ATR-FTIR detection of metal-sensitive structural changes in the light-harvesting 1 reaction center complex from the thermophilic purple sulfur bacterium Thermochromatium tepidum

Biochemistry

Volumn 52, Issue 50, 2013, Pages 9001-9008

  Li, Yong ^a   Kimura, Yukihiro ^a   Arikawa, Teruhisa ^a   Wang Otomo, Zheng Yu ^b   Ohno, Takashi ^a  

^a KOBE UNIVERSITY   (Japan)

^b IBARAKI UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ATTENUATED TOTAL REFLECTIONS; COMPARATIVE ANALYSIS; HIGHEST TEMPERATURE; MESOPHILIC COUNTERPARTS; MOLECULAR MECHANISM; POLYPEPTIDE BACKBONES; STRUCTURAL INFORMATION; STRUCTURAL MODIFICATIONS;

AMINO ACIDS; BACTERIA; CALCIUM; METALS; THERMODYNAMIC STABILITY;

FOURIER TRANSFORM INFRARED SPECTROSCOPY;

AMINO ACID; BARIUM ION; CADMIUM; CALCIUM ION; POLYPEPTIDE; STRONTIUM;

ABSORPTION; ALLOCHROMATIUM VINOSUM; ARTICLE; ATTENUATED TOTAL REFLECTION; BINDING SITE; CALCIUM BINDING; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; ENVIRONMENTAL TEMPERATURE; HYDROGEN BOND; INFRARED SPECTROSCOPY; LIGHT HARVESTING SYSTEM; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE; PROTEOBACTERIA; SIGNAL TRANSDUCTION; SULFUR BACTERIUM; THERMOCHROMATIUM TEPIDUM; THERMOPHILIC BACTERIUM; THERMOSTABILITY;

EID: 84890499882     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi401033y     Document Type: Article

References (55)

