REGULAR PAPER

Imidazolium or guanidinium/layered manganese (III, IV) oxidehybrid as a promising structural model for the water-oxidizingcomplex of Photosystem II for artificial photosynthetic systems

Mohammad Mahdi Najafpour • Mahmoud Amouzadeh Tabrizi •

Behzad Haghighi • Julian J. Eaton-Rye • Robert Carpentier •

Suleyman I. Allakhverdiev

Received: 19 December 2012 / Accepted: 14 March 2013 / Published online: 31 March 2013

� Springer Science+Business Media Dordrecht 2013

Abstract Photosystem II is responsible for the light-dri-

ven biological water-splitting system in oxygenic photo-

synthesis and contains a cluster of one calcium and four

manganese ions at its water-oxidizing complex. This cluster

may serve as a model for the design of artificial or biomi-

metic systems capable of splitting water into oxygen and

hydrogen. In this study, we consider the ability of manga-

nese oxide monosheets to self-assemble with organic

compounds. Layered structures of manganese oxide,

including guanidinium and imidazolium groups, were syn-

thesized and characterized by scanning electron micros-

copy, transmission electron microscopy, X-ray diffraction

spectrometry, and atomic absorption spectroscopy. The

compounds can be considered as new structural models for

the water-oxidizing complex of Photosystem II. The

overvoltage of water oxidation for the compounds in these

conditions at pH = 6.3 is *0.6 V. These compounds may

represent the first step to synthesize a hybrid of guanidinium

or imidazole together with manganese as a biomimetic

system for the water-oxidizing complex of Photosystem II.

Keywords Artificial photosynthesis � Photosystem II �Manganese � Nano-layered manganese oxide �Imidazolium � Guanidinium

Introduction

Interest in developing a hydrogen-energy-based economy is

on the rise to counter the extensive reliance on depleting

fossil fuel reserves (Lewis and Nocera 2006; Balzani et al.

2008; Daniel and Alessandro 2008; Allakhverdiev et al.

2009a, b; Allakhverdiev et al. 2010; Allakhverdiev 2012).

Hydrogen is an important energy carrier that offers theElectronic supplementary material The online version of thisarticle (doi:10.1007/s11120-013-9814-5) contains supplementarymaterial, which is available to authorized users.

M. M. Najafpour (&) � M. A. Tabrizi � B. Haghighi

Department of Chemistry, Institute for Advanced Studies in

Basic Sciences (IASBS), 45137-66731 Zanjan, Iran

e-mail: mmnajafpour@iasbs.ac.ir

M. M. Najafpour � B. Haghighi

Center of Climate Change and Global Warming, Institute for

Advanced Studies in Basic Sciences (IASBS), 45137-66731

Zanjan, Iran

J. J. Eaton-Rye

Department of Biochemistry, University of Otago, P.O. Box 56,

Dunedin 9054, New Zealand

R. Carpentier

Groupe de Recherche En Biologie Vegetale (GRBV), Universite

du Quebec a Trois-Rivieres, C.P. 500, Trois-Rivieres,

QC G9A 5H7, Canada

S. I. Allakhverdiev (&)

Controlled Photobiosynthesis Laboratory, Institute of Plant

Physiology, Russian Academy of Sciences, Botanicheskaya

Street 35, Moscow 127276, Russia

e-mail: suleyman.allakhverdiev@gmail.com

S. I. Allakhverdiev

Institute of Basic Biological Problems, Russian Academy of

Sciences, Pushchino, Moscow 142290, Russia

123

Photosynth Res (2013) 117:413–421

DOI 10.1007/s11120-013-9814-5

advantage of clean and complete conversion to water (Daniel

and Alessandro 2008; Kanan and Nocera 2008; Allakhver-

diev et al. 2009a, b; Allakhverdiev et al. 2010; Allakhverdiev

2012). Currently, the main production of hydrogen comes

from steam reforming of natural gas, consuming natural

resources, and generating carbon dioxide as an undesired

byproduct (Heinzel et al. 2002). Central to the success of

hydrogen technology is the efficient generation of the com-

pound from a renewable energy source such as solar-pow-

ered cells (Alexander et al. 2008) or water splitting by

electrolysis (Kanan and Nocera 2008). Hence, chemical and

biological production of hydrogen using artificial photo-

synthetic systems has received increasing attention in the

literature (Kanan and Nocera 2008; Allakhverdiev et al.

