Light harvesting and state transitions in cyanobacteria

Botanica Acta

Volumn 111, Issue 6, 1998, Pages 430-443

  Van Thor, J J ^a,c   Mullineaux, C W ^b   Matthijs, H C P ^c   Hellingwerf, K J ^a  

^a E C Slater Inst BioCentrum A   (Netherlands)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c ECS I ARISE/MB   (Netherlands)

Author keywords

Energy transfer; Fluorescence spectroscopy; Light harvesting; Mutant; Photosystem I; Photosystem II; Phycobilisome; State transitions

Indexed keywords

BACTERIA (MICROORGANISMS); CYANOBACTERIA; PROKARYOTA;

EID: 0032434707     PISSN: 09328629     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1438-8677.1998.tb00731.x     Document Type: Review

References (101)

1. Allen, J. F., Bennet, J., Steinback, K. E., and Arntzen, C.J. - Chloroplast protein phosphorylation couples plastoquinone redox state to distribution of excitation energy between photosystems. Nature 291 (1981), 25-29.
2. Allen, J. F., Sanders, C. E., and Holmes, N. G. - Correlation of membrane protein phosphorylation with excitation energy distribution in the cyanobacterium Synechococcus 6301. FEBS Lett. 193 (1985), 271-275.
3. Allen, J. F., Mullineaux. C. W., Sanders, C. E., and Melis, A. - State transitions, Photosystem stoichiometry adjustment and non-photochemical in cyanobacterial quenching in cyanobacterial cells acclimated to light absorbed by Photosystem I or Photosystem II. Photosynth. Res. 22 (1989), 157-166.
4. Allen, J. F. - Protein phosphorylation in regulation of photosynthesis. Biochim. Biophys. Acta 1098 (1992), 275 - 335.
5. Ashby, M. K. and Mullineaux, C. W. - The role of ApcD and ApcF in energy transfer from phycobilisomes to PSI and PSII in a cyanobacterium. Submitted (1998).
6. Ashby, M. K., Emlyn-Jones, D., and Mullineaux, C. W. - In preparation (1998).
7. Bald, D., Kruip, J., and Rogner, M. - Supramolecular architecture of cyanobacterial thylakoid membranes: How is the phycobilisome connected with the photosystems? Photosynth. Res. 49 (1996), 103-118.
8. Beddard, G. S., Porter, G., Tredwell, C. J., and Barber, J. - Fluorescence lifetimes in the photosynthetic unit. Nature 258 (1975), 166-168.
9. Biggins, J., Campbell, C. L., and Bruce, D. - Mechanism of the light state transition in photosynthesis. II. Analysis of phosphorylated polypeptides in the red alga, Porphyridium cruentum. Biochim. Biophys. Acta 767 (1984), 138-144.
10. Bittersmann, E. and Vermaas, W. - Fluorescence lifetime studies of cyanobacterial Photosystem II mutants. Biochim. Biophys. Acta 1098 (1991), 105-116.
11. Boekema, E. J., Hankamer, B., Bald, D., Kruip, J., Nield, J., Boonstra, A. F., Barber, J., and Rogner, M. - Supramolecular structure of the Photosystem II complex from green plants and cyanobacteria. Proc. Natl. Acad. Sci. USA 92 (1995), 175-179.
12. Bogorad, L. - Phycobiliproteins and complementary chromatic adaptation. Ann. Rev. Plant. Physiol. 26 (1975), 369-401.
13. Bonavenura, C. and Meyers, J. - Fluorescence and oxygen evolution from Chlorella pyrenoidosa. Biochim. Biophys. Acta 189 (1969), 366-383.
14. Bruce, D., Brimble, S., and Bryant, D. A. - State transitions in a phycobilisome-less mutant of the cyanobacterium Synechococcus sp. PCC 7002. Biochim. Biophys. Acta 974 (1989), 66-73.
15. Bruce, D. and Salehian, O. - Laser-induced optoacoustic calorimetry of cyanobacteria. The efficiency of primary photosynthetic processes in state 1 and state 2. Biochim. Biophys. Acta 1100 (1992), 242-250.
