Predicting the oxidation states of Mn ions in the oxygen-evolving complex of photosystem II using supervised and unsupervised machine learning

Amin, Muhamed

doi:10.1007/s11120-022-00941-8

Title: Predicting the oxidation states of Mn ions in the oxygen-evolving complex of photosystem II using supervised and unsupervised machine learning

Journal Article · 27 July 2022 · Photosynthesis Research

DOI:https://doi.org/10.1007/s11120-022-00941-8· OSTI ID:1976709

Abstract Serial Femtosecond Crystallography at the X-ray Free Electron Laser (XFEL) sources enabled the imaging of the catalytic intermediates of the oxygen evolution reaction of Photosystem II (PSII). However, due to the incoherent transition of the S-states, the resolved structures are a convolution from different catalytic states. Here, we train Decision Tree Classifier and K-means clustering models on Mn compounds obtained from the Cambridge Crystallographic Database to predict the S-state of the X-ray, XFEL, and CryoEM structures by predicting the Mn’s oxidation states in the oxygen-evolving complex. The model agrees mostly with the XFEL structures in the dark S₁state. However, significant discrepancies are observed for the excited XFEL states (S₂, S_3,and S₀) and the dark states of the X-ray and CryoEM structures. Furthermore, there is a mismatch between the predicted S-states within the two monomers of the same dimer, mainly in the excited states. We validated our model against other metalloenzymes, the valence bond model and the Mn spin densities calculated using density functional theory for two of the mismatched predictions of PSII. The model suggests designing a more optimized sample delivery and illumiation systems are crucial to precisely resolve the geometry of the advanced S-states to overcome the noncoherent S-state transition. In addition, significant radiation damage is observed in X-ray and CryoEM structures, particularly at the dangler Mn center (Mn4). Our model represents a valuable tool for investigating the electronic structure of the catalytic metal cluster of PSII to understand the water splitting mechanism.

Cite

Export

Save

Research Organization:: City Univ. of New York (CUNY), NY (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

DOE Contract Number:: SC0001423

OSTI ID:: 1976709

Journal Information:: Photosynthesis Research, Vol. 156, Issue 1; ISSN 0166-8595

Publisher:: Springer

Country of Publication:: United States

Language:: English

References (53)