2009a, b; Allakhverdiev et al. 2010). The development of

artificial photosynthetic systems for hydrogen generation

from water splitting using solar energy—that may be the best

solution not only to face the problem of depletion of fossil

fuels but also global warming—depends on the availability

of an efficient, environmentally friendly, robust, and cheap

catalyst for water oxidation (Daniel and Alessandro 2008;

Kanan and Nocera 2008; Allakhverdiev et al. 2009a, b;

Allakhverdiev et al. 2010; Allakhverdiev 2012; Najafpour

and Allakhverdiev 2012).

Various biomimetic approaches to artificial photosyn-

thesis were designed for the photo-catalytic oxidation of

water to produce hydrogen and oxygen (Bockris 1977; Ka-

nan and Nocera 2008; Najafpour and Allakhverdiev 2012;

Wiechen et al. 2012). Many metal catalysts were employed

for water splitting (Liu and Wang 2012). Although the

mechanism of light-driven activity of these metal catalysts is

not fully known, the studies so far conducted have helped to

understand the natural enzyme and provided hints to further

improve the design of a suitable catalyst. The development of

super anode materials for photoelectrochemical or electrol-

ysis reactors has become one of the foremost challenges in

the development of a solar hydrogen economy (Bockris

1977). In particular, effectiveness and stability of the anodes

are the key factors for hydrogen generation (Bockris 1977).

In Nature, the water-oxidizing complex (WOC) of Photo-

system II (PSII) is the only system to catalyze water oxidation

(Zouni et al. 2001; Kamiya and Shen 2003; Ferreira et al. 2004;

Najafpour 2006; Kawakami et al. 2011; Umena et al. 2011;

Najafpour et al. 2012b;). The first structures of PSII were from

the research groups of H.T. Witt and W. Saenger (Zouni et al.

2001) followed by N. Kamiya and J.-R. Shen (Kamiya and

Shen 2003). In 2004, J. Barber and S. Iwata provided a rather

complete structure of PSII (Ferreira et al. 2004). They showed

that the WOC is an Mn3Ca-cubic cluster with the fourth

‘‘dangling’’ Mn off to the side (Ferreira et al. 2004). In 2011,

J.-R. Shen and N. Kamiya and co-workers significantly

improved the resolution of the PSII crystals from the ther-

mophilic cyanobacterium Thermosynechococcus vulcanus

(T. vulcanus) down to a high resolution of 1.9 A (Kawakami

et al. 2011; Umena et al. 2011). This improvement showed that

in the structure, five oxygen atoms serve as oxo bridges linking

the five metal ions (one calcium and four manganese ions)

(Kawakami et al. 2011; Umena et al. 2011) (Fig. 1). Four

terminal water ligands were found whereby two of them

coordinated to Ca and two to the dangling Mn (Mn(4)). The

structure is thus a manganese–calcium cluster that could be

described as a Mn4CaO5(H2O)4 complex. The four manganese

atoms are coordinated by carboxylates or imidazole groups

from amino acids, and bridging oxido ligands.

Other organic groups from amino acid side-chains are

also around the WOC (Kawakami et al. 2011; Umena et al.

2011) (Fig. 1).

Recently, there has been a major research effort into the

synthesis of various manganese complexes aimed at sim-

ulating the WOC of PSII (Ruttinger and Dismukes 1997;

Sproviero et al. 2008; Hou 2010; Beckmann et al. 2008;

Cady et al. 2008; Najafpour and Allakhverdiev 2012; Na-

jafpour et al. 2012a, b); however, an efficient water-oxi-

dation catalyst could not be found among these manganese

complexes. Nevertheless, a number of other groups have

studied manganese oxides as heterogeneous catalysts for

water oxidation (for a review see Najafpour et al. 2012a).

In a different approach, it was shown that layered manga-

nese oxides are efficient catalysts for water oxidation (Na-

jafpour et al. 2010; Zaharieva et al. 2011). These readily

synthesized oxide layers (Najafpour et al. 2010; Najafpour

2011; Zaharieva et al. 2011) have also been introduced as the

closest structural and functional analogs to the WOC in PSII

found so far (Zaharieva et al. 2011). However, PSII has amino

acid side-chains to stabilize manganese oxides or transfer

protons, oxygen, or water but manganese oxides contain no

groups to perform these tasks. It has also been reported that in

synthetic model complexes for hydrolytic enzymes, the

positioning of groups similar to guanidinium can lead to more

than a 1,000-fold increase in reactivity (Kirin et al. 2006). For

example, it has been reported that guanidinium groups

increased the efficiency of a zinc catalyst more than 3,000-

fold, compared with unfunctionalized analogs (Kirin et al.

