Going around the Kok cycle of the water oxidation reaction with femtosecond X-ray crystallography

Bhowmick, Asmit; Simon, Philipp S.; Bogacz, Isabel; Hussein, Rana; Zhang, Miao; Makita, Hiroki; Ibrahim, Mohamed; Chatterjee, Ruchira; Doyle, Margaret D.; Cheah, Mun Hon; Chernev, Petko; Fuller, Franklin D.; Fransson, Thomas; Alonso-Mori, Roberto; Brewster, Aaron S.; Sauter, Nicholas K.; Bergmann, Uwe; Dobbek, Holger; Zouni, Athina; Messinger, Johannes; Kern, Jan; Yachandra, Vittal K.; Yano, Junko

doi:10.1107/S2052252523008928

Title: Going around the Kok cycle of the water oxidation reaction with femtosecond X-ray crystallography

Journal Article · 23 October 2023 · IUCrJ

DOI: https://doi.org/10.1107/S2052252523008928 · OSTI ID:2203306

;

; Hussein, Rana;

;

The water oxidation reaction in photosystem II (PS II) produces most of the molecular oxygen in the atmosphere, which sustains life on Earth, and in this process releases four electrons and four protons that drive the downstream process of CO ₂ fixation in the photosynthetic apparatus. The catalytic center of PS II is an oxygen-bridged Mn ₄ Ca complex (Mn ₄ CaO ₅ ) which is progressively oxidized upon the absorption of light by the chlorophyll of the PS II reaction center, and the accumulation of four oxidative equivalents in the catalytic center results in the oxidation of two waters to dioxygen in the last step. The recent emergence of X-ray free-electron lasers (XFELs) with intense femtosecond X-ray pulses has opened up opportunities to visualize this reaction in PS II as it proceeds through the catalytic cycle. In this review, we summarize our recent studies of the catalytic reaction in PS II by following the structural changes along the reaction pathway via room-temperature X-ray crystallography using XFELs. The evolution of the electron density changes at the Mn complex reveals notable structural changes, including the insertion of O _X from a new water molecule, which disappears on completion of the reaction, implicating it in the O—O bond formation reaction. We were also able to follow the structural dynamics of the protein coordinating with the catalytic complex and of channels within the protein that are important for substrate and product transport, revealing well orchestrated conformational changes in response to the electronic changes at the Mn ₄ Ca cluster.

View Journal Article

Cite

Export

Save

Sponsoring Organization:: USDOE

Grant/Contract Number:: NONE; AC02-05CH11231

OSTI ID:: 2203306

Alternate ID(s):: OSTI ID: 2327112; OSTI ID: 2368785

Journal Information:: IUCrJ, Journal Name: IUCrJ Journal Issue: 6 Vol. 10; ISSN 2052-2525; ISSN IUCRAJ

Publisher:: International Union of Crystallography (IUCr)Copyright Statement

Country of Publication:: United Kingdom

Language:: English

References (75)

