Taking snapshots of photosynthetic water oxidation using femtosecond X-ray diffraction and spectroscopy

Kern, Jan; Tran, Rosalie; Alonso‐Mori, R.; Koroidov, Sergey; Echols, Nathaniel; Hattne, Johan; Ibrahim, Mohamed; Gul, Sheraz; Laksmono, Hartawan; Sierra, Raymond G.; Gildea, Richard J.; Han, Guangye; Hellmich, Julia; Lassalle‐Kaiser, Benedikt; Chatterjee, Ruchira; Brewster, Aaron S.; Stan, Claudiu A.; Glöckner, Carina; Lampe, Alyssa; DiFiore, D.; Milathianaki, Despina; Fry, Alan; Seibert, M.; Koglin, Jason E.; Gallo, Erik; Uhlig, Jens; Sokaras, Dimosthenis; Weng, Tsu Chien; Zwart, Petrus H.; Skinner, David; Bogan, Michael J.; Messerschmidt, Marc; Glatzel, Pieter; Williams, Garth J.; Boutet, Sébastien; Adams, Paul D.; Zouni, Athina; Messinger, Johannes; Sauter, Nicholas K.; Bergmann, Uwe; Yano, Junko; Yachandra, Vittal K.

doi:10.1038/ncomms5371

Cited by 216 publications

(168 citation statements)

References 72 publications

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“…1b). The high-resolution structures of PSII analyzed so far were for the dark-stable S1 state 4,5 , although a few studies on the low-resolution intermediate S-state structures have been reported by TR-SFX [9][10][11] . During the revision of our manuscript, Young et al reported a 2F-illuminated state structure at 2.25 Å resolution where no apparent changes around O5 were observed 12 , although estimations of the resolution could yield somewhat different values so that small movement of some water molecules may escape the detection.…”

Section: Discussionmentioning

confidence: 99%

Light-induced structural changes and the site of O=O bond formation in PSII caught by XFEL

Suga

Akita

Sugahara

et al. 2017

Nature

552

791

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SummaryPhotosystem II (PSII) is a huge membrane-protein complex consisting of 20 different subunits with a total molecular mass of 350 kDa for a monomer, and catalyzes light-driven water oxidation at its catalytic center, the oxygen-evolving complex (OEC) [1][2][3] . The structure of PSII has been analyzed at 1.9 Å resolution by synchrotron radiation X-rays, which revealed that OEC is a Mn4CaO5 cluster organized in an asymmetric, "distorted-chair" form 4 . This structure was further analyzed with femtosecond X-ray free electron lasers (XFEL), providing the "radiation damage-free" 5 structure. The mechanism of O=O bond formation, however, remains obscure due to the lack of intermediate state structures. Here we report the structural changes of PSII induced by 2-flash (2F) illumination at room temperature at a resolution of 2.35 Å using time-resolved serial femtosecond crystallography (TR-SFX) with an XFEL provided by the SPring-8 angstrom compact free-electron laser (SACLA). Isomorphous differenceFourier map between the 2F and dark-adapted states revealed two areas of apparent changes; they are around QB/non-heme iron and the Mn4CaO5 cluster. The changes around the QB/non-heme iron region reflected the electron and proton transfers induced by the 2F-illumination. In the region around the Mn4CaO5 cluster, a water molecule located 3.5 Å from the Mn4CaO5 cluster disappeared from the map upon 2Fillumination, leading to a closer distance between another water molecule and O4, suggesting also the occurrence of proton transfer. Importantly, the 2F-dark isomorphous difference Fourier map showed an apparent positive peak around O5, a unique μ3-oxo-bridge located in the quasi-center of Mn1 and Mn4 4,5 . This suggests an insertion of a new oxygen atom (O6) close to O5, providing an O=O distance of 1.5 Å between these two oxygen atoms. This provides a mechanism for the O=O bond formation 4 consistent with that proposed by Siegbahn 6,7 . Fig. 1a shows organization of the electron transfer chain of PSII in a pseudo-C2 symmetry by two subunits D1 and D2. The water-oxidation reaction proceeds via the Si-state cycle 8 (with i=0-4), where dioxygen is produced in the transition of S3→(S4)→S0 (Fig. 1b). The high-resolution structures of PSII analyzed so far were for the dark-stable S1 state 4,5 , although a few studies on the low-resolution intermediate S-state structures have been reported by TR-SFX [9][10][11] . During the revision of our manuscript, Young et al. reported a 2F-illuminated state structure at 2.25 Å resolution where no apparent changes around O5 were observed 12 , although estimations of the resolution could yield somewhat different values so that small movement of some water molecules may escape the detection. In order to achieve resolution high enough to uncover small structural changes induced by flash illuminations yet allowing Si-state transition to proceed efficiently, we determined the optimal crystal size of PSII with a maximum length of 100 µm, which diffracted up to a resolution of 2.1 Å by a SACLA-XFEL ...