16. Bryant, D. A. - In: S. E. jr. Stevens and D. A. Bryant, eds., Light-Energy Transduction in Photosynthesis: Higher plants and bacterial models, pp 62-90. American Society of Plant Physiologists. Rockville, 1988.
17. Bryant, D.A. - The photosystems, structure, function and molecular biology, in: J. Barber, ed., pp. 501-549, Elseviers Science publishers B.V.. Amsterdam, 1992.
18. Butler, W. L. - A far-red absorbing form of chlorophyll, in vivo. Arch. Biochem. Biophys. 93 (1961), 413-422.
19. Chitnis, V. P. and Chitnis, P. R. - PsaL subunit is required for the formation of photosystem I trimers in the cyanobacterium Synechocystis sp. PCC 6803. FEBS Lett. 336 (1993), 330-334.
20. Clement-Metral, J. D., Gantt, E., and Redlinger, T. - A photosystem II-phycobilisome preparation from the red alga, Porphyridium cruentum: oxygen evolution, ultrastructure, and polypeptide resolution. Arch. Biochem. Biophys. 238 (1985), 10-17.
21. Delphin, E., Duval, J., Etienne, A., and Kirilovsky, D. - State transitions of ΔpH-dependent quenching of Photosystem II fluorescence in red algae. Biochemistry 35 (1996), 9435-9445.
22. Delrieu, M. J. - Inhibition by ammonium chloride of the oxygen yield of photosynthesis. Biochim. Biophys. Acta 440 (1976), 176-188.
23. DiMagno, L., Chan, C., Jia, Y., Lang, M. L., Newman, J. R., Mets, L., Fleming, G. R., and Haselkorn, R. - Energy transfer and trapping in photosystem I reaction centers from cyanobacteria. Proc. Natl. Acad. Sci. USA 92 (1995), 2715-2719.
24. Förster, Th. W. - Comparative effects of radiation. In: M. Burton, J. S. Kirby-Smith, and J. L. Magee, eds., pp. 300-341. Wiley. New York and London, 1960.
25. Fork, D. C. and Satoh, K. - State I-State II transitions in the thermophilic blue-green alga (cyanobacterium) Synechococcus lividus. Photochem. Photobiol. 37 (1983), 421-427.
26. Gillbro, T., Sandstrom, A., Sundstrom, V., and Holzwarth, A. R. - Polarized absorption picosecond kinetics as a probe of energy transfer in phycobilisomes of Synechococcus 6301. FEBS Lett. 162 (1983), 64-68.
27. Gillbro, T., Sharkov, A. V., Kryukov, I. V., Khoroshilov, E. V., Kryukov, P. G., Fischer, R., and Scheer, H. - Förster energy transfer between neighbouring chromophores in C-phycocyanin trimers. Biochim. Biophys. Acta 1140 (1993), 321-326.
28. Gindt, Y. M., Zhou, J., Bryant, D. A., and Sauer, K. - Core mutations of Synechococcus sp. PCC 7002 phycobilisomes: a spectroscopic study. J. Photochem. Photobiol. 15 (1992), 75-89.
29. Glazer, A. - Disc-to-disc transfer as the rate-limiting step for energy flow in phycobilisomes. Science 227 (1985), 419-423.
30. Glazer, A. N. - Light guides. Directional energy transfer in a photosynthetic antenna. J. Biol. Chem. 264 (1989), 1-4.
31. Goedheer, J. C. - Fluorescence bands and chlorophyll a forms. Biochim. Biophys. Acta 88 (1964), 304-317.
32. Grabowski, J. and Gantt, E. - Photophysical properties of phycobiliproteins from phycobilisomes: Fluorescence lifetimes, quantum yields, and polarization spectra. Photochem. Photobiol. 28 (1978), 39-45.
33. van Grondelle, R. - Exciton energy transfer, trapping and annihilation in photosynthetic systems. Biochim. Biophys. Acta 811 (1984), 147-195.
34. van Grondelle, R., Dekker, J. P., Gillbro, T., and Sundstrom, V. - Energy transfer and trapping in photosynthesis. Biochim. Biophys. Acta 1187 (1994), 1-65.
