Excitons in the LH3 complexes from purple bacteria

Journal of Physical Chemistry B

Volumn 117, Issue 38, 2013, Pages 11058-11068

  Chmeliov, Jevgenij ^a,b   Songaila, Egidijus ^a   Rancova, Olga ^b   Gall, Andrew ^c   Robert, Bruno ^c   Abramavicius, Darius ^b,d   Valkunas, Leonas ^a,b  

^a CENTER FOR PHYSICAL SCIENCES AND TECHNOLOGY   (Lithuania)

^b VILNIUS UNIVERSITY   (Lithuania)

^c CEA SACLAY   (France)

^d Jilin University   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIOCHLOROPHYLLS; EXCITON ABSORPTIONS; FEMTOSECOND TRANSIENT ABSORPTION SPECTROSCOPY; INTERMOLECULAR INTERACTIONS; LIGHT-HARVESTING COMPLEX; RESONANCE INTERACTION; SPECTROSCOPIC PROPERTY; STEADY-STATE ABSORPTION;

AMINO ACIDS; CHLOROPHYLL; CHROMOPHORES; ELECTROMAGNETIC WAVE ABSORPTION; EXCITONS; PROTONATION;

BACTERIA;

BACTERIAL PROTEIN; BACTERIOCHLOROPHYLL; LDS 751; ORGANIC COMPOUND;

ARTICLE; CHEMISTRY; LIGHT HARVESTING SYSTEM; METABOLISM; NEAR INFRARED SPECTROSCOPY; PROTEOBACTERIA; STATIC ELECTRICITY; TEMPERATURE;

BACTERIAL PROTEINS; BACTERIOCHLOROPHYLLS; LIGHT-HARVESTING PROTEIN COMPLEXES; ORGANIC CHEMICALS; PROTEOBACTERIA; SPECTROSCOPY, NEAR-INFRARED; STATIC ELECTRICITY; TEMPERATURE;

EID: 84884941916     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp400239z     Document Type: Article

References (57)

