Triplet exciton formation as a novel photoprotection mechanism in chlorosomes of Chlorobium tepidum

Biophysical Journal

Volumn 93, Issue 1, 2007, Pages 192-201

  Kim, Hanyoup ^a   Li, Hui ^b,c   Maresca, Julia A ^b   Bryant, Donald A ^b   Savikhin, Sergei ^a  

^a PURDUE UNIVERSITY   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIOCHLOROPHYLL; CAROTENOID; SINGLET OXYGEN;

ARTICLE; BACTERIUM MUTANT; CHLOROBI; CHLOROBIUM TEPIDUM; CONTROLLED STUDY; DNA MODIFICATION; ENERGY TRANSFER; LIGHT HARVESTING SYSTEM; NONHUMAN; PHOTODEGRADATION; SIMULATION; TRANSPORT KINETICS; WILD TYPE;

CHLOROBACULUM TEPIDUM;

EID: 34447254235     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.106.103556     Document Type: Article

References (77)

1. Blankenship, R. E., and K. Matsuura. 2003. Antenna complexes from green photosynthetic bacteria. In Light-Harvesting Antennas in Photosynthesis. B. R. Green and W. W. Parson, editors. Kluwer Academic Publishers, Dordrecht, The Netherlands. 195-217.
2. Blankenship, R. E., J. M. Olson, and M. Miller. 1995. Antenna complexes from green photosynthetic bacteria. In Anoxygenic Photosynthetic Bacteria. R. E. Blankenship, M. T. Madigan, and C. E. Bauer, editors. Kluwer Academic Publishers, Dordrecht, The Netherlands. 399-435.
3. Frigaard, N. U., and D. A. Bryant. 2006. Chlorosomes: antenna organelles in green photosynthetic bacteria. In Complex Intracellular Structures in Prokaryotes. J. M. Shively, editor. Springer, Berlin, Germany. 79-114.
4. Montaño, G. A., B. P. Bowen, J. T. LaBelle, N. W. Woodbury, V. B. Pizziconi, and R. E. Blankenship. 2003. Characterization of Chlorobium tepidum chlorosomes: a calculation of bacteriochlorophyll c per chlorosome and oligomer modeling. Biophys. J. 85:2560-2565.
5. Kühlbrandt, W., D. N. Wang, and Y. Fujiyoshi. 1994. Atomic model of plant light-harvesting complex by electron crystallography. Nature. 367:614-621.
6. McDermott, G., S. M. Prince, A. A. Freer, A. M. Hawthornthwaite-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.
7. Miller, M., T. Gillbro, and J. M. Olson. 1993. Aqueous aggregates of bacteriochlorophyll c as a model for pigment organization in chlorosomes. Photochem. Photobiol. 57:98-102.
8. Holzwarth, A. R., K. Griebenow, and K. Schaffner. 1992. Chlorosomes, photosynthetic antennae with novel self-organized pigment structures. J. Photochem. Photobiol. A. 65:61-71.
9. Smith, K. M., L. A. Kehres, and J. Fajer. 1983. Aggregation of the bacteriochlorophylls c, d, and e. Models for the antenna chlorophylls of green and brown photosynthetic bacteria. J. Am. Chem. Soc. 105:1387-1389.
10. Vassilieva, E. V., J. G. Ormerod, and D. A. Bryant. 2002. Biosynthesis of chlorosome proteins is not inhibited in acetylene-treated cultures of Chlorobium vibrioforme. Photosynth. Res. 71:69-81.
11. Frigaard, N. U., H. Li, K. J. Milks, and D. A. Bryant. 2004. Nine mutants of Chlorobium tepidum each unable to synthesize a different chlorosome protein still assemble functional chlorosomes. J. Bacteriol. 186:646-653.
12. 13C NMR. Photosynth. Res. 41:211-223.
13. Psencík, J., T. P. Ikonen, P. Laurinmäki, M. C. Merckel, S. J. Butcher, R. E. Serimaa, and R. Tuma. 2004. Lamellar organization of pigments in chlorosomes, the light harvesting complexes of green photosynthetic bacteria. Biophys. J. 87:1165-1172.
