A five-coordinate Mn(<scp>iv</scp>) intermediate in biological water oxidation: spectroscopic signature and a pivot mechanism for water binding

Retegan, Marius; Krewald, Vera; Mamedov, Fikret; Neese, Frank; Lubitz, Wolfgang; Cox, Nicholas; Pantazis, Dimitrios A.

doi:10.1039/c5sc03124a

Cited by 167 publications

(348 citation statements)

References 122 publications

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“…On the other hand, the weaker H-bonding makes ammonia binding at the W2 site difficult to reconcile with the highly anisotropic nuclear quadrupole parameter of the bound ammonia 13 . We note that our data do not exclude ammonia moving from the W1 to W2 site or detaching from Mn during the S 2 →S 3 transition 27,28 .…”

contrasting

confidence: 68%

Structure of photosystem II and substrate binding at room temperature

Young¹,

Ibrahim²,

Chatterjee³

et al. 2016

Nature

332

361

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Light-induced oxidation of water by photosystem II (PS II) in plants, algae and cyanobacteria has generated most of the dioxygen in the atmosphere. PS II, a membrane-bound multi-subunit pigment-protein complex, couples the one-electron photochemistry at the reaction center with the four-electron redox chemistry of water oxidation at the Mn4CaO5 cluster in the oxygen-evolving complex (OEC) (Fig. 1a, Extended Data Fig. 1). Under illumination, the OEC cycles through five intermediate S-states (S0 to S4)1, where S1 is the dark stable state and S3 is the last semi-stable state before O-O bond formation and O2 evolution2,3. A detailed understanding of the O-O bond formation mechanism remains a challenge, and elucidating the structures of the OEC in the different S-states, as well as the binding of the two substrate waters to the catalytic site4-6, is a prerequisite for this purpose. Here we report the use of femtosecond pulses from an X-ray free electron laser (XFEL) to obtain damage free, room temperature (RT) structures of dark-adapted (S1), two-flash illuminated (2F; S3-enriched), and ammonia-bound two-flash illuminated (2F-NH3; S3-enriched) PS II. Although the recent 1.95 Å structure of PS II7 at cryogenic temperature using an XFEL provided a damage-free view of the S1 state, RT measurements are required to study the structural landscape of proteins under functional conditions8,9, and also for in situ advancement of the S-states. To investigate the water-binding site(s), ammonia, a water analog, has been used as a marker, as it binds to the Mn4CaO5 cluster in the S2 and S3 states10. Since the ammonia-bound OEC is active, the ammonia-binding Mn site is not a substrate water site10-13. Thus, this approach, together with a comparison of the native dark and 2F states, is used to discriminate between proposed O-O bond formation mechanisms.

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contrasting

confidence: 68%

Structure of photosystem II and substrate binding at room temperature

Young¹,

Ibrahim²,

Chatterjee³

et al. 2016

Nature

332

361

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“…Although we do not see any evidence for the presence of more than one S 2 structure in the 1F data under our conditions, we cannot exclude the presence of minor concentrations (< 20%) and further studies will be required to elucidate if such forms exist as transient states between the S 2 and S 3 states as proposed by some theoretical studies, in relation to the water‐insertion pathway (Pantazis et al , Bovi et al , Siegbahn , Isobe et al , , Narzi et al , Shoji et al , Retegan et al , Ugur et al ). We have taken the first step into this direction, by collecting X‐ray diffraction data for two time points during the S 2 ‐S 3 transition (150 μs and 400 μs after the second flash; Kern et al ).…”

Section: Introductionmentioning

confidence: 57%

“…EPR (Cox et al , , Lubitz et al ) and theoretical studies (Bovi et al , Siegbahn , Narzi et al , Isobe et al , Shoji et al , Retegan et al , Ugur et al ) proposed that there is an insertion of a water molecule in the Mn 4 CaO 5 cluster during the S 2 to S 3 transition. As the quality of the room temperature crystallography data of the S 3 state has been improved compared to previous studies (Young et al , Suga et al ), the exact position of the inserted water molecule is becoming clear, although its protonation state is still uncertain (Kern et al ).…”

Section: Introductionmentioning

confidence: 99%

Structural isomers of the S₂ state in photosystem II: do they exist at room temperature and are they important for function?

