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Aydin, A. O., de Lichtenberg, C., Liang, F., Forsman, J., Graça, A. T., Chernev, P., . . . Messinger, J. (2025). Probing substrate water access through the O1 channel of Photosystem II by single site mutations and membrane inlet mass spectrometry. Photosynthesis Research, 163(3), Article ID 28.
Open this publication in new window or tab >>Probing substrate water access through the O1 channel of Photosystem II by single site mutations and membrane inlet mass spectrometry
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2025 (English)In: Photosynthesis Research, ISSN 0166-8595, E-ISSN 1573-5079, Vol. 163, no 3, article id 28Article in journal (Refereed) Published
Abstract [en]

Light-driven water oxidation by photosystem II sustains life on Earth by providing the electrons and protons for the reduction of CO2 to carbohydrates and the molecular oxygen we breathe. The inorganic core of the oxygen evolving complex is made of the earth-abundant elements manganese, calcium and oxygen (Mn4CaO5 cluster), and is situated in a binding pocket that is connected to the aqueous surrounding via water-filled channels that allow water intake and proton egress. Recent serial crystallography and infrared spectroscopy studies performed with PSII isolated from Thermosynechococcus vestitus (T. vestitus) support that one of these channels, the O1 channel, facilitates water access to the Mn4CaO5 cluster during its S2→S3 and S3→S4→S0 state transitions, while a subsequent CryoEM study concluded that this channel is blocked in the cyanobacterium Synechocystis sp. PCC 6803, questioning the role of the O1 channel in water delivery. Employing site-directed mutagenesis we modified the two O1 channel bottleneck residues D1-E329 and CP43-V410 (T. vestitus numbering) and probed water access and substrate exchange via time resolved membrane inlet mass spectrometry. Our data demonstrates that water reaches the Mn4CaO5 cluster via the O1 channel in both wildtype and mutant PSII. In addition, the detailed analysis provides functional insight into the intricate protein-water-cofactor network near the Mn4CaO5 cluster that includes the pentameric, near planar ‘water wheel’ of the O1 channel.

Place, publisher, year, edition, pages
Springer Netherlands, 2025
Keywords
CP43-V410, D1-E329, O1 channel, Oxygen evolving complex, Photosystem II, Substrate water exchange, Synechocystis sp. PCC 6803, Water delivery, Water oxidation, Water wheel
National Category
Biophysics Biochemistry Molecular Biology
Identifiers
urn:nbn:se:umu:diva-238380 (URN)10.1007/s11120-025-01147-4 (DOI)001472389000001 ()40263146 (PubMedID)2-s2.0-105003205091 (Scopus ID)
Funder
Swedish Research Council, 2020-03809Swedish Research Council, 2024-04804
Available from: 2025-05-08 Created: 2025-05-08 Last updated: 2025-05-08Bibliographically approved
Bogacz, I., Szilagyi, E., Makita, H., Simon, P. S., Zhang, M., Doyle, M. D., . . . Yano, J. (2025). X-ray absorption spectroscopy of dilute metalloenzymes at x-ray free-electron lasers in a shot-by-shot mode. The Journal of Physical Chemistry Letters, 16(15), 3778-3787
Open this publication in new window or tab >>X-ray absorption spectroscopy of dilute metalloenzymes at x-ray free-electron lasers in a shot-by-shot mode
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2025 (English)In: The Journal of Physical Chemistry Letters, E-ISSN 1948-7185, Vol. 16, no 15, p. 3778-3787Article in journal (Refereed) Published
Abstract [en]

X-ray absorption spectroscopy (XAS) of 3d transition metals provides important electronic structure information for many fields. However, X-ray-induced radiation damage under physiological temperature has prevented using this method to study dilute aqueous systems, such as metalloenzymes, as the catalytic reaction proceeds. Here we present a new approach to enable operando XAS of dilute biological samples and demonstrate its feasibility with K-edge XAS spectra from the Mn cluster in photosystem II and the Fe-S centers in photosystem I. This approach combines highly efficient sample delivery strategies and a robust signal normalization method with high-transmission Bragg diffraction-based spectrometers at X-ray free-electron lasers (XFELs) in a damage-free, shot-by-shot mode. These photon-out spectrometers have been optimized for discriminating the metal Mn/Fe Kα fluorescence signals from the overwhelming scattering background present on currently available detectors for XFELs that lack suitable energy discrimination. We quantify the enhanced performance metrics of the spectrometer and discuss its potential applications for acquiring time-resolved XAS spectra of biological samples during their reactions at XFELs.

