TRPLSC-1310; No. of Pages 10

Review

The biological water-oxidizing complex at the nano–bio interface Mohammad Mahdi Najafpour1,2, Mohadeseh Zarei Ghobadi1, Anthony W. Larkum3, Jian-Ren Shen4, and Suleyman I. Allakhverdiev5,6,7 1

Department of Chemistry, Institute for Advanced Studies in Basic Sciences (IASBS), Zanjan 45137-66731, Iran Center of Climate Change and Global Warming, Institute for Advanced Studies in Basic Sciences (IASBS), Zanjan 45137-66731, Iran 3 Plant Functional Biology and Climate Change Cluster, University of Technology Sydney, Sydney, Australia 4 Photosynthesis Research Center, Graduate School of Natural Science and Technology, Faculty of Science, Okayama University, Okayama 700-8530, Japan 5 Controlled Photobiosynthesis Laboratory, Institute of Plant Physiology, Russian Academy of Sciences, Botanicheskaya Street 35, Moscow 127276, Russia 6 Institute of Basic Biological Problems, Russian Academy of Sciences, Pushchino, Moscow Region 142290, Russia 7 Department of Plant Physiology, Faculty of Biology, M.V. Lomonosov Moscow State University, Leninskie Gory 1–12, Moscow 119991, Russia 2

Photosynthesis is one of the most important processes on our planet, providing food and oxygen for the majority of living organisms on Earth. Over the past 30 years scientists have made great strides in understanding the central photosynthetic process of oxygenic photosynthesis, whereby water is used to provide the hydrogen and reducing equivalents vital to CO2 reduction and sugar formation. A recent crystal structure at 1.9– 1.95 A˚ has made possible an unparalleled map of the structure of photosystem II (PSII) and particularly the manganese–calcium (Mn–Ca) cluster, which is responsible for splitting water. Here we review how knowledge of the water-splitting site provides important criteria for the design of artificial Mn-based water-oxidizing catalysts, allowing the development of clean and sustainable solar energy technologies. The photosynthetic process and artificial catalysts Photosynthetic organisms were among the first organisms to perform energy transformations on the Earth, emerging 3.8 billion years ago [1,2]. The earliest photosynthetic organisms probably possessed only a single photosystem (see Glossary), either a proto-PSI or a proto-PSII. These early systems relied on reductants such as H2, H2S, organic acids, and Fe2+. Early proto-cyanobacteria combined both photosystems in one organism and later, as cyanobacteria, accomplished the difficult process of using water as a hydrogen (reducing) source. The evolution of this complex biochemical machinery probably occurred over many millions of years. However, it seems to have been perfected at a global level 2.45 billion years ago and the oxygen that was formed Corresponding authors: Najafpour, M.M. ([email protected]); Allakhverdiev, S.I. ([email protected]). Keywords: artificial photosynthesis; nano-sized Mn–Ca oxido cluster; photosynthesis; water oxidation; water-oxidizing complex. 1360-1385/ ß 2015 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tplants.2015.06.005

as a byproduct led to a dramatic change in the oxidation level of the atmosphere and the lithosphere, a change that is known as the Great Oxidation Event (GOE) [1–4]. The pivotal evolutionary changes that occurred in proto-cyanobacteria and cyanobacteria before 2.45 billion years ago involved not only the evolution of PSII (Box 1) [1–10] but also the evolution of PSI [11], which is responsible for producing NADPH, an essential cofactor in the reduction of CO2 (see Box 1 and Figure I in Box 1). However, here we concentrate on PSII, the site of biological water oxidation. Glossary Artificial leaf: a machine that can harness sunlight to split water into molecular hydrogen and oxygen without needing any external connections. It can be compared with real leaves, which convert the energy of sunlight into chemical form. Artificial photosynthesis: refers to processes that mimic natural photosynthesis performed by plants, algae, and cyanobacteria. An important goal of artificial photosynthesis is to use the electrons generated by water oxidation to reduce CO2 to simple organic compounds such as methane, methanol, formaldehyde, formate, or carbon monoxide. Natural photosynthesis includes a series of complicated reactions, whereas artificial systems are usually a simplified way to produce clean and renewable fuels. Photosystem: a complex system comprising several proteins in the thylakoid membranes responsible for the absorption of light and the transfer of energy and electrons. Two types of photosystem exist, designated PSI and PSII. Photosystem I (PSI): one of the two photosystems performing electron transfer from plastocyanin (PC) or cytochrome c6 through the primary electron donor P700 (chlorophyll dimer) and five electron acceptors to ferredoxin (Fd). The photosystem has two main components in its core and more than 110 cofactors as an antenna system. Photosystem II (PSII): another photosystem performing light-induced water oxidation, leading to the generation of electrons, protons, and oxygen. The electrons produced are transferred via plastoquinones (PQs) and the cytochrome b6/f complex (Cytb6/f) to PSI while the protons accumulate in the lumen of the thylakoid membranes to create a proton gradient across the membrane, which is used by ATP synthase to generate ATP. All of the electron transfer components of PSII are bound to two reaction center subunits designated D1 and D2. Water-oxidizing complex (WOC), or oxygen-evolving complex (OEC): the catalytic site for water oxidation in PSII. In 2011 and 2015 [7,10], the structure of the WOC of PSII was solved at atomic resolution, which revealed that the WOC is a Mn4CaO5 cluster organized into a distorted chair form to which four water molecules are coordinated as terminal ligands in addition to seven amino acid ligands.

Trends in Plant Science xx (2015) 1–10

1

TRPLSC-1310; No. of Pages 10

Review

Trends in Plant Science xxx xxxx, Vol. xxx, No. x

Box 1. Oxygenic photosynthesis Carbon fixation and oxygen evolution occur in two distinct spaces in oxygenic photosynthesis. Figure I shows a view of oxygenic photosynthesis as well as carbohydrate production. The photosynthetic processes are driven by the light energy captured by the lightharvesting complexes (Lhcb and Lhca) of PSII and PSI. Electrons are derived from H2O by water oxidation at the WOC of PSII; these electrons are passed along the photosynthetic electron-transport chain via PQ, Cytb6/f, PC, and PSI to Fd. Then, Fd–NADP+ oxidoreductase (FNR) transfers the electrons to NADP+ with the final production of NADPH. Protons (H+ ions) are released into the thylakoid lumen by the WOC as water is oxidized as well as when PQH2

delivers electrons to the Cytb6/f complex. The proton gradient across the thylakoid membrane is used by ATP synthase to produce ATP. The ATP and NADPH generated during the primary photosynthetic processes are consumed for CO2 fixation in the Calvin–Benson cycle, which produces sugars and ultimately starch. Under anaerobic conditions, hydrogenase can accept electrons from the reduced Fd molecules and use them to reduce protons to molecular hydrogen. Anaerobic conditions also allow starch to be used as a source of protons and electrons for H2 production (via NADPH, PQ, Cytb6/f, PC, and PSI) using a hydrogenase enzyme. The thylakoid membrane is denoted with a violet color.

