The biological water-oxidizing complex at the nano-bio interface

Trends in Plant Science

Volumn 20, Issue 9, 2015, Pages 559-568

  Najafpour, Mohammad Mahdi ^a   Ghobadi, Mohadeseh Zarei ^a   Larkum, Anthony W ^b   Shen, Jian Ren ^c   Allakhverdiev, Suleyman I ^d,e,f  

^a INSTITUTE FOR ADVANCED STUDIES IN BASIC SCIENCES IASBS   (Iran)

^b UNIVERSITY OF TECHNOLOGY SYDNEY   (Australia)

^c OKAYAMA UNIVERSITY   (Japan)

^d TIMIRYAZEV INSTITUTE OF PLANT PHYSIOLOGY   (Russian Federation)

^e INSTITUTE OF BASIC BIOLOGICAL PROBLEMS   (Russian Federation)

^f MOSCOW STATE UNIVERSITY   (Russian Federation)

Author keywords

Artificial photosynthesis; Nano sized Mn Ca oxido cluster; Photosynthesis; Water oxidation; Water oxidizing complex

Indexed keywords

MANGANESE DERIVATIVE; WATER;

CATALYSIS; METABOLISM; OXIDATION REDUCTION REACTION; PHOTOSYNTHESIS; PLANT; SOLAR ENERGY;

CATALYSIS; MANGANESE COMPOUNDS; OXIDATION-REDUCTION; PHOTOSYNTHESIS; PLANTS; SOLAR ENERGY; WATER;

EID: 84940872118     PISSN: 13601385     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tplants.2015.06.005     Document Type: Review

References (88)

