Excitation energy trapping and dissipation by Ni-substituted bacteriochlorophyll a in reconstituted LH1 complexes from Rhodospirillum rubrum

Journal of Physical Chemistry B

Volumn 117, Issue 38, 2013, Pages 11260-11271

  Lambrev, Petar H ^a   Miloslavina, Yuliya ^a   Van Stokkum, Ivo H M ^b   Stahl, Andreas D ^b   Michalik, Maciej ^c   Susz, Anna ^c   Tworzydło, Jedrzej ^c   Fiedor, Joanna ^d   Huhn, Gabriella ^e   Groot, Marie Louise ^b   Van Grondelle, Rienk ^b   Garab, Gyózó ^a   Fiedor, Leszek ^c  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^b VU UNIVERSITY AMSTERDAM   (Netherlands)

^c JAGIELLONIAN UNIVERSITY   (Poland)

^d AGH UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Poland)

^e EÖTVÖS LORÁND UNIVERSITY   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIOCHLOROPHYLLS; EXCITED-STATE DYNAMICS; EXCITED-STATE LIFETIME; INTER-SYSTEM CROSSINGS; INTERNAL CONVERSIONS; RHODOSPIRILLUM RUBRUM; TRANSIENT ABSORPTION SPECTROSCOPIES; VISIBLE AND NEAR INFRARED;

CHLOROPHYLL; ENERGY DISSIPATION; EXCITATION ENERGY; EXCITED STATES; NUCLEAR PHYSICS; PIGMENTS; QUENCHING;

NICKEL;

BACTERIAL PROTEIN; BACTERIOCHLOROPHYLL A; CAROTENOID; HOLOCHROME PROTEIN, RHODOSPIRILLUM RUBRUM; ION; NICKEL; PROTOCHLOROPHYLLIDE; SPHEROIDENE;

ARTICLE; ATOMIC FORCE MICROSCOPY; CHEMISTRY; ENERGY TRANSFER; LIGHT HARVESTING SYSTEM; METABOLISM; RHODOSPIRILLUM RUBRUM; SPECTROFLUOROMETRY; TIME;

BACTERIAL PROTEINS; BACTERIOCHLOROPHYLL A; CAROTENOIDS; ENERGY TRANSFER; IONS; LIGHT-HARVESTING PROTEIN COMPLEXES; MICROSCOPY, ATOMIC FORCE; NICKEL; PROTOCHLOROPHYLLIDE; RHODOSPIRILLUM RUBRUM; SPECTROMETRY, FLUORESCENCE; TIME FACTORS;

EID: 84884936983     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp4020977     Document Type: Article

References (74)