Carbon fixing reacons

hν hν

WY

Lhcb5

B

M L Te I

S

C Fe

QA D

J K Z N XH

QB

e–

A

cytb6 IV

½PQH2

Q

Phe

PQpool P680 Y7 e–

Y

½ H2O

O

e– e–

P700

Car

N

ISP

Tn

¼ O 2 + H+

H+ H+

CF1 d F0

A

b a

CF0

C10

e–

2Fe-2S

R Q

A0

oscp

α

ε γ δ

A

Fx A 1

B

β

ATP

β

Cytbt

QH2

Mm Mn Mm Mn

P

B

E F

Membrane (5 nm)

Lumen

M G e– C E D HJ K I LO F F

GM LN

Fe Cyt

bi

α

Fd

Cyclic e– transport

α

Lhca 2 Lhca 3

Lhcb6

16 nm

Lhcb1

Lhca 1

Lhcb1+2+3

β

Non-cyclic e– transport

Lhca 4

Stroma

ADP + Pi

NADP+

H+

H+

3H+

cyt f

PC

Fe e–

F C14 = 50–100 rpm

PC

C (CP43)

(CP47) B

PSII (*dimer)

Cyt b6f

PSI

ATP synthase

(*dimer)

TRENDS in Plant Science

Figure I. Model of the photosynthetic electron transport pathway and ATP-forming mechanism of the thylakoid membrane: for an explanation see Box 1. Adapted, with permission, from J. Nield.

The central process of PSII is the absorption of light and the channeling of excitation energy to a special pair of Chl a molecules (P680) that form a strong oxidation–reduction couple with an adjacent phaeophytin molecule (P680+/ Phaeo ) (Box 1). The primary oxidant (P680+) is of sufficient potential to extract electrons first from a special tyrosine, Yz, and then in an integrated series of steps from water (Figure 1A). It does this by entraining a series of electron and proton sequestrations, which are brought about by the water-oxidizing complex (WOC) [also known as the oxygen-evolving complex (OEC)] [5]. Now that the natural system of water oxidation involved in water splitting is at last becoming understood, new vistas of artificial photosynthesis are opening, promising the storage of clean and sustainable energy on a large scale [12–15]. We note that fossil fuels, on which modern societies have become reliant, represent the accumulation of photosynthetic activity over millions of years and are a limited resource for exploitation. Furthermore, the excessive combustion of fossil fuels has led to an accumulation of CO2 in the atmosphere, one of the major contributors to global climate change. By comparison, hydrogen is a clean and highly efficient energy source and/or fuel. However, its utilization is dependent on further technological 2

developments. What is needed are low-cost, environmentally friendly, stable, and efficient catalysts for water oxidation and reduction to decrease the high over-potential of these reactions [12–15]. To solve this bottleneck, researchers are turning to the Mn cluster PSII blueprint for a synthetic water oxidation catalyst [13–15]. In this review we describe the structural details of the WOC of PSII, resolved by recent high-resolution structural analysis [7,10], and then cover the recent advances in our understanding of the natural biological water oxidation mechanism. Finally, we deal with artificial photosynthesis, the potential chemical processes inspired by the natural process of photosynthesis. Overall structure of the WOC For many years it was known that there is a Mn complex attached to the reaction centre of PSII. It was also known that a cycle (Kok cycle) of five discrete flash-induced transition states known as Si states, where i is the number of oxidizing equivalents accumulated (i = 0–4), is associated with this Mn complex (Figure 1A) [5,16]. However, it was only with better-resolution crystal structures of PSII that the situation was clarified. A great step forward was with ˚ structure of Ferreira et al. in 2004, which the 3.5-A

TRPLSC-1310; No. of Pages 10

Review

Trends in Plant Science xxx xxxx, Vol. xxx, No. x

(A)

S 1A

S 2A

0

IV

O5

H+ e–

hν

e–

hν

0 S0

H2O S3

O2

III

S 3A

+

O5

IV

+

IV

IV

hν

IV

IV

H+

S4

H+

SG = 1/2

III

III

+

S2

hν

H+

III

O5

e– S1

III

+

IV IV

IV

III

SG = 0

IV

S 2B

IV

IV III

S 0A

+

IV

SG = 3

e–

H2O

(B)

W3

W4 2.6

2.5

W2 Ca 2.1

2.5

O5

2.7

2.3

III 2.3 Mn4A W1

2.6

III 1.8

2.7

1.8

2.2

2.0

O1

Mn1D

1.9

O2 O4

1.9

IV

Mn3B

1.9 2.1

1.8 2.0

O3

IV

Mn2C TRENDS in Plant Science

Figure 1. (A) S-state cycle of photosynthetic water oxidation (Kok cycle). Starting in the dark-stable S1 state, absorption of a photon causes electron transfer from the wateroxidizing complex (WOC) to the YZ tyrosine radical and Si–Si+1 transitions. The electron transfer steps are accompanied by charge-compensating deprotonation steps. A plausible set of oxidation-state combinations of the four Mn ions is shown for the various Si states. Models show the optimized geometry, protonation pattern, and Mn oxidation states of the inorganic core. The cofactor exists in two forms in the S2 state, an open cubane (S2A) and a closed cubane (S2B) structure, which differ in their core connectivity by the reorganization of O5. Adapted, with permission, from [16,25,48]; copyright American Chemical Society and Royal Society. (B) Structure of the Mn4CaO5 cluster. Distances (A˚) are between metal ions and oxo bridges or water molecules [10]. Adapted, with permission, from [10]; copyright McMillan Publications.

revealed an arrangement of three Mn atoms and one Ca atom in a cubane structure (with one additional Mn dislodged to the outside of the cubane structure). Subsequently there was much discussion regarding the validity of the cubane structure [6]. In 2011, Jian-Ren Shen and his group developed a new method for producing crystals that allowed much higher˚ resolution [7]. These new resolution structures of 1.9 A structures confirmed beyond doubt that the WOC has a cubane structure and a stoichiometry of Mn4CaO5 coordinated by many amino acid residues as well as a few water molecules (W1–W4) (Figure 1B). Although Cl ions were previously known [6], the high-resolution structure [7,10] revealed several new features such as well-defined hydrogen-bonded networks and hitherto unknown Cl -binding sites [5–7,10]. However, there were indications that the crystal structure was damaged by X-ray irradiation, which accounted for differences between the Mn–Mn distances measured by X-ray diffraction (XRD) versus extended X-ray absorption fine structure (EXAFS) (for a review see 16]). Then, in

