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

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Abstract

Photosystem II is responsible for the light-driven biological water-splitting system in oxygenic photosynthesis 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 biomimetic systems capable of splitting water into oxygen and hydrogen. In this study, we consider the ability of manganese oxide monosheets to self-assemble with organic compounds. Layered structures of manganese oxide, including guanidinium and imidazolium groups, were synthesized and characterized by scanning electron microscopy, 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.

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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

    Article  CAS  Google Scholar 

  • Allakhverdiev SI (2012) Photosynthetic and biomimetic hydrogen production. Int J Hydrogen Energy 37:8744–8752

    Article  CAS  Google Scholar 

  • Allakhverdiev SI, Casal J, Nagata T (2009a) Photosynthesis from molecular perspectives: towards future energy production. Photochem Photobiol Sci 8:137–138

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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 Photochem Photobiol C 11:101–113

    Article  CAS  Google Scholar 

  • Balzani V, Credi A, Venturi M (2008) Photochemical conversion of solar energy. ChemSusChem 1:26–58

    Article  PubMed  CAS  Google Scholar 

  • 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 of 18O-enriched water mediated by a dinuclear manganese complex: a mass spectrometry and EPR study. Energy Environ Sci 1:668–676

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Cady CW, Crabtree RH, Brudvig GW (2008) Functional models for the oxygen-evolving complex of Photosystem II. Coord Chem Rev 252:444–455

    Article  PubMed  CAS  Google Scholar 

  • Daniel M, Alessandro DE (2008) Economical electrolyser solution. Int J Hydrogen Energy 33:3041–3044

    Article  Google Scholar 

  • Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303:183–188

    Article  Google Scholar 

  • Hara M, Mallouk TE (2000) Photocatalytic water oxidation by Nafion-stabilized iridium oxide colloids. Chem Commun 19:1903–1904

    Article  Google Scholar 

  • Hays AMA, Vassiliev IR, Golbeck JH, Debus RJ (1998) Role of D1-His190 in proton-coupled electron transfer reactions in Photosystem II: a chemical complementation study. Biochemistry 37:11352–11365

    Article  PubMed  CAS  Google Scholar 

  • Heinzel A, Vogel B, Hübner P (2002) Reforming of naturalgas-hydrogen generation for small scale stationary fuel cell systems. J Power Source 105:202–207

    Article  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Kamiya N, Shen JR (2003) Crystal structure of oxygen-evolving Photosystem II from Thermosynechococcus vulcanus at 3.7 Å resolution. Proc Natl Acad Sci USA 100:98–103

    Article  PubMed  CAS  Google Scholar 

  • Kanan WMW, Nocera DG (2008) In situ formation of an oxygen evolving catalyst in neutral water containing phosphate and Co2+. Science 32:1072–1075

    Article  Google Scholar 

  • Kawakami K, Umena Y, Kamiya N, Shen JR (2011) Structure of the catalytic, inorganic core of oxygen evolving Photosystem II at 1.9 Å resolution. J Photochem Photobiol B 104:9–18

    Article  PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • Lewis NS, Nocera DG (2006) Powering the planet: chemical challenges in solar energy utilization. Proc Natl Acad Sci USA 103:15729–15735

    Article  PubMed  CAS  Google Scholar 

  • Liu X, Wang F (2012) Transition metal complexes that catalyze oxygen formation from water: 1979–2010. Coord Chem Rev 256:1115–1136

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • McEvoy JP, Brudvig GW (2006) Water-splitting chemistry of Photosystem II. Chem Rev 106:4455–4483

    Article  PubMed  CAS  Google Scholar 

  • Najafpour MM (2006) Current molecular mechanisms of photosynthetic oxygen evolution. Plant Biosyst 140(2):163–170

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Ruttinger W, Dismukes GC (1997) Synthetic water oxidation catalysts for artificial photosynthetic water oxidation. Chem Rev 97:1–24

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Umena Y, Kawakami K, Shen JR, Kamiya N (2011) Crystal structure of oxygen-evolving Photosystem II at a resolution of 1.9 Å. Nature 473:55–60

    Article  PubMed  CAS  Google Scholar 

  • Wiechen M, Berends HM, Kurz P (2012) Water oxidation catalysed by manganese compounds: from complexes to ‘biomimetic rocks’. Dalton Trans 41:21–31

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Young KJ, Gao Y, Brudvig GW (2011) Photocatalytic water oxidation using manganese compounds immobilized in Nafion polymer membranes. Aust J Chem 64:1221–1228

    Article  PubMed  Google Scholar 

  • 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 structurally. Energy Environ Sci 4:2400–2408

    Article  CAS  Google Scholar 

  • 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 Å resolution. Nature 409:739–743

    Google Scholar 

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Acknowledgments

MMN, MAT, and BH are grateful to the Institute 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 Molecular and Cell Biology Programs of the Russian Academy of Sciences, by BMBF (No: 8125) Bilateral Cooperation between Germany and Russia, to SIA.

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Correspondence to Mohammad Mahdi Najafpour or Suleyman I. Allakhverdiev.

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Najafpour, M.M., Tabrizi, M.A., Haghighi, B. et al. Imidazolium or guanidinium/layered manganese (III, IV) oxide hybrid as a promising structural model for the water-oxidizing complex of Photosystem II for artificial photosynthetic systems. Photosynth Res 117, 413–421 (2013). https://doi.org/10.1007/s11120-013-9814-5

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