Glutamate-354 of the CP43 polypeptide interacts with the oxygen-evolving Mn4Ca cluster of photosystem II: A preliminary characterization of the Glu354Gln mutant

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 363, Issue 1494, 2008, Pages 1179-1188

  Strickler, Melodie A ^a   Hwang, Hong Jin ^b   Burnap, Robert L ^b   Yano, Junko ^c   Walker, Lee M ^a   Service, Rachel J ^a   Britt, R David ^d   Hillier, Warwick ^e   Debus, Richard J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b OKLAHOMA STATE UNIVERSITY   (United States)

^c LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

Author keywords

Fourier transform infrared spectroscopy (FTIR); Mn cluster; Oxygen evolution; S state cycle; Site directed mutagenesis; Water oxidation

Indexed keywords

CALCIUM; COMPARATIVE STUDY; CYANOBACTERIUM; ELECTRON SPIN RESONANCE; FTIR SPECTROSCOPY; MANGANESE; MUTATION; OXIDATION; OXYGEN; PEPTIDE; PHOTOSYNTHESIS; REACTION KINETICS; SULFUR; WATER; X-RAY SPECTROSCOPY;

SYNECHOCYSTIS; SYNECHOCYSTIS SP.; SYNECHOCYSTIS SP. PCC 6803;

EID: 38949175451     PISSN: 09628436     EISSN: None     Source Type: Journal    
DOI: 10.1098/rstb.2007.2213     Document Type: Article

References (51)

