Going around the Kok cycle of the water oxidation reaction with femtosecond X-ray crystallography
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 CO2 fixation in the photosynthetic apparatus. The catalytic...
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| Format: | Article |
| Language: | English |
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International Union of Crystallography
2023-11-01
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| Series: | IUCrJ |
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| Online Access: | http://scripts.iucr.org/cgi-bin/paper?S2052252523008928 |
| _version_ | 1827774884266115072 |
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| author | Asmit Bhowmick Philipp S. Simon Isabel Bogacz Rana Hussein Miao Zhang Hiroki Makita Mohamed Ibrahim Ruchira Chatterjee Margaret D. Doyle Mun Hon Cheah Petko Chernev Franklin D. Fuller Thomas Fransson Roberto Alonso-Mori Aaron S. Brewster Nicolas K. Sauter Uwe Bergmann Holger Dobbek Athina Zouni Johannes Messinger Jan Kern Vittal K. Yachandra Junko Yano |
| author_facet | Asmit Bhowmick Philipp S. Simon Isabel Bogacz Rana Hussein Miao Zhang Hiroki Makita Mohamed Ibrahim Ruchira Chatterjee Margaret D. Doyle Mun Hon Cheah Petko Chernev Franklin D. Fuller Thomas Fransson Roberto Alonso-Mori Aaron S. Brewster Nicolas K. Sauter Uwe Bergmann Holger Dobbek Athina Zouni Johannes Messinger Jan Kern Vittal K. Yachandra Junko Yano |
| author_sort | Asmit Bhowmick |
| collection | DOAJ |
| description | 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 CO2 fixation in the photosynthetic apparatus. The catalytic center of PS II is an oxygen-bridged Mn4Ca complex (Mn4CaO5) 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 OX 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 Mn4Ca cluster. |
| first_indexed | 2024-03-11T13:44:00Z |
| format | Article |
| id | doaj.art-1786f5eb911749f7b7abfce1fd690bcd |
| institution | Directory Open Access Journal |
| issn | 2052-2525 |
| language | English |
| last_indexed | 2024-03-11T13:44:00Z |
| publishDate | 2023-11-01 |
| publisher | International Union of Crystallography |
| record_format | Article |
| series | IUCrJ |
| spelling | doaj.art-1786f5eb911749f7b7abfce1fd690bcd2023-11-02T10:54:51ZengInternational Union of CrystallographyIUCrJ2052-25252023-11-0110664265510.1107/S2052252523008928it5029Going around the Kok cycle of the water oxidation reaction with femtosecond X-ray crystallographyAsmit Bhowmick0Philipp S. Simon1Isabel Bogacz2Rana Hussein3Miao Zhang4Hiroki Makita5Mohamed Ibrahim6Ruchira Chatterjee7Margaret D. Doyle8Mun Hon Cheah9Petko Chernev10Franklin D. Fuller11Thomas Fransson12Roberto Alonso-Mori13Aaron S. Brewster14Nicolas K. Sauter15Uwe Bergmann16Holger Dobbek17Athina Zouni18Johannes Messinger19Jan Kern20Vittal K. Yachandra21Junko Yano22Molecular Biophysics and Integrated Bioimaging Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USAMolecular Biophysics and Integrated Bioimaging Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USAMolecular Biophysics and Integrated Bioimaging Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USADepartment of Biology, Humboldt-Universität zu Berlin, 10099 Berlin, GermanyMolecular Biophysics and Integrated Bioimaging Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USAMolecular Biophysics and Integrated Bioimaging Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USADepartment of Biology, Humboldt-Universität zu Berlin, 10099 Berlin, GermanyMolecular Biophysics and Integrated Bioimaging Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USAMolecular Biophysics and Integrated Bioimaging Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USAMolecular Biomimetics, Department of Chemistry- Ångström, Uppsala University, Uppsala SE 75120, SwedenMolecular Biomimetics, Department of Chemistry- Ångström, Uppsala University, Uppsala SE 75120, SwedenLinac Coherent Light Source, SLAC National Accelerator Laboratory, Menlo Park, CA 94025, USADepartment of Physics, AlbaNova University Center, Stockholm University, Stockholm SE-10691, SwedenLinac Coherent Light Source, SLAC National Accelerator Laboratory, Menlo Park, CA 94025, USAMolecular Biophysics and Integrated Bioimaging Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USAMolecular Biophysics and Integrated Bioimaging Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USADepartment of Physics, University of Wisconsin–Madison, Madison, WI 53706, USADepartment of Biology, Humboldt-Universität zu Berlin, 10099 Berlin, GermanyDepartment of Biology, Humboldt-Universität zu Berlin, 10099 Berlin, GermanyMolecular Biomimetics, Department of Chemistry- Ångström, Uppsala University, Uppsala SE 75120, SwedenMolecular Biophysics and Integrated Bioimaging Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USAMolecular Biophysics and Integrated Bioimaging Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USAMolecular Biophysics and Integrated Bioimaging Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USAThe 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 CO2 fixation in the photosynthetic apparatus. The catalytic center of PS II is an oxygen-bridged Mn4Ca complex (Mn4CaO5) 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 OX 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 Mn4Ca cluster.http://scripts.iucr.org/cgi-bin/paper?S2052252523008928photosystem iioxygen evolving complexmanganese metalloenzymeswater-oxidationwater-splittingx-ray free-electron lasersx-ray spectroscopy |
| spellingShingle | Asmit Bhowmick Philipp S. Simon Isabel Bogacz Rana Hussein Miao Zhang Hiroki Makita Mohamed Ibrahim Ruchira Chatterjee Margaret D. Doyle Mun Hon Cheah Petko Chernev Franklin D. Fuller Thomas Fransson Roberto Alonso-Mori Aaron S. Brewster Nicolas K. Sauter Uwe Bergmann Holger Dobbek Athina Zouni Johannes Messinger Jan Kern Vittal K. Yachandra Junko Yano Going around the Kok cycle of the water oxidation reaction with femtosecond X-ray crystallography IUCrJ photosystem ii oxygen evolving complex manganese metalloenzymes water-oxidation water-splitting x-ray free-electron lasers x-ray spectroscopy |
| title | Going around the Kok cycle of the water oxidation reaction with femtosecond X-ray crystallography |
| title_full | Going around the Kok cycle of the water oxidation reaction with femtosecond X-ray crystallography |
| title_fullStr | Going around the Kok cycle of the water oxidation reaction with femtosecond X-ray crystallography |
| title_full_unstemmed | Going around the Kok cycle of the water oxidation reaction with femtosecond X-ray crystallography |
| title_short | Going around the Kok cycle of the water oxidation reaction with femtosecond X-ray crystallography |
| title_sort | going around the kok cycle of the water oxidation reaction with femtosecond x ray crystallography |
| topic | photosystem ii oxygen evolving complex manganese metalloenzymes water-oxidation water-splitting x-ray free-electron lasers x-ray spectroscopy |
| url | http://scripts.iucr.org/cgi-bin/paper?S2052252523008928 |
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