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Title: 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 in this paper, 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–Omore » 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.« less

Authors:
 [1];  [1];  [1];  [1];  [1];  [2];  [1];  [3];  [1];  [4];  [2];  [2];  [1];  [5];  [6];  [7];  [2];  [2];  [8];  [1] more »;  [4];  [8];  [4];  [9];  [9];  [9];  [4];  [4];  [4];  [4];  [4];  [1];  [10];  [2];  [11];  [12];  [1];  [2];  [5];  [1];  [1] « less
  1. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Molecular Biophysics and Integrated Bioimaging Division
  2. Humboldt-Univ Berlin, Berlin (Germany). Inst. fur Biologie
  3. 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
  4. SLAC National Accelerator Lab., Menlo Park, CA (United States). Linac Coherent Light Source (LCLS)
  5. Umeå Univ., Umeå (Sweden). Inst. för Kemi, Kemiskt Biologiskt Centrum; Uppsala Univ. (Sweden). Dept. of Chemistry-Ångström, Molecular Biomimetics
  6. Uppsala Univ. (Sweden). Dept. of Chemistry-Ångström, Molecular Biomimetics
  7. Umeå Univ., Umeå (Sweden). Inst. för Kemi, Kemiskt Biologiskt Centrum
  8. SLAC National Accelerator Lab., Menlo Park, CA (United States). Stanford Synchrotron Radiation Lightsource (SSRL)
  9. Science and Technology Facilities Council (STFC), Harwell Campus, Oxford (United Kingdom). Diamond Light Source, Ltd.
  10. 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
  11. 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
  12. SLAC National Accelerator Lab., Menlo Park, CA (United States). Photon Ultrafast Laser Science and Engineering Inst. (PULSE)
Publication Date:
Research Org.:
SLAC National Accelerator Lab., Menlo Park, CA (United States); Lawrence Berkeley National Lab. (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 in this paper, 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 = {2018},
month = {11}
}

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Works referencing / citing this record:

Artificial Mn 4 Ca Clusters with Exchangeable Solvent Molecules Mimicking the Oxygen‐Evolving Center in Photosynthesis
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A Gas‐Phase Ca n Mn 4− n O 4 + Cluster Model for the Oxygen‐Evolving Complex of Photosystem II
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A High‐Valent Manganese(IV)–Oxo–Cerium(IV) Complex and Its Enhanced Oxidizing Reactivity
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Artificial Mn 4 Ca Clusters with Exchangeable Solvent Molecules Mimicking the Oxygen-Evolving Center in Photosynthesis
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A Gas‐Phase Ca n Mn 4− n O 4 + Cluster Model for the Oxygen‐Evolving Complex of Photosystem II
journal, June 2019

  • Mauthe, Silvia; Fleischer, Irene; Bernhardt, Thorsten M.
  • Angewandte Chemie International Edition, Vol. 58, Issue 25
  • DOI: 10.1002/anie.201903738

Across the Board: Licheng Sun on the Mechanism of O−O Bond Formation in Photosystem II
journal, June 2019


Generation and Electron‐Transfer Reactivity of the Long‐Lived Photoexcited State of a Manganese(IV)‐Oxo‐Scandium Nitrate Complex
journal, January 2020

  • Sharma, Namita; Lee, Yong‐Min; Nam, Wonwoo
  • Israel Journal of Chemistry, Vol. 60, Issue 10-11
  • DOI: 10.1002/ijch.201900147

Relative stability of the S2 isomers of the oxygen evolving complex of photosystem II
journal, April 2019


Water oxidation in photosystem II
journal, June 2019


In situ observation of picosecond polaron self-localisation in α-Fe2O3 photoelectrochemical cells
journal, September 2019


Promoting proton coupled electron transfer in redox catalysts through molecular design
journal, January 2019