35. Harrison, M. A. - Molecular mechanisms of adaptation in the photosynthetic aparatus. Ph.D. thesis, University of Leeds, 1990.
36. Harrison, M. A., Tsinoremas, N. F., and Allen, J. F. - Cyanobacterial thylakoid membrane proteins are reversibly phosphorylated under plastoquinone-reducing conditions in vitro. FEBS Lett. 282 (1991), 295-299.
37. Holzwarth, A. R., Schatz, G., Brock, H., and Bittersmann, E. - Energy transfer and charge separation kinetics in photosystem I. Part 1: Picosecond transient absorption and fluorescence study of cyanobacterial photosystem I particles. Biophys. J. 64 (1993), 1813-1826.
38. Homer-Dixon, J. A., Gantt, E., and Bruce, D. - Pigment orientation changes accompanying the light state transition in Synechococcus sp. PCC 6301. Photosynth. Res 40 (1994), 35-44.
39. Horton, P., Allen, J. F., Black, M. T., and Bennett, J. - Regulation of phosphorylation of chloroplast membrane polypeptides by the redox state of plastoquinone. FEBS Lett. 125 (1981), 193-196.
40. Kaneko, T., Sato, S., Kotani, H., Tanaka, A., Asamizu, E., Nakamura, Y., Miyajima, N., Hirosawa, M., Sugiura, M., Sasamoto, S., Kimura, T., Hosouchi, T., Matsuno, A., Muraki, A., Nakazaki, N., Naruo, K., Okumura, S., Shimpo, S., Takeuchi, C., Wada, T., Watanabe, A., Yamada, M., Yasuda, M.. and Tabata, S. - Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. II. - Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res. 3 (1996), 185-209.
41. Karapetyan, N. V., Dorra, D., Schweitzer, G., Bezsmertnaya, I. N., and Holzwarth, A. R. - Fluorescence spectroscopy of the longwave chlorophylls in trimeric and monomeric photosystem I core complexes from the cyanobacterium Spirulina platensis. Biochem. 36 (1997), 13830-13837.
42. Koenig, F. and Schmidt, M. - Gloebacter violaceus - Investigation of an unusual photosynthetic apparatus. Absence of the long wave-length emission of Photosystem I in 77 K fluorescence spectra. Physiol. Planta 94 (1995), 621-628.
43. Krauss, N., Hinrichs, W., Witt, I., Fromme, P., Pritzkow, W., Dauter, Z., Betzel, C., Wilson, K. S., Witt, H. T., and Saenger, W.-3-Dimensional structure of system-I of photosynthesis at 6 Angstrom resolution. Nature 361 (1993), 326-331.
44. Kruip, J., Bald, D., Boekema, E., and Rogner, M. - Evidence for the existence of trimeric and monomeric photosystem I complexes in the thylakoid membranes from cyanobacteria. Photosynth. Res. 40 (1994), 279-286.
45. Lavergne, J. and Briantais, J. M. - Oxygenic Photosynthesis: The Light Reactions, in: R. Ort and C. F. Yocum, eds., pp. 265-287. Kluwer Academic Publishers, 1996.
46. Ley, A. C. and Butler, W. L. - Energy distribution in the photochemical apparatus of Porphyridium cruentum in state I and state II. Biochim Biophys Acta 592 (1980), 349-363.
47. MacColl, R., Csatorday, K., Berns, D. S., and Traeger, E. - Chromophore interactions in allophycocyanin. Biochemistry 19 (1980), 2817-2820.
48. MacLachlan, D. J., Nugent, J. H. A., Warden, J. T., and Evans, M. C. W. - Investigation of the ammonium chloride and ammonium acetate inhibition of oxygen evolution by photosystem II. Biochim Biophys Acta 1188 (1994), 325-334.
49. Mann, N. H. and Newman, J. - Phosphorylation of β-phycocyanin and effect on light harvesting in Synechocystis sp. PCC 6803. Proceedings of the Ixth International Symposium on Photosynthetic Prokaryotes, Vienna, Austria September 6-13, 1997.
