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

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 - Nat Commun (2014)

Bottom Line: The spectra show that the initial O-O bond formation, coupled to Mn reduction, does not yet occur within 250 μs 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 Å.This study represents the initial frames in a molecular movie of the structural changes during the catalytic reaction in photosystem II.

View Article: PubMed Central - PubMed

Affiliation: 1] Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, California 94720, USA [2] LCLS, SLAC National Accelerator Laboratory, Menlo Park, California 94025, USA.

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 (250 μs 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 250 μs 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 Å. This study represents the initial frames in a molecular movie of the structural changes during the catalytic reaction in photosystem II.

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Flash-induced changes in PS II and experimental setup used at LCLS A) Kok-cycle describing the different stable intermediate states of the catalytic water oxidation reaction in PS II. B) Scheme for the illumination setup used to advance PS II in the catalytic cycle and measure simultaneously the XRD and XES signal at LCLS. Lasers 2 and 3 were used to generate 2F samples, lasers 1, 2, 3 for 3F samples and lasers 2, 3 and 4 to generate the 3F′ samples.
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Figure 1: Flash-induced changes in PS II and experimental setup used at LCLS A) Kok-cycle describing the different stable intermediate states of the catalytic water oxidation reaction in PS II. B) Scheme for the illumination setup used to advance PS II in the catalytic cycle and measure simultaneously the XRD and XES signal at LCLS. Lasers 2 and 3 were used to generate 2F samples, lasers 1, 2, 3 for 3F samples and lasers 2, 3 and 4 to generate the 3F′ samples.

Mentions: During the water oxidation reaction, the OEC functions as a redox capacitor by storing four oxidizing equivalents before the release of molecular oxygen. Starting from the dark stable S1 state, the oxidation state of the OEC is increased by one upon each light excitation of PS II until the highest oxidized stable intermediate state, S3, is reached. Following the next light-excitation, the OEC is oxidized one more time to form the transient S3YZox and S4 states that lead to dioxygen formation, which converts the OEC to its most reduced state, S03. The fourth light-excitation sets the OEC back to the S1 state, and thereby completes the cycle (Fig. 1A).


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

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 - Nat Commun (2014)

Flash-induced changes in PS II and experimental setup used at LCLS A) Kok-cycle describing the different stable intermediate states of the catalytic water oxidation reaction in PS II. B) Scheme for the illumination setup used to advance PS II in the catalytic cycle and measure simultaneously the XRD and XES signal at LCLS. Lasers 2 and 3 were used to generate 2F samples, lasers 1, 2, 3 for 3F samples and lasers 2, 3 and 4 to generate the 3F′ samples.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4151126&req=5

Figure 1: Flash-induced changes in PS II and experimental setup used at LCLS A) Kok-cycle describing the different stable intermediate states of the catalytic water oxidation reaction in PS II. B) Scheme for the illumination setup used to advance PS II in the catalytic cycle and measure simultaneously the XRD and XES signal at LCLS. Lasers 2 and 3 were used to generate 2F samples, lasers 1, 2, 3 for 3F samples and lasers 2, 3 and 4 to generate the 3F′ samples.
Mentions: During the water oxidation reaction, the OEC functions as a redox capacitor by storing four oxidizing equivalents before the release of molecular oxygen. Starting from the dark stable S1 state, the oxidation state of the OEC is increased by one upon each light excitation of PS II until the highest oxidized stable intermediate state, S3, is reached. Following the next light-excitation, the OEC is oxidized one more time to form the transient S3YZox and S4 states that lead to dioxygen formation, which converts the OEC to its most reduced state, S03. The fourth light-excitation sets the OEC back to the S1 state, and thereby completes the cycle (Fig. 1A).

Bottom Line: The spectra show that the initial O-O bond formation, coupled to Mn reduction, does not yet occur within 250 μs 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 Å.This study represents the initial frames in a molecular movie of the structural changes during the catalytic reaction in photosystem II.

View Article: PubMed Central - PubMed

Affiliation: 1] Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, California 94720, USA [2] LCLS, SLAC National Accelerator Laboratory, Menlo Park, California 94025, USA.

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 (250 μs 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 250 μs 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 Å. This study represents the initial frames in a molecular movie of the structural changes during the catalytic reaction in photosystem II.

Show MeSH
Related in: MedlinePlus