In Vitro Self-Assembly of the Light Harvesting Pigment-Protein LH2 Revealed by Ultrafast Spectroscopy and Electron Microscopy

Biophysical Journal

Volumn 86, Issue 4, 2004, Pages 2363-2373

  Schubert, Axel ^a   Stenstam, Anna ^a   Beenken, Wichard J D ^a   Herek, Jennifer L ^b   Cogdell, Richard ^c   Pullerits, Tõnu ^a   Sundström, Villy ^a  

^a LUND UNIVERSITY   (Sweden)

^b FOM INSTITUTE AMOLF   (Netherlands)

^c UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DODECYLAMINE; N,N DIMETHYLDODECYLAMINE OXIDE; OXIDE; PIGMENT; PROTEIN; PROTEIN LH2; SURFACTANT; UNCLASSIFIED DRUG; WATER;

ARTICLE; DEVICE; ELECTRON MICROSCOPY; LIGHT HARVESTING SYSTEM; PROTEIN ASSEMBLY; RHODOBACTER SPHAEROIDES; SPECTROSCOPY; THERMODYNAMICS; TRANSMISSION ELECTRON MICROSCOPY;

BACTERIA (MICROORGANISMS); RHODOBACTER; RHODOBACTER SPHAEROIDES; RHODOPSEUDOMONAS;

EID: 1942423239     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(04)74293-9     Document Type: Article

References (59)

