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Title: Structure of photosystem II and substrate binding at room temperature

Abstract

Light-induced oxidation of water by photosystem II (PS II) in plants, algae and cyanobacteria has generated most of the dioxygen in the atmosphere. PS II, a membrane-bound multi-subunit pigment protein complex, couples the one-electron photochemistry at the reaction centre with the four-electron redox chemistry of water oxidation at the Mn 4 CaO 5 cluster in the oxygen-evolving complex (OEC). Under illumination, the OEC cycles through five intermediate S-states (S 0 to S 4), in which S 1 is the dark-stable state and S 3 is the last semi-stable state before O-O bond formation and O 2 evolution. A detailed understanding of the O-O bond formation mechanism remains a challenge, and will require elucidation of both the structures of the OEC in the different S-states and the binding of the two substrate waters to the catalytic site. Here we report the use of femtosecond pulses from an X-ray free electron laser (XFEL) to obtain damage-free, room temperature structures of dark-adapted (S 1), two-flash illuminated (2F; S 3 -enriched), and ammonia-bound two-flash illuminated (2F-NH 3; S 3 -enriched) PS II. Although the recent 1.95 Å resolution structure of PS II at cryogenic temperature using an XFEL provided a damage-free view of themore » S 1 state, measurements at room temperature are required to study the structural landscape of proteins under functional conditions, and also for in situ advancement of the S-states. To investigate the water-binding site(s), ammonia, a water analogue, has been used as a marker, as it binds to the Mn 4 CaO 5 cluster in the S 2 and S 3 states. Since the ammonia-bound OEC is active, the ammonia-binding Mn site is not a substrate water site. This approach, together with a comparison of the native dark and 2F states, is used to discriminate between proposed O-O bond formation mechanisms.« less

Authors:
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Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)
OSTI Identifier:
1379614
DOE Contract Number:  
AC02-05CH11231
Resource Type:
Journal Article
Journal Name:
Nature (London)
Additional Journal Information:
Journal Volume: 540; Journal Issue: 7633; Journal ID: ISSN 0028-0836
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English