Radiation damage in macromolecular crystallography: what is it and why should we care? Garman, Elspeth F. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/S0907444910008656	journal	March 2010
Native structure of photosystem II at 1.95 Å resolution viewed by femtosecond X-ray pulses Suga, Michihiro; Akita, Fusamichi; Hirata, Kunio Nature, Vol. 517, Issue 7532 https://doi.org/10.1038/nature13991	journal	November 2014
Direct observation of ultrafast collective motions in CO myoglobin upon ligand dissociation Barends, T. R. M.; Foucar, L.; Ardevol, A. Science, Vol. 350, Issue 6259 https://doi.org/10.1126/science.aac5492	journal	September 2015
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
Energetics and Kinetics of S-State Transitions Monitored by Delayed Chlorophyll Fluorescence Zaharieva, Ivelina; Dau, Holger Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.00386	journal	March 2019
Fourier transform infrared difference and time-resolved infrared detection of the electron and proton transfer dynamics in photosynthetic water oxidation Noguchi, Takumi Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1847, Issue 1 https://doi.org/10.1016/j.bbabio.2014.06.009	journal	January 2015
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
Advances and challenges in time-resolved macromolecular crystallography Brändén, Gisela; Neutze, Richard Science, Vol. 373, Issue 6558 https://doi.org/10.1126/science.aba0954	journal	August 2021
Improvements in serial femtosecond crystallography of photosystem II by optimizing crystal uniformity using microseeding procedures Ibrahim, Mohamed; Chatterjee, Ruchira; Hellmich, Julia Structural Dynamics, Vol. 2, Issue 4 https://doi.org/10.1063/1.4919741	journal	July 2015
Probing the Accessibility of the Mn4Ca Cluster in Photosystem II: Channels Calculation, Noble Gas Derivatization, and Cocrystallization with DMSO Gabdulkhakov, Azat; Guskov, Albert; Broser, Matthias Structure, Vol. 17, Issue 9 https://doi.org/10.1016/j.str.2009.07.010	journal	September 2009
Radiolytic Mapping of Solvent-Contact Surfaces in Photosystem II of Higher Plants: EXPERIMENTAL IDENTIFICATION OF PUTATIVE WATER CHANNELS WITHIN THE PHOTOSYSTEM Frankel, Laurie K.; Sallans, Larry; Bellamy, Henry Journal of Biological Chemistry, Vol. 288, Issue 32 https://doi.org/10.1074/jbc.M113.487033	journal	June 2013
Structural evidence for intermediates during O2 formation in photosystem II Bhowmick, Asmit; Hussein, Rana; Bogacz, Isabel Nature, Vol. 617, Issue 7961 https://doi.org/10.1038/s41586-023-06038-z	journal	May 2023
XFELs for structure and dynamics in biology Spence, J. C. H. IUCrJ, Vol. 4, Issue 4 https://doi.org/10.1107/S2052252517005760	journal	May 2017
Mn ₄ Ca Cluster in Photosynthesis: Where and How Water is Oxidized to Dioxygen Yano, Junko; Yachandra, Vittal Chemical Reviews, Vol. 114, Issue 8 https://doi.org/10.1021/cr4004874	journal	March 2014
Few-fs resolution of a photoactive protein traversing a conical intersection Hosseinizadeh, A.; Breckwoldt, N.; Fung, R. Nature, Vol. 599, Issue 7886 https://doi.org/10.1038/s41586-021-04050-9	journal	November 2021
Snapshot of an oxygen intermediate in the catalytic reaction of cytochrome c oxidase Ishigami, Izumi; Lewis-Ballester, Ariel; Echelmeier, Austin Proceedings of the National Academy of Sciences, Vol. 116, Issue 9 https://doi.org/10.1073/pnas.1814526116	journal	February 2019
Crystal structure of oxygen-evolving photosystem II from Thermosynechococcus vulcanus at 3.7-A resolution Kamiya, N.; Shen, J. -R. Proceedings of the National Academy of Sciences, Vol. 100, Issue 1 https://doi.org/10.1073/pnas.0135651100	journal	December 2002
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
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
Room temperature femtosecond X-ray diffraction of photosystem II microcrystals Kern, J.; Alonso-Mori, R.; Hellmich, J. Proceedings of the National Academy of Sciences, Vol. 109, Issue 25, p. 9721-9726 https://doi.org/10.1073/pnas.1204598109	journal	June 2012
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
Retinal isomerization in bacteriorhodopsin captured by a femtosecond x-ray laser Nogly, Przemyslaw; Weinert, Tobias; James, Daniel Science https://doi.org/10.1126/science.aat0094	journal	June 2018
Access channels and methanol binding site to the CaMn4 cluster in Photosystem II based on solvent accessibility simulations, with implications for substrate water access Ho, Felix M.; Styring, Stenbjörn Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1777, Issue 2 https://doi.org/10.1016/j.bbabio.2007.08.009	journal	February 2008
Native-like Photosystem II Superstructure at 2.44 Å Resolution through Detergent Extraction from the Protein Crystal Hellmich, Julia; Bommer, Martin; Burkhardt, Anja Structure, Vol. 22, Issue 11 https://doi.org/10.1016/j.str.2014.09.007	journal	November 2014
Femtosecond X-ray protein nanocrystallography Chapman, Henry N.; Fromme, Petra; Barty, Anton Nature, Vol. 470, Issue 7332, p. 73-77 https://doi.org/10.1038/nature09750	journal	February 2011