1. Cardona T., et al. Origin and evolution of water oxidation before the last common ancestor of the cyanobacteria. Mol. Biol. Evol. 2015, 32:1310-1328.
2. Blankenship R.E. Molecular Mechanisms of Photosynthesis 2013, 336. John Wiley & Sons.
3. Summons R.E., et al. 2-Methylhopanoids as biomarkers for cyanobacterial oxygenic photosynthesis. Nature 1999, 400:554-557.
4. Konhauser K.O., et al. Aerobic bacterial pyrite oxidation and acid rock drainage during the great oxidation event. Nature 2011, 478:369-373.
5. McEvoy J.P., Brudvig G.W. Water-splitting chemistry of photosystem II. Chem. Rev. 2006, 106:4455-4483.
6. Ferreira K.N., et al. Architecture of the photosynthetic oxygen-evolving center. Science 2004, 303:1831-1838.
7. Umena Y., et al. Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9Å. Nature 2011, 473:55-60.
8. Guskov A., et al. Cyanobacterial photosystem II at 2.9-Å resolution and the role of quinones, lipids, channels and chloride. Nat. Struct. Mol. Biol. 2009, 16:334-342.
9. Kamiya N., Shen J.-R. Crystal structure of oxygen-evolving photosystem II from Thermosynechococcus vulcanus at 3.7-Å resolution. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:98-103.
10. Suga M., et al. Native structure of photosystem II at 1.95Å resolution viewed by femtosecond X-ray pulses. Nature 2015, 517:99-103.
11. Jordan P., et al. Three-dimensional structure of cyanobacterial photosystem I at 2.5Å resolution. Nature 2011, 411:909-917.
12. 2+. Science 2008, 321:1072-1075.
13. Liu L., Wang F. Transition metal complexes that catalyze oxygen formation from water: 1979-2010. Coord. Chem. Rev. 2012, 256:1115-1136.
14. Tachibana Y., et al. Artificial photosynthesis for solar water-splitting. Nat. Photon. 2013, 6:511-518.
15. Ruttinger W., Dismukes G.C. Synthetic water oxidation catalysts for artificial photosynthetic water oxidation. Chem. Rev. 1997, 97:1-24.
16. 4Ca cluster in photosynthesis: where and how water is oxidized to dioxygen. Chem. Rev. 2014, 114:4175-4205.
17. Rappaport F., et al. Ca determines the entropy changes associated with the formation of transition states during water oxidation by photosystem II. Energy Environ. Sci. 2011, 4:2520-2524.
18. Polander B.C., Barry B.A. Ca and the hydrogen-bonded water network in the photosynthetic oxygen-evolving complex. J. Phys. Chem. Lett. 2013, 4:786-791.
19. Hirahara M., et al. Artificial manganese center models for photosynthetic oxygen evolution in photosystem II. Eur. J. Inorg. Chem. 2014, 2014:595-606.
20. Mukherjee S., et al. Comproportionation reactions to Mn (III/IV) pivalate clusters: a new half-integer spin single-molecule magnet. Inorg. Chem. 2012, 52:873-884.
21. 4 cubanes as structural units of natural and artificial water-oxidizing catalysts. J. Am. Chem. Soc. 2013, 135:5726-5739.
22. Glatzel P., et al. Electronic structural changes of Mn in the oxygen-evolving complex of photosystem II during the catalytic cycle. Inorg. Chem. 2013, 52:5642-5644.
23. Kanady J.S., et al. Role of oxido incorporation and ligand lability in expanding redox accessibility of structurally related Mn4 clusters. Chem. Sci. 2013, 4:3986-3996.
24. Kern J., et al. Simultaneous femtosecond X-ray spectroscopy and diffraction of photosystem II at room temperature. Science 2013, 340:491-495.
25. 2H) water in Mn catalase and its relevance to the oxygen-evolving complex of photosystem II. J. Am. Chem. Soc. 2012, 134:1504-1512.
26. 17O electron-electron double resonance-detected NMR spectroscopy. J. Am. Chem. Soc. 2012, 134:16619-16634.
27. 4 transitions in photosystem II. Phys. Chem. Chem. Phys. 2012, 14:4849-4856.
28. 2 state: a combined EPR and DFT study. Phys. Chem. Chem. Phys. 2014, 16:11877-11892.
29. Koua F.H., et al. Structure of Sr-substituted photosystem II at 2.1Å resolution and its implications in the mechanism of water oxidation. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:3889-3894.
30. Nilsson H., et al. Substrate-water exchange in photosystem II is arrested before dioxygen formation. Nat. Commun. 2014, 5:4305.
31. Kupitz C., et al. Serial time-resolved crystallography of photosystem II using a femtosecond X-ray laser. Nature 2014, 513:261-265.
32. Cox N., et al. Electronic structure of the oxygen-evolving complex in photosystem II prior to O-O bond formation. Science 2014, 345:804-808.
