Multifrequency electron spin-echo envelope modulation studies of nitrogen ligation to the manganese cluster of photosystem II

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 363, Issue 1494, 2008, Pages 1157-1166

  Yeagle, Gregory J ^a   Gilchrist Jr , M Lane ^c   Walker, Lee M ^b   Debus, Richard J ^b   Britt, R David ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c CITY COLLEGE OF NEW YORK   (United States)

Author keywords

Histidine ligation; Manganese cluster; Multifrequency electron spin echo envelope modulation; Photosystem II

Indexed keywords

AMINO ACID; ELECTRON SPIN RESONANCE; MANGANESE; MICROWAVE RADIATION; NITROGEN; PHOTOSYNTHESIS; SPECTROMETER; SULFUR;

EID: 38949172108     PISSN: 09628436     EISSN: None     Source Type: Journal    
DOI: 10.1098/rstb.2007.2211     Document Type: Article

References (29)

1. Allahverdiyeva, Y., Deak, Z., Szilard, A., Diner, B. A., Nixon, P. J. & Vass, I. 2004 The function of D1-H332 in photosystem II electron transport studied by thermoluminescence and chlorophyll fluorescence in site-directed mutants of Synechocystis 6803. Eur. J. Biochem. 27, 3523-3532. (doi:10.1111/j.0014-2956.2004.04287.x)
2. Britt, R.D., Zimmermann, J. L., Sauer,K.&Klein, M. P. 1989 Ammonia binds to the catalytic manganese of the oxygen-evolving complex of photosystem II. Evidence by electron spin-echo envelope modulation spectroscopy. J. Am. Chem. Soc. 111, 3522-3532. (doi:10.1021/ja00192a006)
3. Britt, R. D., Campbell, K. A., Peloquin, J. M., Gilchrist, M. L., Aznar, C. P., Dicus, M. M., Robblee, J. & Messinger, J. 2004 Recent pulsed EPR studies of the photosystem II oxygen-evolving complex: implications as to water oxidation mechanisms. Biochim. Biophys. Acta 1655, 158-171. (doi:10.1016/j.bbabio.2003.11.009)
4. Campbell, K. A., Force, D. A., Nixon, P. J., Dole, F., Diner, B. A. & Britt, R. D. 2000 Dual-Mode EPR detects the initial intermediate in photoassembly of the photosystem II Mn cluster: the influence of amino acid residue 170 of the D1 polypeptide on Mn coordination. J. Am. Chem. Soc. 122, 3754-3761. (doi:10.1021/ja000142t)
5. Chu, H.-A., Nguyen, A. P. & Debus, R. J. 1995 Amino acid residues that influence the binding of manganese or calcium to photosystem II. 1. The lumenal interhelical domains of the D1 polypeptide. Biochemistry 34, 5839-5858. (doi:10.1021/bi00017a016)
6. Debus, R. J. 1992 The manganese and calcium ions of photosynthetic oxygen evolution. Biochim. Biophys. Acta 1102, 269-352. (doi:10.1016/0005-2728(92)90133-M)
7. Z in photosystem II. Biochemistry 39, 470-478. (doi:10.1021/bi9917737)
8. Debus, R. J., Campbell, K. A., Gregor, W., Li, Z.-L., Burnap, R. L. & Britt, R. D. 2001 Does histidine 332 of the D1 polypeptide ligate the manganese cluster in photosystem II? An electron spin echo envelope modulation study. Biochemistry 40, 3690-3699. (doi:10.1021/bi002394c)
9. Debus, R. J., Strickler, M. A., Walker, L. M. & Hillier, W. 2005 No evidence from FTIR difference spectroscopy that aspartate-170 of the D1 polypeptide ligates a manganese ion that undergoes oxidation during the S0 to S1, S1 to S2, or S2 to S3 transitions in photosystem II. Biochemistry 44, 1367-1374. (doi:10.1021/bi047558u)
10. Dismukes, G. C. & Siderer, Y. 1981 Intermediates of a polynuclear manganese center involved in photosynthetic oxidation of water. Proc. Natl Acad. Sci. USA 78, 274-278. (doi:10.1073/pnas.78.1.274)
11. Ferreira, K. N., Iverson, T. M., Maghlaoui, K., Barber, J. & Iwata, S. 2004 Architecture of the photosynthetic oxygen-evolving center. Science 303, 1831-1838. (doi:10.1126/science.1093087)