2006). In this study, we have synthesized layered structures of

manganese oxide, including both guanidinium and imidazo-

lium groups, and both structure and functionality have been

studied. These aggregated monosheets can be considered as

new structural models for the WOC of PSII.

Experimental

Materials and methods

All reagents and solvents were purchased from commercial

sources and were used without further purification. Mid

414 Photosynth Res (2013) 117:413–421

123

infrared (MIR) spectra of KBr pellets of compounds were

recorded on a Bruker vector 22 in the range between 400

and 4,000 cm-1. Transmission electron microscopy (TEM)

and scanning electron microscopy (SEM) were carried out

with Philips CM120 and LEO 1430VP microscopes,

respectively. The X-ray powder patterns were recorded

with a Bruker, D8 ADVANCE diffractometer (Cu-Karadiation). Manganese atomic absorption spectroscopy

(AAS) was performed on a Varian Spectra AA 110 atomic

absorption spectrometer. Prior to analysis, the oxides

(10.0 mg metal) were added to 1 mL of concentrated nitric

acid and H2O2, and then left at room temperature for at

least 1 h to ensure that the oxides were completely dissolved.

The solutions were then diluted to 25.0 mL and analyzed

by AAS. Cyclic voltammetry (CV) and amperometric

studies were performed using an Autolab potentiostat–

galvanostat model PGSTAT30 (Utrecht, The Netherlands).

In this case, a conventional three electrode set-up was used

in which a Pt electrode or Pt electrode modified with nano

manganese oxide, an Ag|AgCl|KClsat electrode, and a

platinum rod served as the working, reference, and auxil-

iary electrodes, respectively. The working potential was

applied in the standard way using the potentiostat and the

output signal was acquired by Autolab Nova software.

Synthesis

To synthesize the structural model compounds for the

WOC of PSII, manganese oxide monosheets were synthe-

sized with a very simple method from reacting MnCl2 and

H2O2 in the presence of tetramethyl ammonium (TMA)

hydroxide (Kai et al. 2008): 20.0 mL of a mixed aqueous

solution of TMA hydroxide (0.6 M) and 3.0 wt% H2O2

was added to 10 mL of 0.3 M MnCl2�4H2O aqueous

solution. The resulting dark brown suspension was stirred

vigorously overnight in the open air at room temperature.

Dried aggregate was separated by filtration (Millipore,

type-JH, 0.45 lm pore size), washed with copious amounts

of distilled water, and then air-dried at room temperature.

The manganese (III, IV) oxide monosheets, similar to other

monosheets, could aggregate to form layered structures

with cationic organic and inorganic compounds (Kai et al.

2008). Manganese oxide monosheets were also prepared in

the presence of imidazole (compound 1) or guanidinium

(compound 2). For synthesizing compound 1 (1), imidazole

(1.5 g, 22.0 mmol at pH *6 using glacial acetic acid) was

dissolved in 10 mL water and the solution was added to

50 mL of the colloidal suspension of MnO2 monosheets

(4 mM) during argon bubbling at room temperature.

Immediately after the addition, flocculation occurred in the

mixed solution. pH *6 is important as at higher pH,

imidazole is not in the protonated form and at lower pH,

H3O? may be incorporated between manganese layers

instead of imidazolium. The resulting brown precipitate

was filtered off, washed with distilled water, and air-dried

at room temperature. The manganese was estimated to be

40.2 % in 1 based on the AAS, and microanalysis for CHN

gave C:5.7; H:3.9; N:4.2. Assuming all organic com-

pounds were imidazolium, then 1 can be formulated as

(imidazolium)0.2MnO2.2H2O (C:5.3; H:3.7; N:4.1; Mn:

40.2).

A similar procedure was used to synthesize compound 2

(2). In this case, a saturated solution of guanidinium car-

bonate (10 mL) was added to 50 mL of the colloidal sus-

pension of MnO2 monosheets (4 mM) during argon

bubbling at room temperature. After the addition, floccu-

lation occurred in the mixed solution. The resulting brown

precipitate was filtered off, washed with distilled water,

and air-dried at room temperature. The manganese was

estimated to be 40.9 % in 2 based on the AAS, and

microanalysis for CHN gave C:2.2; H:4.1; N:5.9. Assum-

ing all organic compounds were guanidinium, then 2 can

be formulated as (guanidinium)0.2MnO2.2H2O (C:1.8;

H:3.9; N:6.2; Mn:40.7).