14. van Rossum, B.-J., D. B. Steensgaard, F. M. Mulder, G. J. Boender, K. Schaffner, A. R. Holzwarth, and H. J. M. de Groot. 2001. A refined model of the chlorosomal antennae of the green bacterium Chlorobium tepidum from proton chemical shift constraints obtained with high-field 2-D and 3-D MAS NMR dipolar correlation spectroscopy. Biochemistry. 40:1587-1595.
15. Bryant, D. A., E. V. Vassilieva, N. U. Frigaard, and H. Li. 2002. Selective protein extraction from Chlorobium tepidum chlorosomes using detergents. evidence that csmA forms multimers and binds bacteriochlorophyll a. Biochemistry. 41:14403-14411.
16. Sakuragi, Y., N. U. Frigaard, K. Shimada, and K. Matsuura. 1999. Association of bacteriochlorophyll a with the CsmA protein in chlorosomes of the photosynthetic green filamentous bacterium Chloroflexus aurantiacus. Biochim. Biophys. Acta. 1413:172-180.
17. Montaño, G. A., H.-M. Wu, S. Lin, D. C. Brune, and R. E. Blankenship. 2003. Isolation and characterization of the b798 light-harvesting baseplate from the chlorosomes of Chloroflexus aurantiacus. Biochemistry. 42:10246-10251.
18. Li, H., N. U. Frigaard, and D. A. Bryant. 2006. Molecular contacts for chlorosome envelope proteins revealed by cross-linking studies with chlorosomes from chlorobium tepidum. Biochemistry. 45:9095-9103.
19. Frigaard, N. U., S. Takaichi, M. Hirota, K. Shimada, and K. Matsuura. 1997. Quinones in chlorosomes of green sulfur bacteria and their role in the redox-dependent fluorescence studied in chlorosome-like bacteriochlorophyll c aggregates. Arch. Microbiol. 167:343-349.
20. Olson, J. M. 1998. Chlorophyll organization and function in green photosynthetic bacteria. Photochem. Photobiol. 67:61-75.
21. van Dorssen, R. J., P. D. Gerola, J. M. Olson, and J. Amesz. 1986. Optical and structural properties of chlorosomes of the photosynthetic green sulfur bacterium Chlorobium limicola. Biochim. Biophys. Acta. 848:77-82.
22. Psencík, J., Y.-Z. Ma, J. B. Arellano, J. Garcia-Gil, A. R. Holzwarth, and T. Gillbro. 2002. Excitation energy transfer in chlorosomes of Chlorobium phaeobacteroides strain CL1401: the role of carotenoids. Photosynth. Res. 71:5-18.
23. Melø, T. B., N. U. Frigaard, K. Matsuura, and K. R. Naqvi. 2000. Electronic energy transfer involving carotenoid pigments in chlorosomes of two green bacteria: Chlorobium tepidum and Chloroflexus aurantiacus. Spectrochim. Acta A Mol. Biomol. Spectrosc. 56:2001-2010.
24. Krueger, B. P., G. D. Scholes, R. Jimenez, and G. R. Fleming. 1998. Electronic excitation transfer from carotenoid to bacteriochlorophyll in the purple bacterium Rhodopseudomonas acidophila. J. Phys. Chem. B. 102:2284-2292.
25. Dexter, D. L. 1953. A theory of sensitized luminescence in solids. J. Chem. Phys. 21:836-850.
26. Schödel, R., K.-D. Irrgang, J. Voigt, and G. Renger. 1998. Rate of carotenoid triplet formation in solubilized light-harvesting complex II (LHCII) from spinach. Biophys. J. 75:3143-3153.
27. Psencík, J., J. B. Arellano, T. P. Ikonen, C. M. Borrego, P. A. Laurinmäki, S. J. Butcher, R. E. Serimaa, and R. Tuma. 2006. Internal structure of chlorosomes from brown-colored chlorobium species and the role of carotenoids in their assembly. Biophys. J. 91:1433-1440.
28. Psencík, J., G. F. W. Searle, J. Hála, and T. J. Schaafsma. 1994. Fluorescence detected magnetic resonance (FDMR) of green sulfur photosynthetic bacteria Chlorobium sp. Photosynth. Res. 40:1-10.
