The manganese complex of photosystem II in its reaction cycle—Basic framework and possible realization at the atomic level

Dau, Holger; Haumann, Michael

doi:10.1016/j.ccr.2007.09.001

Cited by 372 publications

(485 citation statements)

References 230 publications

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“…In photosynthetic organisms, highly efficient water oxidation is catalyzed by a metal-oxo Mn 4 Ca complex 8,9 embedded in a specific protein environment. Inspired by nature's catalyst for water oxidation, functional Mn-based molecular mimics [10][11][12] and Mn oxides [13][14][15][16][17][18] have been synthesized.…”

Section: Introductionmentioning

confidence: 99%

Electrosynthesis, functional, and structural characterization of a water-oxidizing manganese oxide

Zaharieva

Chernev

Risch

et al. 2012

Energy Environ. Sci.

416

583

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In the sustainable production of non-fossil fuels, water oxidation is pivotal. Development of efficient catalysts based on manganese is desirable because this element is earth-abundant, inexpensive, and largely non-toxic. We report an electrodeposited Mn oxide (MnCat) that catalyzes electrochemical water oxidation at neutral pH at rates that approach the level needed for direct coupling to photoactive materials. By choice of the voltage protocol we could switch between electrodeposition of inactive Mn oxides (deposition at constant anodic potentials) and synthesis of the active MnCat (deposition by voltage-cycling protocols). Electron microscopy reveals that the MnCat consists of nanoparticles (100 nm) with complex fine-structure. X-ray spectroscopy reveals that the amorphous MnCat resembles the biological paragon, the water-splitting Mn 4 Ca complex of photosynthesis, with respect to mean Mn oxidation state (ca. +3.8 in the MnCat) and central structural motifs. Yet the MnCat functions without calcium or other bivalent ions. Comparing the MnCat with electrodeposited Mn oxides inactive in water oxidation, we identify characteristics that likely are crucial for catalytic activity. In both inactive Mn oxides and active ones (MnCat), extensive di-m-oxo bridging between Mn ions is observed. However in the MnCat, the voltage-cycling protocol resulted in formation of Mn III sites and prevented formation of well-ordered and unreactive Mn IV O 2 . Structure-function relations in Mn-based wateroxidation catalysts and strategies to design catalytically active Mn-based materials are discussed. Knowledge-guided performance optimization of the MnCat could pave the road for its technological use. Broader contextThreatening global climate changes and unsecured supply of fossil fuels call for a global transition toward sustainable energyconversion systems. The storage of wind or solar energy by formation of energy-rich fuel molecules could play a central role in both transient storage of the intermittently provided energy and replacement of fossil fuels in the transportation sector. Whether hydrogen or a carbon-based fuel is the target, in any event the extraction of reducing equivalents and protons from water (that is, water oxidation) is pivotal. In search of water-oxidation catalysts that ultimately could play a role at a global scale, we and others are aiming at development of simple routes towards formation of Mn-based catalysts. Manganese excels by high availability and low toxicity; and in oxygenic photosynthesis, nature has demonstrated that a Mn-based catalyst can oxidize water efficiently. When aiming at an 'artificial leaf' with a Mn-based catalyst directly coupled to a solar-energy-converting material, the activity of the catalyst (per area) needs to cope with the incoming photon flux. Moreover the device design typically requires the use of benign synthesis and operation conditions, that is, temperatures close to room temperature and pH close to neutral. As an important first step, we report a simple protocol for e...

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Section: Introductionmentioning

confidence: 99%

Electrosynthesis, functional, and structural characterization of a water-oxidizing manganese oxide

Zaharieva

Chernev

Risch

et al. 2012

Energy Environ. Sci.

