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      Structural basis of light‐harvesting in the photosystem II core complex

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          Abstract

          Photosystem II (PSII) is a membrane‐spanning, multi‐subunit pigment–protein complex responsible for the oxidation of water and the reduction of plastoquinone in oxygenic photosynthesis. In the present review, the recent explosive increase in available structural information about the PSII core complex based on X‐ray crystallography and cryo‐electron microscopy is described at a level of detail that is suitable for a future structure‐based analysis of light‐harvesting processes. This description includes a proposal for a consistent numbering scheme of protein‐bound pigment cofactors across species. The structural survey is complemented by an overview of the state of affairs in structure‐based modeling of excitation energy transfer in the PSII core complex with emphasis on electrostatic computations, optical properties of the reaction center, the assignment of long‐wavelength chlorophylls, and energy trapping mechanisms.

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          Most cited references173

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          Comparing photosynthetic and photovoltaic efficiencies and recognizing the potential for improvement.

          Comparing photosynthetic and photovoltaic efficiencies is not a simple issue. Although both processes harvest the energy in sunlight, they operate in distinctly different ways and produce different types of products: biomass or chemical fuels in the case of natural photosynthesis and nonstored electrical current in the case of photovoltaics. In order to find common ground for evaluating energy-conversion efficiency, we compare natural photosynthesis with present technologies for photovoltaic-driven electrolysis of water to produce hydrogen. Photovoltaic-driven electrolysis is the more efficient process when measured on an annual basis, yet short-term yields for photosynthetic conversion under optimal conditions come within a factor of 2 or 3 of the photovoltaic benchmark. We consider opportunities in which the frontiers of synthetic biology might be used to enhance natural photosynthesis for improved solar energy conversion efficiency.
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            Biochemistry. The resolution revolution.

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              Native structure of photosystem II at 1.95 Å resolution viewed by femtosecond X-ray pulses.

              Photosynthesis converts light energy into biologically useful chemical energy vital to life on Earth. The initial reaction of photosynthesis takes place in photosystem II (PSII), a 700-kilodalton homodimeric membrane protein complex that catalyses photo-oxidation of water into dioxygen through an S-state cycle of the oxygen evolving complex (OEC). The structure of PSII has been solved by X-ray diffraction (XRD) at 1.9 ångström resolution, which revealed that the OEC is a Mn4CaO5-cluster coordinated by a well defined protein environment. However, extended X-ray absorption fine structure (EXAFS) studies showed that the manganese cations in the OEC are easily reduced by X-ray irradiation, and slight differences were found in the Mn-Mn distances determined by XRD, EXAFS and theoretical studies. Here we report a 'radiation-damage-free' structure of PSII from Thermosynechococcus vulcanus in the S1 state at a resolution of 1.95 ångströms using femtosecond X-ray pulses of the SPring-8 ångström compact free-electron laser (SACLA) and hundreds of large, highly isomorphous PSII crystals. Compared with the structure from XRD, the OEC in the X-ray free electron laser structure has Mn-Mn distances that are shorter by 0.1-0.2 ångströms. The valences of each manganese atom were tentatively assigned as Mn1D(III), Mn2C(IV), Mn3B(IV) and Mn4A(III), based on the average Mn-ligand distances and analysis of the Jahn-Teller axis on Mn(III). One of the oxo-bridged oxygens, O5, has significantly longer distances to Mn than do the other oxo-oxygen atoms, suggesting that O5 is a hydroxide ion instead of a normal oxygen dianion and therefore may serve as one of the substrate oxygen atoms. These findings provide a structural basis for the mechanism of oxygen evolution, and we expect that this structure will provide a blueprint for the design of artificial catalysts for water oxidation.
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                Author and article information

                Contributors
                frank.mueh@jku.at
                Journal
                Protein Sci
                Protein Sci
                10.1002/(ISSN)1469-896X
                PRO
                Protein Science : A Publication of the Protein Society
                John Wiley & Sons, Inc. (Hoboken, USA )
                0961-8368
                1469-896X
                24 February 2020
                May 2020
                24 February 2020
                : 29
                : 5 ( doiID: 10.1002/pro.v29.5 )
                : 1090-1119
                Affiliations
                [ 1 ] Department of Theoretical Biophysics, Institute for Theoretical Physics Johannes Kepler University Linz Linz Austria
                [ 2 ] Humboldt‐Universität zu Berlin, Institute for Biology, Biophysics of Photosynthesis Berlin Germany
                Author notes
                [*] [* ] Correspondence

                Frank Müh, Department of Theoretical Biophysics, Institute for Theoretical Physics, Johannes Kepler University Linz, Altenberger Strasse 69, AT‐4040 Linz, Austria.

                Email: frank.mueh@ 123456jku.at

                Author information
                https://orcid.org/0000-0002-8818-2616
                Article
                PRO3841
                10.1002/pro.3841
                7184784
                32067287
                9730f978-474c-411f-bdfb-ec9f2485480c
                © 2020 The Authors. Protein Science published by Wiley Periodicals, Inc. on behalf of The Protein Society.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 26 January 2020
                : 06 February 2020
                : 06 February 2020
                Page count
                Figures: 9, Tables: 3, Pages: 30, Words: 23250
                Funding
                Funded by: Bundesministerium für Bildung und Forschung (BMBF) , open-funder-registry 10.13039/501100002347;
                Award ID: 031B0557 A+B
                Funded by: German Research Foundation (DFG) , open-funder-registry 10.13039/501100001659;
                Award ID: EXC 2008/1‐390540038
                Award ID: SFB 1078 project A5
                Categories
                Review
                Reviews
                Custom metadata
                2.0
                May 2020
                Converter:WILEY_ML3GV2_TO_JATSPMC version:5.8.1 mode:remove_FC converted:27.04.2020

                Biochemistry
                carotenoid,charge separation,chlorophyll,cryo‐electron microscopy,excitation energy transfer,reaction center,x‐ray crystallography

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