Preparation of modified electrodes

The cleaned Pt electrode was dried with nitrogen gas. The

prepared oxide suspension was dispersed in water by

ultrasonics. The modified electrode was prepared by

dropping 20 lL of 1 or 2 (0.1 mg mL-1) on the Pt elec-

trode surface and dried at room temperature. Finally, 10 lL

of 1 wt% Nafion solution was deposited onto the center of

the modified electrode. The electrochemical properties of

different electrodes were also investigated by CV in a

0.1 M lithium perchlorate solution pH 6.3. Cyclic vol-

tammograms (CVs) were recorded at a scan rate of

50 mV s-1.

Results and discussion

While a large number of amino acids are placed around the

manganese–calcium cluster, only a small fraction of the

residues come in contact with the inorganic core, and an

even smaller fraction, 3–4 residues on the average, are

directly involved in ligation of manganese or calcium ions.

Roles for the residues that come in contact directly with the

inorganic core could be: regulation of charges and elec-

trochemistry; help in coordinating water molecules at

appropriate metal sites, and stabilization (McEvoy and

Brudvig 2006). Other residues not in contact directly with

the inorganic core still have important roles since their

deletion causes a dramatic lowering of the reaction rate;

many of these amino acid residues are important in sub-

strate or proton transfer.

Photosynth Res (2013) 117:413–421 415

123

Hydrogen bonds around the manganese–calcium cluster

are very important and proposed as a very important factor

in decreasing the activation energy of water oxidation

(Fig. 1b). There is also an arginine in the second coordi-

nation sphere of the WOC, CP43-Arg357, which may play

an important role in maintaining the structure of the metal

cluster, either in stabilizing the cubic structure and/or in

providing partial positive charges to compensate for the

negative charges induced by the oxo bridges and carbox-

ylate ligands of the WOC (Fig. 1). The side chain of

arginine may stabilize the structure of the WOC as it is

hydrogen-bonded to two l-O bridges and one carboxylate

Fig. 1 a The structure of the WOC of PSII. The locations of Arg357 (R 357) and Histidine (H 337) near the Mn4O5Ca cluster (Adapted from

Umena et al. (2011). b The hydrogen-bonding network around the manganese–calcium cluster (Adapted from from Yamaguchi et al. 2013)

Scheme 1 The proposed

mechanism for the role of

Arg357 in water oxidation

reported by Brudvig’s group.

(Reprinted with permission

from McEvoy and Brudvig

(2006). Copyright American

Chemical Society)

416 Photosynth Res (2013) 117:413–421

123

group bridging between Ca2? and Mn(2). It has been

suggested that Arg357 is involved in proton transfer

whereby the positive charge on the oxidized tyrosine-

161(YZ)/D1-His190 pair (Scheme 1) is responsible for the

deprotonation of CP43-Arg357 and, thus, its momentary

activation as a catalytic base (McEvoy and Brudvig 2006).

In other words, as shown in Scheme 1, the CP430-Arg357

appears to be uniquely positioned to abstract protons from

the proposed substrate waters of the WOC and to deliver

them to the proton-exit pathway (McEvoy and Brudvig

2006).

There are also three imidazole groups near the Mn4CaO5

cluster in PSII. D1-His332 is coordinated to Mn1, whereas

D1-His337 is not directly coordinated to the metal cluster

(Fig. 1a). Another imidazole group from D1-190 forms a

strong hydrogen bond with YZ. D1-His190 is 2.5 A in length

and lies on the opposite side of the Mn4CaO5 cluster (Umena

et al. 2011). The hydrogen bond between D1-His190 and YZ

is very important for the electron transfer from WOC to a

chlorophyll center (for a review see: McEvoy and Brudvig

2006). When His190 is deleted, the function of tyrosine is

severely altered. However, the function of His190 could be

replaced by a buffer (Hays et al. 1998) or high pH (Mamedov

et al. 1998) and thereby the Yz could perform its function.