416

583

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“…Later, Grabolle and Dau (10) analyzed the delayed and prompt Chl fluorescence of PS II membranes in the absence of inhibitor and assessed the E m (P680/P680 ϩ ) value to be ϩ1.25 V, by citing E m (Q A /Q A Ϫ ) to be Ϫ80 mV. Since then, the value of approximately ϩ1.25 V is generally accepted for E m (P680/P680 ϩ ) (1)(2)(3)(4)(5) and is used as a reference in computational chemistry (13)(14)(15)(16).…”

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confidence: 99%

“…PS II appears to catalyze water oxidation at a pentanuclear Mn 4 Ca cluster that accumulates oxidizing equivalents (see recent reviews in refs. [1][2][3][4][5]. It is generally supposed that the water oxidation is triggered by charge separation between the primary electron donor, P680, and the primary electron acceptor, pheophytin (Phe) a.…”

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confidence: 99%

Spectroelectrochemical determination of the redox potential of pheophytina, the primary electron acceptor in photosystem II

Kato

Sugiura

Oda

et al. 2009

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

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Thin-layer cell spectroelectrochemistry, featuring rigorous potential control and rapid redox equilibration within the cell, was used to measure the redox potential Em(Phe a/Phe a ؊ ) of pheophytin (Phe) a, the primary electron acceptor in an oxygen-evolving photosystem (PS) II core complex from a thermophilic cyanobacterium Thermosynechococcus elongatus. Interferences from dissolved O 2 and water reductions were minimized by airtight sealing of the sample cell added with dithionite and mercury plating on the gold minigrid working electrode surface, respectively. The result obtained at a physiological pH of 6.5 was E m(Phe a/Phe a ؊ ) ‫؍‬ ؊505 ؎ 6 mV vs. SHE, which is by Ϸ100 mV more positive than the values measured Ϸ30 years ago at nonphysiological pH and widely accepted thereafter in the field of photosynthesis research. Using the P680* ؊ Phe a free energy difference, as estimated from kinetic analyses by previous authors, the present result would locate the E m(P680/P680 ؉ ) value, which is one of the key parameters but still resists direct measurements, at approximately ؉1,210 mV. In view of these pieces of information, a renewed diagram is proposed for the energetics in PS II.charge separation ͉ photosynthesis ͉ spectroelectrochemistry ͉ water oxidation I n the photosynthetic primary process of higher plants, algae, and cyanobacteria, photosystem (PS) I and PS II cooperate in series to convert photon energy into chemical energy through light-induced charge separation and subsequent electron transfers. PS II appears to catalyze water oxidation at a pentanuclear Mn 4 Ca cluster that accumulates oxidizing equivalents (see recent reviews in refs. 1-5). It is generally supposed that the water oxidation is triggered by charge separation between the primary electron donor, P680, and the primary electron acceptor, pheophytin (Phe) a. The initial radical pair P680 ϩ Phe a Ϫ formed by the charge separation, drives forward electron transfer from Phe a Ϫ to the first plastoquinone Q A , and hole transfer from P680 ϩ to the Mn 4 Ca cluster through a redox-active tyrosine residue denoted Y Z , thus preventing charge recombination. Recent X-ray crystallography clarified the arrangement of protein subunits and cofactors in PS II with 2.9-3.7-Å resolution (6-9), visualizing the electron transfer pathway.To date, the nature of P680 remains controversial. Available experimental data and theoretical analyses suggest that P680 is assignable to the pigment cluster of the four chlorophyll a molecules (denoted P D1 , P D2 , Chl D1 , and Chl D2 ) in the PS II reaction center (1, 5). Further uncertainty surrounds the value of the redox potential E m (P680/P680 ϩ ). Although the E m (P680/ P680 ϩ ) value is an essential parameter to draw a whole picture of the PS II energetics, its direct measurement has never been attained (10) because water, present as dominant (solvent) molecules in most sample solutions, is oxidized first heavily and tends to mask the subsequent oxidation of the target entity P680 at a higher potential. The E m ...