Analysis of the Radiation-Damage-Free X-ray Structure of Photosystem II in Light of EXAFS and QM/MM Data Askerka, Mikhail; Vinyard, David J.; Wang, Jimin Biochemistry, Vol. 54, Issue 9 https://doi.org/10.1021/acs.biochem.5b00089	journal	February 2015
Photosystem II: Its function, structure, and implications for artificial photosynthesis Barber, James Biochemistry (Moscow), Vol. 79, Issue 3 https://doi.org/10.1134/S0006297914030031	journal	March 2014
Characterization of the Mn Oxidation States in Photosystem II by Kβ X-ray Fluorescence Spectroscopy Bergmann, U.; Grush, M. M.; Horne, C. R. The Journal of Physical Chemistry B, Vol. 102, Issue 42 https://doi.org/10.1021/jp982038s	journal	October 1998
Biosynthetic Ca2+/Sr2+ Exchange in the Photosystem II Oxygen-evolving Enzyme of Thermosynechococcus elongatus Boussac, Alain; Rappaport, Fabrice; Carrier, Patrick Journal of Biological Chemistry, Vol. 279, Issue 22 https://doi.org/10.1074/jbc.M401677200	journal	May 2004
Recent Developments in the Methods and Applications of the Bond Valence Model Brown, Ian David Chemical Reviews, Vol. 109, Issue 12 https://doi.org/10.1021/cr900053k	journal	December 2009
What is the best way to determine bond-valence parameters? Brown, I. David IUCrJ, Vol. 4, Issue 5 https://doi.org/10.1107/S2052252517011782	journal	September 2017
Water oxidation chemistry of photosystem II Brudvig, Gary W. Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 363, Issue 1494 https://doi.org/10.1098/rstb.2007.2217	journal	October 2007
New software for searching the Cambridge Structural Database and visualizing crystal structures Bruno, Ian J.; Cole, Jason C.; Edgington, Paul R. Acta Crystallographica Section B Structural Science, Vol. 58, Issue 3 https://doi.org/10.1107/S0108768102003324	journal	May 2002
The Photochemistry of the Future Ciamician, G. Science, Vol. 36, Issue 926 https://doi.org/10.1126/science.36.926.385	journal	September 1912
Biopython: freely available Python tools for computational molecular biology and bioinformatics Cock, P. J. A.; Antao, T.; Chang, J. T. Bioinformatics, Vol. 25, Issue 11 https://doi.org/10.1093/bioinformatics/btp163	journal	March 2009
Proton Isomers Rationalize the High- and Low-Spin Forms of the S ₂ State Intermediate in the Water-Oxidizing Reaction of Photosystem II Corry, Thomas A.; O’Malley, Patrick J. The Journal of Physical Chemistry Letters, Vol. 10, Issue 17 https://doi.org/10.1021/acs.jpclett.9b01372	journal	August 2019
Reflections on substrate water and dioxygen formation Cox, Nicholas; Messinger, Johannes Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1827, Issue 8-9 https://doi.org/10.1016/j.bbabio.2013.01.013	journal	August 2013
Effect of Ca ²⁺ /Sr ²⁺ Substitution on the Electronic Structure of the Oxygen-Evolving Complex of Photosystem II: A Combined Multifrequency EPR, ⁵⁵ Mn-ENDOR, and DFT Study of the S ₂ State Cox, Nicholas; Rapatskiy, Leonid; Su, Ji-Hu Journal of the American Chemical Society, Vol. 133, Issue 10 https://doi.org/10.1021/ja110145v	journal	March 2011
Electronic structure of the oxygen-evolving complex in photosystem II prior to O-O bond formation Cox, N.; Retegan, M.; Neese, F. Science, Vol. 345, Issue 6198 https://doi.org/10.1126/science.1254910	journal	August 2014
Radiation damage in macromolecular crystallography: what is it and why should we care? Garman, Elspeth F. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/S0907444910008656	journal	March 2010
Progress in research into radiation damage in cryo-cooled macromolecular crystals Garman, Elspeth F.; McSweeney, Sean M. Journal of Synchrotron Radiation, Vol. 14, Issue 1 https://doi.org/10.1107/S0909049506053015	journal	December 2006
Radiation damage in protein crystals examined under various conditions by different methods Garman, Elspeth F.; Nave, Colin Journal of Synchrotron Radiation, Vol. 16, Issue 2 https://doi.org/10.1107/S0909049509005238	journal	February 2009
Macromolecular crystallography radiation damage research: what's new? Garman, Elspeth F.; Weik, Martin Journal of Synchrotron Radiation, Vol. 18, Issue 3 https://doi.org/10.1107/S0909049511013859	journal	April 2011
Radiation damage to biological macromolecules: some answers and more questions Garman, Elspeth F.; Weik, Martin Journal of Synchrotron Radiation, Vol. 20, Issue 1 https://doi.org/10.1107/S0909049512050418	journal	December 2012
High-resolution cryo-electron microscopy structure of photosystem II from the mesophilic cyanobacterium, Synechocystis sp. PCC 6803 Gisriel, Christopher J.; Wang, Jimin; Liu, Jinchan Proceedings of the National Academy of Sciences, Vol. 119, Issue 1 https://doi.org/10.1073/pnas.2116765118	journal	December 2021