Citation Formats

Young, Iris D., Ibrahim, Mohamed, Chatterjee, Ruchira, Gul, Sheraz, Fuller, Franklin D., Koroidov, Sergey, Brewster, Aaron S., Tran, Rosalie, Alonso-Mori, Roberto, Kroll, Thomas, Michels-Clark, Tara, Laksmono, Hartawan, Sierra, Raymond G., Stan, Claudiu A., Hussein, Rana, Zhang, Miao, Douthit, Lacey, Kubin, Markus, de Lichtenberg, Casper, Vo Pham, Long, Nilsson, Håkan, Cheah, Mun Hon, Shevela, Dmitriy, Saracini, Claudio, Bean, Mackenzie A., Seuffert, Ina, Sokaras, Dimosthenis, Weng, Tsu-Chien, Pastor, Ernest, Weninger, Clemens, Fransson, Thomas, Lassalle, Louise, Bräuer, Philipp, Aller, Pierre, Docker, Peter T., Andi, Babak, Orville, Allen M., Glownia, James M., Nelson, Silke, Sikorski, Marcin, Zhu, Diling, Hunter, Mark S., Lane, Thomas J., Aquila, Andy, Koglin, Jason E., Robinson, Joseph, Liang, Mengning, Boutet, Sébastien, Lyubimov, Artem Y., Uervirojnangkoorn, Monarin, Moriarty, Nigel W., Liebschner, Dorothee, Afonine, Pavel V., Waterman, David G., Evans, Gwyndaf, Wernet, Philippe, Dobbek, Holger, Weis, William I., Brunger, Axel T., Zwart, Petrus H., Adams, Paul D., Zouni, Athina, Messinger, Johannes, Bergmann, Uwe, Sauter, Nicholas K., Kern, Jan, Yachandra, Vittal K., and Yano, Junko. Structure of photosystem II and substrate binding at room temperature. United States: N. p., 2016. Web. doi:10.1038/nature20161.
Young, Iris D., Ibrahim, Mohamed, Chatterjee, Ruchira, Gul, Sheraz, Fuller, Franklin D., Koroidov, Sergey, Brewster, Aaron S., Tran, Rosalie, Alonso-Mori, Roberto, Kroll, Thomas, Michels-Clark, Tara, Laksmono, Hartawan, Sierra, Raymond G., Stan, Claudiu A., Hussein, Rana, Zhang, Miao, Douthit, Lacey, Kubin, Markus, de Lichtenberg, Casper, Vo Pham, Long, Nilsson, Håkan, Cheah, Mun Hon, Shevela, Dmitriy, Saracini, Claudio, Bean, Mackenzie A., Seuffert, Ina, Sokaras, Dimosthenis, Weng, Tsu-Chien, Pastor, Ernest, Weninger, Clemens, Fransson, Thomas, Lassalle, Louise, Bräuer, Philipp, Aller, Pierre, Docker, Peter T., Andi, Babak, Orville, Allen M., Glownia, James M., Nelson, Silke, Sikorski, Marcin, Zhu, Diling, Hunter, Mark S., Lane, Thomas J., Aquila, Andy, Koglin, Jason E., Robinson, Joseph, Liang, Mengning, Boutet, Sébastien, Lyubimov, Artem Y., Uervirojnangkoorn, Monarin, Moriarty, Nigel W., Liebschner, Dorothee, Afonine, Pavel V., Waterman, David G., Evans, Gwyndaf, Wernet, Philippe, Dobbek, Holger, Weis, William I., Brunger, Axel T., Zwart, Petrus H., Adams, Paul D., Zouni, Athina, Messinger, Johannes, Bergmann, Uwe, Sauter, Nicholas K., Kern, Jan, Yachandra, Vittal K., & Yano, Junko. Structure of photosystem II and substrate binding at room temperature. United States. doi:10.1038/nature20161.
Young, Iris D., Ibrahim, Mohamed, Chatterjee, Ruchira, Gul, Sheraz, Fuller, Franklin D., Koroidov, Sergey, Brewster, Aaron S., Tran, Rosalie, Alonso-Mori, Roberto, Kroll, Thomas, Michels-Clark, Tara, Laksmono, Hartawan, Sierra, Raymond G., Stan, Claudiu A., Hussein, Rana, Zhang, Miao, Douthit, Lacey, Kubin, Markus, de Lichtenberg, Casper, Vo Pham, Long, Nilsson, Håkan, Cheah, Mun Hon, Shevela, Dmitriy, Saracini, Claudio, Bean, Mackenzie A., Seuffert, Ina, Sokaras, Dimosthenis, Weng, Tsu-Chien, Pastor, Ernest, Weninger, Clemens, Fransson, Thomas, Lassalle, Louise, Bräuer, Philipp, Aller, Pierre, Docker, Peter T., Andi, Babak, Orville, Allen M., Glownia, James M., Nelson, Silke, Sikorski, Marcin, Zhu, Diling, Hunter, Mark S., Lane, Thomas J., Aquila, Andy, Koglin, Jason E., Robinson, Joseph, Liang, Mengning, Boutet, Sébastien, Lyubimov, Artem Y., Uervirojnangkoorn, Monarin, Moriarty, Nigel W., Liebschner, Dorothee, Afonine, Pavel V., Waterman, David G., Evans, Gwyndaf, Wernet, Philippe, Dobbek, Holger, Weis, William I., Brunger, Axel T., Zwart, Petrus H., Adams, Paul D., Zouni, Athina, Messinger, Johannes, Bergmann, Uwe, Sauter, Nicholas K., Kern, Jan, Yachandra, Vittal K., and Yano, Junko. Mon . "Structure of photosystem II and substrate binding at room temperature". United States. doi:10.1038/nature20161. https://www.osti.gov/servlets/purl/1379614.