Place, publisher, year, edition, pages
American Chemical Society (ACS), 2025
National Category
Atom and Molecular Physics and Optics
Identifiers
urn:nbn:se:umu:diva-237783 (URN)10.1021/acs.jpclett.5c00399 (DOI)001461004900001 ()40193717 (PubMedID)2-s2.0-105002211132 (Scopus ID)
Funder
Swedish Research Council, 2020−03809Swedish Foundation for Strategic ResearchEU, European Research Council, 101021166-GAS-WAT
Available from: 2025-04-22 Created: 2025-04-22 Last updated: 2025-04-22Bibliographically approved
de Lichtenberg, C., Rapatskiy, L., Reus, M., Heyno, E., Schnegg, A., Nowaczyk, M. M., . . . Cox, N. (2024). Assignment of the slowly exchanging substrate water of nature's water-splitting cofactor. Proceedings of the National Academy of Sciences of the United States of America, 121(11), Article ID e2319374121.
Open this publication in new window or tab >>Assignment of the slowly exchanging substrate water of nature's water-splitting cofactor
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2024 (English)In: Proceedings of the National Academy of Sciences of the United States of America, ISSN 0027-8424, E-ISSN 1091-6490, Vol. 121, no 11, article id e2319374121Article in journal (Refereed) Published
Abstract [en]

Identifying the two substrate water sites of nature's water-splitting cofactor (Mn4CaO5 cluster) provides important information toward resolving the mechanism of O-O bond formation in Photosystem II (PSII). To this end, we have performed parallel substrate water exchange experiments in the S1 state of native Ca-PSII and biosynthetically substituted Sr-PSII employing Time-Resolved Membrane Inlet Mass Spectrometry (TR-MIMS) and a Time-Resolved 17O-Electron-electron Double resonance detected NMR (TR-17O-EDNMR) approach. TR-MIMS resolves the kinetics for incorporation of the oxygen-isotope label into the substrate sites after addition of H218O to the medium, while the magnetic resonance technique allows, in principle, the characterization of all exchangeable oxygen ligands of the Mn4CaO5 cofactor after mixing with H217O. This unique combination shows i) that the central oxygen bridge (O5) of Ca-PSII core complexes isolated from Thermosynechococcus vestitus has, within experimental conditions, the same rate of exchange as the slowly exchanging substrate water (WS) in the TR-MIMS experiments and ii) that the exchange rates of O5 and WS are both enhanced by Ca2+→Sr2+ substitution in a similar manner. In the context of previous TR-MIMS results, this shows that only O5 fulfills all criteria for being WS. This strongly restricts options for the mechanism of water oxidation.

Place, publisher, year, edition, pages
Proceedings of the National Academy of Sciences (PNAS), 2024
Keywords
electron paramagnetic resonance (EPR), membrane inlet mass spectrometry (MIMS), photosynthesis, photosystem II, water oxidation mechanism
National Category
Biochemistry Molecular Biology
Identifiers
urn:nbn:se:umu:diva-222362 (URN)10.1073/pnas.2319374121 (DOI)001206387400004 ()38437550 (PubMedID)2-s2.0-85186844144 (Scopus ID)
Funder
Max Planck SocietySwedish Research Council, 2016-05183Swedish Research Council, 2020-03809
Available from: 2024-03-15 Created: 2024-03-15 Last updated: 2025-04-24Bibliographically approved
Guo, Y., He, L., Ding, Y., Kloo, L., Pantazis, D. A., Messinger, J. & Sun, L. (2024). Closing Kok’s cycle of nature’s water oxidation catalysis. Nature Communications, 15(1), Article ID 5982.
Open this publication in new window or tab >>Closing Kok’s cycle of nature’s water oxidation catalysis
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2024 (English)In: Nature Communications, E-ISSN 2041-1723, Vol. 15, no 1, article id 5982Article in journal (Refereed) Published
Abstract [en]

The Mn4CaO5(6) cluster in photosystem II catalyzes water splitting through the Si state cycle (i = 0–4). Molecular O2 is formed and the natural catalyst is reset during the final S3 → (S4) → S0 transition. Only recently experimental breakthroughs have emerged for this transition but without explicit information on the S0-state reconstitution, thus the progression after O2 release remains elusive. In this report, our molecular dynamics simulations combined with density functional calculations suggest a likely missing link for closing the cycle, i.e., restoring the first catalytic state. Specifically, the formation of closed-cubane intermediates with all hexa-coordinate Mn is observed, which would undergo proton release, water dissociation, and ligand transfer to produce the open-cubane structure of the S0 state. Thereby, we theoretically identify the previously unknown structural isomerism in the S0 state that acts as the origin of the proposed structural flexibility prevailing in the cycle, which may be functionally important for nature’s water oxidation catalysis.