1. Ambroise, A., R. W. Wagner, P. D. Rao, J. A. Riggs, P. Hascoat, J. R. Diers, J. Seth, R. K. Lammi, D. F. Bocian, D. Holten, and J. S. Lindsey. 2001. Design and synthesis of porphyrin-based optoelectronic gates. Chem. Mat. 13:1023-1034.
2. Bergström, H., V. Sundström, R. van Grondelle, T. Gillbro, and R. Cogdell. 1988. Energy transfer dynamics of isolated B800-850 and B800-820 pigment-protein complexes of Rhodobacter sphaeroides and Rhodopseudomonas acidophila. Biochim. Biophys. Acta. 936:90-98.
3. Bibby, T. S., J. Nield, and J. Barber. 2001. Iron deficiency induces the formation of an antenna ring around trimeric photosystem I in cyanobacteria. Nature. 412:743-745.
4. Brown, W. 1993. Dynamic Light Scattering: The Method and Some Applications. Oxford University Press, Oxford, UK.
5. Brüggemann, B., J. L. Herek, V. Sundström, T. Pullerits, and V. May. 2001. Microscopic theory of excitation annihilation: application to the LH2 antenna system. J. Phys. Chem. B. 105:11391-11394.
6. Chachisvilis, M., O. Kühn, T. Pullerits, and V. Sundström. 1997. Excitons in photosynthetic purple bacteria: wavelike motion or incoherent hopping? J. Phys. Chem. B. 101:7275-7283.
7. Dahlbom, M., T. Pullerits, S. Mukamel, and V. Sundström. 2001. Exciton delocalization in the B850 light-harvesting complex: comparison of different measures. J. Phys. Chem. B. 105:5515-5524.
8. Den Hollander, W. T. F., J. G. C. Bakker, and R. Van Grondelle. 1983. Trapping loss and annihilation of excitation in a photosynthetic system I. Theoretical aspects. Biochim. Biophys. Acta. 725:492-507.
9. Evans, D. F., and H. Wennerström. 1999. The Colloidal Domain: Where Physics, Chemistry, Biology and Technology Meet. Wiley, New York, NY.
10. Fattal, D. R., and A. Ben-Shaul. 1993. A molecular model for lipid-protein interaction in membranes: the role of hydrophobic mismatch. Biophys. J. 65:1795-1809.
11. Fiedor, L., H. Scheer, C. N. Hunter, F. Tschirschwitz, B. Voigt, J. Ehlert, E. Nibbering, D. Leupold, and T. Elsaesser. 2000. Introduction of a 60-fs deactivation channel in the photosynthetic antenna LH1 by Ni-bacteriopheophytin a. Chem. Phys. Lett. 319:145-152.
12. Förster, T. 1948. Zwischenmolekulare energiewanderung und fluoreszenz. Ann. Phys. 2:55-67.
13. Fowler, G. J. S., W. Crielaard, R. W. Visschers, and R. van Grondelle. 1993. Site-directed mutagenesis of the LH2 light-harvesting complex of Rhodobacter sphaeroides: changing bLys23 to Gln results in a shift in the 850-nm absorption peak. Photochem. Photobiol. 57:2-5.
14. Freiberg, A., V. I. Godik, T. Pullerits, and K. Timpmann. 1989. Picosecond dynamics of directed excitation transfer in spectrally heterogeneous light-harvesting antenna of purple bacteria. Biochim. Biophys. Acta. 973: 93-104.
15. Frese, R. N., J. D. Olsen, R. Branvall, W. H. J. Westerhuis, C. N. Hunter, and R. van Grondelle. 2000. The long-range supraorganization of the bacterial photosynthetic unit: a key role for PufX. Proc. Natl. Acad. Sci. USA. 97:5197-5202.
16. Hawthornthwaite, A. M., and R. Cogdell. 1991. Bacteriochlorophyll binding proteins. In The Chlorophylls. H. Scheer, editor. CRC Press, Boca Raton, FL. 493-528.
17. Henderson, R., and P. N. T. Unwin. 1975. Three-dimensional model of purple membrane obtained by electron-microscopy. Nature, 257:28-32.
18. Herek, J. L., N. J. Fraser, T. Pullerits, P. Martinsson, T. Polivka, H. Scheer, R. J. Cogdell, and V. Sundström. 2000. B800-B850 energy transfer mechanism in bacterial LH2 complexes investigated by B800 pigment exchange. Biophys. J. 78:2590-2596.
19. Hess, S., M. Chachisvilis, K. Timpmann, M. R. Jones, G. J. S. Fowler, C. N. Hunter, and V. Sundström. 1995. Temporally and spectrally resolved subpicosecond energy transfer within the peripheral antenna complex (LH2) and from LH2 to the core antenna complex in photo-synthetic purple bacteria. Proc. Natl. Acad. Sci. USA. 92:12333-12337.
