Fluorescence Spectral Dynamics of Single LHCII Trimers

Overview

Journal Biophys J

Publisher Cell Press

Specialty Biophysics

Date 2010 Jun 17

PMID 20550923

Citations 50

Authors

Tjaart P J Kruger

Vladimir I Novoderezhkin

Cristian Ilioaia

Rienk van Grondelle

Affiliations

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Abstract

Single-molecule spectroscopy was employed to elucidate the fluorescence spectral heterogeneity and dynamics of individual, immobilized trimeric complexes of the main light-harvesting complex of plants in solution near room temperature. Rapid reversible spectral shifts between various emitting states, each of which was quasi-stable for seconds to tens of seconds, were observed for a fraction of the complexes. Most deviating states were characterized by the appearance of an additional, red-shifted emission band. Reversible shifts of up to 75 nm were detected. By combining modified Redfield theory with a disordered exciton model, fluorescence spectra with peaks between 670 nm and 705 nm could be explained by changes in the realization of the static disorder of the pigment-site energies. Spectral bands beyond this wavelength window suggest the presence of special protein conformations. We attribute the large red shifts to the mixing of an excitonic state with a charge-transfer state in two or more strongly coupled chlorophylls. Spectral bluing is explained by the formation of an energy trap before excitation energy equilibration is completed.

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References

Brecht M, Studier H, Radics V, Nieder J, Bittl R . Spectral diffusion induced by proton dynamics in pigment-protein complexes. J Am Chem Soc. 2008; 130(51):17487-93. DOI: 10.1021/ja806216p. View

McLuskey K, Prince S, Cogdell R, Isaacs N . The crystallographic structure of the B800-820 LH3 light-harvesting complex from the purple bacteria Rhodopseudomonas acidophila strain 7050. Biochemistry. 2001; 40(30):8783-9. DOI: 10.1021/bi010309a. View

Croce R, Chojnicka A, Morosinotto T, Ihalainen J, van Mourik F, Dekker J . The low-energy forms of photosystem I light-harvesting complexes: spectroscopic properties and pigment-pigment interaction characteristics. Biophys J. 2007; 93(7):2418-28. PMC: 1965455. DOI: 10.1529/biophysj.107.106955. View

Schonle A, Hell S . Heating by absorption in the focus of an objective lens. Opt Lett. 2007; 23(5):325-7. DOI: 10.1364/ol.23.000325. View

Rutkauskas D, Olsen J, Gall A, Cogdell R, Hunter C, van Grondelle R . Comparative study of spectral flexibilities of bacterial light-harvesting complexes: structural implications. Biophys J. 2006; 90(7):2463-74. PMC: 1403163. DOI: 10.1529/biophysj.105.075895. View

van Oort B, van Hoek A, Ruban A, van Amerongen H . Equilibrium between quenched and nonquenched conformations of the major plant light-harvesting complex studied with high-pressure time-resolved fluorescence. J Phys Chem B. 2007; 111(26):7631-7. DOI: 10.1021/jp070573z. View

Weber G . Energetics of ligand binding to proteins. Adv Protein Chem. 1975; 29:1-83. DOI: 10.1016/s0065-3233(08)60410-6. View

van Roon H, van Breemen J, de Weerd F, Dekker J, Boekema E . Solubilization of green plant thylakoid membranes with n-dodecyl-alpha,D-maltoside. Implications for the structural organization of the Photosystem II, Photosystem I, ATP synthase and cytochrome b6 f complexes. Photosynth Res. 2005; 64(2-3):155-66. DOI: 10.1023/A:1006476213540. View

Nieder J, Brecht M, Bittl R . Dynamic intracomplex heterogeneity of phytochrome. J Am Chem Soc. 2009; 131(1):69-71. DOI: 10.1021/ja8058292. View

10.

Renger T . Theory of optical spectra involving charge transfer states: dynamic localization predicts a temperature dependent optical band shift. Phys Rev Lett. 2004; 93(18):188101. DOI: 10.1103/PhysRevLett.93.188101. View

11.

van Leeuwen P, Nieveen M, van de Meent E, Dekker J, Van Gorkom H . Rapid and simple isolation of pure photosystem II core and reaction center particles from spinach. Photosynth Res. 2014; 28(3):149-53. DOI: 10.1007/BF00054128. View

12.

Rutkauskas D, Novoderezhkin V, Cogdell R, van Grondelle R . Fluorescence spectroscopy of conformational changes of single LH2 complexes. Biophys J. 2004; 88(1):422-35. PMC: 1305019. DOI: 10.1529/biophysj.104.048629. View

13.

Kuhlbrandt W, Wang D, Fujiyoshi Y . Atomic model of plant light-harvesting complex by electron crystallography. Nature. 1994; 367(6464):614-21. DOI: 10.1038/367614a0. View

14.

Hofmann C, Aartsma T, Michel H, Kohler J . Direct observation of tiers in the energy landscape of a chromoprotein: a single-molecule study. Proc Natl Acad Sci U S A. 2003; 100(26):15534-8. PMC: 307602. DOI: 10.1073/pnas.2533896100. View

15.

Cogdell R, Isaacs N, Freer A, Arrelano J, Howard T, Papiz M . The structure and function of the LH2 (B800-850) complex from the purple photosynthetic bacterium Rhodopseudomonas acidophila strain 10050. Prog Biophys Mol Biol. 1997; 68(1):1-27. DOI: 10.1016/s0079-6107(97)00010-2. View

16.

Gulbinas V, Karpicz R, Garab G, Valkunas L . Nonequilibrium heating in LHCII complexes monitored by ultrafast absorbance transients. Biochemistry. 2006; 45(31):9559-65. DOI: 10.1021/bi060048a. View

17.

Jennings R, Garlaschi F, Engelmann E, Zucchelli G . The room temperature emission band shape of the lowest energy chlorophyll spectral form of LHCI. FEBS Lett. 2003; 547(1-3):107-10. DOI: 10.1016/s0014-5793(03)00687-2. View

18.

van Grondelle R, Novoderezhkin V . Energy transfer in photosynthesis: experimental insights and quantitative models. Phys Chem Chem Phys. 2006; 8(7):793-807. DOI: 10.1039/b514032c. View

19.

Gradinaru C, Ozdemir S, Gulen D, van Stokkum I, van Grondelle R, van Amerongen H . The flow of excitation energy in LHCII monomers: implications for the structural model of the major plant antenna. Biophys J. 1998; 75(6):3064-77. PMC: 1299977. DOI: 10.1016/S0006-3495(98)77747-1. View

20.

Novoderezhkin V, Palacios M, van Amerongen H, van Grondelle R . Excitation dynamics in the LHCII complex of higher plants: modeling based on the 2.72 Angstrom crystal structure. J Phys Chem B. 2006; 109(20):10493-504. DOI: 10.1021/jp044082f. View