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Light-Dependent Production of Dioxygen in Photosynthesis

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Sustaining Life on Planet Earth: Metalloenzymes Mastering Dioxygen and Other Chewy Gases

Part of the book series: Metal Ions in Life Sciences ((MILS,volume 15))

Abstract

Oxygen, that supports all aerobic life, is abundant in the atmosphere because of its constant regeneration by photosynthetic water oxidation, which is catalyzed by a Mn4CaO5 cluster in photosystem II (PS II), a multi subunit membrane protein complex. X-ray and other spectroscopy studies of the electronic and geometric structure of the Mn4CaO5 cluster as it advances through the intermediate states have been important for understanding the mechanism of water oxidation. The results and interpretations, especially from X-ray spectroscopy studies, regarding the geometric and electronic structure and the changes as the system proceeds through the catalytic cycle will be summarized in this review. This review will also include newer methodologies in time-resolved X-ray diffraction and spectroscopy that have become available since the commissioning of the X-ray free electron laser (XFEL) and are being applied to study the oxygen-evolving complex (OEC). The femtosecond X-ray pulses of the XFEL allows us to outrun X-ray damage at room temperature, and the time-evolution of the photo-induced reaction can be probed using a visible laser-pump followed by the X-ray-probe pulse. XFELs can be used to simultaneously determine the light-induced protein dynamics using crystallography and the local chemistry that occurs at the catalytic center using X-ray spectroscopy under functional conditions. Membrane inlet mass spectrometry has been important for providing direct information about the exchange of substrate water molecules, which has a direct bearing on the mechanism of water oxidation. Moreover, it has been indispensable for the time-resolved X-ray diffraction and spectroscopy studies and will be briefly reviewed in this chapter. Given the role of PS II in maintaining life in the biosphere and the future vision of a renewable energy economy, understanding the structure and mechanism of the photosynthetic water oxidation catalyst is an important goal for the future.

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Acknowledgments

The research reviewed here was supported by the NIH Grant GM 55302 (V.K.Y.) and the Director, Office of Science, Office of Basic Energy Sciences (OBES), Division of Chemical Sciences, Geosciences, and Biosciences of the Department of Energy (DOE) under Contract DE-AC02-05CH11231 (J.Y. and V.K.Y.). The Solar Fuels Strong Research Environment (Umeå University), the Artificial Leaf Project (K&A Wallenberg Foundation), VR and Energimyndigheten (J.M.), and the Human Frontier Research Grant, RGP0063/2013 (J.Y.) are acknowledged for supporting this project. The LCLS, and the synchrotron facilities at Stanford Synchrotron Radiation Lightsource (SSRL), the Advanced Light Source (ALS), and the Advanced Photon Source (APS), used in the course of these studies are all supported by DOE OBES. We thank all our students, postdoctoral fellows, and collaborators for their very important contributions to the PS II studies at LCLS, and the staff at LCLS for their support of the XFEL experiments.

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Authors and Affiliations

  1. Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, CA, 94720, USA

    Junko Yano, Jan Kern & Vittal K. Yachandra

  2. Department of Chemistry, Chemistry Biology Centre (KBC), Umeå University, S-90187, Umeå, Sweden

    Håkan Nilsson, Sergey Koroidov & Johannes Messinger

Authors
  1. Junko Yano
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  2. Jan Kern
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  3. Vittal K. Yachandra
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  4. Håkan Nilsson
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  5. Sergey Koroidov
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  6. Johannes Messinger
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Corresponding author

Correspondence to Vittal K. Yachandra .

Editor information

Editors and Affiliations

  1. Fachbereich Biologie, Universita¨t Konstanz, Konstanz, Germany

    Peter M. H Kroneck

  2. Facultad de Química Departamento de Química Inorganica y Nuc, Universidad Nacional Autónoma de México, Ciudad de México, Distrito Federal, Mexico

    Martha E. Sosa Torres

Abbreviations and Definitions

Abbreviations and Definitions

Chl:

chlorophyll

CXI:

coherent X-ray imaging

Dbm:

dibenzoylmethane

DFT:

density functional theory

ENDOR:

electron nuclear double resonance

EPR:

electron paramagnetic resonance

EXAFS:

extended X-ray absorption fine structure

fs:

femtosecond

FTIR:

Fourier transform infrared spectroscopy

Htphpn:

N,N,N’,N’-tetra(2-methylpyridyl)-2-hydroxypropanediamine

IR:

infrared spectroscopy

LCLS:

Linac coherent light source

MIMS:

membrane inlet mass spectrometry

OAc:

acetate

OEC:

oxygen-evolving complex

PS II:

photosystem II

PSD:

position sensitive detector

RIXS:

resonant inelastic X-ray scattering

RT:

room temperature

SACLA:

Spring-8 Ångstrom compact free electron laser

SFX:

serial femtosecond crystallography

SR:

synchrotron radiation

Terpy:

2,2':6',2"-terpyridine

TR-MIMS:

time-resolved membrane inlet mass spectrometry

XANES:

X-ray absorption near edge spectroscopy

XAS:

X-ray absorption spectroscopy

XES:

X-ray emission spectroscopy

XFEL:

X-ray free electron laser

XRD:

X-ray diffraction

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Yano, J., Kern, J., Yachandra, V.K., Nilsson, H., Koroidov, S., Messinger, J. (2015). Light-Dependent Production of Dioxygen in Photosynthesis. In: Kroneck, P., Sosa Torres, M. (eds) Sustaining Life on Planet Earth: Metalloenzymes Mastering Dioxygen and Other Chewy Gases. Metal Ions in Life Sciences, vol 15. Springer, Cham. https://doi.org/10.1007/978-3-319-12415-5_2

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