1. Niyogi, K. K. Safety Valves for Photosynthesis Curr. Opin. Plant Biol. 2000, 3, 455-460
2. Li, Z.; Wakao, S.; Fischer, B. B.; Niyogi, K. K. Sensing and Responding to Excess Light Annu. Rev. Plant Biol. 2009, 60, 239-260
3. Bixon, M.; Jortner, J. Intramolecular Radiationless Transitions J. Chem. Phys. 1968, 48, 715-726
4. Nakashima, N.; Yoshihara, K. Role of Hot Molecules Formed by Internal Conversion in UV Single-Photon and Multiphoton Chemistry J. Phys. Chem. 1989, 93, 7763-7771
5. Cseh, Z.; Rajagopal, S.; Tsonev, T.; Busheva, M.; Papp, E.; Garab, G. Thermooptic Effect in Chloroplast Thylakoid Membranes. Thermal and Light Stability of Pigment Arrays with Different Levels of Structural Complexity Biochemistry 2000, 39, 15250-15257
6. Musewald, C.; Hartwich, G.; Lossau, H.; Gilch, P.; Pöllinger-Dammer, F.; Scheer, H.; Michel-Beyerle, M. E. Ultrafast Photophysics and Photochemistry of [Ni]-Bacteriochlorophyll a J. Phys. Chem. B 1999, 103, 7055-7060 (Pubitemid 129702491)
7. Hartwich, G.; Fiedor, L.; Simonin, I.; Cmiel, E.; Schäfer, W.; Noy, D.; Scherz, A.; Scheer, H. Metal-Substituted Bacteriochlorophylls. 1. Preparation and Influence of Metal and Coordination on Spectra J. Am. Chem. Soc. 1998, 120, 3675-3683 (Pubitemid 28218444)
8. Fiedor, L.; Scheer, H.; Hunter, C. N.; Tschirschwitz, F.; Voigt, B.; Ehlert, J.; Nibbering, E.; Leupold, D.; Elsaesser, T. Introduction of a 60 fs Deactivation Channel in the Photosynthetic Antenna LH1 by Ni-Bacteriopheophytin A Chem. Phys. Lett. 2000, 319, 145-152
9. Fiedor, L.; Leupold, D.; Teuchner, K.; Voigt, B.; Hunter, C. N.; Scherz, A.; Scheer, H. Excitation Trap Approach to Analyze Size and Pigment-Pigment Coupling: Reconstitution of LH1 Antenna of Rhodobacter sphaeroides with Ni-Substituted Bacteriochlorophyll Biochemistry 2001, 40, 3737-3747 (Pubitemid 32242833)
10. Pilch, M.; Dudkowiak, A.; Jurzyk, B.; Lukasiewicz, J.; Susz, A.; Stochel, G.; Fiedor, L. Molecular Symmetry Determines the Mechanism of a Very Efficient Ultrafast Excitation-to-Heat Conversion in Ni-Substituted Chlorophylls Biochim. Biophys. Acta 2013, 1827, 30-37
11. Robert, B.; Cogdell, R. J.; van Grondelle, R. The Light-Harvesting System of Purple Bacteria. In Light-Harvesting Antennas in Photosynthesis; Green, B. R.; Parson, W. W., Eds.; Kluwer Academic Publishers: Dordrecht, The Netherlands, 2003; pp 169-194.
12. Law, C. J.; Roszak, A. W.; Southall, J.; Gardiner, A. T.; Isaacs, N. W.; Cogdell, R. J. The Structure and Function of Bacterial Light-Harvesting Complexes (Review) Mol. Membr. Biol. 2004, 21, 183-191 (Pubitemid 38745647)
13. Cogdell, R. J.; Gall, A.; Köhler, J. The Architecture and Function of the Light-Harvesting Apparatus of Purple Bacteria: From Single Molecules to in vivo Membranes Q. Rev. Biophys. 2006, 39, 227-324 (Pubitemid 44963429)
14. Law, C. J.; Cogdell, R. J. The Light Harvesting System of Purple Anoxygenic Photsynthetic Bacteria. In Primary Processes of Photosynthesis: Basic Principles and Apparatus; Renger, G., Ed.; The Royal Society of Chemistry: Cambridge, U.K., 2008; pp 205-259.
15. Hu, X. C.; Ritz, T.; Damjanovic, A.; Autenrieth, F.; Schulten, K. Photosynthetic Apparatus of Purple Bacteria Q. Rev. Biophys. 2002, 35, 1-62 (Pubitemid 34408145)
