The origin of the unusual Qy red shift in LH1-RC complexes from purple bacteria Thermochromatium tepidum as revealed by Stark absorption spectroscopy

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1847, Issue 12, 2015, Pages 1479-1486

  Ma, Fei ^a   Yu, Long Jiang ^b   Wang Otomo, Zheng Yu ^b   Van Grondelle, Rienk ^a  

^a VU UNIVERSITY AMSTERDAM   (Netherlands)

^b IBARAKI UNIVERSITY   (Japan)

Author keywords

Exciton charge transfer state mixing; Inhomogeneous narrowing; LH1 RC; Red shift; Stark spectroscopy; Thermochromatium (Tch.) tepidum

Indexed keywords

AMINO ACID; BACTERIAL PROTEIN; BACTERIOCHLOROPHYLL; CAROTENOID; LH1 RC COMPLEX; UNCLASSIFIED DRUG; LIGHT HARVESTING SYSTEM;

ABSORPTION; ABSORPTION SPECTROSCOPY; ARTICLE; CHEMICAL MODIFICATION; CIRCULAR DICHROISM; CONTROLLED STUDY; CRYSTAL STRUCTURE; DIPOLE; ENERGY; MEASUREMENT; NONHUMAN; OSCILLATION; PRIORITY JOURNAL; PROTEIN STRUCTURE; PROTEOBACTERIA; ROOM TEMPERATURE; STARK ABSORPTION SPECTROSCOPY; STATIC ELECTRICITY; THERMOCHROMATIUM TEPIDUM; GAMMAPROTEOBACTERIA; LIGHT HARVESTING SYSTEM; METABOLISM; PHYSIOLOGY; PROCEDURES; SPECTROSCOPY;

CAROTENOIDS; GAMMAPROTEOBACTERIA; LIGHT-HARVESTING PROTEIN COMPLEXES; SPECTRUM ANALYSIS;

EID: 84941975799     PISSN: 00052728     EISSN: 18792650     Source Type: Journal    
DOI: 10.1016/j.bbabio.2015.08.007     Document Type: Article

References (42)

