High-spin Mn-oxo complexes and their relevance to the oxygen-evolving complex within photosystem II

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 17, 2015, Pages 5319-5324

  Gupta, Rupal ^a   Taguchi, Taketo ^b   Lassalle Kaiser, Benedikt ^c   Bominaar, Emile L ^a   Yano, Junko ^c   Hendrich, Michael P ^a   Borovik, A S ^b  

^a CARNEGIE MELLON UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

Inorganic chemistry; Metal oxo complexes; Oxygen evolving complex; Photosynthesis; Water oxidation

Indexed keywords

LIGAND; MANGANESE; OXYGEN; OXYGEN 17; WATER; PHOTOSYSTEM II;

ACCELERATION; ARTICLE; CHEMICAL BOND; CHEMICAL STRUCTURE; DENSITY; DENSITY FUNCTIONAL THEORY; ELECTRON SPIN RESONANCE; OXIDATION; PHOTOSYSTEM II; PRIORITY JOURNAL; CHEMISTRY; OXIDATION REDUCTION REACTION; PHOTON ABSORPTIOMETRY;

ABSORPTIOMETRY, PHOTON; ELECTRON SPIN RESONANCE SPECTROSCOPY; MANGANESE; OXIDATION-REDUCTION; OXYGEN; PHOTOSYSTEM II PROTEIN COMPLEX; WATER;

EID: 84928568260     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1422800112     Document Type: Article

References (34)