16. Cogdell, R. J.; Lindsay, J. G.; Valentine, J.; Durant, I. A Further Characterisation of the B890 Light-Harvesting Pigment-Protein Complex from Rhodospirillum rubrum Strain S1 FEBS Lett. 1982, 150, 151-154 (Pubitemid 13149318)
17. Miller, J. F.; Hinchigeri, S. B.; Parkes-Loach, P. S.; Callahan, P. M.; Sprinkle, J. R.; Riccobono, J. R.; Loach, P. A. Isolation and Characterization of a Subunit Form of the Light-Harvesting Complex of Rhodospirillum rubrum Biochemistry 1987, 26, 5055-5062
18. Visschers, R. W.; Chang, M. C.; van Mourik, F.; Parkes-Loach, P. S.; Heller, B. A.; Loach, P. A.; van Grondelle, R. Fluorescence Polarization and Low-Temperature Absorption Spectroscopy of a Subunit Form of Light-Harvesting Complex I from Purple Photosynthetic Bacteria Biochemistry 1991, 30, 5734-5742
19. Fiedor, L.; Scheer, H. Trapping of an Assembly Intermediate of Photosynthetic LH1 Antenna Beyond B820 Subunit J. Biol. Chem. 2005, 280, 20921-20926
20. Nakagawa, K.; Suzuki, S.; Fujii, R.; Gardiner, A. T.; Cogdell, R. J.; Nango, M.; Hashimoto, H. 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 2008, 112, 9467-9475
21. Karrasch, S.; Bullough, P. A.; Ghosh, R. The 8.5 Å Projection Map of the Light-Harvesting Complex I from Rhodospirillum rubrum Reveals a Ring Composed of 16 Subunits EMBO J. 1995, 14, 631-638
22. Walz, T.; Ghosh, R. Two-Dimensional Crystallization of the Light-Harvesting I Reaction Centre Photounit from Rhodospirillum rubrum J. Mol. Biol. 1997, 265, 107-111 (Pubitemid 27110649)
23. Scherz, A.; Parson, W. W. Exciton Interactions in Dimers of Bacteriochlorophyll and Related Molecules Biochim. Biophys. Acta 1984, 766, 666-678
24. Alden, R. G.; Johnson, E.; Nagarajan, V.; Parson, W. W.; Law, C. J.; Cogdell, R. J. Calculations of Spectroscopic Properties of the LH2 Bacteriochlorophyll-Protein Antenna Complex from Rhodopseudomonas acidophila J. Phys. Chem. B 1997, 101, 4667-4680 (Pubitemid 127596268)
25. Beekman, L. M. P.; Steffen, M.; van Stokkum, I. H. M.; Olsen, J. D.; Hunter, C. N.; Boxer, S. G.; van Grondelle, R. 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 1997, 101, 7284-7292 (Pubitemid 127609302)
26. Monshouwer, R.; Abrahamsson, M.; van Mourik, F.; van Grondelle, R. Superradiance and Exciton Delocalization in Bacterial Photosynthetic Light-Harvesting Systems J. Phys. Chem. B 1997, 101, 7241-7248 (Pubitemid 127609296)
27. Hu, X.; Ritz, T.; Damjanovic, A.; Schulten, K. Pigment Organization and Transfer of Electronic Excitation in the Photosynthetic Unit of Purple Bacteria J. Phys. Chem. B 1997, 101, 3854-3871 (Pubitemid 127581143)
28. Sundström, V.; Pullerits, T.; van Grondelle, R. Photosynthetic Light-Harvesting: Reconciling Dynamics and Structure of Purple Bacterial LH2 Reveals Function of Photosynthetic Unit J. Phys. Chem. B 1999, 103, 2327-2346 (Pubitemid 129702493)
29. van Grondelle, R.; Novoderezhkin, V. Dynamics of Excitation Energy Transfer in the LH1 and LH2 Light-Harvesting Complexes of Photosynthetic Bacteria Biochemistry 2001, 40, 15057-15068 (Pubitemid 33151920)
30. Renger, T.; May, V.; Kühn, O. Ultrafast Excitation Energy Transfer Dynamics in Photosynthetic Pigment-Protein Complexes Phys. Rep. Rev. Sect. Phys. Lett. 2001, 343, 137-254 (Pubitemid 33668075)
31. van Grondelle, R.; Novoderezhkin, V. I. Energy Transfer in Photosynthesis: Experimental Insights and Quantitative Models Phys. Chem. Chem. Phys. 2006, 8, 793-807
