Structures of the intermediates of Kok’s photosynthetic water oxidation clock
Abstract
Inspired by the period-four oscillation in flash-induced oxygen evolution of photosystem II discovered by Joliot in 1969, Kok performed additional experiments and proposed a five-state kinetic model for photosynthetic oxygen evolution, known as Kok's S-state clock or cycle. The model comprises four (meta)stable intermediates (S0, S1, S2 and S3) and one transient S4 state, which precedes dioxygen formation occurring in a concerted reaction from two water-derived oxygens bound at an oxo-bridged tetra manganese calcium (Mn4CaO5) cluster in the oxygen-evolving complex. This reaction is coupled to the two-step reduction and protonation of the mobile plastoquinone QB at the acceptor side of PSII. Here, using serial femtosecond X-ray crystallography and simultaneous X-ray emission spectroscopy with multi-flash visible laser excitation at room temperature, we visualize all (meta)stable states of Kok's cycle as high-resolution structures (2.04-2.08 Å). In addition, we report structures of two transient states at 150 and 400 µs, revealing notable structural changes including the binding of one additional 'water', Ox, during the S2→S3 state transition. Our results suggest that one water ligand to calcium (W3) is directly involved in substrate delivery. The binding of the additional oxygen Ox in the S3 state between Ca and Mn1 supports O-O bond formation mechanisms involving O5more »
- Authors:
-
more »
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Molecular Biophysics and Integrated Bioimaging Division
- Humboldt-Univ Berlin, Berlin (Germany). Inst. fur Biologie
- SLAC National Accelerator Lab., Menlo Park, CA (United States). Photon Ultrafast Laser Science and Engineering Inst. (PULSE); Univ. of Heidelberg, Heidelberg (Germany). Interdisciplinary Center for Scientific Computing
- SLAC National Accelerator Lab., Menlo Park, CA (United States). Linac Coherent Light Source (LCLS)
- Umeå Univ., Umeå (Sweden). Inst. för Kemi, Kemiskt Biologiskt Centrum; Uppsala Univ. (Sweden). Dept. of Chemistry-Ångström, Molecular Biomimetics
- Uppsala Univ. (Sweden). Dept. of Chemistry-Ångström, Molecular Biomimetics
- Umeå Univ., Umeå (Sweden). Inst. för Kemi, Kemiskt Biologiskt Centrum
- SLAC National Accelerator Lab., Menlo Park, CA (United States). Stanford Synchrotron Radiation Lightsource (SSRL)
- Science and Technology Facilities Council (STFC), Harwell Campus, Oxford (United Kingdom). Diamond Light Source, Ltd.
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Molecular Biophysics and Integrated Bioimaging Division; SLAC National Accelerator Lab., Menlo Park, CA (United States). Stanford Synchrotron Radiation Lightsource (SSRL); Univ. of California, San Francisco, CA (United States). Dept. of Biochemistry and Biophysics
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Molecular Biophysics and Integrated Bioimaging Division; Univ. of California, Berkeley, CA (United States). Dept. of Bioengineering
- SLAC National Accelerator Lab., Menlo Park, CA (United States). Photon Ultrafast Laser Science and Engineering Inst. (PULSE)
- Publication Date:
- Research Org.:
- SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences, and Biosciences Division
- OSTI Identifier:
- 1490667
- Alternate Identifier(s):
- OSTI ID: 1487213; OSTI ID: 1506373
- Grant/Contract Number:
- AC02-76SF00515; AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Nature (London)
- Additional Journal Information:
- Journal Name: Nature (London); Journal Volume: 563; Journal Issue: 7731; Journal ID: ISSN 0028-0836
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
Citation Formats
Kern, Jan, Chatterjee, Ruchira, Young, Iris D., Fuller, Franklin D., Lassalle, Louise, Ibrahim, Mohamed, Gul, Sheraz, Fransson, Thomas, Brewster, Aaron S., Alonso-Mori, Roberto, Hussein, Rana, Zhang, Miao, Douthit, Lacey, de Lichtenberg, Casper, Cheah, Mun Hon, Shevela, Dmitry, Wersig, Julia, Seuffert, Ina, Sokaras, Dimosthenis, Pastor, Ernest, Weninger, Clemens, Kroll, Thomas, Sierra, Raymond G., Aller, Pierre, Butryn, Agata, Orville, Allen M., Liang, Mengning, Batyuk, Alexander, Koglin, Jason E., Carbajo, Sergio, Boutet, Sébastien, Moriarty, Nigel W., Holton, James M., Dobbek, Holger, Adams, Paul D., Bergmann, Uwe, Sauter, Nicholas K., Zouni, Athina, Messinger, Johannes, Yano, Junko, and Yachandra, Vittal K. Structures of the intermediates of Kok’s photosynthetic water oxidation clock. United States: N. p., 2018.