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“…Dioxygen (O 2 ) is formed as product of the water oxidation chemistry of the photosystem II (PSII) protein complex (1)(2)(3)(4)(5). Photosynthetic CO 2 fixation and O 2 formation have shaped the Earth's atmosphere (6) by (i) lowering the CO 2 level to Ͻ0.04% and (ii) creation of a maximal O 2 concentration of 35% (7), Ϸ300 million years before the present and a current level of Ϸ20%.…”

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confidence: 99%

Photosynthetic water oxidation at elevated dioxygen partial pressure monitored by time-resolved X-ray absorption measurements

Haumann

Grundmeier

Zaharieva

et al. 2008

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

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The atmospheric dioxygen (O2) is produced at a tetramanganese complex bound to the proteins of photosystem II (PSII). To investigate product inhibition at elevated oxygen partial pressure (pO 2 ranging from 0.2 to 16 bar), we monitored specifically the redox reactions of the Mn complex in its catalytic S-state cycle by rapid-scan and time-resolved X-ray absorption near-edge spectroscopy (XANES) at the Mn K-edge. By using a pressure cell for X-ray measurements after laser-flash excitation of PSII particles, we found a clear pO 2 influence on the redox reactions of the Mn complex, with a similar half-effect pressure as determined (2-3 bar). However, XANES spectra and the time courses of the X-ray fluorescence collected with microsecond resolution suggested that the O 2 evolution transition itself (S3fS0؉O2) was not affected. Additional (nonstandard) oxidation of the Mn complex at high pO 2 explains our experimental findings more readily. Our results suggest that photosynthesis at ambient conditions is not limited by product inhibition of the O 2 formation step. manganese complex ͉ photosystem II ͉ X-ray spectroscopy ͉ bioinorganic chemistry ͉ oxygen pressure I n oxygenic photosynthesis, plants, algae, and cyanobacteria facilitate the primary biomass formation by exploiting solar energy for driving the conversion of water (H 2 O) and carbon dioxide (CO 2 ) into carbohydrates (C n H 2n O n ). Dioxygen (O 2 ) is formed as product of the water oxidation chemistry of the photosystem II (PSII) protein complex (1-5). Photosynthetic CO 2 fixation and O 2 formation have shaped the Earth's atmosphere (6) by (i) lowering the CO 2 level to Ͻ0.04% and (ii) creation of a maximal O 2 concentration of 35% (7), Ϸ300 million years before the present and a current level of Ϸ20%.In photosynthetic organisms, the low level of atmospheric CO 2 can limit photosynthesis, related to the activity of CO 2 -fixing ribulose bisphosphate carboxylase (8, 9). It is less clear whether water oxidation by PSII is directly affected by the concentration of O 2 , the immediate product of light-driven water splitting. This question was only recently addressed experimentally by Clausen and Junge (10). They exposed PSII from cyanobacteria to oxygen partial pressures (pO 2 ) ranging from 0.2 to 30 bar and, analyzing flash-induced near-UV absorption changes, discovered a pO 2 effect with a half-saturation pressure of only Ϸ2 bar (10). Subsequently, in measurements of delayed Chl fluorescence, together with Clausen and Junge we confirmed that also the donor side of the plant PSII in its native membrane environment is affected by elevated pO 2 (11). The surprisingly low halfpressure of only 2-3 bar was taken as an indication that the efficiency of the O 2 formation step could be reduced significantly by product inhibition. Such a limitation of the water oxidation chemistry may have imposed restraints on the evolution of oxygenic photosynthesis (10). Notably, the pO 2 inside of photosynthetic cells in microbial mats and bioreactors can be severalfold higher th...

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The manganese complex of photosystem II in its reaction cycle—Basic framework and possible realization at the atomic level

Cited by 372 publications

References 230 publications

Electrosynthesis, functional, and structural characterization of a water-oxidizing manganese oxide

Electrosynthesis, functional, and structural characterization of a water-oxidizing manganese oxide

Spectroelectrochemical determination of the redox potential of pheophytina, the primary electron acceptor in photosystem II

Photosynthetic water oxidation at elevated dioxygen partial pressure monitored by time-resolved X-ray absorption measurements

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