29. Carbonera, D., G. Giacometti, C. Vannini, P. D. Gerola, A. Vianelli, A. Maniero, and L. C. Brunel. 1998. Electron Magnetic Resonance of the Chlorosomes from Green Sulfur Bacterium Chlorobium tepidum. G. Garab, editor. Kluwer, Dordrecht, The Netherlands.
30. Arellano, J. B., T. B. Melø, C. M. Borrego, J. Garcia-Gil, and K. R. Naqvi. 2000. Nanosecond laser photolysis studies of chlorosomes and artificial aggregates containing bacteriochlorophyll e: evidence for the proximity of carotenoids and bacteriochlorophyll a in chlorosomes from Chlorobium phaeobacteroidesstrain CL1401. Photochem. Photobiol. 72:669-675.
31. Arellano, J. B., J. Psencík, C. M. Borrego, Y.-Z. Ma, R. Guyoneaud, J. Garcia-Gil, and T. Gillbro. 2000. Effect of carotenoid biosynthesis inhibition on the chlorosome organization in chlorobium phaeobacteroides strain CL1401. Photochem. Photobiol. 71:715-723.
32. Frigaard, N. U., J. A. Maresca, C. E. Yunker, A. D. Jones, and D. A. Bryant. 2004. Genetic manipulation of carotenoid biosynthesis in the green sulfur bacterium Chlorobium tepidum. J. Bacteriol. 186:5210-5220.
33. Maresca, J. A., and D. A. Bryant. 2006. Two genes encoding new carotenoid-modifying enzymes in the green sulfur bacterium chlorobium tepidum. J. Bacteriol. 188:6217-6223.
34. Vassilieva, E. V., V. L. Stirewalt, C. U. Jakobs, N. U. Frigaard, K. Inoue-Sakamoto, M. A. Baker, A. Sotak, and D. A. Bryant. 2002. Subcellular localization of chlorosome proteins in Chlorobium tepidum and characterization of three new chlorosome proteins: CsmF, CsmH, and CsmX. Biochemistry. 41:4358-4370.
35. van Walree, C. A., Y. Sakuragi, D. B. Steensgaard, C. S. Bösinger, N. U. Frigaard, R. P. Cox, A. R. Holzwarth, and M. Miller. 1999. Effect of alkaline treatment on bacteriochlorophyll a, quinones and energy transfer in chlorosomes from Chlorobium tepidum and Chlorobium phaeobacteoides. Photochem. Photobiol. 69:322-328.
36. Buck, D. R., and W. S. Struve. 1996. Tubular exciton models for BChl c antennae in chlorosomes from green photosynthetic bacteria. Photosynth. Res. 48:367-377.
37. Struve, W. S. 1995. Theory of electronic energy transfer. In Anoxygenic Photosynthetic Bacteria. R. E. Blankenship, M. T. Madigan, and C. E. Bauer, editors. Kluwer Academic Publishers, Dordrecht, The Netherlands. 297-313.
38. van Amerongen, H., L. Valkunas, and R. van Grondelle. 2000. Photosynthetic Excitons. World Scientific, Singapore.
39. Press, W. H., S. A. Teukolsky, W. T. Vetterling, and B. P. Flannery. 1992. Jacobi transformation of a symmetric matrix. In Numerical Recipes in C. The Art of Scientific Computing, 2nd Ed. Cambridge University Press, Cambridge, UK. 463-469.
40. Krasnovsky, A. A., Jr., P. Cheng, R. E. Blankenship, T. A. Moore, and D. Gust. 1993. The photophysics of monomeric bacteriochlorophylls c and d and their derivatives: properties of the triplet state and singlet oxygen photogeneration and quenching. Photochem. Photobiol. 57:324-330.
41. Liaaen-Jensen, S., E. Hegge, and L. M. Jackman. 1964. Bacterial carotenoids. XVII. The carotenoids of photosynthetic green bacteria. Acta Chem. Scand. 18:1703-1718.
42. Wahlund, T. M., C. R. Woese, R. W. Castenholz, and M. T. Madigan. 1991. A thermophilic green sulfur bacterium from New Zealand hot springs, Chlorobium tepidum sp. nov. Arch. Microbiol. 156:81-90.