32. Freiberg, A.; Timpmann, K.; Jackson, J. A.; Lin, S.; Woodbury, N. W. Exciton Relaxation and Transfer in the Antenna Network of Photosynthetic Bacteria. In Photosynthesis: Mechanism and Effects; Proceedings of the XI International Congress on Photosynthesis Budapest, Hungary, August 17-22, 1998; Garab, G., Ed.; Kluwer Academic Publishers: Dordrecht, 1998; pp 771.
33. Cheng, Y. C.; Fleming, G. R. Dynamics of Light Harvesting in Photosynthesis Annu. Rev. Phys. Chem. 2009, 60, 241-262
34. Scholes, G. D.; Fleming, G. R.; Olaya-Castro, A.; van Grondelle, R. Lessons from Nature About Solar Light Harvesting Nat. Chem. 2011, 23, 763-774
35. Novoderezhkin, V.; Monshouwer, R.; van Grondelle, R. Disordered Exciton Model for the Core Light-Harvesting Antenna of Rhodopseudomonas viridis Biophys. J. 1999, 77, 666-681 (Pubitemid 29362442)
36. Jimenez, R.; van Mourik, F.; Yu, J. Y.; Fleming, G. R. Three-Pulse Photon Echo Measurements on LH1 and LH2 Complexes of Rhodobacter sphaeroides: A Nonlinear Spectroscopic Probe of Energy Transfer J. Phys. Chem. B 1997, 101, 7350-7359 (Pubitemid 127609310)
37. Chachisvilis, M.; Kühn, O.; Pullerits, T.; Sundström, V. Excitons in Photosynthetic Purple Bacteria: Wavelike Motion or Incoherent Hopping? J. Phys. Chem. B 1997, 101, 7275-7283 (Pubitemid 127609301)
38. Novoderezhkin, V.; Monshouwer, R.; van Grondelle, R. Exciton (De)Localization in the LH2 Antenna of Rhodobacter sphaeroides as Revealed by Relative Difference Absorption Measurements of the LH2 Antenna and the B820 Subunit J. Phys. Chem. B 1999, 103, 10540-10548 (Pubitemid 129614115)
39. Pullerits, T.; Chachisvilis, M.; Sundström, V. Exciton Delocalization Length in the B850 Antenna of Rhodobacter sphaeroides J. Phys. Chem. 1996, 100, 10787-10792 (Pubitemid 126788674)
40. Damjanovic, A.; Kosztin, I.; Kleinekathöfer, U.; Schulten, K. Excitons in a Photosynthetic Light-Harvesting System: A Combined Molecular Dynamics, Quantum Chemistry, and Polaron Model Study Phys. Rev. E 2002, 65, 031919
41. Leupold, D.; Stiel, H.; Teuchner, K.; Nowak, F.; Sandner, W.; Ücker, B.; Scheer, H. Size Enhancement of Transition Dipoles to One-and Two-Exciton Bands in a Photosynthetic Antenna Phys. Rev. Lett. 1996, 77, 4675-4678 (Pubitemid 126632012)
42. Ritz, T.; Damjanovic, A.; Schulten, K.; Zhang, J.-P.; Koyama, Y. Efficient Light Harvesting through Carotenoids Photosynth. Res. 2000, 66, 125-144 (Pubitemid 32540455)
43. Koyama, Y.; Kakitani, Y. Mechanisms of Carotenoid-to-Bacteriochlorophyll Energy Transfer in the Light Harvesting Antenna Complexes 1 and 2: Dependence on the Conjugation Length of Carotenoids. In Chlorophylls and Bacteriochlorophylls: Biochemistry, Biophysics, Functions and Applications; Grimm, B.; Porra, R. J.; Rüdiger, W.; Scheer, H., Eds.; Springer: Dordrecht, The Netherlands, 2006; pp 431-443.
44. Krueger, B. P.; Scholes, G. D.; Jimenez, R.; Fleming, G. R. Electronic Excitation Transfer from Carotenoid to Bacteriochlorophyll in the Purple Bacterium Rhodopseudomonas Acidophila J. Phys. Chem. B 1998, 102, 2284-2292 (Pubitemid 128581088)
45. Akahane, J.; Rondonuwu, F. S.; Fiedor, L.; Watanabe, Y.; Koyama, Y. Dependence of Singlet-Energy Transfer on the Conjugation Length of Carotenoids Reconstituted into the LH1 Complex from Rhodospirillum rubrum G9 Chem. Phys. Lett. 2004, 393, 184-191