2015, Jian-Ren Shen and his group reported a radiationdamage-free structure of PSII for Thermosynechococcus ˚ by vulcanus in the S1 state at a resolution of 1.95 A ˚ compact femtosecond X-ray pulses from an SPring 8-A free-electron laser (SACLA); this allowed firm determination of Mn–ligand distances and even allowed the possible assignment of the Jahn–Teller axis, using isomorphous PSII crystals [10]. This new methodology provides final proof of the radiation-damage-free structure [10]. Importantly, O5 has significantly longer distances to Mn than the other oxo-oxygen atoms, suggesting that O5 is a hydroxide ion and may serve as one of the substrates for oxygen (Figure 1B) [7,10], although this remains to be tested spectroscopically. The characteristics and position of each metal ion in the Mn4CaO5 cluster have been studied compared with artificial models [16–32] and using various methods [5–11,33–35]. However, the positions of the metal ions, together with the five oxygen atoms bridging the five metal ions, were clearly resolved by the high-resolution crystal structure analysis [10]. The Mn4CaO5 can be recognized as a nano-sized Mn–Ca 3

TRPLSC-1310; No. of Pages 10

Review oxido cluster (Figure 1B) embedded in a huge protein environment (10.5 3 20.5 3 11.0 nm3 for cyanobacterial PSII dimers [6,7]) in which three Mn and one Ca2+ ion occupy four corners of a cubane-like structure and four oxygen atoms form the other four corners. As shown in Figure 1B, the remaining Mn (Mn4) is connected to two Mn ions (Mn1 and Mn3) inside the cubane structure by two oxygen atoms, O4 and O5 [7,10]. Also, the interatomic bond lengths in the Mn3CaO4 cubane are not regular, making the cluster distorted and asymmetric. The ligands around the Mn ions can act to stabilize the oxidation states of Mn(III) and Mn(IV). Probing with intense femtosecond X-ray pulses of microcrystals of PSII at room temperature has shown that an oxidation state of Mn2(III)Mn2(IV) exists for the S1 state [24], which is in agreement with many previous studies (for a review see [16]). The S4 states have been mostly elusive and may be Mn3(IV)Mn(V) or Mn4(IV)(O) [16]. Multifrequency multidimensional magnetic resonance spectroscopy showed that all four Mn ions of the WOC are structurally and electronically similar immediately before the oxygen evolution step, where all Mn ions have oxidation states of Mn(IV) and an octahedral local geometry, which may have important consequences for the water-splitting mechanism [32]. The details of ligand structures and their bond distances with the metal ions were determined from ˚ structure, which showed that each Mn ion has the 1.9-A six and the Ca2+ ion has seven direct ligands [10]. These ligands include two monodentate ligands – D1-His332 and D1-Glu189 – and five carboxylate bidentate ligands – D1Asp170, D1-Glu333, D1-Asp342, D1-Ala344, and CP43Glu354. Water and oxo bridges are other direct ligands that provide a saturating ligand environment for the Mn4CaO5 cluster. Moreover, D1-Asp61, D1-His337, and CP43-Arg357 served as indirect ligands in the second coordination domain to form hydrogen bonds with the oxo bridges directly or indirectly [7,10]. The structural coupling of CP43-Arg357 with the Mn4Ca cluster was discerned with the aid of isotopeedited Fourier transform infrared (FTIR) spectroscopy and selective isotope labeling of Arg side chains [5,36]. The observation of strong coupling between Arg and the Mn4Ca cluster has led to the proposal that Arg is a key factor in the O2-evolving reaction by serving as a proton acceptor [5,36]. Although the Mn ions within the Mn4CaO5 cluster can undergo redox changes, the Ca2+ ion cannot, and various studies have been conducted to examine the function of the Ca2+ ion in water oxidation [6,16], since the Ca2+ is necessary for water oxidation. Based on studies on the effects of Ca2+/Sr2+ exchange by pulse electron paramagnetic resonance (EPR) spectroscopy, two functions can be considered for Ca2+ [17] (see [5,16] for reviews). First, its connection with tyrosine (Yz) in a hydrogen bond network helps to constrain the structure and ensure fast proton transfer. Second, Ca2+ may be involved in the transference of one water molecule to its catalytic site or may bind one of the substrate water molecules for O–O bond formation. Changes in peptide carbonyl frequencies caused by electrostatic alterations and the substitution of Ca2+ by Sr2+ monitored by FTIR spectroscopy also suggested that Ca2+ is responsible for the regulation of the electrostatic environment of the WOC hydrogen bond network surrounding the WOC [5,11,18,37–40]. 4

Trends in Plant Science xxx xxxx, Vol. xxx, No. x

Water molecules and the water-oxidation mechanism The high-resolution crystal structure showed that only four water molecules (W1–W4) are linked to the Mn4CaO5 cluster [7,10], among which two are coordinated to Mn4 (W1, W2) and the other two coordinate to the Ca2+ ion (W3, W4) (Figure 1B). It is these water molecules and the oxo bridges O4 and O5, which connect the outer Mn4 to the cuboidal unit, that have been proposed as possible substrates for the water-oxidation reaction (Figure 2). Mass spectrometry with injection of labeled heavy water (H218O) have been crucial in deciphering the exchange of substrates during the cycle of S states and these are nearing total resolution of the reaction mechanism [5,26] The results can be summarized as follows. (i) Water exchange occurs in all S states. (ii) There are two kinetic phases; ergo, the two waters bind at different chemical sites. (iii) One phase is seen in all S states, so one of the waters is bound in all S states. The second water is likely to bind later (in line with spectroscopic results; i.e., 17O electron electron double-resonance-detected NMR spectroscopy [26], FTIR [41], EPR [42], and EXAFS [43]). (iv) The exchange rates are S state-dependent, suggesting that they represent waters/oxygens bound to Mn ions. (v) The slow exchange rate is also perturbed by Ca/Sr exchange [44]. (vi) The assignments generally agree with comparisons with model systems [25,45,46]. (vii) The exchange rates are typically considered too fast for the existence of an m-oxo bridge, based on comparison with model complex data [45,46] and catalase data [25]. (viii) The exchange rates also seem too slow for ligands of Ca2+. For robust assignments of the sites of substrate water binding, similar experiments have been attempted spectroscopically. H217O and 2H2O labeling, in combination with high-field EPR spectroscopy, has been applied for the detection of water binding to the Mn4O5Ca cluster in the S2 state [26]. The results showed three discernible classes of 17O nuclei: (i) one m-oxo bridge; (ii) a terminal Mn OH/OH2 ligand; and (iii) Mn/Ca H2O ligands. In situ perturbation experiments, where the Ca2+ ion was replaced with Sr2+ [47,48] and the displacement of NH3 by W1 and O5 was assigned as the exchangeable bridge [49], the results showed that all ‘waters’, including the moxo bridge, were exchanged within 15 s. It can be concluded that all exchangeable sites could serve as a bound substrate in the S1 state. The observation of small 1H/2H couplings in the ENDOR experiments may prove that all m-oxo bridges of the Mn4O5Ca cluster are deprotonated in the S2 state [26]. Theoretical analysis of the water exchange in the S1, S2, and S3 states showed a rational exchange rate for a water molecule bound to a Mn(III) center [27]. The factor required for the exchange to occur was clarified as being a reduction of Mn3 to a Mn(III) state to release the oxygen bond. Time-dependent mass spectrometry studies further reduced the possibilities for the reaction pathways of photosynthetic water splitting and presented a basis for