Place, publisher, year, edition, pages
Springer Nature, 2024
National Category
Physical Chemistry
Identifiers
urn:nbn:se:umu:diva-227957 (URN)10.1038/s41467-024-50210-6 (DOI)001270192000023 ()39013902 (PubMedID)2-s2.0-85198619455 (Scopus ID)
Available from: 2024-07-22 Created: 2024-07-22 Last updated: 2025-04-24Bibliographically approved
Hussein, R., Graça, A. T., Forsman, J., Aydin, A. O., Hall, M., Gaetcke, J., . . . Schröder, W. P. (2024). Cryo-electron microscopy reveals hydrogen positions and water networks in photosystem II. Science, 384(6702), 1349-1355
Open this publication in new window or tab >>Cryo-electron microscopy reveals hydrogen positions and water networks in photosystem II
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2024 (English)In: Science, ISSN 0036-8075, E-ISSN 1095-9203, Vol. 384, no 6702, p. 1349-1355Article in journal (Refereed) Published
Abstract [en]

Photosystem II starts the photosynthetic electron transport chain that converts solar energy into chemical energy and thus sustains life on Earth. It catalyzes two chemical reactions: water oxidation to molecular oxygen and plastoquinone reduction. Coupling of electron and proton transfer is crucial for efficiency; however, the molecular basis of these processes remains speculative owing to uncertain water binding sites and the lack of experimentally determined hydrogen positions. We thus collected high-resolution cryo-electron microscopy data of fully hydrated photosystem II from the thermophilic cyanobacterium Thermosynechococcus vestitus to a final resolution of 1.71 angstroms. The structure reveals several previously undetected partially occupied water binding sites and more than half of the hydrogen and proton positions. This clarifies the pathways of substrate water binding and plastoquinone B protonation.

Place, publisher, year, edition, pages
American Association for the Advancement of Science (AAAS), 2024
National Category
Biochemistry Molecular Biology
Identifiers
urn:nbn:se:umu:diva-227578 (URN)10.1126/science.adn6541 (DOI)001273959200032 ()38900892 (PubMedID)2-s2.0-85196874000 (Scopus ID)
Funder
Swedish Research Council, 2020-03809Carl Tryggers foundation , 19.324The Kempe Foundations, JCK-2030 2021-2023
Available from: 2024-07-01 Created: 2024-07-01 Last updated: 2025-04-24Bibliographically approved
Yano, J., Kern, J., Blankenship, R. E., Messinger, J. & Yachandra, V. K. (2024). Editorial for the special issue ‘Energy conversion reactions in natural and artificial photosynthesis’: a tribute to Ken Sauer. Photosynthesis Research, 162(2-3), 101-102
Open this publication in new window or tab >>Editorial for the special issue ‘Energy conversion reactions in natural and artificial photosynthesis’: a tribute to Ken Sauer
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2024 (English)In: Photosynthesis Research, ISSN 0166-8595, E-ISSN 1573-5079, Vol. 162, no 2-3, p. 101-102Article in journal, Editorial material (Other academic) Published
Place, publisher, year, edition, pages
Springer Nature, 2024
National Category
Botany
Identifiers
urn:nbn:se:umu:diva-230956 (URN)10.1007/s11120-024-01121-6 (DOI)001335669200001 ()39382761 (PubMedID)2-s2.0-85205840016 (Scopus ID)
Available from: 2024-10-21 Created: 2024-10-21 Last updated: 2024-12-13Bibliographically approved
Shevela, D., Schröder, W. P. & Messinger, J. (2024). Measurements of oxygen evolution in photosynthesis (2ed.). In: Sarah Covshoff (Ed.), Photosynthesis: methods and protocols (pp. 133-148). New York: Humana Press, 2790
Open this publication in new window or tab >>Measurements of oxygen evolution in photosynthesis
2024 (English)In: Photosynthesis: methods and protocols / [ed] Sarah Covshoff, New York: Humana Press, 2024, 2, Vol. 2790, p. 133-148Chapter in book (Refereed)
Abstract [en]

This chapter compares two different techniques for monitoring photosynthetic O2 production; the wide-spread Clark-type O2 electrode and the more sophisticated membrane inlet mass spectrometry (MIMS) technique. We describe how a simple membrane inlet for MIMS can be made out of a commercial Clark-type cell and outline the advantages and drawbacks of the two techniques to guide researchers in deciding which method to use. Protocols and examples are given for measuring O2 evolution rates and for determining the number of chlorophyll molecules per active photosystem II reaction center.

