Ammonia binds to the manganese site of the oxygen-evolving complex of photosystem II in the S2 state

Beck, Warren F.; Paula, Julio C. de; Brudvig, Gary W.

doi:10.1021/ja00274a027

Cited by 143 publications

(202 citation statements)

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“…No change was observed in the background cytochrome c550/b559 signals upon annealing the sample at 260 K. The ammonia-modified S 2 -state multiline signal is also centered about g ≈ 2.0, spread over the 250-to 430-mT field range and characteristically contains more hyperfine peaks than the control sample (at least 24 vs. 20; see Fig. 1C) (24,29). Simulations of the EPR and 55 Mn-ENDOR spectra using the spin Hamiltonian formalism are given in Fig.…”

Section: Resultsmentioning

confidence: 91%

“…This model also provides a simple rationale for ammonia binding/release during the S-state cycle (24,26). In the lower S states (S 0 , S 1 ), Mn A4 is usually considered to be in the Mn III oxidation state and is thus potentially five-coordinate, with W1 being only a weakly associated ligand.…”

Section: Ammonia Perturbs All Exchangeable Oxygen Ligands Of the Mangmentioning

confidence: 99%

“…Ammonia binding at the SYI site is chloride-concentration dependent, is S-state independent, and results in the inhibition of oxygen-evolving activity (21)(22)(23), indicating that SYI likely represents one of the chloride sites identified in the crystal structure (1). In contrast, ammonia binding to SYII is independent of the chloride concentration (21,22,24,25) and does not reduce O 2 evolution. It binds only upon formation of the S 2 state, to be subsequently released at some later point during the S state cycle (after S 3 ), such that it is not bound upon return to the S 1 state (26).…”

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Ammonia binding to the oxygen-evolving complex of photosystem II identifies the solvent-exchangeable oxygen bridge (μ-oxo) of the manganese tetramer

Navarro

Ames

Nilsson

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

148

238

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The assignment of the two substrate water sites of the tetramanganese penta-oxygen calcium (Mn 4 O 5 Ca) cluster of photosystem II is essential for the elucidation of the mechanism of biological O-O bond formation and the subsequent design of bio-inspired water-splitting catalysts. We recently demonstrated using pulsed EPR spectroscopy that one of the five oxygen bridges (μ-oxo) exchanges unusually rapidly with bulk water and is thus a likely candidate for one of the substrates. Ammonia, a water analog, was previously shown to bind to the Mn 4 O 5 Ca cluster, potentially displacing a water/substrate ligand [Britt RD, et al. (1989) J Am Chem Soc 111(10):3522-3532]. Here we show by a combination of EPR and time-resolved membrane inlet mass spectrometry that the binding of ammonia perturbs the exchangeable μ-oxo bridge without drastically altering the binding/exchange kinetics of the two substrates. In combination with broken-symmetry density functional theory, our results show that (i) the exchangable μ-oxo bridge is O5 {using the labeling of the current crystal structure [Umena Y, et al. (2011) Nature 473(7345):55-60]}; (ii) ammonia displaces a water ligand to the outer manganese (Mn A4 -W1); and (iii) as W1 is trans to O5, ammonia binding elongates the Mn A4 -O5 bond, leading to the perturbation of the μ-oxo bridge resonance and to a small change in the water exchange rates. These experimental results support O-O bond formation between O5 and possibly an oxyl radical as proposed by Siegbahn and exclude W1 as the second substrate water.PSII | OEC | water oxidizing complex | water-oxidation | Mn cluster I n oxygenic photosynthesis, light-driven water splitting is catalyzed by the oxygen-evolving complex (OEC) of the membrane bound, pigment-protein complex photosystem II (PSII). The OEC consists of an inorganic tetra-manganese penta-oxygen calcium (Mn 4 O 5 Ca) cluster (1-3) and the nearby redox-active tyrosine residue Y Z (D1-Tyr161) that couples electron transfer from the Mn 4 O 5 Ca cluster to P680, the photo-oxidant of PSII. The cluster resembles a "distorted chair", where the base is formed by an oxygen-bridged (μ-oxo) cuboidal Mn 3 O 4 Ca unit (1) (Fig. 1A). The fourth Mn (Mn A4 ) is located outside of the cuboidal unit and is linked via a μ-oxo-bridged ligation (O4) to one of its corners (Mn B3 ). A second linkage between the outer Mn and the cube is provided by a fifth oxygen O5. The Mn 4 O 5 Ca cluster is also held together by six carboxylate ligands and has only one directly coordinating nitrogen ligand, D1-His332 (Fig. 1B).The OEC cycles through a series of five intermediate states that are known as S states (4) (Fig. 1A): S 0 , S 1 (dark stable), S 2 , S 3 , and S 4 (not yet isolated), where the subscript refers to the number of oxidizing equivalents stored in the OEC through successive electron withdrawals by Y Z • . In the 1.9-Å resolution structure, the S state of the cluster was assigned to be S 1 (1). However, this is unlikely as all Mn-Mn, Mn-Ca, and Mn-O/N distances of the crystal structure are ∼...