50. Manodori, A. and Melis, A. - Cyanobacterial acclimation to Photosystem I or Photosystem II light. Plant Physiol 82 (1986), 185-189.
51. Manodori, A. and Melis, A. - Phycobilisome-photosystem II association in Synechococcus 6301 (Cyanophyceae). FEBS Lett. 181 (1985), 79-82.
52. Meunier, P. C., Colon-Lopez, M. S., and Sherman, L. A. - Temporal changes in state transitions and photosystem organization in the unicellular, diazotrophic cyanobacterium Cyanothece sp. ATCC 51142. Plant Physiol. in press, 1998.
53. Mi, H. Endo, T., Schreiber, U., Ogawa, T., and Asada, K. - NAD(P)H dehydrogenase-dependent cyclic electron flow around photosystem I in the cyanobacterium Synechocystis PCC 6803: a study of dark-starved cells and speroplasts. Plant Cell Physiol 33 (1992), 1233-1237.
54. Montoya, C., Yruela, I., and Picorel, R. - Pigment stoichiometry of a newly isolated D1-D2-Cyt b559 complex from the higher plant Beta vulgaris L. FEBS Lett. 283 (1991), 255-258.
55. Mörschel, E. and Mühlethaler, K. - On the linkage of exoplasmatic freeze-fracture particles to phycobilisomes. Planta 1983 (1983), 451-457.
56. Mullineaux, C. W. and Allen, J. F. - The state 2 transition in the cyanobacterium Synechococcus 6301 can be driven by respiratory electron flow into the plastoquinone pool. FEBS Lett. 205 (1986), 155-160.
57. Mullineaux, C. W. and Allen, J. F. - State 1-State 2 transitions in the cyanobacterium Synechococcus 6301 are controlled by the redox state of electron carriers between Photosystems I and II. Photosynth. Res. 23 (1990), 297-311.
58. Mullineaux, C. W., Bittersmann, E., Allen, J. F., and Holzwarth, A. R. -Picosecond time-resolved fluorescence emission spectra indicate decreased energy transfer from the phycobilisome to Photosystem II in light-state 2 in the cyanobacterium Synechococcus 6301. Biochim. Biophys. Acta 1015 (1990), 231-242.
59. Mullineaux, C. W. and Holzwarth, A. R. - Kinetics of excitation energy transfer in the Cyanobacterial phycobilisome-Photosystem II complex . Biochim. Biophys. Acta 1098 (1991), 68-78.
60. Mullineaux, C. W., Griebenow, S., and Braslavsky, S. E. - Photosynthetic energy storage in Cyanobacterial cells adapted to light-states 1 and 2. A laser-induced optoacoustic study. Biochim. Biophys. Acta 1060 (1991), 315-318.
61. Mullineaux, C. W. - Excitation energy transfer from phycobilisomes to Photosystem I in a cyanobacterium. Biochim. Biophys. Acta 1100 (1992), 285-292.
62. Mullineaux, C. W. - Inhibition by phosphate of light-state transitions in cyanobacterial cells. Photosynth. Res. 38 (1993), 135-140.
63. Mullineaux, C. W. - Excitation energy transfer from phycobilisomes to Photosystem 1 in a cyanobacterial mutant lacking Photosystem II. Biochim. Biophys. Acta 1184 (1994), 71-77.
64. Mullineaux, C. W., Tobin, M. J., and Jones, G. R. - Mobility of photosynthetic complexes in thylakoid membranes. Nature 390 (1997), 421-424.
65. Mullineaux, C. W. and Wilde, A. - unpublished results, (1998).
66. Mullineaux, C. W. and Holzwarth, A. R. - unpublished results, (1998).
67. Murata, N. - Control of excitation transfer in photosynthesis. I. Light-induced change of chlorophyll a fluorescence in Porphyridium cruentum. Biochim. Biophys. Acta 172 (1969), 242-251.
68. Nilsson, F., Andersson, B., and Jansson, C. - Photosystem II characteristics of a constructed Synechocystis 6803 mutant lacking synthesis of the D1 polypeptide. Plant Mol. Biol. 14 (1990), 1051 - 1054.