Calcium Ion Coordination: A Comparison with That of Beryllium, Magnesium, and Zinc Katz, Amy Kaufman; Glusker, Jenny P.; Beebe, Scott A. Journal of the American Chemical Society, Vol. 118, Issue 24 https://doi.org/10.1021/ja953943i	journal	January 1996
Proton transfer pathway from the oxygen-evolving complex in photosystem II substantiated by extensive mutagenesis Kuroda, Hiroshi; Kawashima, Keisuke; Ueda, Kazuyo Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1862, Issue 1 https://doi.org/10.1016/j.bbabio.2020.148329	journal	January 2021
Serial femtosecond crystallography Barends, Thomas R. M.; Stauch, Benjamin; Cherezov, Vadim Nature Reviews Methods Primers, Vol. 2, Issue 1 https://doi.org/10.1038/s43586-022-00141-7	journal	August 2022
Crystal structure of rhodopsin bound to arrestin by femtosecond X-ray laser Kang, Yanyong; Zhou, X. Edward; Gao, Xiang Nature, Vol. 523, Issue 7562 https://doi.org/10.1038/nature14656	journal	July 2015
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
XFEL diffraction: developing processing methods to optimize data quality Sauter, Nicholas K. Journal of Synchrotron Radiation, Vol. 22, Issue 2 https://doi.org/10.1107/S1600577514028203	journal	January 2015
Improving signal strength in serial crystallography with DIALS geometry refinement Brewster, Aaron S.; Waterman, David G.; Parkhurst, James M. Acta Crystallographica Section D Structural Biology, Vol. 74, Issue 9 https://doi.org/10.1107/S2059798318009191	journal	September 2018
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
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
SAD phasing of XFEL data depends critically on the error model Brewster, Aaron S.; Bhowmick, Asmit; Bolotovsky, Robert Acta Crystallographica Section D Structural Biology, Vol. 75, Issue 11 https://doi.org/10.1107/S2059798319012877	journal	October 2019
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
Molecular basis for turnover inefficiencies (misses) during water oxidation in photosystem II Han, Guangye; Chernev, Petko; Styring, Stenbjörn Chemical Science, Vol. 13, Issue 29 https://doi.org/10.1039/D2SC00854H	journal	January 2022
Energetics of a Possible Proton Exit Pathway for Water Oxidation in Photosystem II ^† Ishikita, Hiroshi; Saenger, Wolfram; Loll, Bernhard Biochemistry, Vol. 45, Issue 7 https://doi.org/10.1021/bi051615h	journal	February 2006
X-ray Emission Spectroscopy as an in Situ Diagnostic Tool for X-ray Crystallography of Metalloproteins Using an X-ray Free-Electron Laser Fransson, Thomas; Chatterjee, Ruchira; Fuller, Franklin D. Biochemistry, Vol. 57, Issue 31 https://doi.org/10.1021/acs.biochem.8b00325	journal	April 2018
Macromolecular structure determination using X-rays, neutrons and electrons: recent developments in Phenix Liebschner, Dorothee; Afonine, Pavel V.; Baker, Matthew L. Acta Crystallographica Section D Structural Biology, Vol. 75, Issue 10 https://doi.org/10.1107/S2059798319011471	journal	October 2019
Effects of x-ray free-electron laser pulse intensity on the Mn Kβ_1,3 x-ray emission spectrum in photosystem II—A case study for metalloprotein crystals and solutions Fransson, Thomas; Alonso-Mori, Roberto; Chatterjee, Ruchira Structural Dynamics, Vol. 8, Issue 6 https://doi.org/10.1063/4.0000130	journal	November 2021
Electron paramagnetic resonance kinetic studies of the S states in spinach PSII membranes Reza Razeghifard, M.; Pace, Ronald J. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1322, Issue 2-3 https://doi.org/10.1016/S0005-2728(97)00069-8	journal	December 1997
Current status and future opportunities for serial crystallography at MAX IV Laboratory Shilova, Anastasya; Lebrette, Hugo; Aurelius, Oskar Journal of Synchrotron Radiation, Vol. 27, Issue 5 https://doi.org/10.1107/S1600577520008735	journal	August 2020
Ultrafast structural changes within a photosynthetic reaction centre Dods, Robert; Båth, Petra; Morozov, Dmitry Nature, Vol. 589, Issue 7841, p. 310-314 https://doi.org/10.1038/s41586-020-3000-7	journal	December 2020
X-ray damage to the Mn4Ca complex in single crystals of photosystem II: A case study for metalloprotein crystallography Yano, J.; Kern, J.; Irrgang, K. -D. Proceedings of the National Academy of Sciences, Vol. 102, Issue 34 https://doi.org/10.1073/pnas.0505207102	journal	August 2005
On-line mass spectrometry: membrane inlet sampling Beckmann, Katrin; Messinger, Johannes; Badger, Murray Ronald Photosynthesis Research, Vol. 102, Issue 2-3 https://doi.org/10.1007/s11120-009-9474-7	journal	August 2009
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
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
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
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
Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II Loll, Bernhard; Kern, Jan; Saenger, Wolfram Nature, Vol. 438, Issue 7070 https://doi.org/10.1038/nature04224	journal	December 2005
Structural dynamics in the water and proton channels of photosystem II during the S2 to S3 transition Hussein, Rana; Ibrahim, Mohamed; Bhowmick, Asmit Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-021-26781-z	journal	November 2021