12. Flanagan, H. L. & Singel, D. J. 1987 The impact of excitation frequency on the nuclear modulation of electron spin echoes: nitrogen-14 hyperfine and quadrupole interactions of DPPH in disordered solids. Chem. Phys. Lett. 137, 391-397. (doi:10.1016/0009-2614(87)80906-5)
13. Gilchrist, M. L. 1996 Pulsed electron paramagnetic resonance of photosynthetic oxygen evolution. PhD thesis, University of California, Davis, CA, USA.
14. Goldfarb,D. 2006 High field ENDOR as a characterizationtool for functional sites in microporous materials. Phys. Chem. Chem. Phys. 8, 2325-2343. (doi:10.1039/b601513c)
15. 2 formation tracked by time-resolved X-ray experiments. Science 310, 1019-1021. (doi:10.1126/science. 1117551)
16. Kevan, L. & Schwartz, R. N. 1979 Modulation of electron spin-echo decay in solids. In Time domain electron spin resonance (eds L. Kevan & R. N. Schwartz), pp. 279-341. New York, NY: Wiley.
17. Kok, B., Forbush, B. & McGloin, M. 1970 Coorperation and charges in phototsynthetic oxygen evolution. I. A linear four step mechanism. Photochem. Photobiol. 11, 457-475.
18. Krzystek, J., Ozarowski, A. & Telser, J. 2006 Multi-frequency, high-field EPR as a powerful tool to accurately determine zero-field splitting in high-spin transition metal coordination complexes. Coord. Chem. Rev. 250, 2308-2324. (doi:10.1016/j.ccr.2006.03.016)
19. Kulik, L. V., Lubitz, W. & Messinger, J. 2005 Electron spin-lattice relaxation of the S0 state of the oxygen-evolving complex in photosystem II and of dinuclear manganese model complexes. Biochemistry 44, 9368-9374. (doi:10.1021/bi050411y)
20. Lai, A., Flanagan, H. L. & Singel, D. J. 1989 Multifrequency electron spin echo envelope modulation in S=1/2, I=1/2 systems: analysis of the spectral amplitudes, line shapes, and linewidths. J. Chem. Phys. 89, 7161-7166. (doi:10.1063/1.455293)
21. Loll, B., Kern, J., Saenger,W., Zouni, A. & Biesiadka, J. 2005 Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II. Nature 438, 1040-1044. (doi:10.1038/nature04224)
22. 0-state manganese cluster in single crystals of cyanobacterial photosystem II studied by W-band electron paramagnetic resonance spectroscopy. J. Phys. Chem. B 110, 13 242-13 247. (doi:10.1021/jp055008f)
23. McEvoy, J. P. & Brudvig, G. W. 2006 Water-splitting chemistry of photosystem II. Chem. Rev. 106, 4455-4483. (doi:10.1021/cr0204294)
24. Mims, W. B. 1972 Envelope modulation in spin-echo experiments. Phys. Rev. B 5, 2409-2419. (doi:10.1103/PhysRevB.5.2409)
25. Peloquin, J. M., Campbell, K. A., Randall, D. W., Evanchik, M. A., Pecoraro, V. L., Armstrong, W. H. & Britt, R. D. 2000 55Mn ENDOR of the S2-state multiline EPR signal of photosystem II: implications on the structure of the tetranuclear Mn cluster. J. Am. Chem. Soc. 122, 10 926-10 942. (doi:10.1021/ja002104f)
26. Stich, T. A., Lahiri, S., Yeagle, G. J., Dicus, M., Brynda, M., Gunn, A., Aznar, C., DeRose, V. J. & Britt, R. D. 2007 Multifrequency pulsed EPR studies of biologically relevant manganese(II ) complexes. Appl. Magn. Reson. 3, 321-341.
27. Sturgeon, B. E. & Britt, R. D. 1992 Sensitive pulsed EPR spectrometer with an 8-18 GHz frequency range. Rev. Sci. Instrum. 63, 2187-2192. (doi:10.1063/1.1143136)
28. Tang, X. S., Diner, B. A., Larsen, B. S., Gilchrist, M., Lane, J., Lorigan, G. A. & Britt, R. D. 1994 Identification of histidine at the catalytic site of the photosynthetic oxygen-evolving complex. Proc. Natl Acad. Sci. USA 91, 704-708. (doi:10.1073/pnas.91.2.704)
29. 4Ca cluster. Science 314, 821-825. (doi:10.1126/science.1128186)