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Section: Resultsmentioning

confidence: 91%

Section: Ammonia Perturbs All Exchangeable Oxygen Ligands Of the Mangmentioning

confidence: 99%

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confidence: 99%

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Ammonia binding to the oxygen-evolving complex of photosystem II identifies the solvent-exchangeable oxygen bridge (μ-oxo) of the manganese tetramer

Navarro

Ames

Nilsson

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

148

238

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“…Ammonia, a substrate water analogue, is known to bind to the water oxidizing cofactor in the S 2 state [69,70]. Its binding mode was recently determined as a terminal ligand to the Mn4 ion, replacing the water ligand W1 [71,72].…”

Section: The Structure Of the Catalystmentioning

confidence: 99%

Artificial photosynthesis: understanding water splitting in nature

et al. 2015

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One contribution of 11 to a theme issue 'Do we need a global project on artificial photosynthesis (solar fuels and chemicals)?'. In the context of a global artificial photosynthesis (GAP) project, we review our current work on nature's water splitting catalyst. In a recent report (Cox et al. 2014 Science 345, 804-808 (doi:10.1126/science.1254910)), we showed that the catalyst-a Mn 4 O 5 Ca cofactor-converts into an 'activated' form immediately prior to the O-O bond formation step. This activated state, which represents an all Mn IV complex, is similar to the structure observed by X-ray crystallography but requires the coordination of an additional water molecule. Such a structure locates two oxygens, both derived from water, in close proximity, which probably come together to form the product O 2 molecule. We speculate that formation of the activated catalyst state requires inherent structural flexibility. These features represent new design criteria for the development of biomimetic and bioinspired model systems for water splitting catalysts using first-row transition metals with the aim of delivering globally deployable artificial photosynthesis technologies.

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“…No data from Br -substituted samples in the S 2 state were presented. In the case of EPR, Beck et al (1986) showed that the S 2 multiline signal was modified (narrowed line spacings) when PSII was illuminated in the presence of NH 3 and sufficient Cl -to block amine binding to the halide-sensitive site and concluded that NH 3 was bound to Mn. Britt et al (1989) used ESEEM to show, by direct detection, that under Cl -sufficient conditions, NH 3 was bound directly to Mn and proposed a model in which the amine bridged two Mn atoms.…”

Section: Spectroscopic Probing Of the Role Of CL -In The Oecmentioning

confidence: 99%

Current status of the role of Cl− ion in the oxygen-evolving complex

Popelková

Yocum

2007

Photosynth Res

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This minireview summarizes the current state of knowledge concerning the role of Cl(-) in the oxygen-evolving complex (OEC) of photosystem II (PSII). The model that proposes that Cl(-) is a Mn ligand is discussed in light of more recent work. Studies of Cl(-) specificity, stoichiometry, kinetics, and retention by extrinsic polypeptides are discussed, as are the results that fail to detect Cl(-) ligation to Mn and results that show a lack of a requirement for Cl(-) in PSII-catalyzed H(2)O oxidation. Mutagenesis experiments in cyanobacteria and higher plants that produce evidence for a correlation between Cl(-) retention and stable interactions among intrinsic and extrinsic polypeptides are summarized, and spectroscopic data on the interaction between PSII and Cl(-) are discussed. Lastly, the question of the site of Cl(-) action in PSII is discussed in connection with the current crystal structures of the enzyme.

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Ammonia binds to the manganese site of the oxygen-evolving complex of photosystem II in the S2 state

Cited by 143 publications

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Ammonia binding to the oxygen-evolving complex of photosystem II identifies the solvent-exchangeable oxygen bridge (μ-oxo) of the manganese tetramer

Ammonia binding to the oxygen-evolving complex of photosystem II identifies the solvent-exchangeable oxygen bridge (μ-oxo) of the manganese tetramer

Artificial photosynthesis: understanding water splitting in nature

Current status of the role of Cl− ion in the oxygen-evolving complex

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