Coot model-building tools for molecular graphics Emsley, Paul; Cowtan, Kevin Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132 https://doi.org/10.1107/S0907444904019158	journal	November 2004
Short-lived intermediate in N ₂ O generation by P450 NO reductase captured by time-resolved IR spectroscopy and XFEL crystallography Nomura, Takashi; Kimura, Tetsunari; Kanematsu, Yusuke Proceedings of the National Academy of Sciences, Vol. 118, Issue 21 https://doi.org/10.1073/pnas.2101481118	journal	May 2021
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
Solar energy conversion by photosystem II: principles and structures Shevela, Dmitry; Kern, Jan F.; Govindjee, Govindjee Photosynthesis Research, Vol. 156, Issue 3 https://doi.org/10.1007/s11120-022-00991-y	journal	February 2023
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
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
Potential for biomolecular imaging with femtosecond X-ray pulses Neutze, Richard; Wouts, Remco; van der Spoel, David Nature, Vol. 406, Issue 6797 https://doi.org/10.1038/35021099	journal	August 2000
Earth-Abundant Heterogeneous Water Oxidation Catalysts Hunter, Bryan M.; Gray, Harry B.; Müller, Astrid M. Chemical Reviews, Vol. 116, Issue 22 https://doi.org/10.1021/acs.chemrev.6b00398	journal	October 2016
Serial femtosecond crystallography on in vivo-grown crystals drives elucidation of mosquitocidal Cyt1Aa bioactivation cascade Tetreau, Guillaume; Banneville, Anne-Sophie; Andreeva, Elena A. Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-14894-w	journal	March 2020
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
Biological Water Oxidation Cox, Nicholas; Pantazis, Dimitrios A.; Neese, Frank Accounts of Chemical Research, Vol. 46, Issue 7 https://doi.org/10.1021/ar3003249	journal	March 2013
High-Resolution XFEL Structure of the Soluble Methane Monooxygenase Hydroxylase Complex with its Regulatory Component at Ambient Temperature in Two Oxidation States Srinivas, Vivek; Banerjee, Rahul; Lebrette, Hugo Journal of the American Chemical Society, Vol. 142, Issue 33 https://doi.org/10.1021/jacs.0c05613	journal	July 2020
First lasing and operation of an ångstrom-wavelength free-electron laser Emma, P.; Akre, R.; Arthur, J. Nature Photonics, Vol. 4, Issue 9 https://doi.org/10.1038/nphoton.2010.176	journal	August 2010
A simplified description of X-ray free-electron lasers Margaritondo, G.; Rebernik Ribic, Primoz Journal of Synchrotron Radiation, Vol. 18, Issue 2 https://doi.org/10.1107/S090904951004896X	journal	January 2011
X-ray free-electron laser studies reveal correlated motion during isopenicillin N synthase catalysis Rabe, Patrick; Kamps, Jos J. A. G.; Sutherlin, Kyle D. Science Advances, Vol. 7, Issue 34 https://doi.org/10.1126/sciadv.abh0250	journal	August 2021
Accurate macromolecular structures using minimal measurements from X-ray free-electron lasers Hattne, Johan; Echols, Nathaniel; Tran, Rosalie Nature Methods, Vol. 11, Issue 5 https://doi.org/10.1038/nmeth.2887	journal	March 2014
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
Best practices for time-resolved serial synchrotron crystallography Schulz, Eike C.; Yorke, Briony A.; Pearson, Arwen R. Acta Crystallographica Section D Structural Biology, Vol. 78, Issue 1 https://doi.org/10.1107/S2059798321011621	journal	January 2022
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
Un Nouveau Modele des Centres Photochimiques du Systeme ii Joliot, P.; Barbieri, G.; Chabaud, R. Photochemistry and Photobiology, Vol. 10, Issue 5 https://doi.org/10.1111/j.1751-1097.1969.tb05696.x	journal	November 1969
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
Energy-dispersive X-ray emission spectroscopy using an X-ray free-electron laser in a shot-by-shot mode Alonso-Mori, R.; Kern, J.; Gildea, R. J. Proceedings of the National Academy of Sciences, Vol. 109, Issue 47, p. 19103-19107 https://doi.org/10.1073/pnas.1211384109	journal	November 2012
Calcium limits substrate accessibility or reactivity at the manganese cluster in photosynthetic water oxidation Tso, J.; Sivaraja, M.; Dismukes, G. C. Biochemistry, Vol. 30, Issue 19 https://doi.org/10.1021/bi00233a014	journal	May 1991

Similar Records

Structural Changes in the Mn(4)Ca Cluster And the Mechanism of Photosynthetic Water Splitting

Journal Article · 2009 · Proc. Nat. Acad. Sci.105:1879,2008 · OSTI ID:953052

Pushkar, Y; Yano, J; Sauer, K; +2 more

Structure of photosystem II and substrate binding at room temperature

Journal Article · 2016 · Nature (London) · OSTI ID:1379614

Young, Iris D.; Ibrahim, Mohamed; Chatterjee, Ruchira; +65 more

Structural Changes in the Mn4Ca Cluster and the Mechanism of Photosynthetic Water Splitting

Journal Article · 2007 · Proceedings of the National Academy of Science · OSTI ID:971344

Pushkar, Y; Yano, J; Sauer, K; +2 more

Title: Going around the Kok cycle of the water oxidation reaction with femtosecond X-ray crystallography

Citation Formats

References (75)

Similar Records

Related Subjects