Web. doi:10.1038/s41586-018-0681-2.
Kern, Jan, Chatterjee, Ruchira, Young, Iris D., Fuller, Franklin D., Lassalle, Louise, Ibrahim, Mohamed, Gul, Sheraz, Fransson, Thomas, Brewster, Aaron S., Alonso-Mori, Roberto, Hussein, Rana, Zhang, Miao, Douthit, Lacey, de Lichtenberg, Casper, Cheah, Mun Hon, Shevela, Dmitry, Wersig, Julia, Seuffert, Ina, Sokaras, Dimosthenis, Pastor, Ernest, Weninger, Clemens, Kroll, Thomas, Sierra, Raymond G., Aller, Pierre, Butryn, Agata, Orville, Allen M., Liang, Mengning, Batyuk, Alexander, Koglin, Jason E., Carbajo, Sergio, Boutet, Sébastien, Moriarty, Nigel W., Holton, James M., Dobbek, Holger, Adams, Paul D., Bergmann, Uwe, Sauter, Nicholas K., Zouni, Athina, Messinger, Johannes, Yano, Junko, & Yachandra, Vittal K. Structures of the intermediates of Kok’s photosynthetic water oxidation clock. United States. https://doi.org/10.1038/s41586-018-0681-2
Kern, Jan, Chatterjee, Ruchira, Young, Iris D., Fuller, Franklin D., Lassalle, Louise, Ibrahim, Mohamed, Gul, Sheraz, Fransson, Thomas, Brewster, Aaron S., Alonso-Mori, Roberto, Hussein, Rana, Zhang, Miao, Douthit, Lacey, de Lichtenberg, Casper, Cheah, Mun Hon, Shevela, Dmitry, Wersig, Julia, Seuffert, Ina, Sokaras, Dimosthenis, Pastor, Ernest, Weninger, Clemens, Kroll, Thomas, Sierra, Raymond G., Aller, Pierre, Butryn, Agata, Orville, Allen M., Liang, Mengning, Batyuk, Alexander, Koglin, Jason E., Carbajo, Sergio, Boutet, Sébastien, Moriarty, Nigel W., Holton, James M., Dobbek, Holger, Adams, Paul D., Bergmann, Uwe, Sauter, Nicholas K., Zouni, Athina, Messinger, Johannes, Yano, Junko, and Yachandra, Vittal K. Wed .
"Structures of the intermediates of Kok’s photosynthetic water oxidation clock". United States. https://doi.org/10.1038/s41586-018-0681-2. https://www.osti.gov/servlets/purl/1490667.
