PSII manganese cluster: Protonation of W2, O5, O4 and His337 in the S1 state explored by combined quantum chemical and electrostatic energy computations

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1837, Issue 8, 2014, Pages 1316-1321

  Robertazzi, Arturo ^a   Galstyan, Artur ^a   Knapp, Ernst Walter ^a  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

Mn cluster; pKa; Protonation of the OEC; PSII; Redox states

Indexed keywords

CALCIUM; HYDROXYL GROUP; MANGANESE; OXYGEN; PROTON; WATER;

ARTICLE; ATOM; CRYSTAL STRUCTURE; DENSITY FUNCTIONAL THEORY; DIELECTRIC CONSTANT; OXIDATION; OXIDATION REDUCTION STATE; PHOTOSYSTEM II; PRIORITY JOURNAL; PROTON TRANSPORT; STATIC ELECTRICITY;

MN-CLUSTER; PKA; PROTONATION OF THE OEC; PSII; REDOX STATES;

CRYSTALLOGRAPHY, X-RAY; ELECTRONS; HISTIDINE; IONS; MANGANESE; MODELS, CHEMICAL; OXIDATION-REDUCTION; OXYGEN; PHOTOSYNTHESIS; PHOTOSYSTEM II PROTEIN COMPLEX; PLANT LEAVES; THYLAKOIDS; WATER;

EID: 84901098819     PISSN: 00052728     EISSN: 18792650     Source Type: Journal    
DOI: 10.1016/j.bbabio.2014.03.018     Document Type: Article

References (41)