@article{osti_1379614,
title = {Structure of photosystem II and substrate binding at room temperature},
author = {Young, Iris D. and Ibrahim, Mohamed and Chatterjee, Ruchira and Gul, Sheraz and Fuller, Franklin D. and Koroidov, Sergey and Brewster, Aaron S. and Tran, Rosalie and Alonso-Mori, Roberto and Kroll, Thomas and Michels-Clark, Tara and Laksmono, Hartawan and Sierra, Raymond G. and Stan, Claudiu A. and Hussein, Rana and Zhang, Miao and Douthit, Lacey and Kubin, Markus and de Lichtenberg, Casper and Vo Pham, Long and Nilsson, Håkan and Cheah, Mun Hon and Shevela, Dmitriy and Saracini, Claudio and Bean, Mackenzie A. and Seuffert, Ina and Sokaras, Dimosthenis and Weng, Tsu-Chien and Pastor, Ernest and Weninger, Clemens and Fransson, Thomas and Lassalle, Louise and Bräuer, Philipp and Aller, Pierre and Docker, Peter T. and Andi, Babak and Orville, Allen M. and Glownia, James M. and Nelson, Silke and Sikorski, Marcin and Zhu, Diling and Hunter, Mark S. and Lane, Thomas J. and Aquila, Andy and Koglin, Jason E. and Robinson, Joseph and Liang, Mengning and Boutet, Sébastien and Lyubimov, Artem Y. and Uervirojnangkoorn, Monarin and Moriarty, Nigel W. and Liebschner, Dorothee and Afonine, Pavel V. and Waterman, David G. and Evans, Gwyndaf and Wernet, Philippe and Dobbek, Holger and Weis, William I. and Brunger, Axel T. and Zwart, Petrus H. and Adams, Paul D. and Zouni, Athina and Messinger, Johannes and Bergmann, Uwe and Sauter, Nicholas K. and Kern, Jan and Yachandra, Vittal K. and Yano, Junko},
abstractNote = {Light-induced oxidation of water by photosystem II (PS II) in plants, algae and cyanobacteria has generated most of the dioxygen in the atmosphere. PS II, a membrane-bound multi-subunit pigment protein complex, couples the one-electron photochemistry at the reaction centre with the four-electron redox chemistry of water oxidation at the Mn 4 CaO 5 cluster in the oxygen-evolving complex (OEC). Under illumination, the OEC cycles through five intermediate S-states (S 0 to S 4), in which S 1 is the dark-stable state and S 3 is the last semi-stable state before O-O bond formation and O 2 evolution. A detailed understanding of the O-O bond formation mechanism remains a challenge, and will require elucidation of both the structures of the OEC in the different S-states and the binding of the two substrate waters to the catalytic site. Here we report the use of femtosecond pulses from an X-ray free electron laser (XFEL) to obtain damage-free, room temperature structures of dark-adapted (S 1), two-flash illuminated (2F; S 3 -enriched), and ammonia-bound two-flash illuminated (2F-NH 3; S 3 -enriched) PS II. Although the recent 1.95 Å resolution structure of PS II at cryogenic temperature using an XFEL provided a damage-free view of the S 1 state, measurements at room temperature are required to study the structural landscape of proteins under functional conditions, and also for in situ advancement of the S-states. To investigate the water-binding site(s), ammonia, a water analogue, has been used as a marker, as it binds to the Mn 4 CaO 5 cluster in the S 2 and S 3 states. Since the ammonia-bound OEC is active, the ammonia-binding Mn site is not a substrate water site. This approach, together with a comparison of the native dark and 2F states, is used to discriminate between proposed O-O bond formation mechanisms.},
doi = {10.1038/nature20161},
journal = {Nature (London)},
issn = {0028-0836},
number = 7633,
volume = 540,
place = {United States},
year = {2016},
month = {11}
}

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