@article{osti_1490667,
title = {Structures of the intermediates of Kok’s photosynthetic water oxidation clock},
author = {Kern, Jan and Chatterjee, Ruchira and Young, Iris D. and Fuller, Franklin D. and Lassalle, Louise and Ibrahim, Mohamed and Gul, Sheraz and Fransson, Thomas and Brewster, Aaron S. and Alonso-Mori, Roberto and Hussein, Rana and Zhang, Miao and Douthit, Lacey and de Lichtenberg, Casper and Cheah, Mun Hon and Shevela, Dmitry and Wersig, Julia and Seuffert, Ina and Sokaras, Dimosthenis and Pastor, Ernest and Weninger, Clemens and Kroll, Thomas and Sierra, Raymond G. and Aller, Pierre and Butryn, Agata and Orville, Allen M. and Liang, Mengning and Batyuk, Alexander and Koglin, Jason E. and Carbajo, Sergio and Boutet, Sébastien and Moriarty, Nigel W. and Holton, James M. and Dobbek, Holger and Adams, Paul D. and Bergmann, Uwe and Sauter, Nicholas K. and Zouni, Athina and Messinger, Johannes and Yano, Junko and Yachandra, Vittal K.},
abstractNote = {Inspired by the period-four oscillation in flash-induced oxygen evolution of photosystem II discovered by Joliot in 1969, Kok performed additional experiments and proposed a five-state kinetic model for photosynthetic oxygen evolution, known as Kok's S-state clock or cycle. The model comprises four (meta)stable intermediates (S0, S1, S2 and S3) and one transient S4 state, which precedes dioxygen formation occurring in a concerted reaction from two water-derived oxygens bound at an oxo-bridged tetra manganese calcium (Mn4CaO5) cluster in the oxygen-evolving complex. This reaction is coupled to the two-step reduction and protonation of the mobile plastoquinone QB at the acceptor side of PSII. Here, using serial femtosecond X-ray crystallography and simultaneous X-ray emission spectroscopy with multi-flash visible laser excitation at room temperature, we visualize all (meta)stable states of Kok's cycle as high-resolution structures (2.04-2.08 Å). In addition, we report structures of two transient states at 150 and 400 µs, revealing notable structural changes including the binding of one additional 'water', Ox, during the S2→S3 state transition. Our results suggest that one water ligand to calcium (W3) is directly involved in substrate delivery. The binding of the additional oxygen Ox in the S3 state between Ca and Mn1 supports O-O bond formation mechanisms involving O5 as one substrate, where Ox is either the other substrate oxygen or is perfectly positioned to refill the O5 position during O2 release. Thus, our results exclude peroxo-bond formation in the S3 state, and the nucleophilic attack of W3 onto W2 is unlikely.},
doi = {10.1038/s41586-018-0681-2},
journal = {Nature (London)},
number = 7731,
volume = 563,
place = {United States},
year = {Wed Nov 07 00:00:00 EST 2018},
month = {Wed Nov 07 00:00:00 EST 2018}
}
Web of Science
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- Physical Chemistry Chemical Physics, Vol. 22, Issue 1
Origin of the heat-induced improvement of catalytic activity and stability of MnO x electrocatalysts for water oxidation
journal, January 2019
- Abrashev, Miroslav V.; Chernev, Petko; Kubella, Paul
- Journal of Materials Chemistry A, Vol. 7, Issue 28
Impact of substituents on molecular properties and catalytic activities of trinuclear Ru macrocycles in water oxidation
journal, January 2020
- Meza-Chincha, Ana-Lucia; Lindner, Joachim O.; Schindler, Dorothee
- Chemical Science
Quantitative assessment of the high-light tolerance in plants with an impaired photosystem II donor side
journal, May 2019
- Wilson, Sam; Ruban, Alexander V.
- Biochemical Journal, Vol. 476, Issue 9
Binuclear Mn oxo complex as a self-contained photocatalyst in water-splitting cycle: Role of additional Mn oxides as a buffer of electrons and protons
