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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) (SC-22). Chemical Sciences, Geosciences & Biosciences Division; USDOE Office of Science (SC), Basic Energy Sciences (BES)
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. 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, and Yachandra, Vittal K. Wed . "Structures of the intermediates of Kok’s photosynthetic water oxidation clock". United States. doi: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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    • Meza-Chincha, Ana-Lucia; Lindner, Joachim O.; Schindler, Dorothee
    • Chemical Science
    • DOI: 10.1039/d0sc01097a