33. 3 transition in the photosynthetic oxygen-evolving cycle. J. Phys. Chem. Lett. 2013, 4:3356-3362.
34. Gatt P.P., et al. Rationalizing the 1.9Å crystal structure of photosystem II-a remarkable Jahn-Teller balancing act induced by a single proton transfer. Angew. Chem. Int. Ed. Engl. 2012, 51:12025-12028.
35. Kolling D.R.J., et al. What are the oxidation states of manganese required to catalyze photosyntheticwater oxidation?. Biophys. J. 2012, 103:313-322.
36. 4Ca cluster in photosystem II as revealed by isotope-edited Fourier transform infrared spectroscopy. J. Am. Chem. Soc. 2011, 133:3808-3811.
37. Kawakami K., et al. Location of chloride and its possible functions in oxygen-evolving photosystem II revealed by X-ray crystallography. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:8567-8572.
38. Rivalta I., et al. Structural-functional role of chloride in photosystem II. Biochemistry 2011, 50:6312-6315.
39. Boussac A., et al. Probing the role of chloride in photosystem II from Thermosynechococcus elongatus by exchanging chloride for iodide. Biochim. Biophys. Acta 2012, 1817:802-810.
40. Yadav D.K., Pospíšil P. Role of chloride ion in hydroxyl radical production in photosystem II under heat stress: electron paramagnetic resonance spin-trapping study. J. Bioenerg. Biomembr. 2012, 44:365-372.
41. Noguchi T., Sugiura M. FTIR detection of water reactions during the flash-induced S-state cycle of the photosynthetic water-oxidizing complex. Biochemistry 2002, 41:15706-15712.
42. Britt R.D., et al. Recent pulsed EPR studies of the photosystem II oxygen-evolving complex: implications as to water oxidation mechanisms. Biochim. Biophys. Acta 2004, 1655:158-171.
43. Dau H., et al. On the structure of the manganese complex of photosystem II: extended-range EXAFS data and specific atomic-resolution models for four S-states. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 2008, 363:1237-1244.
44. 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 2003, 42:6209-6217.
45. Tagore R., et al. Determination of μ-oxo exchange rates in di-μ-oxo dimanganese complexes by electrospray ionization mass spectrometry. J. Am. Chem. Soc. 2006, 128:9457-9465.
46. Najafpour M.M., et al. Water exchange rate in manganese-based water-oxidizing catalysts in photosynthetic systems: from the water-oxidizing complex in photosystem II to nano-sized manganese oxides. Biochim. Biophys. Acta 2014, 1837:1395-1410.
47. 2+ exchange in the photosystem II oxygen-evolving enzyme of Thermosynechococcus elongatus. J. Biol. Chem. 2004, 279:22809-22819.
48. Krewald V., et al. Metal oxidation states in biological water splitting. Chem. Sci. 2015, 6:1676-1695.
49. Navarro M.P., et al. Ammonia binding to the oxygen-evolving complex of photosystem II identifies the solvent-exchangeable oxygen bridge (μ-oxo) of the manganese tetramer. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:15561-15566.
50. Cox N., Messinger J. Reflections on substrate water and dioxygen formation. Biochim. Biophys. Acta 2013, 1827:1020-1030.
51. Pecoraro V.L., et al. A proposal for water oxidation in photosystem II. Pure Appl. Chem. 1998, 70:925-929.
52. Limburg J., et al. A mechanistic and structural model for the formation and reactivity of a MnV=O species in photosynthetic water oxidation. J. Chem. Soc. Dalton Trans. 1999, 1353-1362.
53. Kusunoki M. Mono-manganese mechanism of the photosystem II water splitting reaction by a unique Mn4Ca cluster. Biochim. Biophys. Acta 2007, 1767:484-492.
54. Faunce T., et al. Artificial photosynthesis as a frontier technology for energy sustainability. Energy Environ. Sci. 2013, 6:1074-1076.
55. Berardi S., et al. Molecular artificial photosynthesis. Chem. Soc. Rev. 2014, 43:7501-7519.
56. Gust D., et al. Solar fuels via artificial photosynthesis. Acc. Chem. Res. 2009, 42:1890-1898.
57. Kato M., et al. Covalent immobilization of oriented photosystem II on a nanostructured electrode for solar water oxidation. J. Am. Chem. Soc. 2013, 135:10610-10613.
58. Nocera D.G. The artificial leaf. Acc. Chem. Res. 2012, 45:767-776.
59. Du P., Eisenberg R. Catalysts made of Earth-abundant elements (Co, Ni, Fe) for water splitting: recent progress and future challenges. Energy Environ. Sci. 2012, 5:6012-6021.