Chatterjee

Lassalle

Gul

et al. 2019

Physiologia Plantarum

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In nature, an oxo‐bridged Mn4CaO5 cluster embedded in photosystem II (PSII), a membrane‐bound multi‐subunit pigment protein complex, catalyzes the water oxidation reaction that is driven by light‐induced charge separations in the reaction center of PSII. The Mn4CaO5 cluster accumulates four oxidizing equivalents to enable the four‐electron four‐proton catalysis of two water molecules to one dioxygen molecule and cycles through five intermediate S‐states, S0 – S4 in the Kok cycle. One important question related to the catalytic mechanism of the oxygen‐evolving complex (OEC) that remains is, whether structural isomers are present in some of the intermediate S‐states and if such equilibria are essential for the mechanism of the O‐O bond formation. Here we compare results from electron paramagnetic resonance (EPR) and X‐ray absorption spectroscopy (XAS) obtained at cryogenic temperatures for the S2 state of PSII with structural data collected of the S1, S2 and S3 states by serial crystallography at neutral pH (∼6.5) using an X‐ray free electron laser at room temperature. While the cryogenic data show the presence of at least two structural forms of the S2 state, the room temperature crystallography data can be well‐described by just one S2 structure. We discuss the deviating results and outline experimental strategies for clarifying this mechanistically important question.

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“…This was supported further by the very slow reaction of S 3 with reductants like hydrazine or hydroxylamine as compared to that with S 2 state (Messinger et al 1991;Messinger and Renger 1990). At present, it appears that this structural change is relatively minor with regard to Mn-Mn and Mn-Ca distances, but may involve the binding of one water molecule to the Mn 4 CaO 5 cluster (Noguchi 2008;Suzuki et al 2008;Siegbahn 2009)-possibly in a complex sequence of events (Cox and Messinger 2013;Siegbahn 2013;Retegan et al 2016;Capone et al 2016;Ugur et al 2016). We note though that substrate water exchange experiments exclude the water molecule binding to the Mn 4 CaO 5 cluster, during this transition, to act as a Fig.…”

Section: Gernot's Legacymentioning

confidence: 96%

Gernot Renger (1937–2013): his life, Max-Volmer Laboratory, and photosynthesis research

2016

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Gernot Renger (October 23, 1937-January 12, 2013), one of the leading biophysicists in the field of photosynthesis research, studied and worked at the Max-Volmer-Institute (MVI) of the Technische Universität Berlin, Germany, for more than 50 years, and thus witnessed the rise and decline of photosynthesis research at this institute, which at its prime was one of the leading centers in this field. We present a tribute to Gernot Renger's work and life in the context of the history of photosynthesis research of that period, with special focus on the MVI. Gernot will be remembered for his thought-provoking questions and his boundless enthusiasm for science.

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A five-coordinate Mn(iv) intermediate in biological water oxidation: spectroscopic signature and a pivot mechanism for water binding

Abstract: The identification of a unique intermediate in biological water oxidation establishes the water binding mechanism in the S2 to S3 state transition.

Cited by 167 publications

References 122 publications

Structure of photosystem II and substrate binding at room temperature

Structure of photosystem II and substrate binding at room temperature

Structural isomers of the S₂ state in photosystem II: do they exist at room temperature and are they important for function?

Gernot Renger (1937–2013): his life, Max-Volmer Laboratory, and photosynthesis research

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A five-coordinate Mn(iv) intermediate in biological water oxidation: spectroscopic signature and a pivot mechanism for water binding

Abstract: The identification of a unique intermediate in biological water oxidation establishes the water binding mechanism in the S2 to S3 state transition.

Cited by 167 publications

References 122 publications

Structure of photosystem II and substrate binding at room temperature

Structure of photosystem II and substrate binding at room temperature

Structural isomers of the S2 state in photosystem II: do they exist at room temperature and are they important for function?

Gernot Renger (1937–2013): his life, Max-Volmer Laboratory, and photosynthesis research

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Structural isomers of the S₂ state in photosystem II: do they exist at room temperature and are they important for function?