1. van Grondelle, R.; Dekker, J. P.; Gillbro, T.; Sundstrom, V. Energy Transfer and Trapping in Photosynthesis Biochim. Biophys. Acta, Bioenerg. 1994, 1187, 1-65 (Pubitemid 24262887)
2. Bahatyrova, S.; Frese, R. N.; Siebert, C. A.; Olsen, J. D.; van der Werf, K. O.; van Grondelle, R.; Niederman, R. A.; Bullough, P. A.; Otto, C.; Hunter, C. N. The Native Architecture of a Photosynthetic Membrane Nature 2004, 430, 1058-1062 (Pubitemid 39128393)
3. McDermott, G.; Prince, S. M.; Freer, A. A.; Hawthornthwaite-Lawless, A. M.; Papiz, M. Z.; Cogdell, R. J.; Isaacs, N. W. Crystal-Structure of an Integral Membrane Light-Harvesting Complex from Photosynthetic Bacteria Nature 1995, 374, 517-521
4. van Amerongen, H.; Valkunas, L.; van Grondelle, R. Photosynthetic Excitons; World Scientific: Singapore, 2000.
5. Urboniene, V.; Vrublevskaja, O.; Gall, A.; Trinkunas, G.; Robert, B.; Valkunas, L. Temperature Broadening of LH2 Absorption in Glycerol Solution Photosynth. Res. 2005, 86, 49-59 (Pubitemid 41361260)
6. Vrublevskaja, O.; Urboniene, V.; Trinkunas, G.; Valkunas, L.; Gall, A.; Robert, B. Estimation of the Spectral Density Function of LH2 Complexes from the Temperature Dependence of the Absorption Spectra Lith. J. Phys. 2006, 46, 39-46
7. Urboniene, V.; Vrublevskaja, O.; Trinkunas, G.; Gall, A.; Robert, B.; Valkunas, L. Solvation Effect of Bacteriochlorophyll Excitons in Light-Harvesting Complex LH2 Biophys. J. 2007, 93, 2188-2198 (Pubitemid 47437602)
8. van Grondelle, R.; Novoderezhkin, V. I. Energy Transfer in Photosynthesis: Experimental Insights and Quantitative Models Phys. Chem. Chem. Phys. 2006, 8, 793-807
9. 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
10. Freiberg, A.; Timpmann, K.; Ruus, R.; Woodbury, N. W. Disordered Exciton Analysis of Linear and Nonlinear Absorption Spectra of Antenna Bacteriochlorophyll Aggregates: LH2-Only Mutant Chromatophores of Rhodobacter sphaeroides at 8 K under Spectrally Selective Excitation J. Phys. Chem. B 1999, 103, 10032-10041 (Pubitemid 129614048)
11. Freiberg, A.; Ratsep, M.; Timpmann, K.; Trinkunas, G.; Woodbury, N. W. Self-Trapped Excitons in LH2 Antenna Complexes between 5 K and Ambient Temperature J. Phys. Chem. B 2003, 107, 11510-11519
12. Wu, H. M.; Reddy, N. R. S.; Small, G. J. Direct Observation and Hole Burning of the Lowest Exciton Level (B870) of the LH2 Antenna Complex of Rhodopseudomonas acidophila (strain 10050) J. Phys. Chem. B 1997, 101, 651-656 (Pubitemid 127617376)
13. Krueger, B. P.; Scholes, G. D.; Fleming, G. R. Calculation of Couplings and Energy-Transfer Pathways between the Pigments of LH2 by the Ab Initio Transition Density Cube Method J. Phys. Chem. B 1998, 102, 5378-5386 (Pubitemid 128578377)
14. Scholes, G. D.; Gould, I. R.; Cogdell, R. J.; Fleming, G. R. Ab Initio Molecular Orbital Calculations of Electronic Couplings in the LH2 Bacterial Light-Harvesting Complex of Rps. Acidophila J. Phys. Chem. B 1999, 103, 2543-2553 (Pubitemid 129702515)
15. Tretiak, S.; Middleton, C.; Chernyak, V.; Mukamel, S. Bacteriochlorophyll and Carotenoid Excitonic Couplings in the LH2 System of Purple Bacteria J. Phys. Chem. B 2000, 104, 9540-9553
16. Rancova, O.; Sulskus, J.; Abramavicius, D. Insight into the Structure of Photosynthetic LH2 Aggregate from Spectroscopy Simulations J. Phys. Chem. B 2012, 116, 7803-7814
17. Cogdell, R. J.; Gall, A.; Kohler, 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)
18. Ketelaars, M.; van Oijen, A. M.; Matsushita, M.; Kohler, J.; Schmidt, J.; Aartsma, T. J. Spectroscopy on the B850 Band of Individual Light-Harvesting 2 Complexes of Rhodopseudomonas Acidophila I. Experiments and Monte Carlo Simulations Biophys. J. 2001, 80, 1591-1603 (Pubitemid 32184292)
19. Trinkunas, G.; Zerlauskiene, O.; Urboniene, V.; Chmeliov, J.; Gall, A.; Robert, B.; Valkunas, L. Exciton Band Structure in Bacterial Peripheral Light-Harvesting Complexes J. Phys. Chem. B 2012, 116, 5192-5198
20. Cogdell, R. J.; Durant, I.; Valentine, J.; Lindsay, J. G.; Schmidt, K. The Isolation and Partial Characterisation of the Light-Harvesting Pigment-Protein Complement of Rhodopseudomonas acidophila Biochim. Biophys. Acta, Bioenerg. 1983, 722, 427-435 (Pubitemid 13126742)