For the purpose of simulating the Mn4O5Ca cluster of

PSII, a good question is how can guanidinium, imidazoli-

um, or other groups be placed near manganese ions in a

manganese oxide? In an effort to synthesize an efficient

and biomimetic catalyst for water oxidation, we tried to

resolve this question with manganese oxide monosheets

containing these types of groups. Monosheets are a class of

two-dimensional nano materials that are characterized by a

thickness on the order of nanometers and lateral dimen-

sions of sub-micro to micrometers (Kai et al. 2008). These

compounds have high specific surface area, structural

diversity, and electronic properties that are important for a

variety of applications. The ability of the nanosheets to

self-assemble allows the formation of restacked lamellar

aggregates (Kai et al. 2008). Thus, guanidinium and imi-

dazolium with positive charge can form a self-assembled

layered hybrid manganese (III, IV) oxide. Indeed, the IR

spectrum of 1 or 2 indicated the presence of either guan-

idinium or imidazolium and manganese oxide units in these

structures (Fig. S1). Regarding AAS, 1 and 2 could be

formulated as (imidazolonium)0.2MnO2.2H2O and (guan-

idinium)0.2MnO2.2H2O, respectively, related to an average

oxidation state of *3.7–3.9 for manganese ions in the

birnessite structure. A broad band at *32,00–3,500 cm-1

related to antisymmetric and symmetric O–H stretchings

and a band at *1,630 cm-1 related to H–O–H bending

were observed. The absorption bands characteristic for an

MnO6 core in the region 400–500 cm-1, assigned to

Fig. 2 a Powder XRD patterns of dried manganese (III, IV) oxide

monosheets (red), 1 (black), and 2 (green). Schematic representations

of the structures of 1 (b) and 2 (c)

Photosynth Res (2013) 117:413–421 417

123

Fig. 3 TEM images of manganese (III, IV) oxide monosheets (a),

1 (b), and 2 (c). Layered manganese oxides clearly can be observed in

(a–c). SEM images of manganese (III, IV) oxide monosheets (d),

1 (e), and 2 (f). Aggregated monosheets could be observed in (e) and

(f). See experimental section for details

418 Photosynth Res (2013) 117:413–421

123

stretching vibrations of Mn–O bonds in manganese oxide,

were also observed in the FTIR spectra of these com-

pounds. Other peaks were related to imidazolium (937,

1,055, 1,443, and 1,488 cm-1), guanidinium (1,177 and

1,392 cm-1), and TMA cations (1,262 and 1,463 cm-1)

(see Fig. S1).

In order to obtain clear evidence that 1 and 2 form dried

manganese (III, IV) oxide monosheets, powder X-ray dif-

fraction (XRD) of dried samples of the colloidal suspen-

sions was measured. The XRD patterns were indexed as a

hexagonal unit cell with intense (00l) reflections associated

with the preferred orientation of the sample, similar to that

of other manganese oxides with the birnessite structures

(Fig. 2) (Kai et al. 2008). A birnessite structure was found

with an interlayer spacing of *0.95 nm for manganese

(III, IV) oxide monosheets (Fig. 2) (Kai et al. 2008). These

XRD patterns indicated the flocculation of the manganese

(III, IV) oxide together with TMA and water molecules

(Kai et al. 2008). XRD patterns of dried samples of 1 and 2

indicated that they have birnessite structures as well, and

the interlayer spacing is *0.9 nm: that is very similar to

dried manganese (III, IV) oxide monosheets (Fig. 2).

The guanidinium and imidazolium cations, similar to the

TMA cations in 1 and 2, are poorly ordered as indicated by

the broad peaks obtained in the XRD pattern. Figure 3

shows TEM and SEM images of manganese (III, IV) oxide

monosheets, 1 and 2. On the basis of XRD patterns and

TEM images, we suggest a tentative model of the struc-

tures of 1 and 2 (Fig. 2b, c). The structures consist of sheets

of imidazolium, guanidinium, and TMA cations and water

molecules found between sheets of edge-sharing molecules

of MnO6 octahedra, and repeated on an average of every

7–9 A. Of the six octahedral sites in the MnO6 octahedral

layer, one is left unoccupied; Mn(III) lies above each

vacant slot on the octahedral. These Mn ions are low-

valence, and associate with O, in both the octahedral and in

the water sheets (Kai et al. 2008). Aggregated layered

manganese oxide with imidazole or guanidinium could be

observed clearly in Fig. 3d–f.

