Oxygen atom transfer and oxidative water incorporation in cuboidal Mn 3MOn complexes based on synthetic, isotopic labeling, and computational studies

Journal of the American Chemical Society

Volumn 135, Issue 3, 2013, Pages 1073-1082

  Kanady, Jacob S ^a   Mendoza Cortes, Jose L ^b   Tsui, Emily Y ^a   Nielsen, Robert J ^b   Goddard III, William A ^b   Agapie, Theodor ^a  

^a California Institute of Technology   (United States)

^b CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATALYTIC SITES; COMPUTATIONAL STUDIES; CUBANES; ISOTOPIC LABELING; MECHANISTIC STUDIES; OXYGEN ATOM; OXYGEN ATOM TRANSFER; OXYGEN-EVOLVING COMPLEXES; PARTIAL DETACHMENT; PHOTOSYSTEM II; REACTION PATHS; TRIMETHYLPHOSPHINES;

LIGANDS; MANGANESE; MANGANESE COMPOUNDS; OXYGEN; PHOSPHORUS COMPOUNDS; QUANTUM THEORY; SCANDIUM; SYNTHESIS (CHEMICAL); WATER TREATMENT;

MANGANESE REMOVAL (WATER TREATMENT);

LIGAND; MANGANESE DERIVATIVE; OXIDE; OXYGEN; OXYGEN 18; PHOSPHINE; WATER;

ARTICLE; ATOM; CATALYSIS; CHEMICAL REACTION; CYCLIC POTENTIOMETRY; ISOTOPE LABELING; MOLECULAR MODEL; OXIDATION; PHOTOSYSTEM II; QUANTUM MECHANICS; SOLID STATE; SYNTHESIS; X RAY DIFFRACTION;

CALCIUM; ISOTOPE LABELING; MANGANESE; OXIDATION-REDUCTION; OXYGEN; QUANTUM THEORY; SCANDIUM; WATER;

EID: 84872805339     PISSN: 00027863     EISSN: 15205126     Source Type: Journal    
DOI: 10.1021/ja310022p     Document Type: Article

References (85)