Native-like Photosystem II Superstructure at 2.44 Å Resolution through Detergent Extraction from the Protein Crystal Hellmich, Julia; Bommer, Martin; Burkhardt, Anja Structure, Vol. 22, Issue 11 https://doi.org/10.1016/j.str.2014.09.007	journal	November 2014
Determination of macromolecular structures from anomalous diffraction of synchrotron radiation Hendrickson, W. Science, Vol. 254, Issue 5028 https://doi.org/10.1126/science.1925561	journal	October 1991
Structural dynamics in the water and proton channels of photosystem II during the S2 to S3 transition Hussein, Rana; Ibrahim, Mohamed; Bhowmick, Asmit Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-021-26781-z	journal	November 2021
Untangling the sequence of events during the S ₂ → S ₃ transition in photosystem II and implications for the water oxidation mechanism Ibrahim, Mohamed; Fransson, Thomas; Chatterjee, Ruchira Proceedings of the National Academy of Sciences, Vol. 117, Issue 23 https://doi.org/10.1073/pnas.2000529117	journal	May 2020
Using collective knowledge to assign oxidation states of metal cations in metal–organic frameworks Jablonka, Kevin Maik; Ongari, Daniele; Moosavi, Seyed Mohamad Nature Chemistry, Vol. 13, Issue 8 https://doi.org/10.1038/s41557-021-00717-y	journal	July 2021
High-resolution cryo-EM structure of photosystem II reveals damage from high-dose electron beams Kato, Koji; Miyazaki, Naoyuki; Hamaguchi, Tasuku Communications Biology, Vol. 4, Issue 1 https://doi.org/10.1038/s42003-021-01919-3	journal	March 2021
Relative stability of the S2 isomers of the oxygen evolving complex of photosystem II Kaur, Divya; Szejgis, Witold; Mao, Junjun Photosynthesis Research, Vol. 141, Issue 3 https://doi.org/10.1007/s11120-019-00637-6	journal	April 2019
Structures of the intermediates of Kok’s photosynthetic water oxidation clock Kern, Jan; Chatterjee, Ruchira; Young, Iris D. Nature, Vol. 563, Issue 7731 https://doi.org/10.1038/s41586-018-0681-2	journal	November 2018
COOPERATION OF CHARGES IN PHOTOSYNTHETIC O ₂ EVOLUTION–I. A LINEAR FOUR STEP MECHANISM Kok, Bessel; Forbush, Bliss; McGLOIN, Marion Photochemistry and Photobiology, Vol. 11, Issue 6 https://doi.org/10.1111/j.1751-1097.1970.tb06017.x	journal	June 1970
Structure of Sr-substituted photosystem II at 2.1 A resolution and its implications in the mechanism of water oxidation Koua, F. H. M.; Umena, Y.; Kawakami, K. Proceedings of the National Academy of Sciences, Vol. 110, Issue 10 https://doi.org/10.1073/pnas.1219922110	journal	February 2013
Capturing structural changes of the S ₁ to S ₂ transition of photosystem II using time-resolved serial femtosecond crystallography Li, Hongjie; Nakajima, Yoshiki; Nomura, Takashi IUCrJ, Vol. 8, Issue 3 https://doi.org/10.1107/S2052252521002177	journal	April 2021
S ₁ -State Model of the O ₂ -Evolving Complex of Photosystem II Luber, Sandra; Rivalta, Ivan; Umena, Yasufumi Biochemistry, Vol. 50, Issue 29 https://doi.org/10.1021/bi200681q	journal	July 2011
Location of two Mn2+ affinity sites in photosystem II detected by pulsed electron–electron double resonance Mino, Hiroyuki; Asada, Mizue Photosynthesis Research, Vol. 152, Issue 3 https://doi.org/10.1007/s11120-021-00885-5	journal	November 2021
Thylakoid membrane lipid sulfoquinovosyl-diacylglycerol (SQDG) is required for full functioning of photosystem II in Thermosynechococcus elongatus Nakajima, Yoshiki; Umena, Yasufumi; Nagao, Ryo Journal of Biological Chemistry, Vol. 293, Issue 38 https://doi.org/10.1074/jbc.RA118.004304	journal	September 2018
The Artificial Leaf Nocera, Daniel G. Accounts of Chemical Research, Vol. 45, Issue 5 https://doi.org/10.1021/ar2003013	journal	January 2012
Solar Fuels and Solar Chemicals Industry Nocera, Daniel G. Accounts of Chemical Research, Vol. 50, Issue 3 https://doi.org/10.1021/acs.accounts.6b00615	journal	March 2017
Automated oxidation-state assignment for metal sites in coordination complexes in the Cambridge Structural Database Reeves, Matthew G.; Wood, Peter A.; Parsons, Simon Acta Crystallographica Section B Structural Science, Crystal Engineering and Materials, Vol. 75, Issue 6 https://doi.org/10.1107/S2052520619013040	journal	November 2019
A five-coordinate Mn( iv ) intermediate in biological water oxidation: spectroscopic signature and a pivot mechanism for water binding Retegan, Marius; Krewald, Vera; Mamedov, Fikret Chemical Science, Vol. 7, Issue 1 https://doi.org/10.1039/C5SC03124A	journal	January 2016
Reduced derivatives of the manganese cluster in the photosynthetic oxygen-evolving complex Riggs, Pamela J.; Yocum, Charles F.; Penner-Hahn, James E. Journal of the American Chemical Society, Vol. 114, Issue 26 https://doi.org/10.1021/ja00052a079	journal	December 1992