21. Angerhofer, A.; Cogdell, R. J.; Hipkins, M. F. A Spectral Characterisation of the Light-Harvesting Pigment-Protein Complexes from Rhodopseudomonas acidophila Biochim. Biophys. Acta, Bioenerg. 1986, 848, 333-341 (Pubitemid 16105444)
22. Gardiner, A. T.; Cogdell, R. J.; Takaichi, S. The Effect of Growth-Conditions on the Light-Harvesting Apparatus in Rhodopseudomonas acidophila Photosynth. Res. 1993, 38, 159-167 (Pubitemid 2024689)
23. Zuber, H.; Brunisholz, R. A. Structure and Function of Antenna Polypeptides and Chlorophyll-Protein Complexes: Principles and Variability. In Chlorophylls; Scheer, H., Ed.; CRC Press: Boca Raton, FL, 1991; pp 627-703.
24. Fowler, G. J. S.; Visschers, R. W.; Grief, G. G.; Vangrondelle, R.; Hunter, C. N. Genetically Modified Photosynthetic Antenna Complexes with Blueshifted Absorbency Bands Nature 1992, 355, 848-850
25. Firsow, N. N.; Drews, G. Differentiation of the Intracytoplasmic Membrane of Rhodopseudomonas palustris Induced by Variations of Oxygen Partial Pressure or Light Intensity Arch. Microbiol. 1977, 115, 299-306 (Pubitemid 8248574)
26. Gall, A.; Robert, B. Characterization of the Different Peripheral Light-Harvesting Complexes from High- and Low-Light Grown Cells from Rhodopseudomonas palustris Biochemistry 1999, 38, 5185-5190
27. Gall, A.; Sogaila, E.; Gulbinas, V.; Ilioaia, O.; Robert, B.; Valkunas, L. Spectral Dependence of Energy Transfer in Wild-Type Peripheral Light-Harvesting Complexes of Photosynthetic Bacteria Biochim. Biophys. Acta, Bioenerg. 2010, 1797, 1465-1469
28. Zerlauskiene, O.; Trinkunas, G.; Gall, A.; Robert, B.; Urboniene, V.; Valkunas, L. Static and Dynamic Protein Impact on Electronic Properties of Light-Harvesting Complex LH2 J. Phys. Chem. B 2008, 112, 15883-15892
29. Abramavicius, D.; Palmieri, B.; Mukamel, S. Extracting Single and Two-Exciton Couplings in Photosynthetic Complexes by Coherent Two-Dimensional Electronic Spectra Chem. Phys. 2009, 357, 79-84
30. Abramavicius, D.; Palmieri, B.; Voronine, D. V.; Sanda, F.; Mukamel, S. Coherent Multidimensional Optical Spectroscopy of Excitons in Molecular Aggregates; Quasiparticle versus Supermolecule Perspectives Chem. Rev. 2009, 109, 2350-2408
31. May, V.; Kühn, O. Charge and Energy Transfer Dynamics in Molecular Systems, 3 rd, rev. and enl. ed.; Wiley-VCH: Weinheim, Germany, 2011.
32. McLuskey, K.; Prince, S. M.; Cogdell, R. J.; Isaacs, N. W. The Crystallographic Structure of the B800-820 LH3 Light-Harvesting Complex from the Purple Bacteria Rhodopseudomonas acidophila Strain 7050 Biochemistry 2001, 40, 8783-8789 (Pubitemid 32709510)
33. Adolphs, J.; Renger, T. How Proteins Trigger Excitation Energy Transfer in the FMO Complex of Green Sulfur Bacteria Biophys. J. 2006, 91, 2778-2797 (Pubitemid 44526469)
34. Adolphs, J.; Muh, F.; Madjet, M. E. A.; Renger, T. Calculation of Pigment Transition Energies in the FMO Protein Photosynth. Res. 2008, 95, 197-209
35. Madjet, M. E.; Abdurahman, A.; Renger, T. Intermolecular Coulomb Couplings from Ab Initio Electrostatic Potentials: Application to Optical Transitions of Strongly Coupled Pigments in Photosynthetic Antennae and Reaction Centers J. Phys. Chem. B 2006, 110, 17268-17281 (Pubitemid 44412355)
36. Muh, F.; Madjet, M. E. A.; Adolphs, J.; Abdurahman, A.; Rabenstein, B.; Ishikita, H.; Knapp, E. W.; Renger, T. α-Helices Direct Excitation Energy Flow in the Fenna-Matthews-Olson Protein Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 16862-16867 (Pubitemid 350210956)
37. Renger, T. Theory of Excitation Energy Transfer: From Structure to Function Photosynth. Res. 2009, 102, 471-485
38. Adolphs, J.; Muh, F.; Madjet, M. E. A.; Busch, M. S. A.; Renger, T. Structure-Based Calculations of Optical Spectra of Photosystem I Suggest an Asymmetric Light-Harvesting Process J. Am. Chem. Soc. 2010, 132, 3331-3343
39. Fowler, G. J. S.; Sockalingum, G. D.; Robert, B.; Hunter, C. N. Blue Shifts in Bacteriochlorophyll Absorbency Correlate with Changed Hydrogen-Bonding Patterns in Light-Harvesting 2 Mutants of Rhodobacter Sphaeroides with Alterations at α-Tyr-44 and α-Tyr-45 Biochem. J. 1994, 299, 695-700 (Pubitemid 24138536)