1. Gray, H. B. Nat. Chem. 2009, 1, 7-7
2. Lewis, N. S.; Nocera, D. G. Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 15729-15735
3. McEvoy, J. P.; Brudvig, G. W. Chem. Rev. 2006, 106, 4455-4483
4. Yano, J.; Kern, J.; Sauer, K.; Latimer, M. J.; Pushkar, Y.; Biesiadka, J.; Loll, B.; Saenger, W.; Messinger, J.; Zouni, A.; Yachandra, V. K. Science 2006, 314, 821-825
5. Peloquin, J. M.; Campbell, K. A.; Randall, D. W.; Evanchik, M. A.; Pecoraro, V. L.; Armstrong, W. H.; Britt, R. D. J. Am. Chem. Soc. 2000, 122, 10926-10942
6. Zouni, A.; Witt, H. T.; Kern, J.; Fromme, P.; Krauss, N.; Saenger, W.; Orth, P. Nature 2001, 409, 739-743
7. Ferreira, K. N.; Iverson, T. M.; Maghlaoui, K.; Barber, J.; Iwata, S. Science 2004, 303, 1831-1838
8. Umena, Y.; Kawakami, K.; Shen, J. R.; Kamiya, N. Nature 2011, 473, 55-U65
9. Luber, S.; Rivalta, I.; Umena, Y.; Kawakami, K.; Shen, J. R.; Kamiya, N.; Brudvig, G. W.; Batista, V. S. Biochemistry 2011, 50, 6308-6311
10. Rapatskiy, L.; Cox, N.; Savitsky, A.; Ames, W. M.; Sander, J.; Nowaczyk, M. M.; Rögner, M.; Boussac, A.; Neese, F.; Messinger, J.; Lubitz, W. J. Am. Chem. Soc. 2012, 134, 16619-16634
11. Joliot, P. Biochim. Biophys. Acta 1965, 102, 116-134
12. Kok, B.; Forbush, B.; Mcgloin, M. Photochem. Photobiol. 1970, 11, 457-475
13. Kolling, D. R. J.; Cox, N.; Ananyev, G. M.; Pace, R. J.; Dismukes, G. C. Biophys. J. 2012, 103, 313-322
14. Pecoraro, V. L.; Baldwin, M. J.; Caudle, M. T.; Hsieh, W. Y.; Law, N. A. Pure Appl. Chem. 1998, 70, 925-929
15. Pecoraro, V. L.; Hsieh, W. Y. The use of Model Complexes to Elucidate the Structure and Function of Manganese Redox Enzymes. In Manganese and its Role in Biological Systems, Sigel, A.; Sigel, H., Eds. Marcel Dekker, Inc.: New York, 2000; Vol. 37, pp 429-504.
16. Sproviero, E. M.; Gascon, J. A.; McEvoy, J. P.; Brudvig, G. W.; Batista, V. S. J. Am. Chem. Soc. 2008, 130, 3428-3442
17. McEvoy, J. P.; Gascon, J. A.; Batista, V. S.; Brudvig, G. W. Photochem. Photobiol. Sci. 2005, 4, 940-949
18. Yachandra, V. K.; Sauer, K.; Klein, M. P. Chem. Rev. 1996, 96, 2927-2950
19. Messinger, J. Phys. Chem. Chem. Phys. 2004, 6, 4764-4771
20. Siegbahn, P. E. M. Chem.-Eur. J. 2008, 14, 8290-8302
21. Siegbahn, P. E. M. Acc. Chem. Res. 2009, 42, 1871-1880
22. Siegbahn, P. E. M. ChemPhysChem 2011, 12, 3274-3280
23. Siegbahn, P. E. M. Phys. Chem. Chem. Phys. 2012, 14, 4849-4856
24. Ames, W.; Pantazis, D. A.; Krewald, V.; Cox, N.; Messinger, J.; Lubitz, W.; Neese, F. J. Am. Chem. Soc. 2011, 133, 19743-19757
25. Siegbahn, P. E. M. J. Am. Chem. Soc. 2009, 131, 18238-18239
26. Kusunoki, M. J. Photochem. Photobiol., B 2011, 104, 100-110
27. Pantazis, D. A.; Ames, W.; Cox, N.; Lubitz, W.; Neese, F. Angew. Chem., Int. Ed. 2012, 51, 9935-9940
28. McEvoy, J. P.; Brudvig, G. W. Phys. Chem. Chem. Phys. 2004, 6, 4754-4763
29. Haumann, M.; Liebisch, P.; Muller, C.; Barra, M.; Grabolle, M.; Dau, H. Science 2005, 310, 1019-1021
30. Najafpour, M. M.; Ehrenberg, T.; Wiechen, M.; Kurz, P. Angew. Chem., Int. Ed. 2010, 49, 2233-2237