60. Tran P.D., et al. Recent advances in hybrid photocatalysts for solar fuel production. Energy Environ. Sci. 2012, 5:5902-5918.
61. Kärkäs D.M., et al. Artificial photosynthesis: molecular systems for catalytic water oxidation. Chem. Rev. 2014, 114:11863-12001.
62. 2 edge site mimic for catalytic hydrogen generation. Science 2012, 335:698-702.
63. Armstrong F.A. Why did nature choose Mn to make oxygen?. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 2008, 363:1263-1270.
64. Morita M., et al. The anodic characteristics of Mn dioxide electrodes prepared by thermal decomposition of Mn nitrate. Electrochim. Acta 1977, 22:325-328.
65. Hocking R.K. Water-oxidation catalysis by Mn in a geochemical-like cycle. Nat. Chem. 2011, 3:461-466.
66. Najafpour M.M., et al. Fragments of layered Mn oxide are the real water oxidation catalyst after transformation of molecular precursor on clay. J. Am. Chem. Soc. 2014, 136:7245-7248.
67. Karlsson E.A., et al. Photosensitized water oxidation by use of a bioinspired Mn catalyst. Angew. Chem. Int. Ed. Engl. 2011, 123:11919-11922.
68. 2-evolving complex in photosystem II. Science 1999, 283:1524-1527.
69. 6 complexes with cubane-like core structure: a new class of models of the active site of the photosynthetic water oxidase. J. Am. Chem. Soc. 1997, 119:6670-6671.
70. Liu R., et al. Water splitting by tungsten oxide prepared by atomic layer deposition and decorated with an oxygen evolving catalyst. Angew. Chem. Int. Ed. Engl. 2011, 50:499-502.
71. Lee W.T., et al. Ligand modification transforms a catalase mimic into a water oxidation catalyst. Angew. Chem. Int. Ed. Engl. 2014, 53:9856-9859.
72. Efrati A., et al. Cytochrome c-coupled photosystem I and photosystem II (PSI/PSII) photo-bioelectrochemical cells. Energy Environ. Sci. 2013, 6:2950-2956.
73. Kato M., et al. Photoelectrochemical water oxidation with photosystem II integrated in a mesoporous indium-tin oxide electrode. J. Am. Chem. Soc. 2012, 134:8332-8335.
74. Pita M., et al. Bioelectrochemical oxidation of water. J. Am. Chem. Soc. 2014, 136:5892-5895.
75. Kato M., et al. Protein film photoelectrochemistry of the water oxidation enzyme photosystem II. Chem. Soc. Rev. 2014, 43:6485-6497.
76. Kothe T., et al. 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. 2013, 52:14233-14236.
77. Yehezkeli O., et al. Integrated photosystem II-based photo-bioelectrochemical cells. Nat. Commun. 2012, 3:742.
78. 2O) as biomimetic oxygen-evolving catalysts. Angew. Chem. Int. Ed. Engl. 2010, 49:2233-2237.
79. Wiechen M., et al. Layered Mn oxides for water-oxidation: alkaline earth cations influence catalytic activity in a photosystem II-like fashion. Chem. Sci. 2012, 3:2330-2339.
80. Najafpour M.M., et al. Comparison of nano-sized Mn oxides with the Mn cluster of photosystem II as catalysts for water oxidation. Biochim. Biophys. Acta 2015, 1847:294-306.
81. Najafpour M.M., et al. An engineered polypeptide around nano-sized manganese-calcium oxide: copying plants for water oxidation. Dalton Trans. 2015, Published online May 28, 2015. 10.1039/C5DT01443C.
82. Najafpour M.M., et al. Nanolayered manganese oxide/poly (4-vinylpyridine) as a biomimetic and very efficient water oxidizing catalyst: toward an artificial enzyme in artificial photosynthesis. Chem. Commun. 2013, 49:8824-8826.
83. Yamaguchi A., et al. Regulating proton-coupled electron transfer for efficient water splitting by Mn oxides at neutral pH. Nat. Commun. 2014, 5:4256.
84. Hingorani K., et al. Photo-oxidation of tyrosine in a bio-engineered bacterioferritin 'reaction centre' - a protein model for artificial photosynthesis. Biochim. Biophys. Acta 2014, 1837:1821-1834.
85. 4] cubane core of the oxygen-evolving complex of photosystem II. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:2257-2262.
86. Tsui E.Y., et al. Redox-inactive metals modulate the reduction potential in heterometallic manganese-oxido clusters. Nat. Chem. 2013, 5:293-299.
87. Herbert D.E. Heterometallic triiron-oxo/hydroxo clusters: effect of redox-inactive metals. J. Am. Chem. Soc. 2013, 135:19075-19078.
88. 4Ca-cluster mimicking the oxygen-evolving center of photosynthesis. Science 2015, 348:690-693.