Light-Induced Structural Changes in a Photosynthetic Reaction Center Caught by Laue Diffraction

Wöhri, Annemarie B.; Katona, Gergely; Johansson, Linda C.; Fritz, Emelie; Malmerberg, Erik; Andersson, Magnus; Vincent, Jonathan; Eklund, Mattias; Cammarata, Marco; Wulff, Michaël; Davidsson, Jan; Groenhof, Gerrit; Neutze, Richard

doi:10.1126/science.1186159

Cited by 103 publications

(85 citation statements)

References 30 publications

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“…6). The quinone reaction at the acceptor side of photosystems seems to be a further member of the growing family of cofactor processes in biology (30,63), in which the Ϫ . Bottom, generalized scheme for formation of a priming state by nuclear rearrangements induced by an initiating reaction.…”

Section: Discussionmentioning

confidence: 99%

Carboxylate Shifts Steer Interquinone Electron Transfer in Photosynthesis

Chernev

Zaharieva

Dau

et al. 2011

Journal of Biological Chemistry

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Understanding the mechanisms of electron transfer (ET) in photosynthetic reaction centers (RCs) may inspire novel catalysts for sunlight-driven fuel production. The electron exit pathway of type II RCs comprises two quinone molecules working in series and in between a non-heme iron atom with a carboxyl ligand (bicarbonate in photosystem II (PSII), glutamate in bacterial RCs). For decades, the functional role of the iron has remained enigmatic. We tracked the iron site using microsecond-resolution x-ray absorption spectroscopy after laser-flash excitation of PSII. After formation of the reduced primary quinone, Q A ؊ , the x-ray spectral changes revealed a transition (t1 ⁄ 2 ≈ 150 s) from a bidentate to a monodentate coordination of the bicarbonate at the Fe(II) (carboxylate shift), which reverted concomitantly with the slower ET to the secondary quinone Q B . A redox change of the iron during the ET was excluded. Density-functional theory calculations corroborated the carboxylate shift both in PSII and bacterial RCs and disclosed underlying changes in electronic configuration. We propose that the iron-carboxyl complex facilitates the first interquinone ET by optimizing charge distribution and hydrogen bonding within the Q A FeQ B triad for high yield Q B reduction. Formation of a specific priming intermediate by nuclear rearrangements, setting the stage for subsequent ET, may be a common motif in reactions of biological redox cofactors.

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Section: Discussionmentioning

confidence: 99%

Carboxylate Shifts Steer Interquinone Electron Transfer in Photosynthesis

Chernev

Zaharieva

Dau

et al. 2011

Journal of Biological Chemistry

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“…In a prototypical SCO compound, [Fe(bpy) 3 ] 2+ (Figure 1), three bipyridine (bpy) ligands generate a ligand field, which splits the Fe(II) 3d molecular orbitals into 3d(t 2g ) 6 at lower energy and 3d(e g ) 0 at higher energy, which are respectively fully occupied and empty in the low-spin (LS) ground state. 17 The stability of the LS state depends critically on the distance of the bpy ligands, where expansion of the Fe−N coordination bonds by ∼10% makes the high-spin (HS) quintet state the lowest energy configuration.…”

Section: ■ Introductionmentioning

confidence: 99%

Femtosecond X-ray Absorption Spectroscopy at a Hard X-ray Free Electron Laser: Application to Spin Crossover Dynamics

Lemke¹,

et al. 2013

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X-ray free electron lasers (XFELs) deliver short (<100 fs) and intense (∼10 12 photons) pulses of hard X-rays, making them excellent sources for time-resolved studies. Here we show that, despite the inherent instabilities of current (SASE based) XFELs, they can be used for measuring high-quality X-ray absorption data and we report femtosecond time-resolved Xray absorption near-edge spectroscopy (XANES) measurements of a spin-crossover system, iron(II) tris(2,2′-bipyridine) in water. The data indicate that the low-spin to high-spin transition can be modeled by single-exponential kinetics convoluted with the overall time resolution. The resulting time constant is ∼160 fs. ■ INTRODUCTIONChemical reactions involve the dynamic evolution of strongly coupled electrons and nuclei on ultrafast time scales from few to a few hundred femtoseconds. Disentangling this complex dynamics has motivated a wide range of experimental and theoretical studies to obtain a more complete picture of the elementary steps underlying these processes. 1 Despite the progresses in ultrafast optical spectroscopies that can resolve dynamics of the valence shell electrons with femtosecond time resolution and in theoretical calculations of many-body dynamics, our understanding of the early chemical transformations still remains incomplete due to the lack of direct structural measurements visualizing both electronic structure and nuclear movements in real time. Information on nuclear dynamics has been obtained with time-resolved scattering with a time resolution of 100 ps on a variety of system from solutions 2,3 to single crystals. 4−6 Recently, femtoseconds studies have been published. 7−9 When the surrounding of specific atoms is of interest, recent advances have demonstrated the utility of time-resolved X-ray absorption spectroscopy (XAS) as a reliable monitor of nuclear and electronic structure during chemical reactions on both the picosecond 10,11 and, more recently, the femtosecond time scale. 12−14 Yet, most of the synchrotron-based experiments are limited to insufficient time resolution (∼100 ps in normal operating conditions) or very low flux (∼10 photons/pulse at kilohertz rate, when operated in femtosecond laser slicing mode 15 ). The development of new X-ray facilities such as X-ray free electron lasers (XFELs) provide unprecedented capabilities in terms of both X-ray pulse durations (down to tens of femtoseconds) and single pulse intensities of more than 10 10 photons when a 1 eV bandwidth monochromator is used. In the present study we exploit XFEL radiation from the Linac Coherent Light Source (LCLS), the first hard XFEL, 16 and present an experimental study of the photoexcited spin transition dynamics in aqueous ferreous bipyridine ([Fe-(bpy) 3 ] 2+ ), which proves the feasibility of femtosecond XAS at the LCLS.Transition metal complexes exhibiting photoinduced spin crossover (SCO) transition provide a good example of the electronic dynamics coupled with nuclear motions. In a

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“…Time-resolved Laue diffraction has been used to observe light-induced electron density changes in a photosynthetic reaction centre 88 , and time-resolved wide-angle X-ray scattering has provided low-resolution overviews of lightinduced helical movements with time in bacteriorhodopsin and proteorhodopsin 89 . Although…”

Section: Increasing Success Rates Of Crystal Optimization and Structumentioning

confidence: 99%