TRPLSC-1310; No. of Pages 10

Review

Trends in Plant Science xxx xxxx, Vol. xxx, No. x

S2 (A)

S4

Ws = W3

W4

2e– 2H+

O1 Wf = W2

D1

D1 Mnv=O

C2

O5

C2

W1 A4

A4

B3

O4

B3

(I) (B)

W4 W3 O1

Ws = W2

Mnv=O

D1

C2

O5

Wf = W1

2e– 2H+

A4 O4

D1

C2 A4 B3

B3

(C) W4 W3

Wf

O1 (II)

D1

D1

W2

Ws C2

O5

2e– 2H+

W1 A4

C2 B3

A4

B3 O4

Key:

55Mn 40Ca

16O

17O

(exchangable, non substrate)

1H

17O

(exchangable, substrate) TRENDS in Plant Science

Figure 2. (A–C) Possible catalytic pathways of O O bond formation, consistent with the recent crystal structure of Jian-Ren Shen and his group [10] and the substrate exchange data presented here. Both class I (nucleophilic attack) and class II (oxo/oxyl radical coupling) are shown. The structure on the left represents the S2 state probed by electron paramagnetic resonance (EPR) spectroscopy/EDNMR. The structure on the right represents the inferred S4 structure before the O O bond formation and release. The MnA4(V)=O may equally be considered a Mn(IV)BO+ or Mn(IV)–O species [23]. Adapted, with permission, from [25]; copyright American Chemical Society.

studies of higher oxidized S states for the identification of the second, fast-exchanging substrate as well as the mechanism of the O–O bond formation [26]. The results showed that the early-binding substrate (Ws) was connected to all of the intermediate states of the WOC. Furthermore, the exchange rate of Ws was perturbed by the Ca2+/Sr2+ substitution, suggesting the coordination of Ws to the Ca2+ ion. As only O5 was joined to both Mn and Ca, and the 17OEDNMR spectral signature was disturbed by the Ca2+/Sr2+ exchange, O5 is likely to be a candidate for Ws. Finally, the O–O bond formation was suggested via coupling between O5 and: (i) the Mn4-bound W2 or Ca-bound W3; and (ii) an additional oxygen in the S3 state [26,27]. The rates of water exchange for Ws are 10, 0.02, 2, and 2 s 1 for S0, S1, S2, and S3, respectively. The fast exchange becomes kinetically resolved in the S2 state and the rates for Wf are >120, >120, and 23 for S1, S2, and S3, respectively (for a review see [50]).

In the S3 state of the WOC, there is slow substrate water exchange at a rate of 2 s 1 and fast exchange at 40 s 1 [50]. The rate of water exchange for Ws with bulk water increases 100-fold in S2 compared with S1, but no further change is observed with S3 state formation despite the known structural changes of the Mn4CaO5 cluster in this latter transition [50]. The exchange of Wf is about threefold slower in S3 than in S2 [50]. Some methods suggest that the S2-to-S3 step is not a simple oxidation of Mn ion. For example, elongation of the Mn Mn is observed for the WOC [16]. In accordance with these results, the following important molecular mechanisms for water oxidation were proposed. (i) Nucleophile–electrophile reaction. In the mechanism proposed by Pecoraro et al. [51], a terminal Mn(V)=O or Mn(IV)–oxyl radical undergoes a nucleophilic attack by a Ca2+-bound hydroxide or water ligand, 5

TRPLSC-1310; No. of Pages 10

Review forming a Mn-bound hydroperoxide [51,52] (see Figure 2A). (ii) The coupling of two terminal water/hydroxo ligands (W1 and W2) on Mn4. This mechanism was proposed by Kusunoki [53] (see Figure 2B). (iii) Coupling of O5 and a Ca- or Mn-bound OH/H2O. The long distances between the O5 atom and the metal ions of the cluster have been interpreted as suggesting that O5 may be one of the substrates for dioxygen formation [7] (Figure 2C). An important question is whether the water exchange occurs immediately before the O–O bond formation. It has been found that, in the transient S3Yz state, the water exchange is arrested [30]. From this result, the fast-exchanging water (Wf) was assigned to be W2. Together with the work above, these measurements support an O–O bond reaction between O5 or W2 (Ws) [31]. Finally, the results of time-resolved serial crystallography of PSII using a femtosecond X-ray laser showed that the WOC undergoes significant conformational changes during the water-oxidation reaction [31], which includes an elongation of the metal cluster accompanied by changes in the protein environment. In addition, the binding of a second substrate water molecule between the more distant protruding Mn has been proposed [31]. Taken together, these results hold the promise that the mechanism of water splitting in oxygenic photosynthesis will be resolved beyond doubt within the next year or two. Artificial photosynthesis Artificial photosynthesis is a general term covering all strategies to mimic the photosynthetic process, especially to provide a solar-based sustainable energy supply in the future (Figure 3A,B) [54–61]. Because most sustainable energy sources are intermittent and fluctuating, it is necessary to find a device or chemical to store the energy. In an artificial photosynthetic system, the following components are necessary [54–61]: (i) a compound to efficiently absorb photons from sunlight; (ii) the formation of a charge-separated state in an appropriated compound; (iii) compounds to transfer electrons to a reducing or oxidizing catalyst; (iv) substrates to be oxidized and reduced. Among the various compounds used to store energy, hydrogen is promising because it is highly efficient and clean [54–61]. However, water-oxidizing catalyst is usually a bottleneck for water splitting [54–61]. Numerous efforts have been devoted to the production of H2 fuel from water (Figure 3B–F) [54,55,62]. For example, an enzymatic photoelectrochemical cell uses enzymes to generate H2 (Figure 3C) [56] and an artificial photosynthetic watersplitting cell uses various compounds to split water into H2 and O2 using strategies similar to those in natural photosynthesis (Figure 3D) [56]. Another strategy is placing PSII on an electrode that is active in water oxidation in the presence of light and potential (Figure 3E) [57]. Nocera designed an artificial leaf that is an advanced solar cell capable of splitting water into H2 and O2 with an efficiency 6