43. Schmidt, K. 1980. A comparative study on the composition of chlorosomes (chlorobium vesicles) and cytoplasmic membranes from Chloroflexus aurantiacus strain OK-70-fl and Chlorobium limicola f. thiosulfatophilum strain 6230. Arch. Microbiol. 124:23-31.
44. Psencík, J., T. J. Schaafsma, G. F. W. Searle, and J. Hala. 1997. Fluorescence detected magnetic resonance of monomers and aggregates of bacteriochlorophylls of green sulfur bacteria Chlorobium sp. Photosynth. Res. 52:83-92.
45. Causgrove, T. P., D. C. Brune, J. Wang, B. P. Wittmershaus, and R. E. Blankenship. 1990. Energy transfer kinetics in whole cells and isolated chlorosomes of green photosynthetic bacteria. Photosynth. Res. 26:39-48.
46. Blankenship, R. E., J. Wang, T. P. Causgrove, and D. C. Brune. 1990. Efficiency and kinetics of energy transfer in chlorosome antennas from green photosynthetic bacteria. In Current Research in Photosynthesis. M. Baltscheffsky, editor. Kluwer Academic Publishers, Dordrecht, The Netherlands. 17-24.
47. Brune, D. C., R. E. Blankenship, and G. R. Seely. 1988. Fluorescence quantum yields and lifetimes for bacteriochlorophyll c. Photochem. Photobiol. 47:759-763.
48. Frank, H. A., and R. J. Codgell. 1996. Carotenoids in photosynthesis. Photochem. Photobiol. 63:257-264.
49. Peterman, E. J. G., F. M. Dukker, R. van Grondelle, and H. van Amerongen. 1995. Chlorophyll a and carotenoid triplet states in light-harvesting complex II of higher plants. Biophys. J. 69:2670-2678.
50. Schödel, R., K.-D. Irrgang, J. Voigt, and G. Renger. 1998. Rate of carotenoid triplet formation in solubilized light-harvesting complex II (LHCII) from spinach. Biophys. J. 75:3143-3153.
51. Siefermann-Harms, D., and A. Angerhofer. 1998. Evidence of an O2-barrier in the light-harvesting chlorophyll-a/b-protein complex LHC II. Photosynth. Res. 55:83-94.
52. Olson, J. M. 1980. Chlorophyll organization in green photosynthetic bacteria. Biochim. Biophys. Acta. 594:33-51.
53. Guerrero, R., E. Montesinos, C. Pedrós-Alió, I. Esteve, J. Mas, H. van Gemerden, P. A. G. Hofman, and J. F. Bakker. 1985. Phototrophic sulfur bacteria in two Spanish lakes: vertical distribution and limiting factors. Limnol. Oceanogr. 30:919-931.
54. van Gemerden, H., and J. Mas. 1995. Ecology of phototrophic sulfur bacteria. In Anoxygenic Photosynthetic Bacteria. R. E. Blankenship, M. T. Madigan, and C. E. Bauer, editors. Kluwer Academic Publishers, Dordrecht, The Netherlands. 49-85.
55. Linschitz, H., and K. Sarkanen. 1958. The absorption spectra and decay kinetics of the metastable states of chlorophyll a and b. J. Am. Chem. Soc. 80:4826-4832.
56. Fujimori, E., and R. Livingston. 1957. Interactions of chlorophyll in its triplet state with oxygen, carotene, etc. Nature. 180:1036-1038.
57. Eisen, J. A., K. E. Nelson, I. T. Paulsen, J. F. Heidelberg, M. Wu, R. J. Dodson, R. Deboy, M. L. Gwinn, W. C. Nelson, D. H. Haft, E. K. Hickey, J. D. Peterson, et al. 2002. The complete genome sequence of Chlorobium tepidum TLS, a photosynthetic, anaerobic, green-sulfur bacterium. Proc. Nat. Aca. Sci. 99:9509-9514.
58. Karapetyan, N. V., T. Swarthoff, C. P. Rijgersberg, and J. Amesz. 1980. Fluorescence emission spectra of cells and subcellular preparations of a green photosynthetic bacterium. Effects of dithionite on the intensity of the emission bands. Biochim. Biophys. Acta. 593:254-260.