31. Shevela, D.; Koroidov, S.; Najafpour, M. M.; Messinger, J.; Kurz, P. Chem.-Eur. J. 2011, 17, 5414-5422
32. Zaharieva, I.; Najafpour, M. M.; Wiechen, M.; Haumann, M.; Kurz, P.; Dau, H. Energy Environ. Sci. 2011, 4, 2400-2408
33. Mukhopadhyay, S.; Mandal, S. K.; Bhaduri, S.; Armstrong, W. H. Chem. Rev. 2004, 104, 3981-4026
34. Mullins, C. S.; Pecoraro, V. L. Coord. Chem. Rev. 2008, 252, 416-443
35. Brimblecombe, R.; Swiegers, G. F.; Dismukes, G. C.; Spiccia, L. Angew. Chem., Int. Ed. 2008, 47, 7335-7338
36. Hocking, R. K.; Brimblecombe, R.; Chang, L. Y.; Singh, A.; Cheah, M. H.; Glover, C.; Casey, W. H.; Spiccia, L. Nat. Chem. 2011, 3, 461-466
37. Mishra, A.; Wernsdorfer, W.; Abboud, K. A.; Christou, G. Chem. Commun. 2005, 54-56
38. Hewitt, I. J.; Tang, J. K.; Madhu, N. T.; Clerac, R.; Buth, G.; Anson, C. E.; Powell, A. K. Chem. Commun. 2006, 2650-2652
39. Kotzabasaki, V.; Siczek, M.; Lis, T.; Milios, C. J. Inorg. Chem. Commun. 2011, 14, 213-216
40. Koumousi, E. S.; Mukherjee, S.; Beavers, C. M.; Teat, S. J.; Christou, G.; Stamatatos, T. C. Chem. Commun. 2011, 47, 11128-11130
41. Nayak, S.; Nayek, H. P.; Dehnen, S.; Powell, A. K.; Reedijk, J. Dalton Trans. 2011, 40, 2699-2702
42. Park, Y. J.; Ziller, J. W.; Borovik, A. S. J. Am. Chem. Soc. 2011, 133, 9258-2961
43. Kanady, J. S.; Tsui, E. Y.; Day, M. W.; Agapie, T. Science 2011, 333, 733-736
44. Mukherjee, S.; Stull, J. A.; Yano, J.; Stamatatos, T. C.; Pringouri, K.; Stich, T. A.; Abboud, K. A.; Britt, R. D.; Yachandra, V. K.; Christou, G. Proc. Natl. Acad. Sci. U.S.A. 2012, 109, 2257-2262
45. Tsui, E. Y.; Day, M. W.; Agapie, T. Angew. Chem., Int. Ed. 2011, 50, 1668-1672
46. Tsui, E. Y.; Kanady, J. S.; Day, M. W.; Agapie, T. Chem. Commun. 2011, 47, 4189-4191
47. Ruettinger, W.; Ho, D.; Dismukes, G. Inorg. Chem. 1999, 38, 1036-1037
48. Ruettinger, W.; Carrell, T.; Baesjou, P.; Boelrijk, A.; Maneiro, M.; Dismukes, G. J. Inorg. Biochem. 1999, 74, 88-88
49. Wang, S. Y.; Folting, K.; Streib, W. E.; Schmitt, E. A.; McCusker, J. K.; Hendrickson, D. N.; Christou, G. Angew. Chem., Int. Ed. 1991, 30, 305-306
50. Wang, S. Y.; Tsai, H. L.; Hagen, K. S.; Hendrickson, D. N.; Christou, G. J. Am. Chem. Soc. 1994, 116, 8376-8377
51. Aubin, S. M. J.; Wemple, M. W.; Adams, D. M.; Tsai, H. L.; Christou, G.; Hendrickson, D. N. J. Am. Chem. Soc. 1996, 118, 7746-7754
52. Aromi, G.; Wemple, M. W.; Aubin, S. J.; Folting, K.; Hendrickson, D. N.; Christou, G. J. Am. Chem. Soc. 1998, 120, 5850-5851
53. Aliaga-Alcalde, N.; Edwards, R. S.; Hill, S. O.; Wernsdorfer, W.; Folting, K.; Christou, G. J. Am. Chem. Soc. 2004, 126, 12503-12516
54. Beck, W. F.; Brudvig, G. W. Biochemistry 1987, 26, 8285-8295
55. Brudvig, G. W.; Beck, W. F. Oxidation-Reduction and Ligand-Substitution Reactions of The Oxygen-Evolving Center of Photosystem II. In Manganese Redox Enzymes; Pecoraro, V. L., Ed.; VCH Publishers, Inc.: New York, 1992; pp 119-140.