69. Nilsson, F., Simpson, D. J., Jansson, C., and Andersson, B. - Ultrastructural and biochemical characterization of a Synechocystis 6803 mutant with inactivated psbA genes. Arch. Biochem. Biophys. 295 (1992), 340-347.
70. Ogawa, T. - A gene homologous to the subunit-2 gene of NADH dehydrogenase is essential to inorganic carbon transport of Synechocystis PCC6803. Proc. Natl. Acad. Sci. USA 88 (1991), 4275-4279.
71. Olive, J., M'Bina, I., Vernotte, C., Astier, C., and Wollman, F. A. -Randomization of the EF particle in thylakoid membranes of Synechocystis 6714 upon transition from state I to state II. FEBS Lett. 208 (1986), 308-312.
72. 559 in photosystem II. EMBOJ. 7 (1988), 325-332.
73. Peterson, R. B., Dolan, E., Calvert, H. E., and Ke, B. - Energy transfer from phycobiliproteins to Photosystem I in vegetative cells and heterocysts of Anabaena variabilis. Biochim Biophys Acta 634 (1981), 237-248.
74. Raps, S., Kycia, J. H., Ledbetter, M. V., and Siegelman, H. W. - Light intensity adaptation and phycobilisome composition of Microcystis aeruginosa. Plant Physiol 79 (1985), 983-987.
75. Sanders, C. E. and Allen, J. F. - Progress in Photosynthesis Research, in: J. Biggins, ed., Vol II, pp. 761-764. Martinus Nijhoff. Dordrecht, 1987.
76. Satoh, K. - The oxygen evolving system in photosynthesis, in: Y. Inoue, A. R. Crofts, Govindjee, N. Murata, G. Renger, and K. Satoh, eds., pp. 27-38, 1983.
77. Sauer, K. and Scheer, H. - Exciton transfer in C-phycocyanin. Förster transfer rate and exciton calculations based on the new crystal structure data for C-phycocyanin from Agmenellum quadruplicatum and Mastigoclaudus laminosus. Biochim. Biophys. Acta 936 (1988), 157-170.
78. Schatz, G. H. Brock, H., and Holzwarth, A. R. - Picosecond kinetics of fluorescence and absorbance changes in photosystem II particles excited at low photon density. Proc. Natl. Acad. Sci. USA 84 (1987), 8414-8418.
79. Schiller, H., Hühn, M., and Dau, H. - On the long-wavelength spectral forms of chlorophyll a in photosystem I: Spectroscopic and immunological investigations of a greening mutant of the green alga Scenedesmus obliquus. Photosynth. Res. 55 (1998), 95-107.
80. Schluchter, W. M., Shen, G., Zhao, J., and Bryant, D. A. - Characterization of psal and psaL mutants of Synechococcus sp. Strain PCC 7002: A new model for state transitions in cyanobacteria. Photochem. Photobiol 64 (1996), 53-66.
81. Schreiber, U., Rijgersberg, C. P., and Amesz, J. - Temperature-dependent reversible changes in phycobilisome-thyalkoid membrane attachment in Anacystis nidulans. FEBS Lett. 104 (1979), 327-331.
82. Schreiber, U. Endo, T., Mi, H., and Asada, K. - Quenching analysis of chlorophyll fluorescence by the saturation pulse method: particular aspects relating to the study of eukaryotic algae and cyanobacteria. Plant Cell Physiol. 36 (1995), 873-882.
83. Schubert, W. D., Klukas, O., Krauss, N., Saenger, W., Fromme, P., and Witt, H. T. - Photosystem I of Synechococcus elongatus at 4 Å resolution: comprehensive structure analysis. J. Mol. Biol. 272 (1997), 741-769.
84. Searle, G. F. W., Barber, J., Porter, G., and Tredwell, C. J. - Picosecond time-resolved energy transfer in Porphyridium cruentum. Part II. In the isolated light harvesting complex (phycobilisomes). Biochim. Biophys. Acta 501 (1987), 246-256.
