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

134 Citations (Scopus)

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

Fingerprint

Photosystem II Protein Complex
X-Ray Diffraction
Spectrum Analysis
Water
X-Rays
Motion Pictures
Manganese
Lasers
Electrons
Oxygen
Light

All Science Journal Classification (ASJC) codes

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

Cite this

Kern, J., Tran, R., Alonso-Mori, R., Koroidov, S., Echols, N., Hattne, J., ... 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
Kern, Jan ; Tran, Rosalie ; Alonso-Mori, Roberto ; 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, Dörte ; Milathianaki, Despina ; Fry, Alan R. ; Seibert, M. Marvin ; Koglin, Jason E. ; Gallo, Erik ; Uhlig, Jens ; Sokaras, Dimosthenis ; Weng, Tsu Chien ; Zwart, Petrus H. ; Skinner, David E. ; 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. / Taking snapshots of photosynthetic water oxidation using femtosecond X-ray diffraction and spectroscopy. In: Nature communications. 2014 ; Vol. 5.
@article{e4a8c05e6bfb43fca774dbdfcd9bff5c,
title = "Taking snapshots of photosynthetic water oxidation using femtosecond X-ray diffraction and spectroscopy",
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 4.5{\AA}. This study represents the initial frames in a molecular movie of the structural changes during the catalytic reaction in photosystem II.",
author = "Jan Kern and Rosalie Tran and Roberto Alonso-Mori and Sergey Koroidov and Nathaniel Echols and Johan Hattne and Mohamed Ibrahim and Sheraz Gul and Hartawan Laksmono and Sierra, {Raymond G.} and Gildea, {Richard J.} and Guangye Han and Julia Hellmich and Benedikt Lassalle-Kaiser and Ruchira Chatterjee and Brewster, {Aaron S.} and Stan, {Claudiu A.} and Carina Gl{\"o}ckner and Alyssa Lampe and D{\"o}rte Difiore and Despina Milathianaki and Fry, {Alan R.} and Seibert, {M. Marvin} and Koglin, {Jason E.} and Erik Gallo and Jens Uhlig and Dimosthenis Sokaras and Weng, {Tsu Chien} and Zwart, {Petrus H.} and Skinner, {David E.} and Bogan, {Michael J.} and Marc Messerschmidt and Pieter Glatzel and Williams, {Garth J.} and S{\'e}bastien Boutet and Adams, {Paul D.} and Athina Zouni and Johannes Messinger and Sauter, {Nicholas K.} and Uwe Bergmann and Junko Yano and Yachandra, {Vittal K.}",
year = "2014",
month = "7",
day = "9",
doi = "https://doi.org/10.1038/ncomms5371",
language = "English (US)",
volume = "5",
journal = "Nature Communications",
issn = "2041-1723",
publisher = "Nature Publishing Group",

}

Kern, J, Tran, R, Alonso-Mori, R, Koroidov, S, Echols, N, Hattne, J, Ibrahim, M, Gul, S, Laksmono, H, Sierra, RG, Gildea, RJ, Han, G, Hellmich, J, Lassalle-Kaiser, B, Chatterjee, R, Brewster, AS, Stan, CA, Glöckner, C, Lampe, A, Difiore, D, Milathianaki, D, Fry, AR, Seibert, MM, Koglin, JE, Gallo, E, Uhlig, J, Sokaras, D, Weng, TC, Zwart, PH, Skinner, DE, Bogan, MJ, Messerschmidt, M, Glatzel, P, Williams, GJ, Boutet, S, Adams, PD, Zouni, A, Messinger, J, Sauter, NK, Bergmann, U, Yano, J & Yachandra, VK 2014, 'Taking snapshots of photosynthetic water oxidation using femtosecond X-ray diffraction and spectroscopy', Nature communications, vol. 5, 4371. https://doi.org/10.1038/ncomms5371

Taking snapshots of photosynthetic water oxidation using femtosecond X-ray diffraction and spectroscopy. / Kern, Jan; Tran, Rosalie; Alonso-Mori, Roberto; 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, Dörte; Milathianaki, Despina; Fry, Alan R.; Seibert, M. Marvin; Koglin, Jason E.; Gallo, Erik; Uhlig, Jens; Sokaras, Dimosthenis; Weng, Tsu Chien; Zwart, Petrus H.; Skinner, David E.; 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.

In: Nature communications, Vol. 5, 4371, 09.07.2014.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Taking snapshots of photosynthetic water oxidation using femtosecond X-ray diffraction and spectroscopy

AU - Kern, Jan

AU - Tran, Rosalie

AU - Alonso-Mori, Roberto

AU - Koroidov, Sergey

AU - Echols, Nathaniel

AU - Hattne, Johan

AU - Ibrahim, Mohamed

AU - Gul, Sheraz

AU - Laksmono, Hartawan

AU - Sierra, Raymond G.

AU - Gildea, Richard J.

AU - Han, Guangye

AU - Hellmich, Julia

AU - Lassalle-Kaiser, Benedikt

AU - Chatterjee, Ruchira

AU - Brewster, Aaron S.

AU - Stan, Claudiu A.

AU - Glöckner, Carina

AU - Lampe, Alyssa

AU - Difiore, Dörte

AU - Milathianaki, Despina

AU - Fry, Alan R.

AU - Seibert, M. Marvin

AU - Koglin, Jason E.

AU - Gallo, Erik

AU - Uhlig, Jens

AU - Sokaras, Dimosthenis

AU - Weng, Tsu Chien

AU - Zwart, Petrus H.

AU - Skinner, David E.

AU - Bogan, Michael J.

AU - Messerschmidt, Marc

AU - Glatzel, Pieter

AU - Williams, Garth J.

AU - Boutet, Sébastien

AU - Adams, Paul D.

AU - Zouni, Athina

AU - Messinger, Johannes

AU - Sauter, Nicholas K.

AU - Bergmann, Uwe

AU - Yano, Junko

AU - Yachandra, Vittal K.

PY - 2014/7/9

Y1 - 2014/7/9

N2 - 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.

AB - 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.

UR - http://www.scopus.com/inward/record.url?scp=84904154463&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84904154463&partnerID=8YFLogxK

U2 - https://doi.org/10.1038/ncomms5371

DO - https://doi.org/10.1038/ncomms5371

M3 - Article

C2 - 25006873

VL - 5

JO - Nature Communications

JF - Nature Communications

SN - 2041-1723

M1 - 4371

ER -