journal, January 2020
- Yamamoto, Kentaro; Takatsuka, Kazuo
- The Journal of Chemical Physics, Vol. 152, Issue 2
Five-coordinate Mn IV intermediate in the activation of nature’s water splitting cofactor
journal, August 2019
- Chrysina, Maria; Heyno, Eiri; Kutin, Yury
- Proceedings of the National Academy of Sciences, Vol. 116, Issue 34
Assessment of the manganese cluster’s oxidation state via photoactivation of photosystem II microcrystals
journal, December 2019
- Cheah, Mun Hon; Zhang, Miao; Shevela, Dmitry
- Proceedings of the National Academy of Sciences, Vol. 117, Issue 1
An outlook on using serial femtosecond crystallography in drug discovery
journal, May 2019
- Mishin, Alexey; Gusach, Anastasiia; Luginina, Aleksandra
- Expert Opinion on Drug Discovery, Vol. 14, Issue 9
The Macromolecular Femtosecond Crystallography Instrument at the Linac Coherent Light Source
journal, February 2019
- Sierra, Raymond G.; Batyuk, Alexander; Sun, Zhibin
- Journal of Synchrotron Radiation, Vol. 26, Issue 2
A guide to sample delivery systems for serial crystallography
journal, August 2019
- Zhao, Feng‐Zhu; Zhang, Bin; Yan, Er‐Kai
- The FEBS Journal, Vol. 286, Issue 22
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
- Chatterjee, Ruchira; Lassalle, Louise; Gul, Sheraz
- Physiologia Plantarum, Vol. 166, Issue 1
Dynamic pH‐induced conformational changes of the PsbO protein in the fluctuating acidity of the thylakoid lumen
journal, March 2019
- Carius, Anke B.; Rogne, Per; Duchoslav, Miloš
- Physiologia Plantarum, Vol. 166, Issue 1
On the comparison between differential vibrational spectroscopy spectra and theoretical data in the carboxyl region of photosystem II
journal, March 2019
- Capone, Matteo; Narzi, Daniele; Tychengulova, Aliya
- Physiologia Plantarum, Vol. 166, Issue 1
Theoretical and computational investigations of geometrical, electronic and spin structures of the CaMn 4 O X (X = 5, 6) cluster in the Kok cycle S i (i = 0–3) of oxygen evolving complex of photosystem II
journal, March 2019
- Yamaguchi, Kizashi; Yamanaka, Shusuke; Isobe, Hiroshi
- Physiologia Plantarum, Vol. 166, Issue 1
An oxyl/oxo mechanism for oxygen-oxygen coupling in PSII revealed by an x-ray free-electron laser
journal, October 2019
- Suga, Michihiro; Akita, Fusamichi; Yamashita, Keitaro
- Science, Vol. 366, Issue 6463
How Plants Handle Trivalent (+3) Elements
journal, August 2019
- Poschenrieder, Charlotte; Busoms, Silvia; Barceló, Juan
- International Journal of Molecular Sciences, Vol. 20, Issue 16
Water Network Dynamics Next to the Oxygen-Evolving Complex of Photosystem II
journal, March 2019
- Reiss, Krystle; Morzan, Uriel; Grigas, Alex
- Inorganics, Vol. 7, Issue 3
The S3 State of the Oxygen-Evolving Complex: Overview of Spectroscopy and XFEL Crystallography with a Critical Evaluation of Early-Onset Models for O–O Bond Formation
journal, April 2019
- Pantazis, Dimitrios A.
- Inorganics, Vol. 7, Issue 4
The Reactivity and Stability of Polyoxometalate Water Oxidation Electrocatalysts
journal, December 2019
- Gao, Dandan; Trentin, Ivan; Schwiedrzik, Ludwig
- Molecules, Vol. 25, Issue 1
Domain-based local pair natural orbital CCSD(T) calculations of strongly correlated electron systems: Examination of dynamic equilibrium models based on multiple intermediates in S1 state of photosystem II
text, January 2020
- Miyagawa, K.; Kawakami, T.; Suzuki, Y.
- Taylor & Francis
A High‐Valent Manganese(IV)–Oxo–Cerium(IV) Complex and Its Enhanced Oxidizing Reactivity
journal, November 2019
- Karmalkar, Deepika G.; Sankaralingam, Muniyandi; Seo, Mi Sook
- Angewandte Chemie International Edition, Vol. 58, Issue 45
The Two Alternative Oxidation State Assignments of Manganese Ions: What S2 CW-EPR Multiline (ML) Signal Simulations Reveal?
