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

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

Research output: Contribution to journalArticle

153 Scopus citations

Abstract

The dioxygen we breathe is formed by light-induced oxidation of water in photosystem II. O2 formation takes place at a catalytic manganese cluster within milliseconds after the photosystem II reaction centre is excited by three single-turnover flashes. Here we present combined X-ray emission spectra and diffraction data of 2-flash (2F) and 3-flash (3F) photosystem II samples, and of a transient 3F′ state (250μs after the third flash), collected under functional conditions using an X-ray free electron laser. The spectra show that the initial O-O bond formation, coupled to Mn reduction, does not yet occur within 250μs after the third flash. Diffraction data of all states studied exhibit an anomalous scattering signal from Mn but show no significant structural changes at the present resolution of 4.5Å. This study represents the initial frames in a molecular movie of the structural changes during the catalytic reaction in photosystem II.

Original languageEnglish (US)
Article number4371
JournalNature communications
Volume5
DOIs
StatePublished - Jul 9 2014

ASJC Scopus subject areas

  • Chemistry(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Physics and Astronomy(all)

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    Kern, J., Tran, R., Alonso-Mori, R., Koroidov, S., Echols, N., Hattne, J., Ibrahim, M., Gul, S., Laksmono, H., Sierra, R. G., Gildea, R. J., Han, G., Hellmich, J., Lassalle-Kaiser, B., Chatterjee, R., Brewster, A. S., Stan, C. A., Glöckner, C., Lampe, A., ... Yachandra, V. K. (2014). Taking snapshots of photosynthetic water oxidation using femtosecond X-ray diffraction and spectroscopy. Nature communications, 5, [4371]. https://doi.org/10.1038/ncomms5371