Trends in Plant Science xxx xxxx, Vol. xxx, No. x

ten times greater than that of natural photosynthesis (Figure 3F) [58]. However, currently, artificial models resembling the structure and function of the WOC with Mn compounds are rare [13]. A comparison between the resonant inelastic X-ray scattering (RIXS) spectra of the S0 and S3 states of PSII and some Mn complexes showed that changes in the RIXS spectra of PSII are weaker than those observed with the MnIV coordination complexes and Mn oxides [22], leading to the suggestion that electrons are largely delocalized over the entire cluster in the WOC. Thus, the involvement of both the Mn4CaO5 cluster and its surrounding ligands in the redox reactions was proposed since the ligands may play a role in charge balancing [22]. In addition, a series of tetra-Mn complexes of differing oxido content and oxidation state (MnII4 through MnIIIMnIV3) were synthesized to mimic the structure and function of the WOC [23]. Several auxiliary ligands can support the Mn cluster over a wide range of oxidation states, such as the active site of the WOC; however, the tendency to form strong oxo-bridge bonds causes an alteration of the coordination environment around the metal centers [23]. The recent high-resolution X-ray structure of PSII [7,11] provided new ideas to researchers for synthesizing new functional water-oxidation catalysts. Accordingly, natural photosynthesis could be simulated by the synthesis of various catalysts based on their functions, such as the absorption of light (photocatalyst), applying external oxidation potential (electrocatalyst), or using a sacrificial redox agent to provide the required electron or oxidative equivalents (Figure 3) [55]. For water oxidation, various catalysts containing tetranuclear Mn, Mn/Ca and Co clusters, Ru mono- and dinuclear complexes, and Ir mononuclear complexes have been reported [13,59,60]. Among these, Mn compounds are of particular interest because of their special properties: having particularly rich redox properties, possessing different oxidizing states, being environmentally friendly, low cost, and abundant and being successfully used in nature for water oxidation [63]. However, many Mn compounds, except for Mn oxides, are inactive in water oxidation [13]. Although Mn oxides were used as electrocatalysts in 1977 by Morita [64], these compounds and other Mn complexes introduced later were not efficient enough or applicable to energy production on an industrial scale. Based on various spectroscopic measurements, Mn oxides were proposed as true catalysts in water oxidation among many Mn complexes [65,66]. Such findings highlight the importance of nano-clusters of Mn oxide in water oxidation as naturally selected millions of years ago. Only a few Mn complexes in special conditions have been suggested as true catalysts for water oxidation [67,68], although more work is needed to prove actual water oxidation and deny the role of Mn oxide in water oxidation. A useful factor, which has been considered, is the smart engineering of the ligand environment around the metallic ion centers, as this agent is highly effective in reducing the over-potential required for the water-oxidation reaction. Several studies have also used various biomimetic systems to obtain a good water-oxidizing catalyst [13,69– 77]. The role of the Ca2+ ion in artificial photosynthesis was examined through the synthesis of CaMn2O4.xH2O,

TRPLSC-1310; No. of Pages 10

Review

Trends in Plant Science xxx xxxx, Vol. xxx, No. x

(A)

(B)

Chromophore: Dye or semiconductor Electron acceptor H2

P∗

Chromophore 2: Dye or semiconductor

Chromophore 1: Dye or semiconductor

Electron acceptor H2

P2∗

Potenal energy

P1∗ Electron donor 2H2O

2H+

Electron donor 2H2O

2H+ Redox

Light P2

Light

4H++O2

P

Light

4H++O2

(C)

P1

(D) H2

Biofuel

TiO2

O2

TiO2

P∗/P +

O OP O

H+ CB

Enzyme

hν

Fuelred

1/ NADH 2

Fuelox

P/P + 1/2NAD+

1/ H 2 2

N

H+

H2

N 2+

Ru O OP O

H2

N

N N

O

N

H2O

O O O

2H+

IrO2.nH2O O2 + 2H+

Membrane TRENDS in Plant ScienceV

e−

e−

4H+ + O2

(E)

(F)

680 nm light

H2O Protecve barrier layer

2H2O e– QA/QB

DET e–N-H N-H – – e COO

C=O

C=O

mesoITO

O Cl

Cl

COO–

MET

Co-OEC for PSII OEC

Si juncon (for photosyn membrane)

2H2

NiMoZn for Ed of PSI

O

e–

+0.5 V vs NHE

O2

4H+ TRENDS in Plant Science

Figure 3. An artificial photosynthetic system: single-step reactions (A) and two-step (Z scheme) reactions (B). P, chromophore of a single-step reaction system; P*, excited state of P; P1, first chromophore of a two-step reaction system; P1*, excited state of P1; P2, second chromophore of a two-step reaction system; P2*, excited state of P2. Schematic diagrams of an enzymatic photoelectrochemical cell (C) and an artificial photosynthetic water-splitting cell (D). Covalent immobilization of oriented photosystem II on a nanostructured electrode for a solar water-oxidation device (E). Construction of an artificial leaf. The photosynthetic membrane is replaced by a Si junction, which performs the light capture and conversion to a wireless current. The oxygen-evolving complex and ferredoxin reductase of the photosynthetic membrane are replaced by Co-OEC and NiMoZn OER and HER catalysts, respectively, to perform water splitting (F). (B) adapted, with permission, from [14]; copyright McMillan Publications. (C) and (D) adapted, with permission, from [56]. (E) adapted, with permission, from [57]. (F) adapted, with permission, from [58]; copyright American Chemical Society.

which showed good catalytic activity toward water oxidation [78]. However, the selective role of Ca2+ ions in the Mn oxide for water oxidation is a controversial issue [79,80]. The amino acids around the Mn–Ca cluster in PSII were known to be important in water oxidation, but similar organic groups around Mn oxide have not been extensively

considered by chemists. The bio-inspired simulation of residues around the Mn4CaO5 cluster has been tested by the synthesis of various layered Mn oxides/polypeptides [81]. Another design was reported in which poly-(4-vinylpyridine) (PVP) was applied as a Mn-stabilizing protein [82]. It was claimed that PVP might act as a proton 7

TRPLSC-1310; No. of Pages 10

Review

Trends in Plant Science xxx xxxx, Vol. xxx, No. x

Acve site

Acve site

Bufferic group

Proton Electrochem Biominerali management ical zaon group regulator

Chelang group

Dispersing group

Electron transfer

Bufferic group

Electrochem Proton Biominerali management ical zaon regulator group

Chelang group

TRENDS in Plant Science

Figure 4. A schematic depiction of engineered groups around catalyst particles. Such groups, as present in enzymes, can efficiently increase the catalytic activity of active sites. Adapted, with permission, from [81]; copyright Royal Society of Chemistry.

