An additional water is introduced into the manganese cluster during the formation of the S3 state of photosystem II
Year: 2026
Type: article
Abstract: During photosynthetic water oxidation, the Mn4Ca cluster in Photosystem II progresses through five intermediate Si (i = 0–4) states. X-ray crystallography studies have reported the insertion of one new O ligand during the formation of the S3 state, but recent studies question the presence of this additional ligand based on cryo-EM and earlier room-temperature crystallography data. There is also controversy about whether the O-O bond interaction already occurs in the S3 state or in the subsequent S3 to S0 transition. Here we report conventional high-resolution data for the S1, S2, and S3 states to a resolution of ~1.9 Å, and anomalous diffraction data at two energies (9.5 keV and 7 keV), that was used to model the Mn positions, followed by determination of oxygen positions using the high-resolution maps. We show that the new oxygen atom, OX (or O6), in the S3 state is observable as a distinct peak without any restraints, confirming its ligation to Mn1 and Ca. The OX-O5 distance is ~2.1 Å, supporting no strong interaction between them in the S3 state, suggesting that if this is the O-O bond formation site, it is formed during the S3 to S0 transition initiated by the final oxidation of the cluster. Here, the authors report the S3 state structure of Photosystem II solved with X-ray crystallography at two different energies using an XFEL. The results provide evidence for an oxygen ligand, OX (or O6) and do not support O-O bond formation in the S3 state.
Source: Nature Communications
Authors: Asmit Bhowmick, Miao Zhang, Philipp S. Simon, Hiroki Makita, Isabela I. Nangca, Erzsi Szilagyi, Moritz Kretzschmar, Margaret D. Doyle, Natalie M. Minnetian, Rana Hussein, Olli Hart, Kuntal Chatterjee, A. Orkun Aydin, Dmitry Shevela, Mun Hon Cheah, Nicholas Croy, Petko Chernev, Thomas Fransson, Vandana Tiwari, Humberto Sanchez, Pamela Schleissner, Randy Lemons, Greg Gate, Meredith Henstridge, James M. Glownia, Frédéric Poitevin, Daniel J. Rosenberg, Sebastian Dehe, Leland B. Gee, Kensuke Tono, Shigeki Owada, Roland Oggenfuss, Dmitry Ozerov, Mathias Sander, Roman Mankowsky, Henrik T. Lemke, Iris D. Young, James M. Holton, David W. Mittan-Moreau, Daniel W. Paley, Pavel V. Afonine, Nigel W. Moriarty, Paul D. Adams, Fikret Mamedov, Holger Dobbek, Athina Zouni, Roberto Alonso-Mori, Uwe Bergmann, Aaron S. Brewster, Nicholas K. Sauter, Johannes Messinger, Jan F. Kern, Vittal K. Yachandra, Junko Yano
Institutions: Lawrence Berkeley National Laboratory, Humboldt-Universität zu Berlin, Goethe University Frankfurt, Lam Research (United States), Uppsala University, Umeå Plant Science Centre, Umeå University, KTH Royal Institute of Technology, SLAC National Accelerator Laboratory, Linac Coherent Light Source, SPring-8, Japan Synchrotron Radiation Research Institute, Paul Scherrer Institute, Universität Hamburg, University of California, San Francisco, University of California, Berkeley, University of Wisconsin–Madison
Language: English
Subfield: Molecular Biology
Domain: Life Sciences
Open Access status: gold
Estimated APC paid: $6,990
Funders: U.S. Department of Energy, University of Wisconsin-Madison, Lam Research, National Energy Research Scientific Computing Center, Deutsche Forschungsgemeinschaft, Paul Scherrer Institut, Kungliga Tekniska Högskolan, Umeå Universitet, Universität Hamburg, Humboldt-Universität zu Berlin, Uppsala Universitet, Erik och Anne Marie Detlofs Stiftelse, National Institutes of Health, Office of Science, University of California, San Francisco, RIKEN, National Institute of General Medical Sciences, Basic Energy Sciences, Chemical Sciences, Geosciences, and Biosciences Division, Lawrence Berkeley National Laboratory, SLAC National Accelerator Laboratory
Awards: G1014846411, G1079818582, Phenix: Integrated algorithms for high quality models from crystallographic and cryo-EM data, G1143651532, G122673668, G1229526393, G1286236842, G1286251239, G1396440249, G1451874870, G1677143136, High Speed Large Area Detector for LCLS, G1767990418, G1804828992, G1992336477, G2037563265, G2371548206, G2539837713, G2618837358, G262532246, G303061748, G30714459, G3083819904, G334911014, G3390287098, G3488436650, G3629260272, G3685081974, Characterisation of haem lyases and their dedicated roles in bacterial cytochrome c biogenesis, G382641700, G3884951186, G419881185, G4235786860, G4280418065, G42916606, G4501827968, G4581610328, G4711507462, G495301720, G498139845, G5076365615, Computational Tools for Neutron Protein Crystallography, G5570207115, G6188209572, G650090426, G6550344761, G6652958823, G7283024673, G7331630580, G7354628648, G7471674696, G7912248388, G8229677252, G8251603445, G8382000481, A Synchrotron Radiation Structural Biology Resource, G8925327636, Phenix: providing high quality software to the research community for crystallography and cryo-EM, ALS Efficiently Networking Advanced Beam Line Experiments (ALS-ENABLE), Biological Spectroscopy and Crystallography Using an X-ray Free Electron Laser, Cctbx.xfel: Serial crystallography computational methods aimed at biomolecular function, Probing chemical dynamics and catalytic mechanisms in metalloenzymes with advanced X-ray spectroscopy techniques, Structural Dynamics at LCLS, High throughput sample delivery method for time resolved studies of enzyme reactions with X-ray and complementary techniques, Taking Snapshots of Enzymatic Reactions Using X-ray Crystallography and Spectroscopy, G911061179, DIALS: supporting structural biology through open source diffraction processing software, G969889393
OpenAlex ID: W7203620168