40. Sturgis, J. N.; Jirsakova, V.; Reisshusson, F.; Cogdell, R. J.; Robert, B. Structure and Properties of the Bacteriochlorophyll Binding-Site in Peripheral Light-Harvesting Complexes of Purple Bacteria Biochemistry 1995, 34, 517-523
41. Gall, A.; Fowler, G. J. S.; Hunter, C. N.; Robert, B. Influence of the Protein Binding Site on the Absorption Properties of the Monomeric Bacteriochlorophyll in Rhodobacter sphaeroides LH2 Complex Biochemistry 1997, 36, 16282-16287 (Pubitemid 28065044)
42. Alia; Matysik, J.; Erkelens, C.; Hulsbergen, F. B.; Gast, P.; Lugtenburg, J.; de Groot, H. J. M. Bacteriochlorophyll/Imidazole and Chlorophyll/Imidazole Complexes are Negatively Charged in an Apolar Environment Chem. Phys. Lett. 2000, 330, 325-330
43. Papiz, M. Z.; Prince, S. M.; Howard, T.; Cogdell, R. J.; Isaacs, N. W. 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. 2003, 326, 1523-1538 (Pubitemid 36277668)
44. Humphrey, W.; Dalke, A.; Schulten, K. VMD: Visual Molecular Dynamics J. Mol. Graph. Modell. 1996, 14, 33-38 (Pubitemid 26152973)
45. Knox, R. S.; Spring, B. Q. Dipole Strengths in the Chlorophylls Photochem. Photobiol. 2003, 77, 497-501
46. Alden, R. G.; Johnson, E.; Nagarajan, V.; Parson, W. W.; Law, C. J.; Cogdell, R. G. Calculations of Spectroscopic Properties of the LH2 Bacteriochlorophyll-Protein Antenna Complex from Rhodopseudomonas acidophila J. Phys. Chem. B 1997, 101, 4667-4680 (Pubitemid 127596268)
47. Abramavicius, D.; Butkus, V.; Valkunas, L. Quantum Dynamics and Spectroscopy of Excitons in Molecular Aggregates. In Quantum Efficiency in Complex Systems. Part II, From Molecular Aggregates to Organic Solar Cells; Würfel, U.; Thorwart, M.; Weber, E. R., Eds.; Elsevier Academic Press: San Diego, CA; London, 2011; pp 3-46.
48. Jang, S.; Newton, M. D.; Silbey, R. J. Multichromophoric Förster Resonance Energy Transfer from B800 to B850 in the Light Harvesting Complex 2: Evidence for Subtle Energetic Optimization by Purple Bacteria J. Phys. Chem. B 2007, 111, 6807-6814 (Pubitemid 47152561)
49. Olbrich, C.; Kleinekathofer, U. Time-Dependent Atomistic View on the Electronic Relaxation in Light-Harvesting System II J. Phys. Chem. B 2010, 114, 12427-12437
50. Butkus, V.; Valkunas, L.; Abramavicius, D. Molecular Vibrations-Induced Quantum Beats in Two-Dimensional Electronic Spectroscopy J. Chem. Phys. 2012, 137
51. Cherezov, V.; Clogston, J.; Papiz, M. Z.; Caffrey, M. Room to Move: Crystallizing Membrane proteins in Swollen Lipidic Mesophases J. Mol. Biol. 2006, 357, 1605-1618
52. Alia; Matysik, J.; Soede-Huijbregts, C.; Baldus, M.; Raap, J.; Lugtenburg, J.; Gast, P.; van Gorkom, H. J.; Hoff, A. J.; de Groot, H. J. M. Ultrahigh Field MAS NMR Dipolar Correlation Spectroscopy of the Histidine Residues in Light-Harvesting Complex II from Photosynthetic Bacteria Reveals partial Internal Charge Transfer in the B850/His Complex J. Am. Chem. Soc. 2001, 123, 4803-4809 (Pubitemid 32895777)
53. 13C) MAS NMR Resolves the Electronic Structure of Coordinated Histidines in Light-Harvesting Complex II: Assessment of Charge Transfer and Electronic Delocalization Effect J. Biomol. NMR 2004, 28, 157-164 (Pubitemid 38232794)
54. Wawrzyniak, P. K.; Alia, A.; Schaap, R. G.; Heemskerk, M. M.; de Groot, H. J. M.; Buda, F. Protein-Induced Geometric Constraints and Charge Transfer in Bacteriochlorophyll-histidine Complexes in LH2 Phys. Chem. Chem. Phys. 2008, 10, 6971-6978
55. He, Z.; Sundstrom, V.; Pullerits, T. Influence of the Protein Binding Site on the Excited States of Bacteriochlorophyll: DFT Calculations of B800 in LH2 J. Phys. Chem. B 2002, 106, 11606-11612 (Pubitemid 35361133)
56. Neugebauer, J. Photophysical Properties of Natural Light-Harvesting Complexes Studied by Subsystem Density Functional Theory J. Phys. Chem. B 2008, 112, 2207-2217 (Pubitemid 351316345)
57. Konig, C.; Neugebauer, J. Quantum Chemical Description of Absorption Properties and Excited-State Processes in Photosynthetic Systems ChemPhysChem 2012, 13, 386-425