The assignment and validation of metal oxidation states in the Cambridge Structural Database Shields, Gregory P.; Raithby, Paul R.; Allen, Frank H. Acta Crystallographica Section B Structural Science, Vol. 56, Issue 3 https://doi.org/10.1107/S0108768199015086	journal	June 2000
Native structure of photosystem II at 1.95 Å resolution viewed by femtosecond X-ray pulses Suga, Michihiro; Akita, Fusamichi; Hirata, Kunio Nature, Vol. 517, Issue 7532 https://doi.org/10.1038/nature13991	journal	November 2014
Light-induced structural changes and the site of O=O bond formation in PSII caught by XFEL Suga, Michihiro; Akita, Fusamichi; Sugahara, Michihiro Nature, Vol. 543, Issue 7643 https://doi.org/10.1038/nature21400	journal	February 2017
An oxyl/oxo mechanism for oxygen-oxygen coupling in PSII revealed by an x-ray free-electron laser Suga, Michihiro; Akita, Fusamichi; Yamashita, Keitaro Science, Vol. 366, Issue 6463 https://doi.org/10.1126/science.aax6998	journal	October 2019
Two Different Structures of the Oxygen-Evolving Complex in the Same Polypeptide Frameworks of Photosystem II Tanaka, Ayako; Fukushima, Yoshimasa; Kamiya, Nobuo Journal of the American Chemical Society, Vol. 139, Issue 5 https://doi.org/10.1021/jacs.6b09666	journal	January 2017
Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å Umena, Yasufumi; Kawakami, Keisuke; Shen, Jian-Ren Nature, Vol. 473, Issue 7345 https://doi.org/10.1038/nature09913	journal	April 2011
Mutual relationships between structural and functional changes in a PsbM-deletion mutant of photosystem II Uto, S.; Kawakami, K.; Umena, Y. Faraday Discussions, Vol. 198 https://doi.org/10.1039/C6FD00213G	journal	January 2017
Progress Toward a Molecular Mechanism of Water Oxidation in Photosystem II Vinyard, David J.; Brudvig, Gary W. Annual Review of Physical Chemistry, Vol. 68, Issue 1 https://doi.org/10.1146/annurev-physchem-052516-044820	journal	May 2017
FTIR Spectra and Normal-Mode Analysis of a Tetranuclear Manganese Adamantane-like Complex in Two Electrochemically Prepared Oxidation States: Relevance to the Oxygen-Evolving Complex of Photosystem II Visser, Hendrik; Dubé, Christopher E.; Armstrong, William H. Journal of the American Chemical Society, Vol. 124, Issue 37 https://doi.org/10.1021/ja020409j	journal	August 2002
Heterogeneous Composition of Oxygen-Evolving Complexes in Crystal Structures of Dark-Adapted Photosystem II Wang, Jimin; Gisriel, Christopher J.; Reiss, Krystle Biochemistry, Vol. 60, Issue 45 https://doi.org/10.1021/acs.biochem.1c00611	journal	October 2021
Mn ₄ Ca Cluster in Photosynthesis: Where and How Water is Oxidized to Dioxygen Yano, Junko; Yachandra, Vittal Chemical Reviews, Vol. 114, Issue 8 https://doi.org/10.1021/cr4004874	journal	March 2014
High-Resolution Mn EXAFS of the Oxygen-Evolving Complex in Photosystem II: Structural Implications for the Mn ₄ Ca Cluster Yano, Junko; Pushkar, Yulia; Glatzel, Pieter Journal of the American Chemical Society, Vol. 127, Issue 43 https://doi.org/10.1021/ja054873a	journal	November 2005
Structure of photosystem II and substrate binding at room temperature Young, Iris D.; Ibrahim, Mohamed; Chatterjee, Ruchira Nature, Vol. 540, Issue 7633 https://doi.org/10.1038/nature20161	journal	November 2016
Advancing photosystem II photoelectrochemistry for semi-artificial photosynthesis Zhang, Jenny Z.; Reisner, Erwin Nature Reviews Chemistry, Vol. 4, Issue 1 https://doi.org/10.1038/s41570-019-0149-4	journal	December 2019

Similar Records

The O ₂ -Evolving Complex of Photosystem II: Recent Insights from Quantum Mechanics/Molecular Mechanics (QM/MM), Extended X-ray Absorption Fine Structure (EXAFS), and Femtosecond X-ray Crystallography Data

Journal Article · 2016 · Accounts of Chemical Research · OSTI ID:1976709

Askerka, Mikhail; Brudvig, Gary W.; Batista, Victor S.

Crystallographic Data Support the Carousel Mechanism of Water Supply to the Oxygen-Evolving Complex of Photosystem II

Journal Article · 2017 · ACS Energy Letters · OSTI ID:1976709

Wang, Jimin; Askerka, Mikhail; Brudvig, Gary W.; +1 more

Thermodynamics of the S₂-to-S₃ state transition of the oxygen-evolving complex of photosystem II

Journal Article · 2019 · Physical Chemistry Chemical Physics. PCCP · OSTI ID:1976709

Amin, Muhamed; Kaur, Divya; Yang, Ke R.; +5 more

Related Subjects

Plant Sciences

Title: Predicting the oxidation states of Mn ions in the oxygen-evolving complex of photosystem II using supervised and unsupervised machine learning

Citation Formats

References (53)

Similar Records

Related Subjects