acceptor, a Mn(III) stabilizer, or an agent to reduce the over-potential and provide a buffered environment for the Mn oxide. A recent report proved that pyridine is a proton acceptor under these conditions [83]. Engineered proteins are also promising for the investigation of protein receptor binding, cofactors, biological electron transfer, and other important tasks in artificial photosynthesis [84]. The detailed knowledge of the structure and functioning of the WOC has led to efforts to prepare artificial Ca2+ and Mn complexes [85–88]. Agapie et al. synthesized a cluster containing a [Mn3CaO4]6+ core in which the three Mn centers were all in the IV oxidation state. When the [Mn3CaO4]6+ complex was converted into a tetranuclear Mn complex, this complex was found to carry only two Mn(IV) centers and the other two Mn centers were in the III oxidation state. The study of a series of tetranuclear mixed-metal complexes with three Mn centers and a redoxinactive metal center (Na+, Ca2+, Sr2+, Zn2+, or Y3+ ion) showed a linear dependence with a slope of 100 mV per pKa unit; it was observed between the Lewis acidity (pKa values) of the redox-inactive metal [86,87]. Recently, it was reported that the reaction of Bu4NMnO4, Mn(CH3CO2)2.4(H2O), and Ca(CH3CO2)2.H2O in boiling acetonitrile and in the presence of pivalic acid forms a Mn4Ca cluster very similar to the Mn–Ca cluster in the WOC [88]. Interestingly, the model, like the native cluster, can undergo four redox transitions and shows two magnetic resonance signals assignable to redox and structural isomerism. It was suggested that the fourth Mn ion determines the redox potentials and magnetic properties of the native WOC [88]. The main difference between the synthetic model and the WOC is the number of the bridged O ligands for the dangling Mn and the lack of water molecules in the synthetic model. Concluding remarks We have reviewed biological water oxidation and the only natural water-oxidizing site; namely, the WOC in PSII. This work on the complex enzymatic structure is becoming recognized as a model for artificial photosynthetic systems. 8

The challenges in artificial photosynthesis are to design and synthesize efficient, stable, and environmentally friendly compounds to absorb photons from sunlight and with this energy to form a charge-separated state, transferring electrons from an oxidized to a reduced substrate. The discovery of the ‘art’ of water oxidation by nature will open new approaches for the design of water-oxidizing catalysts, which should be efficient and stable in the harsh conditions of water oxidation. The solution that nature has provided for selecting a capable catalyst for water oxidation is using a heterogeneous catalyst via abundant and environmentally friendly ions in a nano-sized, chair-like Mn structure. Importantly, the catalyst works well under biological conditions, pH, and the appropriate oxidant and in the presence of outer bonds and channels to access the reactant and remove the products of the reaction. Under these conditions, proton-coupled electron transfer, spinflipping, redox accumulation, a four-electron water-oxidation mechanism with low over-potential, self-repair, protection from light, and regulation of oxidizing power and binding sites for water molecules are all possible. Such sites are efficient, can be easily photo-assembled under biological conditions, and will provide a rich knowledge base for the future (see Figure 4 for details). There have been many attempts to design catalysts for water oxidation with strategies that have not resembled Box 2. Outstanding questions  An outstanding question that has to be tackled initially is whether the Mn4CaO5 complex of natural photosynthesis can be constructed in an artificial system and made to split water. This is no trivial matter since the Mn4CaO5 complex has to be anchored by appropriate ligands and interconnected with a supply of light energy and a sink for protons and electrons.  Inherent to this question is whether it will be possible to construct a four-electron water-oxidation mechanism with self-repair, protection from light, regulation of oxidizing power, and binding sites for water molecules.  Will it then be possible to design systems that can utilize water splitting in combination with other features of photosynthesis to achieve the fixation of carbon dioxide or will a partial system be used to generate hydrogen?

TRPLSC-1310; No. of Pages 10

Review the photosynthetic process, but learning from natural systems (Box 2) makes sense, as these mechanisms have been successful for millions of years. Acknowledgments The authors thank Drs Nick Cox, Wolfgang Lubitz, and Susanne Brink for their helpful and valuable suggestions, discussions, comments, and corrections regarding this work. M.M.N. and M.Z.G. are grateful to the Institute for Advanced Studies in Basic Sciences and the National Elite Foundation for financial support. J-R.S. was supported by a grant-in-aid for Specially Promoted Research No. 24000018 from JSPS, MEXT, Japan, and S.I.A. was supported by a grant from the Russian Science Foundation (no. 14-14-00039).

References 1 Cardona, T. et al. (2015) Origin and evolution of water oxidation before the last common ancestor of the cyanobacteria. Mol. Biol. Evol. 32, 1310–1328 2 Blankenship, R.E. (2013) Molecular Mechanisms of Photosynthesis, p. 336, John Wiley & Sons 3 Summons, R.E. et al. (1999) 2-Methylhopanoids as biomarkers for cyanobacterial oxygenic photosynthesis. Nature 400, 554–557 4 Konhauser, K.O. et al. (2011) Aerobic bacterial pyrite oxidation and acid rock drainage during the great oxidation event. Nature 478, 369–373 5 McEvoy, J.P. and Brudvig, G.W. (2006) Water-splitting chemistry of photosystem II. Chem. Rev. 106, 4455–4483 6 Ferreira, K.N. et al. (2004) Architecture of the photosynthetic oxygenevolving center. Science 303, 1831–1838 7 Umena, Y. et al. (2011) Crystal structure of oxygen-evolving ˚ . Nature 473, 55–60 photosystem II at a resolution of 1.9 A ˚ 8 Guskov, A. et al. (2009) Cyanobacterial photosystem II at 2.9-A resolution and the role of quinones, lipids, channels and chloride. Nat. Struct. Mol. Biol. 16, 334–342 9 Kamiya, N. and Shen, J.-R. (2003) Crystal structure of oxygen-evolving ˚ photosystem II from Thermosynechococcus vulcanus at 3.7-A resolution. Proc. Natl. Acad. Sci. U.S.A. 100, 98–103 ˚ 10 Suga, M. et al. (2015) Native structure of photosystem II at 1.95 A resolution viewed by femtosecond X-ray pulses. Nature 517, 99–103 11 Jordan, P. et al. (2011) Three-dimensional structure of cyanobacterial ˚ resolution. Nature 411, 909–917 photosystem I at 2.5 A 12 Kanan, M.W. and Nocera, D.G. (2008) In situ formation of an oxygenevolving catalyst in neutral water containing phosphate and Co2+. Science 321, 1072–1075 13 Liu, L. and Wang, F. (2012) Transition metal complexes that catalyze oxygen formation from water: 1979–2010. Coord. Chem. Rev. 256, 1115–1136 14 Tachibana, Y. et al. (2013) Artificial photosynthesis for solar watersplitting. Nat. Photon. 6, 511–518 15 Ruttinger, W. and Dismukes, G.C. (1997) Synthetic water oxidation catalysts for artificial photosynthetic water oxidation. Chem. Rev. 97, 1–24 16 Yano, J. and Yachandra, V. (2014) Mn4Ca cluster in photosynthesis: where and how water is oxidized to dioxygen. Chem. Rev. 114, 4175–4205 17 Rappaport, F. et al. (2011) Ca determines the entropy changes associated with the formation of transition states during water oxidation by photosystem II. Energy Environ. Sci. 4, 2520–2524 18 Polander, B.C. and Barry, B.A. (2013) Ca and the hydrogen-bonded water network in the photosynthetic oxygen-evolving complex. J. Phys. Chem. Lett. 4, 786–791 19 Hirahara, M. et al. (2014) Artificial manganese center models for photosynthetic oxygen evolution in photosystem II. Eur. J. Inorg. Chem. 2014, 595–606 20 Mukherjee, S. et al. (2012) Comproportionation reactions to Mn (III/IV) pivalate clusters: a new half-integer spin single-molecule magnet. Inorg. Chem. 52, 873–884 21 Krewald, V. et al. (2013) On the magnetic and spectroscopic properties of high-valent Mn3CaO4 cubanes as structural units of natural and artificial water-oxidizing catalysts. J. Am. Chem. Soc. 135, 5726–5739

