Effects of x-ray free-electron laser pulse intensity on the Mn Kβ1,3 x-ray emission spectrum in photosystem II—A case study for metalloprotein crystals and solutions

Fransson, Thomas; Alonso-Mori, Roberto; Chatterjee, Ruchira; Cheah, Mun Hon; Ibrahim, Mohamed; Hussein, Rana; Zhang, Miao; Fuller, Franklin D.; Gul, Sheraz; Kim, In-Sik; Simon, Philipp S.; Bogacz, Isabel; Makita, Hiroki; Lichtenberg, Casper de; Song, Sanghoon; Batyuk, A.; Sokaras, Dimosthenis; Massad, Ramzi; Doyle, Margaret; Britz, Alexander; Weninger, Clemens; Zouni, Athina; Messinger, Johannes; Yachandra, Vittal K.; Yano, Junko; Kern, Jan; Bergmann, Uwe

doi:10.1063/4.0000130

Cited by 14 publications

(16 citation statements)

References 70 publications

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“…92,132 In terms of the experimental approaches, it is noted that the Berkeley group confirmed with in situ X-ray emission spectroscopy (XES) that the XFEL beams do not affect the OEC under the experimental conditions used. 133,134 In addition, they excluded from the analysis samples that XES had shown to contain Mn(II) and were therefore considered overreduced. Moreover, to quantify the S-state composition in the PSII microcrystals, the Okayama group used flash-induced Fourier transform infrared (FTIR) difference spectroscopy, 135 whereas Berkeley investigators used XES performed simultaneously, and flash-induced oxygen evolution measurements (MIMS) for O 2 detection performed before the XRD experiment.…”

Section: Geometry-based Oxidation State Analysismentioning

confidence: 99%

Does Serial Femtosecond Crystallography Depict State-Specific Catalytic Intermediates of the Oxygen-Evolving Complex?

et al. 2023

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Recent advances in serial femtosecond crystallography (SFX) of photosystem II (PSII), enabled by X-ray free electron lasers (XFEL), provided the first geometric models of distinct intermediates in the catalytic S-state cycle of the oxygen-evolving complex (OEC). These models are obtained by flash-advancing the OEC from the dark-stable state (S1) to more oxidized intermediates (S2 and S3), eventually cycling back to the most reduced S0. However, the interpretation of these models is controversial because geometric parameters within the Mn4CaO5 cluster of the OEC do not exactly match those expected from coordination chemistry for the spectroscopically verified manganese oxidation states of the distinct S-state intermediates. Here we focus on the first catalytic transition, S1 → S2, which represents a one-electron oxidation of the OEC. Combining geometric and electronic structure criteria, including a novel effective oxidation state approach, we analyze existing 1-flash (1F) SFX-XFEL crystallographic models that should depict the S2 state of the OEC. We show that the 1F/S2 equivalence is not obvious, because the Mn oxidation states and total unpaired electron counts encoded in these models are not fully consistent with those of a pure S2 state and with the nature of the S1 → S2 transition. Furthermore, the oxidation state definition in two-flashed (2F) structural models is practically impossible to elucidate. Our results advise caution in the extraction of electronic structure information solely from the literal interpretation of crystallographic models and call for re-evaluation of structural and mechanistic interpretations that presume exact correspondence of such models to specific catalytic intermediates of the OEC.

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Section: Geometry-based Oxidation State Analysismentioning

confidence: 99%

Does Serial Femtosecond Crystallography Depict State-Specific Catalytic Intermediates of the Oxygen-Evolving Complex?

et al. 2023

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“…Fransson et al describe the radiation-induced spectral effects on the Mn-containing metalloenzyme complex photosystem II as minimal up to flux densities of ∼10 11 photons/pulse with the beam focused to ∼10 μm, conditions common to fs XFEL pulses. 11 However, Jensen et al report more significant spectral changes that would interfere with data analysis and defeat the purpose of tandem spectroscopic measurements under similar conditions. 12 The source of these changes was ascribed to a multiphoton absorption process at the metal ions that cannot be avoided by sample dilution or alterations to the metal ion environment.…”

mentioning

confidence: 99%

“…Promising preliminary studies combining the techniques have been attempted at hard X-ray free electron laser (XFEL) sources, but limited availability of these facilities combined with their ill-defined modes of radiation damage have hampered broad application. − To date, no transformative results have emerged, and the ability to evade X-ray-induced damage to sensitive metallocofactors is hotly debated. Fransson et al describe the radiation-induced spectral effects on the Mn-containing metalloenzyme complex photosystem II as minimal up to flux densities of ∼10 11 photons/pulse with the beam focused to ∼10 μm, conditions common to fs XFEL pulses . However, Jensen et al report more significant spectral changes that would interfere with data analysis and defeat the purpose of tandem spectroscopic measurements under similar conditions .…”

mentioning

confidence: 99%

X-ray Emission Spectroscopy of Single Protein Crystals Yields Insights into Heme Enzyme Intermediates