20. Hoff, A., and J. Amesz. 1991. Visible absorption spectroscopy of chlorophylls. In The Chlorophylls. H. Scheer, editor. CRC Press, Boca Raton, FL. 723-738.
21. Jimenez, R., S. N. Dikshit, S. E. Bradforth, and G. R. Fleming. 1996. Electronic excitation transfer in the LH2 complex of Rhodobacter sphaeroides. J. Phys. Chem. 100:6825-6834.
22. Jönsson, B., and H. Wennerström. 1987. Phase equilibria in a three-component water-soap-alcohol system. J. Phys. Chem. 91:338-352.
23. Jones, L. S., N. B. Bam, and T. W. Randolph. 1996. Surfactant-stabilized protein formulations: a review of protein-surfactant interactions and novel analytical methodologies. ACS Sym. Ser. 675:206-222.
24. Jungas, C., J.-L. Ranck, J.-L. Rigaud, P. Joliot, and A. Verméglio. 1999. Supramolecular organization of the photosynthetic apparatus of Rhodobacter sphaeroides. EMBO J. 18:534-542.
25. Landgren, M., M. Aamodt, and B. Jönsson. 1992. Solubilization of uncharged molecules in ionic surfactant aggregates. 2. Phase equilibria. J. Phys. Chem. 96:950-961.
26. Lewis, A., Y. Albeck, Z. Lange, J. Benchowski, and G. Weizman. 1997. Optical communication with negative light intensity with a plastic bacteriorhodopsin film. Science. 275:1462-1464.
27. Le Maire, M., P. Champeil, and J. V. Moller. 2000. Interaction of membrane proteins and lipids with solubilizing detergents. Biochim. Biophys. Acta. 1508:86-111.
28. Li, J., A. Ambroise, S. I. Yang, J. R. Diers, J. Seth, C. R. Wack, D. F. Bocian, D. Holten, and J. S. Lindsey. 1999. Template-directed synthesis, excited-state photodynamics, and electronic communication in a hexameric wheel of porphyrins. J. Am. Chem. Soc. 121:8927-8940.
29. Li, M., H. Schnablegger, and S. Mann. 1999. Coupled synthesis and self-assembly of nanoparticles to give structures with controlled organization. Nature. 402:393-395.
30. Limantara, L., R. Fujii, J.-P. Zhang, T. Kakuno, H. Hara, A. Kawamori, T. Yagura, R. J. Cogdell, and Y. Koyama. 1998. Generation of triplet and cation radical bacteriochlorophyll a in carotenoidless LH1 and LH2 antenna complexes from Rhodobacter sphaeroides. Biochemistry. 37:17469-17486.
31. 2O system. J. Am. Oil Chem. Soc. 43:28-30.
32. Maeda, H., M. A. Tsunoda, and S. Ikeda. 1974. Electric and nonelectric interactions of a nonionic-cationic micelle. J. Phys. Chem. 78:1086-1090.
33. Mauzerall, D. 1976. Multiple excitations in photosynthetic systems. Biophys. J. 16:87-91.
34. McDermott, G., S. M. Prince, A. A. Freer, A. M. Hawthomthwaite-Lawless, M. Z. Papiz, R. J. Cogdell, and N. W. Isaacs. 1995. Crystal structure of an integral membrane light-harvesting complex from photosynthetic bacteria. Nature. 374:517-521.
35. Mizoguchi, K., K. Fukui, H. Yanagishita, T. Nakane, and T. Nakata. 2002. Ultrafiltration behavior of a new type of non-ionic surfactant around the CMC. J. Membr. Sci. 208:285-288.
36. Monshouwer, R., M. Abrahamsson, F. van Mourik, and R. van Grondelle, 1997. Superradiance and exciton delocalization in bacterial photosynthetic light-harvesting systems. J. Phys. Chem. B. 101:7241-7248.
37. Morén, A. K., O. Regev, and A. Khan. 1999. A cryo-TEM study of protein-surfactant gels and solutions. J. Colloid. Interf. Sci. 222:170-178.
38. Nagarajan, V., and W. W. Parson. 1997. Excitation energy transfer between the B850 and B875 antenna complexes of Rhodobacter sphaeroides. Biochemistry. 36:2300-2306.
39. Ogawa, K., T. Zhang, K. Yoshihara, and Y. Kobuke. 2002. Large third-order optical nonlinearity of self-assembled supramolecular porphyrin oligomers. J. Am. Chem. Soc. 124:22-23.
40. 2H nuclear magnetic resonance spectroscopy. Biophys. J. 68:547-557.