Place, publisher, year, edition, pages
New York: Humana Press, 2024 Edition: 2
Series
Methods in Molecular (MIMB), ISSN 1064-3745, E-ISSN 1940-6029 ; 2790
Keywords
Clark-type electrode, Membrane-inlet mass spectrometry, O2 evolution, Oxygenic photosynthesis, Photosynthetic water oxidation, Photosynthetic water splitting, Photosystem II, Chlorophyll, Electrodes, Mass Spectrometry, Oxygen, Photosynthesis, Photosystem II Protein Complex, commercial phenomena, comparative study, controlled study, cost effectiveness analysis, desorption, electrochemical analysis, illumination, ion current, membrane, nonhuman, oxygen evolution, oxygen evolution reaction, pervaporation, water splitting, metabolism, procedures
National Category
Biochemistry Molecular Biology
Identifiers
urn:nbn:se:umu:diva-224657 (URN)10.1007/978-1-0716-3790-6_8 (DOI)38649570 (PubMedID)2-s2.0-85191364750 (Scopus ID)978-1-0716-3789-0 (ISBN)978-1-0716-3792-0 (ISBN)978-1-0716-3790-6 (ISBN)
Funder
Swedish Research Council, 2020-03809Carl Tryggers foundation
Available from: 2024-05-22 Created: 2024-05-22 Last updated: 2025-02-20Bibliographically approved
Yano, J., Kern, J., Blankenship, R. E., Messinger, J. & Yachandra, V. K. (2024). Tribute to Kenneth Sauer (1931–2022): a mentor, a role-model, and an inspiration to all in the field of photosynthesis. Photosynthesis Research, 162(2), 103-138
Open this publication in new window or tab >>Tribute to Kenneth Sauer (1931–2022): a mentor, a role-model, and an inspiration to all in the field of photosynthesis
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2024 (English)In: Photosynthesis Research, ISSN 0166-8595, E-ISSN 1573-5079, Vol. 162, no 2, p. 103-138Article in journal, Editorial material (Refereed) Published
Abstract [en]

Kenneth (Ken) Sauer was a mainstay of research in photosynthesis at the University of California, Berkeley and the Lawrence Berkeley National Laboratory (LBNL) for more than 50 years. Ken will be remembered by his colleagues, and other workers in the field of photosynthesis as well, for his pioneering work that introduced the physical techniques whose application have enriched our understanding of the basic reactions of oxygenic photosynthesis. His laboratory was a training ground for many students and postdocs who went on to success in the field of photosynthesis and many others. Trained as a physical chemist, he always brought that quantitative approach to research questions and used several spectroscopic methods in his research. His broad scientific interests concerned the role of manganese in oxygen evolution, electronic properties of chlorophylls, energy transport in antenna complexes, and electron transport reactions. He was also an enthusiastic teacher, an enormously successful mentor who leaves behind a legion of scientists as his abiding legacy, a lover of music and the outdoors with many interests beyond science, and a dedicated family man with a great sense of humility. In this tribute, we summarize some aspects of Ken Sauer’s life and career, illustrated with selected research achievements, and describe his approach to research and life as we perceived it, which is complemented by reminiscences of several current researchers in photosynthesis and other fields. The supporting material includes Ken Sauers’s CV and publication list, as well as a list of the graduate students and postdocs he trained and of researchers that spent a sabbatical in his lab.

Place, publisher, year, edition, pages
Springer, 2024
Keywords
Biography, Ken Sauer, Photosynthesis, Tribute
National Category
Botany
Identifiers
urn:nbn:se:umu:diva-232142 (URN)10.1007/s11120-024-01119-0 (DOI)001353842300001 ()39535662 (PubMedID)2-s2.0-85209087297 (Scopus ID)
Available from: 2024-12-05 Created: 2024-12-05 Last updated: 2025-01-13Bibliographically approved
Guo, Y., Messinger, J., Kloo, L. & Sun, L. (2023). Alternative mechanism for O2formation in natural photosynthesis via nucleophilic Oxo-Oxo coupling. Journal of the American Chemical Society, 145(7), 4129-4141
Open this publication in new window or tab >>Alternative mechanism for O2formation in natural photosynthesis via nucleophilic Oxo-Oxo coupling
2023 (English)In: Journal of the American Chemical Society, ISSN 0002-7863, E-ISSN 1520-5126, Vol. 145, no 7, p. 4129-4141Article in journal (Refereed) Published
Abstract [en]

