structural changes in the Mn4Ca cluster and the mechanism of photosynthetic water splitting Pushkar, Y.; Yano, J.; Sauer, K. Proceedings of the National Academy of Sciences, Vol. 105, Issue 6 https://doi.org/10.1073/pnas.0707092105	journal	February 2008
Drop-on-demand sample delivery for studying biocatalysts in action at X-ray free-electron lasers Fuller, Franklin D.; Gul, Sheraz; Chatterjee, Ruchira Nature Methods, Vol. 14, Issue 4 https://doi.org/10.1038/nmeth.4195	journal	February 2017
Simultaneous Femtosecond X-ray Spectroscopy and Diffraction of Photosystem II at Room Temperature Kern, J.; Alonso-Mori, R.; Tran, R. Science, Vol. 340, Issue 6131 https://doi.org/10.1126/science.1234273	journal	February 2013
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 ^† Haumann, M.; Müller, C.; Liebisch, P. Biochemistry, Vol. 44, Issue 6 https://doi.org/10.1021/bi048697e	journal	February 2005
Full geometry optimizations of the mixed-valence CaMn ₄ O ₄ X(H ₂ O) ₄ (X=OH or O) cluster in OEC of PS II: Degree of symmetry breaking of the labile Mn-X-Mn bond revealed by several hybrid DFT calculations Yamaguchi, K.; Isobe, H.; Yamanaka, S. International Journal of Quantum Chemistry, Vol. 113, Issue 4 https://doi.org/10.1002/qua.24117	journal	April 2012
Serial time-resolved crystallography of photosystem II using a femtosecond X-ray laser Kupitz, Christopher; Basu, Shibom; Grotjohann, Ingo Nature, Vol. 513, Issue 7517 https://doi.org/10.1038/nature13453	journal	July 2014
Structural Changes of the Oxygen-evolving Complex in Photosystem II during the Catalytic Cycle Glöckner, Carina; Kern, Jan; Broser, Matthias Journal of Biological Chemistry, Vol. 288, Issue 31 https://doi.org/10.1074/jbc.M113.476622	journal	June 2013
Towards characterization of photo-excited electron transfer and catalysis in natural and artificial systems using XFELs Alonso-Mori, R.; Asa, K.; Bergmann, U. Faraday Discussions, Vol. 194 https://doi.org/10.1039/C6FD00084C	journal	January 2016
Kinetics of electron transfer and electrochromic change during the redox transitions of the photosynthetic oxygen-evolving complex Rappaport, Fabrice; Blanchard-Desce, Mireille; Lavergne, Jérôme Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1184, Issue 2-3 https://doi.org/10.1016/0005-2728(94)90222-4	journal	March 1994
Kinetic Modeling of the X-ray-Induced Damage to a Metalloprotein Davis, Katherine M.; Kosheleva, Irina; Henning, Robert W. The Journal of Physical Chemistry B, Vol. 117, Issue 31 https://doi.org/10.1021/jp403654n	journal	July 2013
Structure of the Oxygen Evolving Complex of Photosystem II at Room Temperature Davis, Katherine M.; Pushkar, Yulia N. The Journal of Physical Chemistry B, Vol. 119, Issue 8 https://doi.org/10.1021/acs.jpcb.5b00452	journal	February 2015
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
Fast Detection Allowing Analysis of Metalloprotein Electronic Structure by X-ray Emission Spectroscopy at Room Temperature Davis, Katherine M.; Mattern, Brian A.; Pacold, Joseph I. The Journal of Physical Chemistry Letters, Vol. 3, Issue 14 https://doi.org/10.1021/jz3006223	journal	June 2012
Structure and reactivity of the mixed-valence CaMn4O5(H2O)4 and CaMn4O4(OH)(H2O)4 clusters at oxygen evolution complex of photosystem II. Hybrid DFT (UB3LYP and UBHandHLYP) calculations Yamanaka, S.; Saito, T.; Kanda, K. International Journal of Quantum Chemistry, Vol. 112, Issue 1 https://doi.org/10.1002/qua.23261	journal	October 2011
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
A plastic miniature x-ray emission spectrometer based on the cylindrical von Hamos geometry Mattern, B. A.; Seidler, G. T.; Haave, M. Review of Scientific Instruments, Vol. 83, Issue 2 https://doi.org/10.1063/1.3680598	journal	February 2012
Structure of photosystem II and substrate binding at room temperature Young, Iris D.; Ibrahim, Mohamed; Chatterjee, Ruchira Nature, Vol. 540, Issue 7633 https://doi.org/10.1038/nature20161	journal	November 2016