1. Cogdell, R. J., Gall, A., and Kohler, J. (2006) The architecture and function of the light-harvesting apparatus of purple bacteria: From single molecules to in vivo membranes Q. Rev. Biophys. 39, 227-324 (Pubitemid 44963429)
2. Roszak, A. W., Howard, T. D., Southall, J., Gardiner, A. T., Law, C. J., Isaacs, N. W., and Cogdell, R. J. (2003) Crystal structure of the RC-LH1 core complex from Rhodopseudomonas palustris Science 302, 1969-1972 (Pubitemid 37523505)
3. Karrasch, S., Bullough, P. A., and Ghosh, R. (1995) The 8.5 angstrom projection map of the light-harvesting complex I from Rhodospirillum rubrum reveals a ring composed of 16 subunits EMBO J. 14, 631-638
4. Scheuring, S., Seguin, J., Marco, S., Levy, D., Robert, B., and Rigaud, J. L. (2003) Nanodissection and high-resolution imaging of the Rhodopseudomonas viridis photosynthetic core complex in native membranes by AFM Proc. Natl. Acad. Sci. U.S.A. 100, 1690-1693 (Pubitemid 36254509)
5. Scheuring, S., Francia, F., Busselez, J., Melandri, B. A., Rigaud, J. L., and Levy, D. (2004) Structural role of PufX in the dimerization of the photosynthetic core complex of Rhodobacter sphaeroides J. Biol. Chem. 279, 3620-3626 (Pubitemid 38140603)
6. Fotiadis, D., Qian, P., Philippsen, A., Bullough, P. A., Engel, A., and Hunter, C. N. (2004) Structural analysis of the reaction center light-harvesting complex I photosynthetic core complex of Rhodospirillum rubrum using atomic force microscopy J. Biol. Chem. 279, 2063-2068 (Pubitemid 38084478)
7. Qian, P., Hunter, C. N., and Bullough, P. A. (2005) The 8.5 angstrom projection structure of the core RC-LH1-PufX dimer of Rhodobacter sphaeroides J. Mol. Biol. 349, 948-960 (Pubitemid 40779618)
8. Madigan, M. T. (1984) A novel photosynthetic purple bacterium isolated from a Yellowstone hot-spring Science 225, 313-315
9. Madigan, M. T. (2003) Anoxygenic phototrophic bacteria from extreme environments Photosynth. Res. 76, 157-171 (Pubitemid 37060523)
10. Wang, Z.-Y., Shimonaga, M., Suzuki, H., Kobayashi, M., and Nozawa, T. (2003) Purification and characterization of the polypeptides of core light-harvesting complexes from purple sulfur bacteria Photosynth. Res. 78, 133-141 (Pubitemid 37551471)
11. Nogi, T., Fathir, I., Kobayashi, M., Nozawa, T., and Miki, K. (2000) Crystal structures of photosynthetic reaction center and high-potential iron-sulfur protein from Thermochromatium tepidum: Thermostability and electron transfer Proc. Natl. Acad. Sci. U.S.A. 97, 13561-13566
12. Kobayashi, M., Fujioka, Y., Mori, T., Terashima, M., Suzuki, H., Shimada, Y., Saito, T., Wang, Z.-Y., and Nozawa, T. (2005) Reconstitution of photosynthetic reaction centers and core antenna-reaction center complexes in liposomes and their thermal stability Biosci., Biotechnol., Biochem. 69, 1130-1136 (Pubitemid 41006941)
13. Watson, A. J., Hughes, A. V., Fyfe, P. K., Wakeham, M. C., Holden-Dye, K., Heathcote, P., and Jones, M. R. (2005) On the role of basic residues in adapting the reaction centre-LH1 complex for growth at elevated temperatures in purple bacteria Photosynth. Res. 86, 81-100 (Pubitemid 41361263)
14. y transition of the core complex in thermophilic purple sulfur bacterium Thermochromatium tepidum J. Biol. Chem. 283, 13867-13873
15. Kimura, Y., Yu, L. J., Hirano, Y., Suzuki, H., and Wang, Z.-Y. (2009) Calcium ions are required for the enhanced thermal stability of the light-harvesting-reaction center core complex from thermophilic purple sulfur bacterium Thermochromatium tepidum J. Biol. Chem. 284, 93-99
16. 2+-binding site in the light-harvesting complex 1 of thermophilic purple sulfur bacterium Thermochromatium tepidum Photosynth. Res. 106, 215-220
17. Barth, A. and Zscherp, C. (2002) What vibrations tell us about proteins Q. Rev. Biophys. 35, 369-430 (Pubitemid 36207229)
18. Baenziger, J. E., Miller, K. W., and Rothschild, K. J. (1992) Incorporation of the nicotinic acetylcholine-receptor into planar multilamellar films: Characterization by fluorescence and Fourier-transform infrared difference spectroscopy Biophys. J. 61, 983-992