1. V. Sundström, T. Pullerits, and R. van Grondelle Photosynthetic light-harvesting: reconciling dynamics and structure of purple bacterial LH2 reveals function of photosynthetic unit J. Phys. Chem. B 103 1999 2327 2346
2. R.J. Cogdell, A. Gall, and J. Köhler The architecture and function of the light-harvesting apparatus of purple bacteria: from single molecules to in vivo membranes Q. Rev. Biophys. 39 2006 227 324
3. G.D. Scholes, G.R. Fleming, A. Olaya-Castro, and R. van Grondelle Lessons from nature about solar light harvesting Nat. Chem. 3 2011 763 774
4. L.M.P. Beekman, M. Steffen, I.H.M. van Stokkum, J.D. Olsen, C.N. Hunter, S.G. Boxer, and R. van Grondelle Characterization of the light-harvesting antennas of photosynthetic purple bacteria by Stark spectroscopy. 1. LH1 antenna complex and the B820 subunit from Rhodospirillum rubrum J. Phys. Chem. B 101 1997 7284 7292
5. L.M.P. Beekman, R.N. Frese, G.J.S. Fowler, R. Picorel, R.J. Cogdell, I.H.M. van Stokkum, C.N. Hunter, and R. van Grondelle Characterization of the light-harvesting antennas of photosynthetic purple bacteria by Stark spectroscopy. 2. LH2 complexes: influence of the protein environment J. Phys. Chem. B 101 1997 7293 7301
6. G.J.S. Fowler, R.W. Visschers, G.G. Grief, R. van Grondelle, and C.N. Hunter Genetically modified photosynthetic antenna complexes with blueshifted absorbance bands Nature 355 1992 848 850
7. Y. Kimura, Y. Inada, T. Numata, T. Arikawa, Y. Li, J.-P. Zhang, Z.-Y. Wang, and T. Ohno Metal cations modulate the bacteriochlorophyll-protein interaction in the light-harvesting 1 core complex from Thermochromatium tepidum Biochim. Biophys. Acta 1817 2012 1022 1029
8. M.T. Madigan A novel photosynthetic purple bacterium isolated from a Yellowstone hot spring Science 225 1984 313 315
9. H. Suzuki, Y. Hirano, Y. Kimura, S. Takaichi, M. Kobayashi, K. Miki, and Z.-Y. Wang Purification, characterization and crystallization of the core complex from thermophilic purple sulfur bacterium Thermochromatium tepidum Biochim. Biophys. Acta 1767 2007 1057 1063
10. H.P. Permentier, S. Neerken, K.A. Schmidt, J. Overmann, and J. Amesz Energy transfer and charge separation in the purple non-sulfur bacterium Roseospirillum parvum Biochim. Biophys. Acta 1460 2000 338 345
11. H.P. Permentier, S. Neerken, J. Overmann, and J. Amesz A bacteriochlorophyll a antenna complex from purple bacteria absorbing at 963 nm Biochemistry 40 2001 5573 5578
12. L.M.P. Beekman, F. van Mourik, M.R. Jones, H.M. Visser, C.N. Hunter, and R. van Grondelle Trapping kinetics in mutants of the photosynthetic purple bacterium Rhodobacter sphaeroides: influence of the charge separation rate and consequences for the rate-limiting step in the light-harvesting process Biochemistry 33 1994 3143 3147
13. A. Freiberg, J.P. Allen, J.C. Williams, and N.W. Woodbury Energy trapping and detrapping by wild type and mutant reaction centers of purple non-sulfur bacteria Photosynth. Res. 48 1996 309 319
14. F. Ma, Y. Kimura, X.-H. Zhao, Y.-S. Wu, P. Wang, L.-M. Fu, Z.-Y. Wang, and J.-P. Zhang Excitation dynamics of two spectral forms of the core complexes from photosynthetic bacterium Thermochromatium tepidum Biophys. J. 95 2008 3349 3357
15. G. Mcdermott, S.M. Prince, A.A. Freer, A.M. Hawthornthwaite-lawless, M.Z. Paplz, R.J. Cogdell, and N.W. Isaacs Crystal-structure of an integral membrane light-harvesting complex from photosynthetic bacteria Nature 374 1995 517 521
16. M.Z. Papiz, S.M. Prince, T.D. Howard, R.J. Cogdell, and N.W. Isaacs The structure and thermal motion of the B800-850 LH2 complex from Rps. acidophila at 2.0 Å resolution and 100 K: new structural features and functionally relevant motions J. Mol. Biol. 326 2003 1523 1538
17. J. Koepke, X.-C. Hu, C. Muenke, K. Schulten, and H. Michel The crystal structure of the light-harvesting complex II (B800-850) from Rhodospirillum molischianum Structure 4 1996 581 597
18. P. Qian, M.Z. Papiz, P.J. Jackson, A.A. Brindley, I.W. Ng, J.D. Olsen, M.J. Dickman, P.A. Bullough, and C.N. Hunter Three-dimensional structure of the Rhodobacter sphaeroides RC-LH1-PufX complex: dimerization and quinone channels promoted by PufX Biochemistry 52 2013 7575 7585
19. A.W. Roszak, T.D. Howard, J. Southall, A.T. Gardiner, C.J. Law, N.W. Isaacs, and R.J. Cogdell Crystal structure of the RC-LH1 core complex from Rhodopseudomonas palustris Science 302 2003 1969 1972
20. S. Niwa, L.-J. Yu, K. Takedal, Y. Hirano, T. Kawakami, Z.-Y. Wang-Otomo, and K. Miki Structure of the LH1-RC complex from Thermochromatium tepidum at 3.0 Å Nature 508 2014 228 232