Trends in Plant Science xxx xxxx, Vol. xxx, No. x

22 Glatzel, P. et al. (2013) Electronic structural changes of Mn in the oxygen-evolving complex of photosystem II during the catalytic cycle. Inorg. Chem. 52, 5642–5644 23 Kanady, J.S. et al. (2013) Role of oxido incorporation and ligand lability in expanding redox accessibility of structurally related Mn4 clusters. Chem. Sci. 4, 3986–3996 24 Kern, J. et al. (2013) Simultaneous femtosecond X-ray spectroscopy and diffraction of photosystem II at room temperature. Science 340, 491–495 25 McConnell, I.L. et al. (2012) EPR–ENDOR characterization of (17O, 1H, 2 H) water in Mn catalase and its relevance to the oxygen-evolving complex of photosystem II. J. Am. Chem. Soc. 134, 1504–1512 26 Rapatskiy, L. et al. (2012) Detection of the water-binding sites of the oxygen-evolving complex of photosystem II using W-band 17O electronelectron double resonance-detected NMR spectroscopy. J. Am. Chem. Soc. 134, 16619–16634 27 Siegbahn, P.E. (2012) Mechanisms for proton release during water oxidation in the S2 to S3 and S3 to S4 transitions in photosystem II. Phys. Chem. Chem. Phys. 14, 4849–4856 28 Lohmiller, T. et al. (2014) Structure, ligands and substrate coordination of the oxygen-evolving complex of photosystem II in the S2 state: a combined EPR and DFT study. Phys. Chem. Chem. Phys. 16, 11877–11892 29 Koua, F.H. et al. (2013) Structure of Sr-substituted photosystem II at ˚ resolution and its implications in the mechanism of water 2.1 A oxidation. Proc. Natl. Acad. Sci. U.S.A. 110, 3889–3894 30 Nilsson, H. et al. (2014) Substrate–water exchange in photosystem II is arrested before dioxygen formation. Nat. Commun. 5, 4305 31 Kupitz, C. et al. (2014) Serial time-resolved crystallography of photosystem II using a femtosecond X-ray laser. Nature 513, 261–265 32 Cox, N. et al. (2014) Electronic structure of the oxygen-evolving complex in photosystem II prior to O–O bond formation. Science 345, 804–808 33 Brandon, C. et al. (2013) Calcium, strontium, and protein dynamics during the S2 to S3 transition in the photosynthetic oxygen-evolving cycle. J. Phys. Chem. Lett. 4, 3356–3362 ˚ crystal structure of 34 Gatt, P.P. et al. (2012) Rationalizing the 1.9 A photosystem II—a remarkable Jahn–Teller balancing act induced by a single proton transfer. Angew. Chem. Int. Ed. Engl. 51, 12025–12028 35 Kolling, D.R.J. et al. (2012) What are the oxidation states of manganese required to catalyze photosyntheticwater oxidation? Biophys. J. 103, 313–322 36 Shimada, Y. et al. (2011) Structural coupling of an arginine side chain with the oxygen-evolving Mn4Ca cluster in photosystem II as revealed by isotope-edited Fourier transform infrared spectroscopy. J. Am. Chem. Soc. 133, 3808–3811 37 Kawakami, K. et al. (2009) Location of chloride and its possible functions in oxygen-evolving photosystem II revealed by X-ray crystallography. Proc. Natl. Acad. Sci. U.S.A. 106, 8567–8572 38 Rivalta, I. et al. (2011) Structural–functional role of chloride in photosystem II. Biochemistry 50, 6312–6315 39 Boussac, A. et al. (2012) Probing the role of chloride in photosystem II from Thermosynechococcus elongatus by exchanging chloride for iodide. Biochim. Biophys. Acta 1817, 802–810 40 Yadav, D.K. and Pospı´sˇil, P. (2012) Role of chloride ion in hydroxyl radical production in photosystem II under heat stress: electron paramagnetic resonance spin-trapping study. J. Bioenerg. Biomembr. 44, 365–372 41 Noguchi, T. and Sugiura, M. (2002) FTIR detection of water reactions during the flash-induced S-state cycle of the photosynthetic wateroxidizing complex. Biochemistry 41, 15706–15712 42 Britt, R.D. et al. (2004) Recent pulsed EPR studies of the photosystem II oxygen-evolving complex: implications as to water oxidation mechanisms. Biochim. Biophys. Acta 1655, 158–171 43 Dau, H. et al. (2008) On the structure of the manganese complex of photosystem II: extended-range EXAFS data and specific atomicresolution models for four S-states. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 363, 1237–1244 44 Hendry, G. and Wydrzynski, T. (2003) 18O isotope exchange measurements reveal that calcium is involved in the binding of one substrate-water molecule to the oxygen-evolving complex in photosystem II. Biochemistry 42, 6209–6217