Room-Temperature Energy-Sampling Kβ X-ray Emission Spectroscopy of the Mn ₄ Ca Complex of Photosynthesis Reveals Three Manganese-Centered Oxidation Steps and Suggests a Coordination Change Prior to O ₂ Formation Zaharieva, Ivelina; Chernev, Petko; Berggren, Gustav Biochemistry, Vol. 55, Issue 30 https://doi.org/10.1021/acs.biochem.6b00491	journal	July 2016
X-ray Emission Spectroscopy of Mn Coordination Complexes Toward Interpreting the Electronic Structure of the Oxygen-Evolving Complex of Photosystem II Davis, Katherine M.; Palenik, Mark C.; Yan, Lifen The Journal of Physical Chemistry C, Vol. 120, Issue 6 https://doi.org/10.1021/acs.jpcc.5b10610	journal	February 2016
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
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
How cryo-EM is revolutionizing structural biology Bai, Xiao-chen; McMullan, Greg; Scheres, Sjors H. W. Trends in Biochemical Sciences, Vol. 40, Issue 1 https://doi.org/10.1016/j.tibs.2014.10.005	journal	January 2015
Structure and Orientation of the Mn ₄ Ca Cluster in Plant Photosystem II Membranes Studied by Polarized Range-extended X-ray Absorption Spectroscopy Pushkar, Yulia; Yano, Junko; Glatzel, Pieter Journal of Biological Chemistry, Vol. 282, Issue 10 https://doi.org/10.1074/jbc.M610505200	journal	December 2006
X-ray Emission Spectroscopy of Biomimetic Mn Coordination Complexes Jensen, Scott C.; Davis, Katherine M.; Sullivan, Brendan The Journal of Physical Chemistry Letters, Vol. 8, Issue 12 https://doi.org/10.1021/acs.jpclett.7b01209	journal	May 2017
Possible mechanisms for the O–O bond formation in oxygen evolution reaction at the CaMn4O5(H2O)4 cluster of PSII refined to 1.9Å X-ray resolution Yamanaka, S.; Isobe, H.; Kanda, K. Chemical Physics Letters, Vol. 511, Issue 1-3 https://doi.org/10.1016/j.cplett.2011.06.021	journal	July 2011
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
Time-Resolved Infrared Detection of the Proton and Protein Dynamics during Photosynthetic Oxygen Evolution Noguchi, Takumi; Suzuki, Hiroyuki; Tsuno, Masaya Biochemistry, Vol. 51, Issue 15 https://doi.org/10.1021/bi300294n	journal	April 2012
Quantum Mechanics/Molecular Mechanics Study of the Catalytic Cycle of Water Splitting in Photosystem II Sproviero, Eduardo M.; Gascón, José A.; McEvoy, James P. Journal of the American Chemical Society, Vol. 130, Issue 11 https://doi.org/10.1021/ja076130q	journal	March 2008
A molecular ruthenium catalyst with water-oxidation activity comparable to that of photosystem II Duan, Lele; Bozoglian, Fernando; Mandal, Sukanta Nature Chemistry, Vol. 4, Issue 5 https://doi.org/10.1038/nchem.1301	journal	March 2012
Structure-function relations in photosystem II. Effects of temperature and chaotropic agents on the period four oscillation of flash-induced oxygen evolution Messinger, Johannes; Schroeder, Wolfgang P.; Renger, Gernot Biochemistry, Vol. 32, Issue 30 https://doi.org/10.1021/bi00081a009	journal	August 1993
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
Photosystem II: Structure and mechanism of the water:plastoquinone oxidoreductase Kern, Jan; Renger, Gernot Photosynthesis Research, Vol. 94, Issue 2-3 https://doi.org/10.1007/s11120-007-9201-1	journal	July 2007
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
Crystal structure of photosystem II from Synechococcus elongatus at 3.8 Å resolution Zouni, Athina; Witt, Horst-Tobias; Kern, Jan Nature, Vol. 409, Issue 6821 https://doi.org/10.1038/35055589	journal	February 2001
X-ray Absorption Spectroscopy on Layered Photosystem II Membrane Particles Suggests Manganese-Centered Oxidation of the Oxygen-Evolving Complex for the S ₀ -S ₁ , S ₁ -S ₂ , and S ₂ -S ₃ Transitions of the Water Oxidation Cycle ^† Iuzzolino, Lucia; Dittmer, Jens; Dörner, Wolfgang Biochemistry, Vol. 37, Issue 49 https://doi.org/10.1021/bi9817360	journal	December 1998

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