We have considered 1 and 2 as structural models for the

WOC in PSII. However, in order to characterize the water-

oxidizing activity of the monosheets, 1 and 2, electrochem-

ical characterizations were performed. CV and amperomet-

ric studies were performed with a conventional three

electrode set-up, in which a Pt electrode or Pt electrode

modified with dried manganese (III, IV) oxide monosheets, 1

and 2, served as the working electrode and an Ag|AgCl|KClsat

electrode and a platinum rod, served as the reference and

auxiliary electrodes, respectively. Catalytic activities for the

water oxidation are shown in Fig. 4.

As discussed in the experimental section, we used

Nafion to adhere the catalyst material onto the oxide sur-

face. The method has also been used by other groups to

adhere different catalysts onto electrodes (Yagi et al. 1996;

Hara and Mallouk 2000; Hocking et al. 2011; Suntivich

et al. 2011; Young et al. 2011). Nafion has a perfluorinated

backbone, and it causes Nafion resistances in the highly

oxidizing environments required for water oxidation

(Young et al. 2011). The water oxidation potential on Pt

modified with dried manganese (III, IV) oxide monosheets

that contain TMA cations, 1 and 2, was slightly lower

(*1.25 V vs. Ag|AgCl) than that of the bare Pt electrode

(*1.35 V vs. Ag|AgCl) toward water oxidation. The

reversible potential for the H2O/O2 couple is given by:

E¼þ1:230 V

� 0:059 Vð Þ pH vs: Standard hydrogen electrode SHEð Þ

The potential for H2O oxidation at pH 6.3 can be

calculated to ?0.86 V (0.66 vs. Ag|AgCl). The overvoltage

Fig. 4 Cyclic voltammograms (CVs) of a Pt electrode (blue), or a Pt

electrode modified with dried manganese (III, IV) oxide monosheets

(red), 1 (92; black), and 2 (95; green) in lithium perchlorate solution

(0.1 M in water, pH = 6.3) at a scan rate of 50 mV s-1 in both

0.0–2.0 V (top) and 1.0–1.4 V (below). See experimental section for

details

Photosynth Res (2013) 117:413–421 419

123

of water oxidation—the voltage in addition to E that is

required for water oxidation—for the dried manganese (III,

IV) oxide monosheets, 1 and 2, in these conditions is

*0.6 V. This comparatively low overvoltage suggests that

these compounds could serve as the first step toward

synthesizing a hybrid of guanidinium or imidazole and

manganese as water-oxidizing catalysts to mimic the WOC

of PSII. Our findings suggest that these groups could

perform roles to decrease activation energy in water

oxidation by stabilizing manganese oxide, and optimizing

proton, water, and oxygen transfer (Scheme 2).

Conclusions

We synthesized aggregated layered manganese oxide with

guanidinium and imidazolium to introduce new biomimetic

models for the WOC. Although the WOC of PSII is a

discrete structure, the model introduced here could be the

first step in the synthesis of a self-assembled layered hybrid

of amino acid residues and manganese oxide which could

serve as a good model for the WOC. However, more data

will be required for imidazolium or guanidinium/layered

manganese (III, IV) oxide hybrids to find more about

interactions between imidazolium or guanidinium and

manganese oxide. Dried manganese (III, IV) oxide also

contains an organic group (TMA). Imidazolium, guanidi-

nium, and TMA cations form an open structure and pre-

ferred space with layered manganese oxide to oxidize

water (see Fig. 2b, c). As manganese oxides are efficient

catalysts for water oxidation, further development of this

new model could lead to structures with similar properties

to those which exist in the WOC of PSII (Scheme 2).

Acknowledgments MMN, MAT, and BH are grateful to the Insti-

tute for Advanced Studies in Basic Sciences support and the National

Elite Foundation for financial support. This study was also supported

by Grants from the Russian Foundation for Basic Research (nos.

11-04-01389a, 12-04-92101, 13-04-91372, 13-04-92711), by Molec-

ular and Cell Biology Programs of the Russian Academy of Sciences,

by BMBF (No: 8125) Bilateral Cooperation between Germany and

Russia, to SIA.

References

Alexander BD, Kulesza PJ, Rutkowska I, Solarska R, Augustynski J

(2008) Metal oxide photoanodes for solar hydrogen production.