46. Scholes, G. D.; Harcourt, R. D.; Fleming, G. R. Electronic Interactions in Photosynthetic Light-Harvesting Complexes: The Role of Carotenoids J. Phys. Chem. B 1997, 101, 7302-7312 (Pubitemid 127609304)
47. 1 State in LH2 Complexes from Purple Bacteria J. Phys. Chem. B 2000, 104, 3683-3691
48. Krueger, B. P.; Scholes, G. D.; Fleming, G. R. Calculation of Couplings and Energy-Transfer Pathways between the Pigments of LH2 by the Ab Inito Transition Density Cube Method J. Phys. Chem. B 1998, 102, 5378-5386 (Pubitemid 128578377)
49. Polivka, T.; Sundström, V. Dark Excited States of Carotenoids: Consensus and Controversy Chem. Phys. Lett. 2009, 477, 1-11
50. Fiedor, J.; Pilch, M.; Fiedor, L. Tuning the Thermodynamics of Association of Transmembrane Helices J. Phys. Chem. B 2009, 113, 12831-12838
51. Fiedor, L.; Akahane, J.; Koyama, Y. Carotenoid-Induced Cooperative Formation of Bacterial Photosynthetic LH1 Complex Biochemistry 2004, 43, 16487-16496 (Pubitemid 40041061)
52. Pawlowicz, N. P.; Groot, M. L.; van Stokkum, I. H. M.; Breton, J.; van Grondelle, R. Charge Separation and Energy Transfer in the Photosystem II Core Complex Studied by Femtosecond Midinfrared Spectroscopy Biophys. J. 2007, 93, 2732-2742 (Pubitemid 47607810)
53. van Stokkum, I. H. M.; Larsen, D. S.; van Grondelle, R. Global and Target Analysis of Time-Resolved Spectra Biochim. Biophys. Acta 2004, 1657, 82-104 (Pubitemid 38952870)
54. Snellenburg, J.; Laptenok, S.; Seger, R.; Mullen, K. M.; van Stokkum, I. H. M. Glotaran: A Java-Based Graphical User Interface for the R Package TIMP J. Stat. Software 2012, 49, 1-22
55. Fiedor, L. Hexacoordination of Bacteriochlorophyll in Photosynthetic Antenna LH1 Biochemistry 2006, 45, 1910-1918 (Pubitemid 43222134)
56. Visser, H. M.; Somsen, O. J. G.; van Mourik, F.; Lin, S.; van Stokkum, I. H. M.; van Grondelle, R. Direct Observation of Sub-picosecond Equilibration of Excitation Energy in the Light-Harvesting Antenna of Rhodospirillum rubrum Biophys. J. 1995, 69, 1083-1099
57. Monshouwer, R.; Baltuska, A.; van Mourik, F.; van Grondelle, R. Time-Resolved Absorption Difference Spectroscopy of the LH-1 Antenna of Rhodopseudomonas viridis J. Phys. Chem. A 1998, 102, 4360-4371 (Pubitemid 128611412)
58. Hunter, C. N.; Bergstroem, H.; Van Grondelle, R.; Sundstroem, V. Energy-Transfer Dynamics in Three Light-Harvesting Mutants of Rhodobacter sphaeroides: A Picosecond Spectroscopy Study Biochemistry 1990, 29, 3203-3207 (Pubitemid 20131458)
59. Jirsakova, V.; Reiss-Husson, F.; Ranck, J.-L.; Moya, I. Fluorescence Life-Times and Aggregation States of the Core Light Harvesting Complex B875 from Rubrivivax Gelatinosus Photosynth. Res. 1997, 54, 35-43 (Pubitemid 27518806)
60. Chang, M. C.; Callahan, P. M.; Parkes-Loach, P. S.; Cotton, T. M.; Loach, P. A. Spectroscopic Characterization of the Light-Harvesting Complex of Rhodospirillum rubrum and Its Structural Subunit Biochemistry 1990, 29, 421-429 (Pubitemid 20037649)
61. Loach, P. A.; Parkes-Loach, P. S. Structure-Function Relationships in Core Light-Harvesting Complexes (LH1) as Determined by Characterization of the Structural Subunit and by Reconstitution Experiments. In Anoxygenic Photosynthetic Bacteria; Blankenship, R. E.; Madigan, M. T.; Bauer, C. E., Eds.; Kluwer Academic Publishers: Dordrecht, The Netherelands, 1995; pp 437-471.