19. Ryan, S. E., Hill, D. G., and Baenziger, J. E. (2002) Dissecting the chemistry of nicotinic receptor-ligand interactions with infrared difference spectroscopy J. Biol. Chem. 277, 10420-10426 (Pubitemid 34968162)
20. Iwaki, M., Cotton, N. P. J., Quirk, P. G., Rich, P. R., and Jackson, J. B. (2006) Molecular recognition between protein and nicotinamide dinucleotide in intact, proton-translocating transhydrogenase studied by ATR-FTIR spectroscopy J. Am. Chem. Soc. 128, 2621-2629 (Pubitemid 43327940)
21. Guijarro, J., Engelhard, M., and Siebert, F. (2006) Anion uptake in halorhodopsin from Natromonas pharaonis studied by FTIR spectroscopy: Consequences for the anion transport mechanism Biochemistry 45, 11578-11588 (Pubitemid 44454005)
22. 2+-binding site in cytochrome c using FTIR coupled to an ATR microdialysis setup and NMR spectroscopy Biochemistry 44, 8652-8663 (Pubitemid 40840431)
23. Iwaki, M. and Rich, P. R. (2004) Direct detection of formate ligation in cytochrome c oxidase by ATR-FTIR spectroscopy J. Am. Chem. Soc. 126, 2386-2389 (Pubitemid 38295720)
24. Marechal, A., Iwaki, M., and Rich, P. R. (2013) Structural changes in cytochrome c oxidase induced by binding of sodium and calcium ions: An ATR-FTIR study J. Am. Chem. Soc. 135, 5802-5807
25. Furutani, Y., Murata, T., and Kandori, H. (2011) Sodium or lithium ion-binding-induced structural changes in the K-ring of V-ATPase from Enterococcus hirae revealed by ATR-FTIR spectroscopy J. Am. Chem. Soc. 133, 2860-2863
26. Nyquist, R. M., Heitbrink, D., Bolwien, C., Wells, T. A., Gennis, R. B., and Heberle, J. (2001) Perfusion-induced redox differences in cytochrome c oxidase: ATR/FT-IR spectroscopy FEBS Lett. 505, 63-67 (Pubitemid 32831031)
27. Iwaki, M., Breton, J., and Rich, P. R. (2002) ATR-FTIR difference spectroscopy of the P(M) intermediate of bovine cytochrome c oxidase Biochim. Biophys. Acta, Bioenerg. 1555, 116-121 (Pubitemid 35246016)
28. Nyquist, R. M., Heitbrink, D., Bolwien, C., Gennis, R. B., and Heberle, J. (2003) Direct observation of protonation reactions during the catalytic cycle of cytochrome c oxidase Proc. Natl. Acad. Sci. U.S.A. 100, 8715-8720 (Pubitemid 36899164)
29. Iwaki, M., Puustinen, A., Wikstrom, M., and Rich, P. R. (2006) Structural and chemical changes of the P-M intermediate of Paracoccus denitrificans cytochrome c oxidase revealed by IR spectroscopy with labeled tyrosines and histidine Biochemistry 45, 10873-10885 (Pubitemid 44360157)
30. Iwaki, M., Andrianambinintsoa, S., Rich, P., and Breton, J. (2002) Attenuated total reflection Fourier transform infrared spectroscopy of redox transitions in photosynthetic reaction centers: Comparison of perfusion- and light-induced difference spectra Spectrochim. Acta, Part A 58, 1523-1533 (Pubitemid 34466993)
31. Okubo, T. and Noguchi, T. (2007) Selective detection of the structural changes upon photoreactions of several redox cofactors in photosystem II by means of light-induced ATR-FTIR difference spectroscopy Spectrochim. Acta, Part A 66, 863-868 (Pubitemid 46330886)
32. Iwaki, M., Yakovlev, G., Hirst, J., Osyczka, A., Dutton, P. L., Marshall, D., and Rich, P. R. (2005) Direct observation of redox-linked histidine protonation changes in the iron-sulfur protein of the cytochrome bc (1) complex by ATR-FTIR spectroscopy Biochemistry 44, 4230-4237 (Pubitemid 40403963)
33. Oda, I., Iwaki, M., Fujita, D., Tsutsui, Y., Ishizaka, S., Dewa, M., Nango, M., Kajino, T., Fukushima, Y., and Itoh, S. (2010) Photosynthetic electron transfer from reaction center pigment-protein complex in silica nanopores Langmuir 26, 13399-13406
34. 2+-binding reduces conformational flexibility of RC-LH1 core complex from thermophile Thermochromatium tepidum Photosynth. Res. 111, 139-147
35. Kimura, Y., Inada, Y., Yu, L. J., Wang, Z.-Y., and Ohno, T. (2011) A spectroscopic variant of the light-harvesting 1 core complex from the thermophilic purple sulfur bacterium Thermochromatium tepidum Biochemistry 50, 3638-3648
36. Kimura, Y., Inada, Y., Numata, T., Arikawa, T., Li, Y., Zhang, J. P., Wang, Z.-Y., and Ohno, T. (2012) Metal cations modulate the bacteriochlorophyll- protein interaction in the light-harvesting 1 core complex from Thermochromatium tepidum Biochim. Biophys. Acta 1817, 1022-1029