1. Barth, A. 2007 Infrared spectroscopy of proteins. Biochim. Biophys. Acta 1767, 1073-1101. (doi:10.1016/j.bbabio.2007.06.004)
2. Barth, A. & Zscherp, C. 2002 What vibrations tell us about proteins. Q. Rev. Biophys. 35, 369-430. (doi:10.1017/S0033583502003815)
3. Bricker, T. M. & Frankel, L. K. 2002 The structure and function of CP47 and CP43 in photosystem II. Photosynth. Res. 72, 131-146. (doi:10.1023/A:1016128715865)
4. 2O oxidation complex in Synechocystis sp, PCC 6803. Biochemistry 35, 874-882. (doi:10.1021/bi951964j)
5. Chu, H.-A., Nguyen, A. P. & Debus, R. J. 1994 Site-directed photosystem ii mutants with perturbed oxygen evolving properties: 1. Instability or inefficient assembly of the manganese cluster in vivo. Biochemistry 33, 6137-6149. (doi:10.1021/bi00186a013)
6. Chu, H.-A., Hillier, W., Law, N. A. & Babcock, G. T. 2001 Vibrational spectroscopy of the oxygen-evolving complex and of manganese model compounds. Biochim. Biophys. Acta 1503, 69-82. (doi:10.1016/S0005-2728(00) 00216-4)
7. 2 transition: an isotope-edited FTIR study. Biochemistry 43, 3152-3166. (doi:10.1021/bi035915f)
8. Deacon, G. B. & Phillips, R. J. 1980 Relationships between the carbon-oxygen stretching frequencies of carboxylato complexes and the type of carboxylate coordination. Coord. Chem. Rev. 33, 227-250. (doi:10.1016/S0010-8545(00)80455-5)
9. Debus, R. J. In press. Protein ligation of the photosynthetic oxygen-evolving center. Coord. Chem. Rev.
10. 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)
11. 3 transitions in photosystem II. Biochemistry 44, 1367-1374. (doi:10.1021/bi047558u)
12. 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)
13. Goldfarb, N., Knoepfle, N. & Putnam-Evans, C. 1997 Contruction of a psbC deletion strain in Synechocystis 6803. SAAS Bull. Biochem. Biotechnol. 10, 1-6.
14. Goussias, C., Boussac, A. & Rutherford, A. W. 2002 Photosystem II and photosynthetic oxidation of water: an overview. Phil. Trans. R. Soc. B 357, 1369-1381. (doi:10.1098/rstb.2002.1134)
15. Grabolle, M., Haumann, M., Müller, C., Liebisch, P. & Dau, H. 2006 Rapid loss of structural motifs in the manganese complex of oxygenic photosynthesis by X-ray irradiation at 10-300 K. J. Biol. Chem. 281, 4580-4588. (doi:10.1074/jbc.M509724200)
16. Hillier, W. & Messinger, J. 2005 Mechanism of photosynthetic oxygen production. In Photosystem II: the light-driven water: plastoquinone oxidoreductase (eds T. Wydrzynski & Ki. Satoh), pp. 567-608. Dordrecht, The Netherlands: Springer.
17. 1 FTIR difference spectrum of oxygen-evolving complex. Biochemistry 42, 13 170-13 177. (doi:10.1021/bi035420q)
18. Kimura, Y., Hasegawa, K., Yamanari, T. & Ono, T.-A. 2005a Studies on photosynthetic oxygen-evolving complex by means of Fourier transform infrared spectroscopy: calcium and chloride cofactors. Photosynth. Res. 84, 245-250. (doi:10.1007/s11120-005-0412-z)
19. Kimura, Y., Mizusawa, N., Ishii, A., Nakazawa, S. & Ono, T.-A. 2005b Changes in structural and functional properties of oxygen-evolving complex induced by replacement of D1-glutamate 189 with glutamine in photosystem II: ligation of glutamate 189 carboxylate to the manganese cluster. J. Biol. Chem. 280, 37 895-37 900. (doi:10.1074/jbc.M505887200)
20. Kimura, Y., Mizusawa, N., Yamanari, T., Ishii, A. & Ono, T.-A. 2005c Structural changes of D1 C-terminal α-carboxylate during S-state cycling of photosynthetic oxygen evolution. J. Biol. Chem. 280, 2078-2083. (doi:10.1074/jbc.M410627200)
21. Lavorel, J. 1976 Matrix analysis of the oxygen evolving system of photosynthesis. J. Theor. Biol. 57, 171-185. (doi:10.1016/S0022- 5193(76)80011-2)
22. 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)
23. Mäntele, W. 1996 Infrared and Fourier-transform infrared spectroscopy. In Biophysical techniques in photosynthesis (eds J. Amesz & A. J. Hoff ), pp. 137-160. Dordrecht, The Netherlands: Kluwer Academic Publishers.
24. McEvoy, J. P. & Brudvig, G. W. 2006 Water-splitting chemistry of photosystem II. Chem. Rev. 106, 4455-4483. (doi:10.1021/cr0204294)
25. McEvoy, J. P., Gascón, J. A., Batista, V. S. & Brudvig, G. W. 2005 The mechanism of photosynthetic water splitting. Photobiochem. Photobiophys. Sci. 4, 940-949. (doi:10.1039/b506755c)
26. Meunier, P. C., Burnap, R. L. & Sherman, L. A. 1995 Modelling of the S-state mechanism and photosystem II manganese photoactivation in Cyanobacteriae. Photosynth. Res. 47, 61-76. (doi:10.1007/ BF00017754)
27. Mizusawa, N., Kimura, Y., Ishii, A., Yamanari, T., Nakazawa, S., Teramoto, H. & Ono, T.-A. 2004a Impact of replacement of D1 C-terminal alanine with glycine on structure and function of photosynthetic oxygen-evolving complex. J. Biol. Chem. 279, 29 622-29 627. (doi:10.1074/jbc.M402397200)