62. Arluison, V.; Seguin, J.; Robert, B. Biochemical Characterization of the Dissociated Forms from the Core Antenna Proteins from Purple Bacteria Biochemistry 2002, 41, 11812-11819
63. Picorel, R.; Belanger, G.; Gingras, G. Antenna Holochrome B880 of Rhodospirillum rubrum S1. Pigment, Phospholipid, and Polypeptide Composition Biochemistry 1983, 22, 2491-2497 (Pubitemid 13093553)
64. Valkunas, L.; Trinkunas, G.; Liuolia, V.; van Grondelle, R. Nonlinear Annihilation of Excitations in Photosynthestic Systems Biophys. J. 1995, 69, 1117-1129
65. Theiss, C.; Leupold, D.; Moskalenko, A. A.; Razjivin, A. P.; Eichler, H. J.; Lokstein, H. Femtosecond Spectroscopy of Native and Carotenoidless Purple-Bacterial LH2 Clarifies Functions of Carotenoids Biophys. J. 2008, 94, 4808-4811
66. Lambrev, P. H.; Schmitt, F. J.; Kussin, S.; Schoengen, M.; Várkonyi, Z.; Eichler, H. J.; Garab, G.; Renger, G. Functional Domain Size in Aggregates of Light-Harvesting Complex II and Thylakoid Membranes Biochim. Biophys. Acta 2011, 1807, 1022-1031
67. Polivka, T.; Pullerits, T.; Herek, J. L.; Sundström, V. Exciton Relaxation and Polaron Formation in LH2 at Low Temperature J. Phys. Chem. B 2000, 104, 1088-1096
68. Novoderezhkin, V. I.; van Grondelle, R. Exciton-Vibrational Relaxation and Transient Absorption Dynamics in LH1 of Rhodopseudomonas Viridis: A Redfield Theory Approch J. Phys. Chem. B 2002, 106, 6025-6037 (Pubitemid 35281850)
69. Gradinaru, C. C.; Kennis, J. T. M.; Papagiannakis, E.; van Stokkum, I. H. M.; Cogdell, R. J.; Fleming, G. R.; Niederman, R. A.; van Grondelle, R. An Unusual Pathway of Excitation Energy Deactivation in Carotenoids: Singlet-to-Triplet Conversion on an Ultrafast Timescale in a Photosynthetic Antenna Proc. Natl. Acad. Sci. U.S.A. 2001, 98, 2364-2369 (Pubitemid 32209488)
70. Papagiannakis, E.; Das, S. K.; Gall, A.; van Stokkum, I. H. M.; Robert, B.; van Grondelle, R.; Frank, H. A.; Kennis, J. T. M. Light Harvesting by Carotenoids Incorporated into the B850 Light-Harvesting Complex from Rhodobacter sphaeroides R-26.1: Excited-State Relaxation, Ultrafast Triplet Formation, and Energy Transfer to Bacteriochlorophyll J. Phys. Chem. B 2003, 107, 5642-5649
71. Papagiannakis, E.; Kennis, J. T. M.; van Stokkum, I. H. M.; Cogdell, R. J.; van Grondelle, R. An Alternative Carotenoid-to-Bacteriochlorophyll Energy Transfer Pathway in Photosynthetic Light Harvesting Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 6017-6022 (Pubitemid 34493257)
72. Novoderezhkin, V. I.; Cohen, S. T. A.; van Grondelle, R. Dynamics of Exciton Relaxation in LH2 Antenna Probed by Multipulse Nonlinear Spectroscopy J. Phys. Chem. A 2011, 115, 3834-3844
73. Abramavicius, D.; Valkunas, L.; van Grondelle, R. Exciton Dynamics in Ring-Like Photosynthetic Light-Harvesting Complexes: A Hopping Model Phys. Chem. Chem. Phys. 2004, 6, 3097-3105
74. Bradforth, S. E.; Jimenez, R.; van Mourik, F.; van Grondelle, R.; Fleming, G. R. Excitation Transfer in the Core Light-Harvesting Complex (LH-1) of Rhodobacter Sphaeroides: An Ultrafast Fluorescence Depolarization and Annihilation Study J. Phys. Chem. 1995, 99, 16179-16191