J Mater Chem 18:2298–2303

Allakhverdiev SI (2012) Photosynthetic and biomimetic hydrogen

production. Int J Hydrogen Energy 37:8744–8752

Allakhverdiev SI, Casal J, Nagata T (2009a) Photosynthesis from

molecular perspectives: towards future energy production.

Photochem Photobiol Sci 8:137–138

Allakhverdiev SI, Kreslavski VD, Thavasi V, Zharmukhamedov SK,

Klimov VV, Nagata T, Nishihara H, Ramakrishna S (2009b)

Hydrogen photoproduction by use of photosynthetic organisms

and biomimetic systems. Photochem Photobiol Sci 8:148–156

Allakhverdiev SI, Thavasi V, Kreslavski VD, Zharmukhamedov SK,

Klimov VV, Ramakrishna S, Losa DA, Mimuro M, Nishihara H,

Carpentier R (2010) Photosynthetic hydrogen production. J Pho-

tochem Photobiol C 11:101–113

Balzani V, Credi A, Venturi M (2008) Photochemical conversion of

solar energy. ChemSusChem 1:26–58

Beckmann K, Uchtenhagen H, Berggren G, Anderlund MF, Thapper

A, Messinger J, Styring S, Kurz P (2008) Formation of

stoichiometrically 18O-labelled oxygen from the oxidation of18O-enriched water mediated by a dinuclear manganese com-

plex: a mass spectrometry and EPR study. Energy Environ Sci

1:668–676

Bockris JOM (1977) Energy-the solar hydrogen alternative. Wiley,

New York

Cady CW, Crabtree RH, Brudvig GW (2008) Functional models for

the oxygen-evolving complex of Photosystem II. Coord Chem

Rev 252:444–455

Daniel M, Alessandro DE (2008) Economical electrolyser solution.

Int J Hydrogen Energy 33:3041–3044

Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S (2004)

Architecture of the photosynthetic oxygen-evolving center.

Science 303:183–188

Hara M, Mallouk TE (2000) Photocatalytic water oxidation by

Nafion-stabilized iridium oxide colloids. Chem Commun

19:1903–1904

Hays AMA, Vassiliev IR, Golbeck JH, Debus RJ (1998) Role of D1-

His190 in proton-coupled electron transfer reactions in Photo-

system II: a chemical complementation study. Biochemistry

37:11352–11365

Heinzel A, Vogel B, Hubner P (2002) Reforming of naturalgas-

hydrogen generation for small scale stationary fuel cell systems.

J Power Source 105:202–207

Hocking RK, Brimblecombe R, Chang LY, Singh A, Cheah MH,

Glover C, Casey WH, Spiccia L (2011) Water-oxidation catalysis

by manganese in a geochemical-like cycle. Nat Chem 3:461–466

Hou HJ (2010) Structural and mechanistic aspects of Mn-oxo

Compounds in water oxidation catalysis and Potential. App J

Integr Plant Biol 5:704–711

Kai K, Yoshida Y, Kageyama H, Saito G, Ishigaki T, Furukawa Y,

Kawamata J (2008) Room-temperature synthesis of manganese

oxide monosheets. J Am Chem Soc 130:15938–15943

Scheme 2 A special protein in PSII controls proton and oxygen

movement as well as the access of water. A similar strategy could be

utilized by placing a few groups in manganese compounds to perform

this function. (Adapted from Najafpour and Allakhverdiev 2012)

420 Photosynth Res (2013) 117:413–421

123

Kamiya N, Shen JR (2003) Crystal structure of oxygen-evolving

Photosystem II from Thermosynechococcus vulcanus at 3.7 A

resolution. Proc Natl Acad Sci USA 100:98–103

Kanan WMW, Nocera DG (2008) In situ formation of an oxygen

evolving catalyst in neutral water containing phosphate and

Co2?. Science 32:1072–1075

Kawakami K, Umena Y, Kamiya N, Shen JR (2011) Structure of the

catalytic, inorganic core of oxygen evolving Photosystem II at

1.9 A resolution. J Photochem Photobiol B 104:9–18

Kirin SK, Kramer R, Metzeler-Notle N (2006) Nuclease and

peptidase models. In: Kraatz H, Metzeler-Notle N (eds)