41. Prince, S. M., T. D. Howard, D. A. A. Myles, C. Wilkinson, M. Z. Papiz, A. A. Freer, R. J. Cogdell, and N. W. Isaacs. 2003. Detergent structure in crystals of the integral membrane light-harvesting complex LH2 from Rhodopseudomonas acidophila strain 10050. J. Mol. Biol. 326:307-315.
42. Polivka, T., T. Pullerits, J. L. Herek, and V. Sundström. 2000. Exciton relaxation and polaron formation in LH2 at low temperature. J. Phys. Chem. B. 104:1088-1096.
43. Pullerits, T., M. Chachisvilis, and V. Sundström. 1996. Exciton delocalization length in the B850 antenna of Rhodobacter sphaeroides. J. Phys. Chem. B. 100:10787-10792.
44. Reddy, N. R. S., R. Picorel, and G. J. Small. 1992. B896 and B870 components of the Rhodobacter sphaeroides antenna: a hole-burning study. J. Phys. Chem. 96:6458-6464.
45. Rogl, H., K. Kosemund, W. Kühlbrandt, and I. Collinson. 1998. Refolding of Escherichia coli produced membrane protein inclusion bodies immobilised by nickel chelating chromatography. FEBS Lett. 432:21-26.
46. Roth, M., A. Lewit-Bentley, H. Michel, J. Deisenhofer, R. Huber, and D. Oesterhelt. 1989. Detergent structure in crystals of a photosynthetic reaction centre. Nature. 340:659-661.
47. Scholes, G. 1999. Theory of coupling in multichromophoric systems. In Resonance Energy Transfer. D. L. Andrews and A. A. Demidov, editors. John Wiley and Sons, New York, NY. 213-242.
48. Sirringhaus, H., P. J. Brown, R. H. Friend, M. M. Nielsen, K. Bechgaard, B. M. W. Langeveld-Voss, A. J. H. Spiering, R. A. J. Janssen, E. W. Meijer, P. Herwig, and D. M. de Leeuw. 1999, Two-dimensional charge transport in self-organized, high-mobility conjugated polymers. Nature. 401:685-688.
49. Sundström, V., T. Pullerits, and R. van Grondelle. 1999. Photosynthetic light-harvesting: reconciling dynamics and structure of purple bacterial LH2 reveals function of photosynthetic unit. J. Phys. Chem. B. 103:2327-2346.
50. Tanford, C. 1997. How protein chemists learned about the hydrophobic factor. Protein Sci. 6:1358-1366.
51. Trinkunas, G., J. L. Herek, T. Polivka, V. Sundström, and T. Pullerits. 2001. Exciton delocalization probed by excitation annihilation in the light-harvesting antenna LH2. Phys. Rev. Lett. 86:4167-4170.
52. Unwin, P. N., and R. Henderson. 1975. Molecular-structure determination by electron-microscopy of unstained crystalline specimens. J. Mol. Biol. 94:425-440.
53. van Grondelle, R., C. N. Hunter, J. G. C. Bakker, and H. J. M. Kramer. 1983. Size and structure of antenna complexes of photosynthetic bacteria as studied by singlet-singlet quenching of the bacteriochlorophyll fluorescence yield. Biochim. Biophys. Acta. 723:30-36.
54. Valkunas, L., G. Trinkunas, V. Liuolia, and R. van Grondelle. 1995. Nonlinear annihilation of excitations in photosynthetic systems. Biophys. J. 69:1117-1129.
55. Vasilescu, M., P. Angelescu, M. Almgren, and A. Valstar. 1999. Interactions of globular proteins with surfactants studied with fluorescence probe methods. Langmuir. 15:2635-2643.
56. Vos, M., R. van Grondelle, F. W. van der Kooij, D. van de Poll, J. Amesz, and L. N. M. Duysens. 1986. Singlet-singlet annihilation at low temperatures in the antenna of purple bacteria. Biochim. Biophys. Acta. 850:501-512.
57. Westerhuis, W. H. J., M. Vos, R. van Grondelle, J. Amesz, and R. A. Niederman. 1998. Altered organization of light-harvesting complexes in phospholipid-enriched Rhodobacter sphaeroides chromatophores as determined by fluorescence yield and singlet-singlet annihilation measurements. Biochim. Biophys. Acta. 1366:317-329.
58. Wolf-Klein, H., C. Kohl, K. Müllen, and H. Paulsen. 2002. Biomimetic model of a plant photosystem consisting of a recombinant light-harvesting complex and a terrylene dye. Angew. Chem. Int. Ed. 41:3378-3380.
59. Young, A. J. 1991. The photoprotective role of carotenoids in higher plants. Physiol. Plant. 83:702-708.