56. Messinger, J.; Seaton, G.; Wydrzynski, T.; Wacker, U.; Renger, G. Biochemistry 1997, 36, 6862-6873
57. Schansker, G.; Goussias, C.; Petrouleas, V.; Rutherford, A. W. Biochemistry 2002, 41, 3057-3064
58. Cheniae, G. M.; Martin, I. F. Biochem. Biophys. Res. Commun. 1967, 28, 89-95
59. Siegbahn, P. E. M. J. Biol. Inorg. Chem. 2006, 11, 695-701
60. Lundberg, M.; Blomberg, M. R. A.; Siegbahn, P. E. M. Inorg. Chem. 2004, 43, 264-274
61. Lundberg, M.; Siegbahn, P. E. M. J. Comput. Chem. 2005, 26, 661-667
62. Sproviero, E. M.; Gascon, J. A.; McEvoy, J. P.; Brudvig, G. W.; Batista, V. S. J. Inorg. Biochem. 2006, 100, 786-800
63. Orio, M.; Pantazis, D. A.; Petrenko, T.; Neese, F. Inorg. Chem. 2009, 48, 7251-7260
64. Baik, M. H.; Friesner, R. A. J. Phys. Chem. A 2002, 106, 7407-7412
65. Wieghardt, K.; Bossek, U.; Zsolnai, L.; Huttner, G.; Blondin, G.; Girerd, J. J.; Babonneau, F. J. Chem. Soc., Chem. Commun. 1987, 651-653
66. Chow, W. S.; Aro, E. M. Photoinactivation and Mechanisms of Recovery. In The Light-Driven Water: Plastoquinone Oxidoreductase; Wydrzynski, T. J.; Satoh, K., Eds.; Springer: Dordrecht, 2005; Vol. 22, pp 627-648.
67. Miller, A. F.; Brudvig, G. W. Biochemistry 1989, 28, 8181-8190
68. Miller, A. F.; Brudvig, G. W. Biochemistry 1990, 29, 1385-1392
69. Burnap, R. L. Phys. Chem. Chem. Phys. 2004, 6, 4803-4809
70. Campbell, K. A.; Force, D. A.; Nixon, P. J.; Dole, F.; Diner, B. A.; Britt, R. D. J. Am. Chem. Soc. 2000, 122, 3754-3761
71. Tyryshkin, A. M.; Watt, R. K.; Baranov, S. V.; Dasgupta, J.; Hendrich, M. P.; Dismukes, G. C. Biochemistry 2006, 45, 12876-12889
72. Dasgupta, J.; Tyryshkin, A. M.; Baranov, S. V.; Dismukes, G. C. Appl. Magn. Reson. 2010, 37, 137-150
73. Zaltsman, L.; Ananyev, G. M.; Bruntrager, E.; Dismukes, G. C. Biochemistry 1997, 36, 8914-8922
74. Dasgupta, J.; Ananyev, G. M.; Dismukes, G. C. Coordin. Chem. Rev. 2008, 252, 347-360
75. Ananyev, G. M.; Dismukes, G. C. Biochemistry 1997, 36, 11342-11350
76. 18O, %): 0, 9%; 1, 61%; 2, 17%; 3, 9%; 4, 4%; isotopologue percentages of 3: 0, 28%; 1, 52%; 2, 15%; 3, 5%.
77. 3CN solvent mixture was utilized throughout the study. Calculations of expected isotope distribution for different mechanisms takes into account the incorporation percentage in 2 * and 3.
78. Tagore, R.; Chen, H. Y.; Crabtree, R. H.; Brudvig, G. W. J. Am. Chem. Soc. 2006, 128, 9457-9465
79. Ohlin, C. A.; Brimblecombe, R.; Spiccia, L.; Casey, W. H. Dalton Trans. 2009, 5278-5280
80. Messinger, J.; Badger, M.; Wydrzynski, T. Proc. Natl. Acad. Sci. U.S.A. 1995, 92, 3209-3213
81. Hillier, W.; Messinger, J.; Wydrzynski, T. Biochemistry 1998, 37, 16908-16914
82. Hillier, W.; Messinger, J.; Wydrzynski, T. Photosynthesis: Mechanisms and Effects; Kluwer Academic Publishers: Dordrecht, 1998; Vol I-V, pp 1307-1310.
83. Hillier, W.; Wydrzynski, T. Biochemistry 2000, 39, 4399-4405
84. Hillier, W.; Wydrzynski, T. Phys. Chem. Chem. Phys. 2004, 6, 4882-4889
85. Hillier, W.; Wydrzynski, T. Coord. Chem. Rev. 2008, 252, 306-317