1. Yano J, et al. (2006) Where water is oxidized to dioxygen: Structure of the photosynthetic Mn4Ca cluster. Science 314(5800):821-825.
2. Britt RD, et al. (2004) Recent pulsed EPR studies of the Photosystem II oxygen-evolving complex: Implications as to water oxidation mechanisms. Biochim Biophys Acta Bioenerg 1655(1-3):158-171.
3. Umena Y, Kawakami K, Shen J-R, Kamiya N (2011) Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å. Nature 473(7345):55-60.
4. Suga M, et al. (2015) Native structure of photosystem II at 1.95 Å resolution viewed by femtosecond X-ray pulses. Nature 517(7532):99-103.
5. Rapatskiy L, et al. (2012) Detection of the water-binding sites of the oxygen-evolving complex of Photosystem II using W-band 17O electron-electron double resonance-detected NMR spectroscopy. J Am Chem Soc 134(40):16619-16634.
6. Pantazis DA, Ames W, Cox N, Lubitz W, Neese F (2012) Two interconvertible structures that explain the spectroscopic properties of the oxygen-evolving complex of photosystem II in the S2 state. Angew Chem Int Ed Engl 51(39):9935-9940.
7. Kok B, Forbush B, McGloin M (1970) Cooperation of charges in photosynthetic O2 evolution-I. A linear four step mechanism. Photochem Photobiol 11(6):457-475.
8. Pecoraro VL, Baldwin MJ, Caudle MT, Hsieh W-Y, Law NA (1998) A proposal for water oxidation in photosystem II. Pure Appl Chem 70(4):925-929.
9. Grundmeier A, Dau H (2012) Structural models of the manganese complex of photosystem II and mechanistic implications. Biochim Biophys Acta Bioenerg 1817(1):88-105.
10. Brudvig GW (2008) Water oxidation chemistry of photosystem II. Philos Trans R Soc B 363(1494):1211-1219.
11. Siegbahn PEM (2009) Structures and energetics for O2 formation in photosystem II. Acc Chem Res 42(12):1871-1880.
12. Cox N, Pantazis DA, Neese F, Lubitz W (2013) Biological water oxidation. Acc Chem Res 46(7):1588-1596.
13. Ames W, et al. (2011) Theoretical evaluation of structural models of the S2 state in the oxygen evolving complex of Photosystem II: Protonation states and magnetic interactions. J Am Chem Soc 133(49):19743-19757.
14. Cox N, et al. (2014) Photosynthesis. Electronic structure of the oxygen-evolving complex in photosystem II prior to O-O bond formation. Science 345(6198):804-808.
15. Yocum CF (2008) The calcium and chloride requirements of the O2 evolving complex. Coord Chem Rev 252(3+4):296-305.
16. Collins TJ, Powell RD, Slebodnick C, Uffelman ES (1990) A water-stable manganese(V)-oxo complex: Definitive assignment of a νMn(V)-O infrared vibration. J Am Chem Soc 112(2):899-901.
17. Lansky DE, et al. (2005) Synthesis, characterization, and physicochemical properties of manganese(III) and manganese(V)-oxo corrolazines. Inorg Chem 44(13):4485-4498.
18. Groves JT, Stern MK (1988) Synthesis, characterization, and reactivity of oxomanganese(IV) porphyrin complexes. J Am Chem Soc 110(26):8628-8638.
19. MacBeth CE, et al. (2004) Utilization of hydrogen bonds to stabilize M-O(H) units: Synthesis and properties of monomeric iron and manganese complexes with terminal oxo and hydroxo ligands. J Am Chem Soc 126(8):2556-2567.
20. Parsell TH, Behan RK, Green MT, Hendrich MP, Borovik AS (2006) Preparation and properties of a monomeric Mn(IV)-oxo complex. J Am Chem Soc 128(27):8728-8729.
21. Taguchi T, et al. (2012) Preparation and properties of a monomeric high-spin Mn(V)-oxo complex. J Am Chem Soc 134(4):1996-1999.
22. Taguchi T, et al. (2014) Preparation and properties of an MnIV-hydroxide complex: Proton and electron transfer at a mononuclear manganese site and its relationship to the oxygen evolving complex within photosystem II. Chem Sci 5(8):3064-3071.
23. Weng T-C, et al. (2004) XANES evidence against a manganyl species in the S3 state of the oxygen-evolving complex. J Am Chem Soc 126(26):8070-8071.
24. Yano J, et al. (2007) Polarized X-ray absorption spectroscopy of single-crystal Mn(V) complexes relevant to the oxygen-evolving complex of photosystem II. J Am Chem Soc 129(43):12989-13000.
25. Leto DF, Jackson TA (2014) Mn K-edge X-ray absorption studies of oxo- and hydroxomanganese(IV) complexes: Experimental and theoretical insights into pre-edge properties. Inorg Chem 53(12):6179-6194.
26. Stemmler TL, Sturgeon BE, Randall DW, Britt RD, Penner-Hahn JE (1997) Spectroscopic characterization of inhibitor interactions with the Mn(III)/Mn(IV) core in Lactobacillus plantarum manganese catalase. J Am Chem Soc 119(39):9215-9225.
27. Sinnecker S, Neese F, Noodleman L, Lubitz W (2004) Calculating the electron paramagnetic resonance parameters of exchange coupled transition metal complexes using broken symmetry density functional theory: Application to a MnIII/MnIV model compound. J Am Chem Soc 126(8):2613-2622.
28. Freeman AJ, Watson RE (1964) Magnetism, eds Rado, Suhl, Vol 2A, pp 167-305.
29. Munzarova M (2004) DFT calculations of EPR hyperfine coupling tensors. Calculation of NMR and EPR Parameters. Theory and Applications, eds Kaupp M, Buhl M, Malkin VG (Wiley-VCH, Weinheim, Germany), pp 463-482.
30. Usov OM, et al. (2007) Hyperfine coupling to the bridged 17O in the di-μ-oxo core of a MnIII-MnIV model significant to the core electronic structure of the O2-evolving complex in photosystem II. J Am Chem Soc 129(39):11886-11887.
31. Melamud E, Silver BL (1973) σ-π polarization parameters for oxygen-17 in organic and inorganic π radicals. J Phys Chem 77(15):1896-1900.
32. Gupta R, Taguchi T, Borovik AS, Hendrich MP (2013) Characterization of monomeric MnII/III/IV-hydroxo complexes from X- and Q-band dual mode electron paramagnetic resonance (EPR) spectroscopy. Inorg Chem 52(21):12568-12575.
33. Ye S, Neese F (2011) Nonheme oxo-iron(IV) intermediates form an oxyl radical upon approaching the C-H bond activation transition state. Proc Natl Acad Sci USA 108(4):1228-1233.
34. Srnec M, Wong SD, England J, Que L, Jr, Solomon EI (2012) π-Frontier molecular orbitals in S = 2 ferryl species and elucidation of their contributions to reactivity. Proc Natl Acad Sci USA 109(36):14326-14331.