  • Thammavongsy, Zachary; Mercer, Ian P.; Yang, Jenny Y.
  • Chemical Communications, Vol. 55, Issue 70
  • DOI: 10.1039/c9cc05139b

Significance of hydrogen bonding networks in the proton-coupled electron transfer reactions of photosystem II from a quantum-mechanics perspective
journal, January 2019

  • Chai, Jun; Zheng, Zhaoyang; Pan, Hui
  • Physical Chemistry Chemical Physics, Vol. 21, Issue 17
  • DOI: 10.1039/c9cp00868c

Thermodynamics of the S 2 -to-S 3 state transition of the oxygen-evolving complex of photosystem II
journal, January 2019

  • Amin, Muhamed; Kaur, Divya; Yang, Ke R.
  • Physical Chemistry Chemical Physics, Vol. 21, Issue 37
  • DOI: 10.1039/c9cp02308a

Dynamic water bridging and proton transfer at a surface carboxylate cluster of photosystem II
journal, January 2019

  • Kemmler, Lukas; Ibrahim, Mohamed; Dobbek, Holger
  • Physical Chemistry Chemical Physics, Vol. 21, Issue 45
  • DOI: 10.1039/c9cp03926k

Pivotal role of the redox-active tyrosine in driving the water splitting catalyzed by photosystem II
journal, January 2020

  • Nakamura, Shin; Capone, Matteo; Narzi, Daniele
  • Physical Chemistry Chemical Physics, Vol. 22, Issue 1
  • DOI: 10.1039/c9cp04605d

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
  • DOI: 10.1039/c9ta05108b

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
  • DOI: 10.1039/d0sc01097a

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
  • DOI: 10.1042/bcj20190208

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
  • DOI: 10.1063/1.5139065

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
  • DOI: 10.1073/pnas.1817526116

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
  • DOI: 10.1073/pnas.1915879117

An outlook on using serial femtosecond crystallography in drug discovery
journal, May 2019


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
  • DOI: 10.1107/s1600577519001577

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
  • DOI: 10.1111/febs.15099

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
  • DOI: 10.1111/ppl.12947

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
  • DOI: 10.1111/ppl.12948

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
  • DOI: 10.1111/ppl.12949

An oxyl/oxo mechanism for oxygen-oxygen coupling in PSII revealed by an x-ray free-electron laser
journal, October 2019


How Plants Handle Trivalent (+3) Elements
journal, August 2019

  • Poschenrieder, Charlotte; Busoms, Silvia; Barceló, Juan
  • International Journal of Molecular Sciences, Vol. 20, Issue 16
  • DOI: 10.3390/ijms20163984

Water Network Dynamics Next to the Oxygen-Evolving Complex of Photosystem II
journal, March 2019


The Reactivity and Stability of Polyoxometalate Water Oxidation Electrocatalysts
journal, December 2019


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
  • DOI: 10.1002/anie.201910032

The Two Alternative Oxidation State Assignments of Manganese Ions: What S2 CW-EPR Multiline (ML) Signal Simulations Reveal?
journal, February 2020


Light polarization dependency existing in the biological photosystem and possible implications for artificial antenna systems
journal, October 2019


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
  • DOI: 10.1038/s41467-020-14537-0

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
  • DOI: 10.1039/d0se00232a

The microfluidic laboratory at Synchrotron SOLEIL
journal, January 2020

  • Chaussavoine, Igor; Beauvois, Anthony; Mateo, Tiphaine
  • Journal of Synchrotron Radiation, Vol. 27, Issue 1
  • DOI: 10.1107/S1600577519015042

Dynamic water bridging and proton transfer at a surface carboxylate cluster of photosystem II
text, January 2019


Thermodynamics of the S2-to-S3 State Transition of the Oxygen-Evolving Complex of Photosystem II
text, January 2019


The Reactivity and Stability of Polyoxometalate Water Oxidation Electrocatalysts
text, January 2020


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
  • DOI: 10.1038/s41557-019-0329-3