59. Blankenship, R. E., P. Cheng, T. P. Causgrove, D. C. Brune, S. H.-H. Wang, J.-U. Choh, and J. Wang. 1993. Redox regulation of energy transfer efficiency in antennas of green photosynthetic bacteria. Photochem. Photobiol. 57:103-107.
60. van Noort, P. I., Y. Zhu, R. LoBrutto, and R. E. Blankenship. 1997. Redox effects on the excited-state lifetime in chlorosomes and bacteriochlorophyll c oligomers. Biophys. J. 72:316-325.
61. Marston, G., T. G. Truscott, and R. P. Wayne. 1995. Phosphorescence of β-carotene. J. Chem. Soc. Faraday Trans. 91:4059-4061.
62. Takaichi, S. 2000. Characterization of carotenes in a combination of a C18 HPLC column with isocratic elution and absorption spectra with a photodiode-array detector. Photosynth. Res. 65:93-99.
63. Frank, H. A., and R. J. Cogdell. 1993. Photochemistry and function of carotenoids in photosyntheis. In Carotenoids in Photosynthesis. A. Young and G. Britton, editors. Chapman and Hall. London, UK. 252-326.
64. Farhoosh, R., V. Chynwat, R. Gebhard, J. Lugtenburg, and H. A. Frank. 1994. Triplet energy transfer between bacteriochlorophyll and carotenoids in B850 light-harvesting complexes of Rhodobacter sphaeroides R-26.1. Photosynth. Res. 42:157-166.
65. Hauska, G., T. Schoedl, H. Remigy, and G. Tsiotis. 2001. The reaction center of green sulfur bacteria. Biochim. Biophys. Acta. 1507:260-277.
66. Li, Y., W. Zhou, R. E. Blankenship, and J. P. Allen. 1997. Crystal structure of the bacteriochlorophyll a protein from Chlorobium tepidum. J. Mol. Biol. 271:456-471.
67. Fenna, R. E., and B. W. Matthews. 1975. Chlorophyll arrangement in a bacteriochlorophyll protein from Chlorobium limicola. Nature. 258:573-577.
68. Avakian, P., and R. E. Merrifield. 1968. Triplet excitons in anthracene crystals: a review. Mol. Cryst. 5:37-77.
69. You, Z.-Q., C.-P. Hsu, and G. R. Fleming. 2006. Triplet-triplet energy-transfer coupling: theory and calculation. J. Chem. Phys. 124:044506.
70. 1 NMR spectra and structural analysis of intact bacteriochlorophyll c dimer in solution. J. Phys. Chem. B. 103:3742-3753.
71. Takiff, L., and S. G. Boxer. 1988. Phosphorescence spectra of bacteriochlorophylls. J. Am. Chem. Soc. 110:4425-4426.
72. Krasnovsky Jr., A. A., J. Lopez, P. Cheng, P. A. Liddell, R. E. Blankenship, T. A. Moore, and D. Gust. 1994. Generation and quenching of singlet molecular oxygen by aggregated bacteriochlorophyll d in model systems and chlorosomes. Photosynth. Res. 40:191-198.
73. 1. Proc. R. Soc. Lond. A. 319:319-329.
74. Tollin, G., F. Castelli, G. Cheddar, and F. Rizzuto. 1979. Laser photolysis studies of quinone reduction by chlorophyll a in alcohol solution. Photochem. Photobiol. 29:147-152.
75. Natarajan, L. V., and R. E. Blankenship. 1983. Free energy dependence of the quenching of chlorophyll a fluorescence by substituted quinones. Photochem. Photobiol. 37:329-336.
76. Metzger, S. U., W. A. Cramer, and J. Whitmarsh. 1997. Critical analysis of the extinction coefficient of chloroplast cytochrome f. Biochim. Biophys. Acta. 1319:233-241.
77. Balaban, T. S., H. Tamiaki, and A. R. Holzwarth. 2005. Chlorins programmed for self-assembly. In Supramolecular Dye Chemistry. F. Würthner, editor. Springer, Berlin, Germany. 1-38.