O2 formation in photosystem II (PSII) is a vital event on Earth, but the exact mechanism remains unclear. The presently prevailing theoretical model is "radical coupling"(RC) involving a Mn(IV)-oxyl unit in an "open-cubane"Mn4CaO6 cluster, which is supported experimentally by the S3 state of cyanobacterial PSII featuring an additional Mn-bound oxygenic ligand. However, it was recently proposed that the major structural form of the S3 state of higher plants lacks this extra ligand, and that the resulting S4 state would feature instead a penta-coordinate dangler Mn(V)=oxo, covalently linked to a "closed-cubane"Mn3CaO4 cluster. For this proposal, we explore here a large number of possible pathways of O-O bond formation and demonstrate that the "nucleophilic oxo-oxo coupling"(NOOC) between Mn(V)=oxo and μ3-oxo is the only eligible mechanism in such a system. The reaction is facilitated by a specific conformation of the cluster and concomitant water binding, which is delayed compared to the RC mechanism. An energetically feasible process is described starting from the valid S4 state through the sequential formation of peroxide and superoxide, followed by O2 release and a second water insertion. The newly found mechanism is consistent with available experimental thermodynamic and kinetic data and thus a viable alternative pathway for O2 formation in natural photosynthesis, in particular for higher plants.

Place, publisher, year, edition, pages
American Chemical Society (ACS), 2023
National Category
Biochemistry Molecular Biology
Identifiers
urn:nbn:se:umu:diva-205197 (URN)10.1021/jacs.2c12174 (DOI)000936768400001 ()36763485 (PubMedID)2-s2.0-85147993483 (Scopus ID)
Funder
Swedish Research Council, 2020-03809Swedish Energy Agency, 45421-1
Available from: 2023-02-28 Created: 2023-02-28 Last updated: 2025-02-20Bibliographically approved
Simon, P. S., Makita, H., Bogacz, I., Fuller, F., Bhowmick, A., Hussein, R., . . . Yano, J. (2023). Capturing the sequence of events during the water oxidation reaction in photosynthesis using XFELs. FEBS Letters, 597(1), 30-37
Open this publication in new window or tab >>Capturing the sequence of events during the water oxidation reaction in photosynthesis using XFELs
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2023 (English)In: FEBS Letters, ISSN 0014-5793, E-ISSN 1873-3468, Vol. 597, no 1, p. 30-37Article, review/survey (Refereed) Published
Abstract [en]

Ever since the discovery that Mn was required for oxygen evolution in plants by Pirson in 1937 and the period-four oscillation in flash-induced oxygen evolution by Joliot and Kok in the 1970s, understanding of this process has advanced enormously using state-of-the-art methods. The most recent in this series of innovative techniques was the introduction of X-ray free-electron lasers (XFELs) a decade ago, which led to another quantum leap in the understanding in this field, by enabling operando X-ray structural and X-ray spectroscopy studies at room temperature. This review summarizes the current understanding of the structure of Photosystem II (PS II) and its catalytic centre, the Mn4CaO5 complex, in the intermediate Si (i = 0–4)-states of the Kok cycle, obtained using XFELs.

Place, publisher, year, edition, pages
John Wiley & Sons, 2023
Keywords
manganese metalloenzymes, oxygen evolving complex, photosystem II, water-oxidation/splitting, X-ray free-electron laser, X-ray spectroscopy
National Category
Physical Chemistry Biochemistry Molecular Biology
Identifiers
urn:nbn:se:umu:diva-201329 (URN)10.1002/1873-3468.14527 (DOI)000883333900001 ()36310373 (PubMedID)2-s2.0-85142148043 (Scopus ID)
Note

Special Issue: Visions of bio-inorganic chemistry: Metals and the molecules of life

Available from: 2022-12-15 Created: 2022-12-15 Last updated: 2025-02-20Bibliographically approved
Projects
Water-binding and water-splitting by photosystem II and artificial catalysts [2009-03722_VR]; Umeå UniversityTRANSFORMERS - Integrated biomass production using Swedish microorganisms, local wastewaters and flue gases [2015-92_Formas]; Umeå UniversityMechanism and assembly of the water oxidation catalyst in photosystem II [2016-05183_VR]; Umeå UniversityAktivering av basmetaller för elektrokatalytisk vattenspjälkning [P45421-1_Energi]; Uppsala UniversityAmmonia made from Air, Water and Sunshine ‚Äì the ideal renewable fuel [P46551-1_Energi]; Uppsala UniversityRevealing the mechanism of biological water oxidation [2020-03809_VR]; Uppsala UniversityDisentangling light- and CO2-mediated signalling in green microalgae [2023-04397_VR]; Uppsala University
Organisations
Identifiers
ORCID iD: ORCID iD iconorcid.org/0000-0003-2790-7721

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