21. y transition of the core complex in thermophilic purple sulfur bacterium Thermochromatium tepidum J. Biol. Chem. 283 2008 13867 13873
22. Y. Kimura, L.-J. Yu, Y. Hirano, H. Suzuki, and Z.-Y. Wang 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 2009 93 99
23. 2 +-binding motif in the LH1 complex from photosynthetic bacterium Thermochromatium tepidum as revealed by optical spectroscopy and structural modeling FEBS J. 276 2009 1739 1749
24. E.J.P. Lathrop, and R.A. Friesner Simulation of optical spectra from the reaction center of Rb. sphaeroides. Effects of an internal charge-separated state of the special pair J. Phys. Chem. 98 1994 3056 3066
25. G.U. Bublitz, and S.G. Boxer Stark spectroscopy: application in chemistry, biology, and materials science Annu. Rev. Phys. Chem. 48 1997 213 242
26. S.G. Boxer Stark realities J. Phys. Chem. B 113 2009 2972 2983
27. D.S. Gottfried, J.W. Stocker, and S.G. Boxer Stark effect spectroscopy of bacteriochlorophyll in light-harvesting complexes from photosynthetic bacteria Biochim. Biophys. Acta 1059 1991 63 75
28. B. van Dijk, T. Nozawa, and A.J. Hoff The B800-850 complex of the purple bacterium Chromatium tepidum: low-temperature absorption and Stark spectra Spectrochim. Acta A 54 1998 1269 1278
29. K. Nakagawa, S. Suzuki, R. Fujii, A.T. Gardiner, R.J. Cogdell, M. Nango, and H. Hashimoto Probing binding site of bacteriochlorophyll a and carotenoid in the reconstituted LH1 complex from Rhodospirillum rubrum S1 by Stark spectroscopy Photosynth. Res. 95 2008 339 344
30. M. Lösche, G. Feher, and M.Y. Okamura The Stark effect in reaction centers from Rhodobacter sphaeroides R-26 and Rhodopseudomonas viridis Proc. Natl. Acad. Sci. USA 84 1987 7537 7541
31. S.L. Hammes, L. Mazzola, S.G. Boxer, D.F. Gaul, and C.C. Schenck Stark spectroscopy of the Rhodobacter sphaeroides reaction center heterodimer mutant Proc. Natl. Acad. Sci. USA 87 1990 5682 5686
32. T.R. Middendorf, L.T. Mazzola, K. Lao, M.A. Steffen, and S.G. Boxer Stark effect (electroabsorption) spectroscopy of photosynthetic reaction center at 1.5 K: evidence that the special pair has a large excited-state polarizability Biochim. Biophys. Acta 1143 1993 223 234
33. L.J. Moore, H.-L. Zhou, and S.G. Boxer Excited-state electronic asymmetry of the special pair in photosynthetic reaction center mutants: absorption and Stark spectroscopy Biochemistry 38 1999 11949 11960
34. K. Yanagi, M. Shimizu, H. Hashimoto, A.T. Gardiner, A.W. Roszak, and R.J. Cogdell Local electrostatic field induced by the carotenoid bound to the reaction center of the purple photosynthetic bacterium Rhodobacter Sphaeroides J. Phys. Chem. B 109 2005 992 998
35. J.L. Herek, M. Wendling, Z. He, T. Polívka, G. Garcia-Asua, R.J. Cogdell, C.N. Hunter, R. van Grondelle, V. Sundström, and T. Pullerits Ultrafast carotenoid band shifts: experiment and theory J. Phys. Chem. B 108 2004 10398 10403
36. E. Romero, B.A. Diner, P.J. Nixon, W.J. Coleman, J.P. Dekker, and R. van Grondelle Mixed exciton-charge-transfer states in photosystem II: Stark spectroscopy on site-directed mutants Biophys. J. 103 2012 185 194
37. 2 +-binding reduces conformational flexibility of RC-LH1 core complex from thermophile Thermochromatium tepidum Photosynth. Res. 111 2012 139 147
38. T. Horibe, K. Nakagawa, T. Kusumoto, R. Fujii, R.J. Cogdell, M. Nango, and H. Hashimoto Polarization angle dependence of Stark absorption spectra of spirilloxanthin bound to the reconstituted LH1 complexes using LH1-subunits isolated from the purple photosynthetic bacterium Rhodospirillum rubrum Acta Biochim. Pol. 59 2012 97 100
39. D.S. Gottfried, M.A. Steffen, and S.G. Boxer Large protein-induced dipoles for a symmetric carotenoid in a photosynthetic antenna complex Nature 251 1991 662 665
40. K. Nakagawa, S. Suzuki, R. Fujii, A.T. Gardiner, R.J. Cogdell, M. Nango, and H. Hashimoto Electrostatic effect of surfactant molecules on bacteriochlorophyll a and carotenoid binding sites in the LH1 complex isolated from Rhodospirillum rubrum S1 probed by Stark spectroscopy Photosynth. Res. 95 2008 345 351
41. K. Nakagawa, S. Suzuki, R. Fujii, A.T. Gardiner, R.J. Cogdell, M. Nango, and H. Hashimoto Probing the effect of the binding site on the electrostatic behavior of a series of carotenoids reconstituted into the light-harvesting 1 complex from purple photosynthetic bacterium Rhodospirillum rubrum detected by Stark spectroscopy J. Phys. Chem. B 112 2008 9467 9475
42. L.-J. Yu, in preparation.