journal, February 2020
- Baituti, Bernard; Akofang, Leonard
- Applied Magnetic Resonance, Vol. 51, Issue 5
Light polarization dependency existing in the biological photosystem and possible implications for artificial antenna systems
journal, October 2019
- Im, Sang Won; Ha, Heonjin; Yang, Woojin
- Photosynthesis Research, Vol. 143, Issue 2
Photoswitching mechanism of a fluorescent protein revealed by time-resolved crystallography and transient absorption spectroscopy
journal, February 2020
- Woodhouse, Joyce; Nass Kovacs, Gabriela; Coquelle, Nicolas
- Nature Communications, Vol. 11, Issue 1
A novel nonheme manganese( ii ) complex for (electro) catalytic oxidation of water
journal, January 2020
- Narulkar, Dattaprasad D.; Devulapally, Koteshwar; U., Anil Kumar
- Sustainable Energy & Fuels, Vol. 4, Issue 6
The microfluidic laboratory at Synchrotron SOLEIL
journal, January 2020
- Chaussavoine, Igor; Beauvois, Anthony; Mateo, Tiphaine
- Journal of Synchrotron Radiation, Vol. 27, Issue 1
Dynamic water bridging and proton transfer at a surface carboxylate cluster of photosystem II
text, January 2019
- Kemmler, Lukas; Ibrahim, Mohamed; Dobbek, Holger
- Freie Universität Berlin
Thermodynamics of the S2-to-S3 State Transition of the Oxygen-Evolving Complex of Photosystem II
text, January 2019
- Amin, Muhamed; Matta, Divya; Yang, Ke
- Deutsches Elektronen-Synchrotron, DESY, Hamburg
The Reactivity and Stability of Polyoxometalate Water Oxidation Electrocatalysts
text, January 2020
- Gao, Dandan; Trentin, Ivan; Schwiedrzik, Ludwig
- Karlsruhe
Temperature-jump solution X-ray scattering reveals distinct motions in a dynamic enzyme
journal, September 2019
- Thompson, Michael C.; Barad, Benjamin A.; Wolff, Alexander M.
- Nature Chemistry, Vol. 11, Issue 11
Domain-based local pair natural orbital CCSD(T) calculations of strongly correlated electron systems: Examination of dynamic equilibrium models based on multiple intermediates in S 1 state of photosystem II
journal, September 2019
- Miyagawa, K.; Kawakami, T.; Suzuki, Y.
- Molecular Physics, Vol. 118, Issue 12
The reactivity and stability of polyoxometalate water oxidation electrocatalysts
text, January 2019
- Gao, Dandan; Trentin, Ivan; Schwiedrzik, Ludwig
- Universität Ulm
Water oxidation in photosystem II
journal, June 2019
- Lubitz, Wolfgang; Chrysina, Maria; Cox, Nicholas
- Photosynthesis Research, Vol. 142, Issue 1
Microsolvation of the Redox-Active Tyrosine-D in Photosystem II: Correlation of Energetics with EPR Spectroscopy and Oxidation-Induced Proton Transfer
journal, January 2019
- Sirohiwal, Abhishek; Neese, Frank; Pantazis, Dimitrios A.
- Journal of the American Chemical Society, Vol. 141, Issue 7
In situ observation of picosecond polaron self-localisation in α-Fe2O3 photoelectrochemical cells
journal, September 2019
- Pastor, Ernest; Park, Ji-Sang; Steier, Ludmilla
- Nature Communications, Vol. 10, Issue 1
Photoswitching mechanism of a fluorescent protein revealed by time-resolved crystallography and transient absorption spectroscopy
journal, February 2020
- Woodhouse, Joyce; Nass Kovacs, Gabriela; Coquelle, Nicolas
- Nature Communications, Vol. 11, Issue 1
Temperature-jump solution X-ray scattering reveals distinct motions in a dynamic enzyme
journal, September 2019
- Thompson, Michael C.; Barad, Benjamin A.; Wolff, Alexander M.
- Nature Chemistry, Vol. 11, Issue 11
The reactivity and stability of polyoxometalate water oxidation electrocatalysts
text, January 2019
- Gao, Dandan; Trentin, Ivan; Schwiedrzik, Ludwig
- Universität Ulm
Time-Resolved Macromolecular Crystallography at Pulsed X-ray Sources
journal, March 2019
- Schmidt, Marius
- International Journal of Molecular Sciences, Vol. 20, Issue 6
How Plants Handle Trivalent (+3) Elements
journal, August 2019
- Poschenrieder, Charlotte; Busoms, Silvia; Barceló, Juan
- International Journal of Molecular Sciences, Vol. 20, Issue 16
A tool for visualizing protein motions in time-resolved crystallography
text, January 2020
- Cecilia, Wickstrand,; Gergely, Katona,; Takanori, Nakane,
- ETH Zurich