37. Rich, P. R. and Breton, J. (2002) Attenuated total reflection Fourier transform infrared studies of redox changes in bovine cytochrome c oxidase: Resolution of the redox Fourier transform infrared difference spectrum of heme a (3) Biochemistry 41, 967-973 (Pubitemid 34061999)
38. 2+-binding motif in the LH1 complex from photosynthetic bacterium Thermochromatium tepidum as revealed by optical spectroscopy and structural modeling FEBS J. 276, 1739-1749
39. Suzuki, H., Hirano, Y., Kimura, Y., Takaichi, S., Kobayashi, M., Miki, K., and Wang, Z.-Y. (2007) Purification, characterization and crystallization of the core complex from thermophilic purple sulfur bacterium Thermochromatium tepidum Biochim. Biophys. Acta 1767, 1057-1063 (Pubitemid 47101789)
40. Sturgis, J., Robert, B., and Goormaghtigh, E. (1998) Transmembrane helix stability: The effect of helix-helix interactions studied by Fourier transform infrared spectroscopy Biophys. J. 74, 988-994 (Pubitemid 28345292)
41. Suzuki, H., Sugiura, M., and Noguchi, T. (2008) Monitoring water reactions during the S-state cycle of the photosynthetic water-oxidizing center: Detection of the DOD bending vibrations by means of Fourier transform infrared spectroscopy Biochemistry 47, 11024-11030
42. Nozawa, T., Trost, J. T., Fukada, T., Hatano, M., Mcmanus, J. D., and Blankenship, R. E. (1987) Properties of the reaction center of the thermophilic purple photosynthetic bacterium Chromatium tepidum Biochim. Biophys. Acta 894, 468-476
43. Wang-Otomo, Z.-Y., Yu, L.-J., Niwa, S., Takeda, K., Hirano, Y., Kawakami, T., and Miki, K. (2013) Crystal structure of a LH1-RC core complex from Thermochromatium tepidum, The 16th International Congress on Photosynthesis, St. Louis, MO, Aug 11-16.
44. Socrates, G. (2001) Infrared and Raman Characteristic Group Frequencies: Tables and Charts, 3 rd ed., Wiley, New York.
45. Deacon, G. B. and 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
46. Nakamoto, K. (1997) Infrared and Raman Spectra of Inorganic and Coordination Compounds, Part B: Applications in Coordination, Organometallic, and Bioinorganic Chemistry, 5 th ed., John Wiley & Sons, New York.
47. 2O) solutions 0.2. Amide absorption-bands of polypeptides and fibrous proteins in alpha-coil, beta-coil, and random coil conformations Biopolymers 30, 1259-1271
48. 2O) solutions 0.1. Spectral parameters of amino-acid residue absorption-bands Biopolymers 30, 1243-1257
49. Rucker, O., Kohler, A., Behammer, B., Sichau, K., and Overmann, J. (2012) Puf operon sequences and inferred structures of light-harvesting complexes of three closely related Chromatiaceae exhibiting different absorption characteristics Arch. Microbiol. 194, 123-134
50. Olsen, J. D., Sockalingum, G. D., Robert, B., and Hunter, C. N. (1994) Modification of a hydrogen-bond to a bacteriochlorophyll-a molecule in the light-harvesting 1-antenna of Rhodobacter sphaeroides Proc. Natl. Acad. Sci. U.S.A. 91, 7124-7128 (Pubitemid 24226815)
51. Sturgis, J. N., Olsen, J. D., Robert, B., and Hunter, C. N. (1997) Functions of conserved tryptophan residues of the core light-harvesting complex of Rhodobacter sphaeroides Biochemistry 36, 2772-2778 (Pubitemid 27138558)
52. Nabedryk, E., Bagley, K. A., Thibodeau, D. L., Bauscher, M., Mantele, W., and Breton, J. (1990) A protein conformational change associated with the photoreduction of the primary and secondary quinones in the bacterial reaction center FEBS Lett. 266, 59-62 (Pubitemid 20194173)
53. 1 FTIR difference spectrum of oxygen-evolving complex Biochemistry 42, 13170-13177 (Pubitemid 37420669)
54. Noguchi, T. and Sugiura, M. (2003) Analysis of flash-induced FTIR difference spectra of the S-state cycle in the photosynthetic water-oxidizing complex by uniform N-15 and C-13 isotope labeling Biochemistry 42, 6035-6042 (Pubitemid 36605106)
55. Permentier, H. P., Neerken, S., Overmann, J., and Amesz, J. (2001) A bacteriochlorophyll a antenna complex from purple bacteria absorbing at 963 nm Biochemistry 40, 5573-5578 (Pubitemid 32458260)