9

TRPLSC-1310; No. of Pages 10

Review 45 Tagore, R. et al. (2006) Determination of m-oxo exchange rates in di-moxo dimanganese complexes by electrospray ionization mass spectrometry. J. Am. Chem. Soc. 128, 9457–9465 46 Najafpour, M.M. et al. (2014) Water exchange rate in manganese-based water-oxidizing catalysts in photosynthetic systems: from the wateroxidizing complex in photosystem II to nano-sized manganese oxides. Biochim. Biophys. Acta 1837, 1395–1410 47 Boussac, A. et al. (2004) Biosynthetic Ca2+/Sr2+ exchange in the photosystem II oxygen-evolving enzyme of Thermosynechococcus elongatus. J. Biol. Chem. 279, 22809–22819 48 Krewald, V. et al. (2015) Metal oxidation states in biological water splitting. Chem. Sci. 6, 1676–1695 49 Navarro, M.P. et al. (2013) Ammonia binding to the oxygen-evolving complex of photosystem II identifies the solvent-exchangeable oxygen bridge (m-oxo) of the manganese tetramer. Proc. Natl. Acad. Sci. U.S.A. 110, 15561–15566 50 Cox, N. and Messinger, J. (2013) Reflections on substrate water and dioxygen formation. Biochim. Biophys. Acta 1827, 1020–1030 51 Pecoraro, V.L. et al. (1998) A proposal for water oxidation in photosystem II. Pure Appl. Chem. 70, 925–929 52 Limburg, J. et al. (1999) A mechanistic and structural model for the formation and reactivity of a MnV=O species in photosynthetic water oxidation. J. Chem. Soc. Dalton Trans. 1353–1362 53 Kusunoki, M. (2007) Mono-manganese mechanism of the photosystem II water splitting reaction by a unique Mn4Ca cluster. Biochim. Biophys. Acta 1767, 484–492 54 Faunce, T. et al. (2013) Artificial photosynthesis as a frontier technology for energy sustainability. Energy Environ. Sci. 6, 1074–1076 55 Berardi, S. et al. (2014) Molecular artificial photosynthesis. Chem. Soc. Rev. 43, 7501–7519 56 Gust, D. et al. (2009) Solar fuels via artificial photosynthesis. Acc. Chem. Res. 42, 1890–1898 57 Kato, M. et al. (2013) Covalent immobilization of oriented photosystem II on a nanostructured electrode for solar water oxidation. J. Am. Chem. Soc. 135, 10610–10613 58 Nocera, D.G. (2012) The artificial leaf. Acc. Chem. Res. 45, 767–776 59 Du, P. and Eisenberg, R. (2012) Catalysts made of Earth-abundant elements (Co, Ni, Fe) for water splitting: recent progress and future challenges. Energy Environ. Sci. 5, 6012–6021 60 Tran, P.D. et al. (2012) Recent advances in hybrid photocatalysts for solar fuel production. Energy Environ. Sci. 5, 5902–5918 61 Ka¨rka¨s, D.M. et al. (2014) Artificial photosynthesis: molecular systems for catalytic water oxidation. Chem. Rev. 114, 11863–12001 62 Karunadasa, H.I. et al. (2012) A molecular MoS2 edge site mimic for catalytic hydrogen generation. Science 335, 698–702 63 Armstrong, F.A. (2008) Why did nature choose Mn to make oxygen? Philos. Trans. R. Soc. Lond. B: Biol. Sci. 363, 1263–1270 64 Morita, M. et al. (1977) The anodic characteristics of Mn dioxide electrodes prepared by thermal decomposition of Mn nitrate. Electrochim. Acta 22, 325–328 65 Hocking, R.K. (2011) Water-oxidation catalysis by Mn in a geochemical-like cycle. Nat. Chem. 3, 461–466 66 Najafpour, M.M. et al. (2014) Fragments of layered Mn oxide are the real water oxidation catalyst after transformation of molecular precursor on clay. J. Am. Chem. Soc. 136, 7245–7248 67 Karlsson, E.A. et al. (2011) Photosensitized water oxidation by use of a bioinspired Mn catalyst. Angew. Chem. Int. Ed. Engl. 123, 11919–11922 68 Limburg, J. et al. (1999) A functional model for O–O bond formation by the O2-evolving complex in photosystem II. Science 283, 1524–1527

10

Trends in Plant Science xxx xxxx, Vol. xxx, No. x

69 Ruettinger, W.F. et al. (1997) Synthesis and characterization of Mn4O4L6 complexes with cubane-like core structure: a new class of models of the active site of the photosynthetic water oxidase. J. Am. Chem. Soc. 119, 6670–6671 70 Liu, R. et al. (2011) Water splitting by tungsten oxide prepared by atomic layer deposition and decorated with an oxygen evolving catalyst. Angew. Chem. Int. Ed. Engl. 50, 499–502 71 Lee, W.T. et al. (2014) Ligand modification transforms a catalase mimic into a water oxidation catalyst. Angew. Chem. Int. Ed. Engl. 53, 9856–9859 72 Efrati, A. et al. (2013) Cytochrome c-coupled photosystem I and photosystem II (PSI/PSII) photo-bioelectrochemical cells. Energy Environ. Sci. 6, 2950–2956 73 Kato, M. et al. (2012) Photoelectrochemical water oxidation with photosystem II integrated in a mesoporous indium–tin oxide electrode. J. Am. Chem. Soc. 134, 8332–8335 74 Pita, M. et al. (2014) Bioelectrochemical oxidation of water. J. Am. Chem. Soc. 136, 5892–5895 75 Kato, M. et al. (2014) Protein film photoelectrochemistry of the water oxidation enzyme photosystem II. Chem. Soc. Rev. 43, 6485–6497 76 Kothe, T. et al. (2013) Combination of a photosystem I-based photocathode and a photosystem II-based photoanode to a Z-scheme mimic for biophotovoltaic applications. Angew. Chem. Int. Ed. Engl. 52, 14233–14236 77 Yehezkeli, O. et al. (2012) Integrated photosystem II-based photobioelectrochemical cells. Nat. Commun. 3, 742 78 Najafpour, M.M. et al. (2010) CaMn (III) oxides (CaMn2O4
xH2O) as biomimetic oxygen-evolving catalysts. Angew. Chem. Int. Ed. Engl. 49, 2233–2237 79 Wiechen, M. et al. (2012) Layered Mn oxides for water-oxidation: alkaline earth cations influence catalytic activity in a photosystem II-like fashion. Chem. Sci. 3, 2330–2339 80 Najafpour, M.M. et al. (2015) Comparison of nano-sized Mn oxides with the Mn cluster of photosystem II as catalysts for water oxidation. Biochim. Biophys. Acta 1847, 294–306 81 Najafpour, M.M. et al. (2015) An engineered polypeptide around nanosized manganese–calcium oxide: copying plants for water oxidation. Dalton Trans. Published online May 28, 2015. http://dx.doi.org/10. 1039/C5DT01443C 82 Najafpour, M.M. et al. (2013) Nanolayered manganese oxide/poly (4vinylpyridine) as a biomimetic and very efficient water oxidizing catalyst: toward an artificial enzyme in artificial photosynthesis. Chem. Commun. 49, 8824–8826 83 Yamaguchi, A. et al. (2014) Regulating proton-coupled electron transfer for efficient water splitting by Mn oxides at neutral pH. Nat. Commun. 5, 4256 84 Hingorani, K. et al. (2014) Photo-oxidation of tyrosine in a bioengineered bacterioferritin ‘reaction centre’ – a protein model for artificial photosynthesis. Biochim. Biophys. Acta 1837, 1821–1834 85 Mukherjee, S. et al. (2012) Synthetic model of the asymmetric [Mn3CaO4] cubane core of the oxygen-evolving complex of photosystem II. Proc. Natl. Acad. Sci. U.S.A. 109, 2257–2262 86 Tsui, E.Y. et al. (2013) Redox-inactive metals modulate the reduction potential in heterometallic manganese–oxido clusters. Nat. Chem. 5, 293–299 87 Herbert, D.E. (2013) Heterometallic triiron-oxo/hydroxo clusters: effect of redox-inactive metals. J. Am. Chem. Soc. 135, 19075–19078 88 Zhang, C. et al. (2015) A synthetic Mn4Ca-cluster mimicking the oxygen-evolving center of photosynthesis. Science 348, 690–693