28. Mizusawa, N., Yamanari, T., Kimura, Y., Ishii, A., Nakazawa, S. & Ono, T.-A. 2004b Changes in the functional and structural properties of the Mn cluster induced by replacing the side group of the C-terminus of the D1 protein of photosystem II. Biochemistry 43, 14 644-14 652. (doi:10.1021/bi0486076)
29. Nakamoto, K. 1997 Infrared and Raman spectra of inorganic and coordination compounds, Part b: applications in coordination, organometallic, and bioinorganic chemistry, 5th edn. New York, NY: Wiley.
30. Nara, M., Torii, H. & Tasumi, M. 1996 Correlation between the vibrational frequencies of the carboxylate group and types of its coordination to a metal ion: an ab Initio molecular orbital study. J. Phys. Chem. 100, 19 812-19 817. (doi:10.1021/jp9615924)
31. Noguchi, T. 2007 Light-induced FTIR difference spectroscopy as a powerful tool toward understanding the molecular mechanism of photosynthetic oxygen evolution. Photosyn. Res. 91, 59-69. (doi:10.1007/s11120-007-9137- 5)
32. Noguchi, T. In press. Fourier transform infrared analysis of the photosynthetic oxygen-evolving center. Coord. Chem. Rev.
33. Noguchi, T. & Berthomieu, C. 2005 Molecular analysis by vibrational spectroscopy. In Photosystem II: the light-driven water:plastoquinone oxidoreductase (eds T. Wydrzynski & Ki. Satoh), pp. 367-387. Dordrecht, The Netherlands: Springer.
34. Noguchi, T. & Sugiura, M. 2002 Flash-induced FTIR difference spectra of the water oxidizing complex in moderately hydrated photosystem II core films: effect of hydration extent on S-state transitions. Biochemistry 41, 2322-2330. (doi:10.1021/bi011954k)
35. 13C isotope labeling. Biochemistry 42, 6035-6042. (doi:10.1021/bi0341612)
36. 2+ in the photosynthetic oxygen-evolving center by means of Fourier transform infrared spectroscopy. Biochim. Biophys. Acta 1228, 189-200. (doi:10.1016/0005-2728(94) 00171-Z)
37. 2O-oxidation in Synechocystis sp, PCC 6803. Biochemistry 38, 6070-6081. (doi:10.1021/bi982331i)
38. Rosenberg, C., Christian, J., Bricker, T. M. & Putnam-Evans, C. 1999 Site-directed mutagenesis of glutamate residues in the large extrinsic loop of the photosystem II protein CP 43 affects oxygen-evolving activity and PSII assembly. Biochemistry 38, 15 994-16 000. (doi:10.1021/bi991326r)
39. Sauer, K. & Yachandra, V. K. 2004 The water-oxidation complex in photosynthesis. Biochim. Biophys. Acta 1655, 140-148. (doi:10.1016/j.bbabio.2003.07.004)
40. 4Ca cluster in the water-oxidation complex of photosystem II. Photosyn. Res. 85, 73-86. (doi:10.1007/s11120-005-0638-9)
41. 2-evolving complex of photosystem II. J. Chem. Theory Comput. 2, 1119-1134. (doi:10.1021/ct060018l)
42. Strickler, M. A., Walker, L. M., Hillier, W. & Debus, R. J. 2005 Evidence from biosynthetically incorporated strontium and FTIR difference spectroscopy that the C-terminus of the D1 polypeptide of photosystem II does not ligate calcium. Biochemistry 44, 8571-8577. (doi:10.1021/bi050653y)
43. 3 transitions in photosystem II. Biochemistry 45, 8801-8811. (doi:10.1021/ bi060583a)
44. 3 transitions in photosystem II. Biochemistry 46, 3151-3160. (doi:10.1021/bi062195e)
45. 2+ exchange in the S-state cycle of photosynthetic oxygen evolution as studied by flash-induced FTIR difference spectroscopy. Biochemistry 45, 13 454-13 464. (doi:10.1021/bi061232z)
46. 2+ depletion as revealed by FTIR difference spectroscopy. Biochim. Biophys. Acta 1767, 535-540. (doi:10.1016/j.bbabio.2006.11.002)
47. Tang, X.-S. & Diner, B. A. 1994 Biochemical and spectroscopic characterization of a new oxygen-evolving photosystem II core complex from the Cyanobacterium Synechocystis sp, PCC 6803. Biochemistry 33, 4594-4603. (doi:10.1021/bi00181a021)
48. Yachandra, V. K. 2005 The catalytic manganese cluster: organization of the metal ions. In Photosystem II: the lightdriven water:plastoquinone oxidoreductase (eds T. Wydrzynski & Ki. Satoh), pp. 235-260. Dordrecht, The Netherlands: Springer.
49. Yamanari, T., Kimura, Y., Mizusawa, N., Ishii, A. & Ono, T.-A. 2004 Mid- to low-frequency Fourier transform infrared spectra of S-state cycle for photosynthetic water oxidation in Synechocystis sp, PCC 6803. Biochemistry 43, 7479-7490. (doi:10.1021/bi0362323)
50. 4Ca complex in single crystals of photosystem II: a case study for metalloprotein crystallography. Proc. Natl Acad. Sci. USA 102, 12 047-12 052. (doi:10.1073/pnas.0505207102)
51. 4Ca cluster. Science 314, 821-825. (doi:10.1126/science.1128186)