Emamian

Ireland

Purohit

et al. 2022

J. Phys. Chem. Lett.

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Enzyme reactivity is often enhanced by changes in oxidation state, spin state, and metal–ligand covalency of associated metallocofactors. The development of spectroscopic methods for studying these processes coincidentally with structural rearrangements is essential for elucidating metalloenzyme mechanisms. Herein, we demonstrate the feasibility of collecting X-ray emission spectra of metalloenzyme crystals at a third-generation synchrotron source. In particular, we report the development of a von Hamos spectrometer for the collection of Fe Kβ emission optimized for analysis of dilute biological samples. We further showcase its application in crystals of the immunosuppressive heme-dependent enzyme indoleamine 2,3-dioxygenase. Spectra from protein crystals in different states were compared with relevant reference compounds. Complementary density functional calculations assessing covalency support our spectroscopic analysis and identify active site conformations that correlate to high- and low-spin states. These experiments validate the suitability of an X-ray emission approach for determining spin states of previously uncharacterized metalloenzyme reaction intermediates.

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“…[8][9][10] To date, no transformative results have emerged, and the ability to evade X-ray-induced damage to sensitive metallocofactors is hotly debated. Fransson et al describe the radiation-induced spectral effects on the Mn-containing metalloenzyme complex photosystem II as minimal up to flux densities of ~10 11 photons/pulse with the beam focused to ~10 µm, conditions common to fs XFEL pulses. 11 However, Jensen et al report more significant spectral changes that would interfere with data analysis and defeat the purpose of tandem spectroscopic measurements under similar conditions.…”

mentioning

confidence: 99%

“…Fransson et al describe the radiation-induced spectral effects on the Mn-containing metalloenzyme complex photosystem II as minimal up to flux densities of ~10 11 photons/pulse with the beam focused to ~10 µm, conditions common to fs XFEL pulses. 11 However, Jensen et al report more significant spectral changes that would interfere with data analysis and defeat the purpose of tandem spectroscopic measurements under similar conditions. 12 The source of these changes was ascribed to a multi-photon absorption process at the metal ions which cannot be avoided by sample dilution or alterations to the metal ion environment.…”

mentioning

confidence: 99%

X-ray Emission Spectroscopy of Single Protein Crystals Yields Insights into Heme Enzyme Intermediates

Emamian

Ireland

Purohit

et al. 2022

Preprint

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Enzyme reactivity is often enhanced by changes in oxidation state, spin state, and metal-ligand covalency of associated metallocofactors. The development of spectroscopic methods for studying these processes coincidentally with structural rearrangements is essential for elucidating metalloenzyme mechanisms. Herein, we demonstrate the feasibility of collecting X-ray emission spectra of metalloenzyme crystals at a 3rd generation synchrotron source. In particular, we report the development of a von Hamos spectrometer for the collection of Fe Kβ emission optimized for analysis of dilute biological samples. We further showcase its application in crystals of the immunosuppressive heme-dependent enzyme indoleamine 2,3-dioxygenase. Spectra from protein crystals in different states were compared with relevant reference compounds. Complementary density functional calculations assessing covalency support our spectroscopic analysis and identify active site conformations that correlate to high- and low-spin states. These experiments validate the suitability of an X-ray emission approach for determining spin states of previously uncharacterized metalloenzyme reaction intermediates.

show abstract

Effects of x-ray free-electron laser pulse intensity on the Mn Kβ_1,3 x-ray emission spectrum in photosystem II—A case study for metalloprotein crystals and solutions

Cited by 14 publications

References 70 publications

Does Serial Femtosecond Crystallography Depict State-Specific Catalytic Intermediates of the Oxygen-Evolving Complex?

Does Serial Femtosecond Crystallography Depict State-Specific Catalytic Intermediates of the Oxygen-Evolving Complex?

X-ray Emission Spectroscopy of Single Protein Crystals Yields Insights into Heme Enzyme Intermediates

X-ray Emission Spectroscopy of Single Protein Crystals Yields Insights into Heme Enzyme Intermediates

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