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Section: Discussionmentioning

confidence: 99%

Light-induced structural changes and the site of O=O bond formation in PSII caught by XFEL

Suga

Akita

Sugahara

et al. 2017

Nature

552

791

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“…However, the composition of these protrusions in grana membranes from plants and algae is not completely resolved. The precise locations of PsbP and PsbQ are still uncertain (Ido et al, 2014;Mummadisetti et al, 2014) because only cyanobacterial PSII-OEC crystal structures have been solved (Zouni et al, 2001;Kamiya and Shen, 2003;Ferreira et al, 2004;Loll et al, 2005;Umena et al, 2011;Kern et al, 2013Kern et al, , 2014Kupitz et al, 2014, Suga et al, 2015 and they do not have the PsbP and PsbQ proteins. PsbO is conserved among cyanobacteria, algae, and plants, and its position within PSII-OEC is more certain (Nield and Barber, 2006).…”

Section: Discussionmentioning

confidence: 99%

The Use of Contact Mode Atomic Force Microscopy in Aqueous Medium for Structural Analysis of Spinach Photosynthetic Complexes

et al. 2015

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To investigate the dynamics of photosynthetic pigment-protein complexes in vascular plants at high resolution in an aqueous environment, membrane-protruding oxygen-evolving complexes (OECs) associated with photosystem II (PSII) on spinach (Spinacia oleracea) grana membranes were examined using contact mode atomic force microscopy. This study represents, to our knowledge, the first use of atomic force microscopy to distinguish the putative large extrinsic loop of Photosystem II CP47 reaction center protein (CP47) from the putative oxygen-evolving enhancer proteins 1, 2, and 3 (PsbO, PsbP, and PsbQ) and large extrinsic loop of Photosystem II CP43 reaction center protein (CP43) in the PSII-OEC extrinsic domains of grana membranes under conditions resulting in the disordered arrangement of PSII-OEC particles. Moreover, we observed uncharacterized membrane particles that, based on their physical characteristics and electrophoretic analysis of the polypeptides associated with the grana samples, are hypothesized to be a domain of photosystem I that protrudes from the stromal face of single thylakoid bilayers. Our results are interpreted in the context of the results of others that were obtained using cryo-electron microscopy (and single particle analysis), negative staining and freeze-fracture electron microscopy, as well as previous atomic force microscopy studies.

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“…Furthermore, by combining temporally resolved infrared spectroscopy of surface intermediates with monitoring of the electronic structure of the metal oxide surface using ultrafast hard and soft X-ray free electron laser sources will greatly enhance our understanding of these multi-electron catalytic processes. The recent demonstration of timeresolved X-ray emission spectroscopy for elucidating the O 2 -forming step of Nature's water oxidation cycle at the CaMn 4 O 4 cluster of Photosystem II provides an inspiring example of the use of the emerging ultrafast X-ray free electron laser techniques [100]. Such efforts will play a key role in accelerating progress towards efficient metal oxide catalysts for water oxidation, and the coupling to carbon dioxide reduction.…”

Section: Discussionmentioning

confidence: 99%

Towards a Molecular Level Understanding of the Multi-Electron Catalysis of Water Oxidation on Metal Oxide Surfaces

Zhang

Frei

2014

Catal Lett

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Earth abundant metal oxides play a central role as catalysts in the essential chemical transformations of sunlight to fuel conversion, which are the oxidation of water and the reduction of carbon dioxide. The rapidly growing interest in renewable fuel generation by using the energy of the sun has recently led to substantial breakthroughs in the use of first row transition metal oxides as catalysts for oxygen evolution from water. Substantive improvements of rates and lowering of overpotentials have been achieved by exploiting materials properties on the nanoscale, or taking advantage of the synergy of multiple metals. Moreover, knowledge derived from mechanistic investigations with structure specific spectroscopy is accelerating efficiency improvements. Monitoring by timeresolved FT-infrared spectroscopy reveals the molecular nature of active sites, while in situ X-ray and optical spectroscopy under reaction conditions provides insights into the electronic structure of the surface metal centers participating in the catalysis. By combining the bond specificity of vibrational spectroscopy with the metal electronic structure specificity of optical, X-ray absorption or photoelectron spectroscopy, a complete understanding of active surface sites on metal oxides begins to emerge. Charge flow driving the chemical transformations probed by optical spectroscopy across time scales from ultrafast to very slow reveals the processes that control the productive use of charges delivered to the catalyst. Coupling of the water oxidation catalysis at a metal oxide catalyst with carbon dioxide reduction at a heterobinuclear chromophore, which is the goal of the artificial photosystem approach, is demonstrated by a well-defined all-inorganic polynuclear unit.

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Taking snapshots of photosynthetic water oxidation using femtosecond X-ray diffraction and spectroscopy

Cited by 216 publications

References 72 publications

Light-induced structural changes and the site of O=O bond formation in PSII caught by XFEL

Light-induced structural changes and the site of O=O bond formation in PSII caught by XFEL

The Use of Contact Mode Atomic Force Microscopy in Aqueous Medium for Structural Analysis of Spinach Photosynthetic Complexes

Towards a Molecular Level Understanding of the Multi-Electron Catalysis of Water Oxidation on Metal Oxide Surfaces

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