1. M. Leslie On the origin of photosynthesis Science 323 2009 1286 1287
2. N. Cox, D.A. Pantazis, F. Neese, and W. Lubitz Biological water oxidation Acc. Chem. Res. 46 2013 1588 1596
3. A. Zouni, H.T. Witt, J. Kern, P. Fromme, N. Krauß, W. Saenger, and P. Orth Crystal structure of photosystem II from Synechococcus elongatus at 3.8 A resolution Nature 409 2001 739 743 (Pubitemid 32144521)
4. N. Kamiya, and J.R. Shen Crystal structure of oxygen-evolving photosystem II from Thermosynechococcus vulcanus at 3.7-A resolution Proc. Natl. Acad. Sci. U. S. A. 100 2003 98 103 (Pubitemid 36078036)
5. K.N. Ferreira, T.M. Iverson, K. Maghlaoui, J. Barber, and S. Iwata Architecture of the photosynthetic oxygen-evolving center Science 2004 1831-1838 303
6. B. Loll, J. Kern, W. Saenger, A. Zouni, and J. Biesiadka Towards complete cofactor arrangement in the 3.0 Å resolution structure of Photosystem II Nature 438 2005 1040 1044 (Pubitemid 43093979)
7. A. Guskov, J. Kern, A. Gabdulkhakov, M. Broser, A. Zouni, and W. Saenger Cyanobacterial photosystem II at 2.9-A resolution and the role of quinones, lipids, channels and chloride Nat. Struct. Mol. Biol. 16 2009 334 342
8. Y. Umena, K. Kawakami, J.-R. Shen, and N. Kamiya Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å Nature 473 2011 55 61
9. A. Galstyan, A. Robertazzi, and E.W. Knapp Oxygen-evolving Mn Cluster in Photosystem II: The protonation pattern and oxidation state in the high-resolution crystal structure J. Am. Chem. Soc. 134 2012 7442 7449
10. H. Dau, P. Liebisch, and M. Haumann The structure of the manganese complex of Photosystem II in its dark-stable S1-state - EXAFS results in relation to recent crystallographic data Phys. Chem. Chem. Phys. 6 2004 4781 4792
11. M. Grabolle, M. Haumann, C. Müller, P. Liebisch, and H. Dau Rapid loss of structural motifs in the manganese complex of oxygenic photosynthesis by X-ray irradiation at 10-300 K J. Biol. Chem. 481 2006 4580 4588 (Pubitemid 43847716)
12. J. Yano, J. Kern, K.-D. Irrgang, M.J. Latimer, U. Bergmann, P. Glatzel, Y. Pushkar, J. Biesiadka, B. Loll, K. Sauer, J. Messinger, A. Zouni, and V.K. Yachandra X-ray damage to the Mn4Ca complex in single crystals of Photosystem II studied using in situ X-ray spectroscopy: a case study for metallo-protein crystallography Proc. Natl. Acad. Sci. U. S. A. 102 2005 12047 12052 (Pubitemid 41291126)
13. S. Luber, I. Rivalta, Y. Umena, K. Kawakami, J.R. Shen, N. Kamiya, G.W. Brudvig, and V.S. Batista S1-state model of the O2-evolving complex of Photosystem II Biochemistry 50 2011 6308 6311
14. K. Saito, and H. Ishikita Influence of the Ca2 + ion on the Mn4Ca conformation and the H-bond network arrangement in Photosystem II Biochim. Biophys. Acta 2014 1837 159 166
15. W. Ames, D.A. Pantazis, V. Krewald, N. Cox, J. Messinger, W. Lubitz, and F. Neese 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 2011 19743 19757
16. S. Petrie, P. Gatt, R. Stranger, and R.J. Pace Modelling the metal atom positions of the Photosystem II water oxidising complex: a density functional theory appraisal of the 1.9 Å resolution crystal structure Phys. Chem. Chem. Phys. 14 2012 11333 11343
17. P.E.M. Siegbahn Structures and energetics for O2 formation in Photosystem II Acc. Chem. Res. 2009 1871-1880 42
18. C.P. Aznar, and D.R. Britt Simulations of the (1)H electron spin echo-electron nuclear double resonance and (2)H electron spin echo envelope modulation spectra of exchangeable hydrogen nuclei coupled to the S(2)-state photosystem II manganese cluster Phil. Trans. R. Soc. B 357 2002 1359 1366 (Pubitemid 35293776)
19. M. Kusunoki S1-state Mn4Ca complex of Photosystem II exists in equilibrium between the two most-stable isomeric substates: XRD and EXAFS evidence J. Photochem. Photobiol. B 104 2011 100 110
20. L. Rapatskiy, N. Cox, A. Savitsky, W.M. Ames, J. Sander, M.M. Nowaczyk, M. Ragner, A. Boussac, F. Neese, J. Messinger, and W. Lubitz Detection of the water-binding sites of the oxygen-evolving complex of Photosystem II Using W-Band 17O Electron ÄìElectron double resonance-detected NMR spectroscopy J. Am. Chem. Soc. 134 2012 16619 16634
21. S. Petrie, P. Gatt, R. Stranger, and R.J. Pace The interaction of His337 with the Mn4Ca cluster of photosystem II Phys. Chem. Chem. Phys. 14 2012 4651 4657
22. M.S.a. Busch, and E.W. Knapp Accurate pk(a) determination for a heterogeneous group of organic molecules ChemPhysChem 5 2004 1513 1522
23. Jaguar 7.7 2010 Schrödinger, L.L.C. New York
24. A.D. Bochevarov, E. Harder, T.F. Hughes, J.R. Greenwood, D.A. Braden, D.M. Philipp, D. Rinaldo, M.D. Halls, J. Zhang, and R.A. Friesner Jaguar: a high-performance quantum chemistry software program with strengths in life and materials sciences Int. J. Quantum Chem. 113 2013 2110 2142
25. A.D. Becke Density-functional exchange-energy approximation with correct asymptotic behavior Phys. Rev. A 38 1988 3098 3100
26. C. Lee, W. Yang, and R.G. Paar Development of the Colle-Salvetti correlation-energy formula into a functional of the electron density Phys. Rev. B 37 1988 785 789
27. J.C. Slater Quantum theory of molecules and solids vol. 4 1974 McGraw-Hill New York
28. S.H. Vosko, L. Wilk, and M. Nusair Accurate spin-dependent electron liquid correlation energies for local spin density calculations: a critical analysis Can. J. Phys. 58 1980 1200 1211
29. P.J. Hay, and W.R. Wadt Ab initio effective core potentials for molecular calculations. Potentials for K to Au including the outermost core orbitals J. Chem. Phys. 82 1985 299 310
30. D. Koulougliotis, D.J. Hirsh, and G.W. Brudvig The oxygen-evolving center of photosystem II is diamagnetic in the S1 resting state J. Am. Chem. Soc. 114 1992 8322 8323
31. M. Gilson, and B. Honig The dielectric constant of a folded protein Biopolymers 25 1986 2097 2119
32. C.N. Schutz, and A. Warshel What are the dielectric "constants" of proteins and how to validate electrostatic models? Proteins 44 2001 400 417 (Pubitemid 32768578)
33. A. Galstyan, S.D. Zaric, and E.W. Knapp Computational studies on imidazole heme conformations J. Biol. Inorg. Chem. 10 2005 343 354 (Pubitemid 40922393)
34. D. Bashford, and K. Gerwert Electrostatic calculations of the pKa values of ionizable groups in bacteriorhodopsin J. Mol. Biol. 224 1992 473 486
35. A. Galstyan, and E.W. Knapp Accurate redox potentials of mononuclear iron, manganese, and nickel model complexes J. Comput. Chem. 30 2009 203 211
36. M. Schmidt am Busch, and E.W. Knapp Accurate pKa determination for a heterogeneous group of organic molecules ChemPhysChem 5 2004 1513 1522
37. G.M. Ullmann, and E.W. Knapp Electrostatic models for computing protonation and redox equilibria in proteins Eur. Biophys. J. 28 1999 533 551 (Pubitemid 29496251)
38. B. Rabenstein, and E.W. Knapp Problems evaluating energetics of electron transfer from QA to QB: the light exposed and dark-adapted bacterial reaction center Molecular Bioenergetics American Chemical Society vol. 883 2004 71 92
39. E.M. Sproviero, J.A. Gascón, J.P. McEvoy, G.W. Brudvig, and V.S. Batista Quantum mechanics/molecular mechanics study of the catalytic cycle of water splitting in photosystem II J. Am. Chem. Soc. 130 2008 3428 3442 (Pubitemid 351456044)
40. A. Grundmeier, and H. Dau Structural models of the manganese complex of Photosystem II and mechanistic implications Biochim. Biophys. Acta 2012 1817 88 105
41. D.A. Pantazis, W. Ames, N. Cox, W. Lubitz, and F. Neese 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 2012 9935 9939