85. Sharkov, A. V., Kryukov, I. V., Khoroshilov, E. V., Kruykov, P. G., Fischer, R., Scheer, H., and Gillbro, T. - Femtosecond energy transfer between chromophores in allophycocyanin trimers. Chem. Phys. Lett. 1991 (1992), 633-638.
86. Shen, G., Boussiba, S., and Vermaas, W. F. J. - Synechocystis sp. PCC 6803 strains lacking Photosystem I and phycobilisome function. The Plant Cell 5 (1993), 1853-1863.
87. Shen, G. and Bryant, D. A. - Characterization of a Synechococcus sp. strain PCC 7002 mutant lacking Photosystem I. Protein assembly and energy distribution in the absence of the photosystem I reaction center core complex. Photosynth. Res. 44 (1995), 41-53.
88. Sidler, W. A. - Phycobilisome and Phycobiliprotein Structure, in: D. A. Bryant, ed., The Molecular Biology of Cyanobacteria, pp. 139-216, 1994.
89. Su, X., Goodman Fraenkel, P., and Bogorad, L. - Excitation Energy Transfer from Phycocyanin to Chlorophyll in an apcA-defective Mutant of Synechocystis sp. PCC 6803. J. Biol. Chem. 267 (1992), 22944-22950.
90. Suter, G. W., Mazzola, P., Wendler, J., and Holzwarth, A. R. -Fluorescence decay kinetics in phycobilisomes isolated from the blue-green alga Synechococcus 6301. Biochim. Biophys. Acta 766 (1984), 269-276.
91. Thor, van, J. J. - unpublished results (1997).
92. Trinkunas, G. and Holzwarth, A. R. - Kinetic modeling of exciton migration in photosynthetic systems. 3. Application of genetic algorithms to simulations of excitation dynamics in three-dimensional photosystem I core antenna/reaction center complexes. Biophys. J. 66 (1994), 415-429.
93. Tyagi, V. V. S., Ray, T. B., Mayne, B. C., and Peters, G. A. - The Azolla-Anabaena azollae relationship. Plant Physiol 68 (1981), 1479-1484.
94. Van Mieghem, F. J. E., Searle, G. F. W., Rutherford, A. W., and Schaafsma, T. J. - The influence of the double reduction of Qa on the fluorescence decay kinetics of photosystem II. Biochim. Biophys Acta 1100 (1992), 198-206.
95. Vermaas, W. F. J., Charite, J., and Eggers, B. - Current Research in Photosynthesis. M. Baltscheffsky, ed., Vol. 1. pp. 231-238, Kluwer Academic publishers. Dordrecht, 1990.
96. Vernotte, C., Astier, C., and Olive, J. - Changes in the photosynthetic apparatus in the cyanobacterium Synechocystis sp. PCC 6714 following light-to-dark and dark-to-light transitions. Photosynth. Res. 26 (1990), 203-212.
97. Wang, R. T. and Meyers, J. - On the state 1-state 2 phenomenon in photosynthesis. Biochim. Biophys. Acta 347 (1973), 134-140.
98. Wittmershaus, B. P., Woolf, V. M., and Vermaas, W. F. J. - Temperature dependence and polarization of fluorescence from photosystem 1 in the cyanobacterium Synechocystis sp. PCC 6803. Photosynth Res 31 (1992), 75-87.
99. Woolf, V. M., Wittmershaus, B. P., Vermaas, W. F. J., and Tran, T. D. -Resolution of low-energy chlorophylls in photosystem I of Synechocystis sp. PCC 6803 at 77 and 295 K through fluorescence excitation anisotropy. Photosynth. Res. 40 (1994), 21-34.
100. Zhang, J., Zhao, J., Jiang, L., Zheng, X., Zhao, F., and Wang, H. - Studies on the energy transfer among the rod-core complex from phycobilisome of Anabaena variabilis by time resolved fluorescence emission and anisotropy spectra. Biochim. Biophys. Acta 1320 (1997), 285-296.
101. Zhao, J., Zhou, J., and Bryant, D. A. - Energy transfer processes in phycobilisomes as deduced from analyses of mutants of Synechococcus sp. PCC 7002. In: N. Murata, ed., Research in photosynthesis, Vol. 1, pp. 25-32. Kluwer academic publishers. Dordrecht, 1992.