Concepts and models in bioinorgnic chemistry. Wiley,

New York, pp 170–172

Lewis NS, Nocera DG (2006) Powering the planet: chemical

challenges in solar energy utilization. Proc Natl Acad Sci USA

103:15729–15735

Liu X, Wang F (2012) Transition metal complexes that catalyze

oxygen formation from water: 1979–2010. Coord Chem Rev

256:1115–1136

Mamedov F, Sayre RT, Styring S (1998) Involvement of histidine 190

on the D1 protein in electron/proton transfer reactions on the

donor side of Photosystem II. Biochemistry 37:14245–14256

McEvoy JP, Brudvig GW (2006) Water-splitting chemistry of

Photosystem II. Chem Rev 106:4455–4483

Najafpour MM (2006) Current molecular mechanisms of photosyn-

thetic oxygen evolution. Plant Biosyst 140(2):163–170

Najafpour MM (2011) Self-assembled layered hybrid [Ru(bpy)3]?2/

manganese (III, IV) oxide: a new and efficient strategy for water

oxidation. Chem Commun 47:11724–11726

Najafpour MM, Allakhverdiev SI (2012) Manganese compounds as

water oxidizing catalysts for hydrogen production via water

splitting: from manganese complexes to nano-sized manganese

oxides. Int J Hydrogen Energy 37:8753–8764

Najafpour MM, Ehrenberg T, Wiechen M, Kurz P (2010) Calcium

manganese(III) oxides (CaMn2O4.xH2O) as biomimetic oxygen-

evolving catalysts. Angew Chem Int Ed 49:2233–2237

Najafpour MM, Rahimi F, Aro EM, Lee CH, Allakhverdiev SI

(2012a) Nano-sized manganese oxides as biomimetic catalysts

for water oxidation in artificial photosynthesis: a review. J Roy

Soc Interface 9:2383–2395

Najafpour MM, Moghaddam AN, Yang YN, Aro E-M, Carpentier R,

Eaton-Rye JJ, Lee CH, Allakhverdiev SI (2012b) Biological

water-oxidizing complex: a nano-sized manganese-calcium

oxide in a protein environment. Photosynth Res 114:1–13

Ruttinger W, Dismukes GC (1997) Synthetic water oxidation

catalysts for artificial photosynthetic water oxidation. Chem

Rev 97:1–24

Sproviero EM, Gascon JA, McEvoy JP, Brudvig GW, Batista VS

(2008) Computational studies of the O2-evolving complex of

Photosystem II and biomimetic oxomanganese complexes.

Coord Chem Rev 252:395–415

Suntivich J, May KJ, Gasteiger HA, Goodenough JB, Shao-Horn Y

(2011) A perovskite oxide optimized for oxygen evolution catalysis

from molecular orbital principles. Science 334:1383–1385

Umena Y, Kawakami K, Shen JR, Kamiya N (2011) Crystal structure

of oxygen-evolving Photosystem II at a resolution of 1.9 A.

Nature 473:55–60

Wiechen M, Berends HM, Kurz P (2012) Water oxidation catalysed

by manganese compounds: from complexes to ‘biomimetic

rocks’. Dalton Trans 41:21–31

Yagi M, Tokita S, Nagoshi K, Isamu Ogino I, Kaneko M (1996)

Activity analysis of a water oxidation catalyst immobilized in a

polymer membrane. J Chem Soc Faraday Trans 92:2457–2461

Yamaguchi K, Isobe H, Yamanaka S, Saito T, Kanda K, Shoji M,

Umena Y, Kawakami K, Shen JR, Kamiya N, Okumura M

(2013) Full geometry optimizations of the mixed-valence

CaMn4O4X(H2O)4 (X = OH or O) cluster in OEC of PS II:

degree of symmetry breaking of the labile Mn-X-Mn bond

revealed by several hybrid DFT calculations. Int J Quantum

Chem 113:525–541

Young KJ, Gao Y, Brudvig GW (2011) Photocatalytic water

oxidation using manganese compounds immobilized in Nafion

polymer membranes. Aust J Chem 64:1221–1228

Zaharieva I, Najafpour MM, Wiechen M, Haumann M, Kurz P, Dau

H (2011) Synthetic manganese-calcium oxides mimic the water-

oxidizing complex of photosynthesis functionally and structur-

ally. Energy Environ Sci 4:2400–2408

Zouni A, Witt HT, Kern J, Fromme P, Krauss N, Saenger W, Orth P

(2001) Crystal structure of Photosystem II from Synechococcus

elongatus at 3.8 A resolution. Nature 409:739–743

Photosynth Res (2013) 117:413–421 421

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