Skip to main content
Biophysical Journal logoLink to Biophysical Journal
. 2001 May;80(5):2409–2421. doi: 10.1016/S0006-3495(01)76210-8

Singlet-singlet annihilation kinetics in aggregates and trimers of LHCII.

V Barzda 1, V Gulbinas 1, R Kananavicius 1, V Cervinskas 1, H van Amerongen 1, R van Grondelle 1, L Valkunas 1
PMCID: PMC1301429  PMID: 11325740

Abstract

Singlet-singlet annihilation experiments have been performed on trimeric and aggregated light-harvesting complex II (LHCII) using picosecond spectroscopy to study spatial equilibration times in LHCII preparations, complementing the large amount of data on spectral equilibration available in literature. The annihilation kinetics for trimers can well be described by a statistical approach, and an annihilation rate of (24 ps)(-1) is obtained. In contrast, the annihilation kinetics for aggregates can well be described by a kinetic approach over many hundreds of picoseconds, and it is shown that there is no clear distinction between inter- and intratrimer transfer of excitation energy. With this approach, an annihilation rate of (16 ps)(-1) is obtained after normalization of the annihilation rate per trimer. It is shown that the spatial equilibration in trimeric LHCII between chlorophyll a molecules occurs on a time scale that is an order of magnitude longer than in Photosystem I-core, after correcting for the different number of chlorophyll a molecules in both systems. The slow transfer in LHCII is possibly an important factor in determining excitation trapping in Photosystem II, because it contributes significantly to the overall trapping time.

Full Text

The Full Text of this article is available as a PDF (152.3 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Barzda V., Mustárdy L., Garab G. Size dependency of circular dichroism in macroaggregates of photosynthetic pigment-protein complexes. Biochemistry. 1994 Sep 6;33(35):10837–10841. doi: 10.1021/bi00201a034. [DOI] [PubMed] [Google Scholar]
  2. Boekema E. J., Hankamer B., Bald D., Kruip J., Nield J., Boonstra A. F., Barber J., Rögner M. Supramolecular structure of the photosystem II complex from green plants and cyanobacteria. Proc Natl Acad Sci U S A. 1995 Jan 3;92(1):175–179. doi: 10.1073/pnas.92.1.175. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Boekema E. J., Van Roon H., Van Breemen J. F., Dekker J. P. Supramolecular organization of photosystem II and its light-harvesting antenna in partially solubilized photosystem II membranes. Eur J Biochem. 1999 Dec;266(2):444–452. doi: 10.1046/j.1432-1327.1999.00876.x. [DOI] [PubMed] [Google Scholar]
  4. Boekema E. J., van Breemen J. F., van Roon H., Dekker J. P. Arrangement of photosystem II supercomplexes in crystalline macrodomains within the thylakoid membrane of green plant chloroplasts. J Mol Biol. 2000 Sep 1;301(5):1123–1133. doi: 10.1006/jmbi.2000.4037. [DOI] [PubMed] [Google Scholar]
  5. Boekema E. J., van Roon H., Calkoen F., Bassi R., Dekker J. P. Multiple types of association of photosystem II and its light-harvesting antenna in partially solubilized photosystem II membranes. Biochemistry. 1999 Feb 23;38(8):2233–2239. doi: 10.1021/bi9827161. [DOI] [PubMed] [Google Scholar]
  6. Boekema E. J., van Roon H., Dekker J. P. Specific association of photosystem II and light-harvesting complex II in partially solubilized photosystem II membranes. FEBS Lett. 1998 Mar 6;424(1-2):95–99. doi: 10.1016/s0014-5793(98)00147-1. [DOI] [PubMed] [Google Scholar]
  7. Breton J., Geacintov N. E., Swenberg C. E. Quenching of fluorescence by triplet excited states in chloroplasts. Biochim Biophys Acta. 1979 Dec 6;548(3):616–635. doi: 10.1016/0005-2728(79)90069-0. [DOI] [PubMed] [Google Scholar]
  8. Burke J. J., Ditto C. L., Arntzen C. J. Involvement of the light-harvesting complex in cation regulation of excitation energy distribution in chloroplasts. Arch Biochem Biophys. 1978 Apr 15;187(1):252–263. doi: 10.1016/0003-9861(78)90031-0. [DOI] [PubMed] [Google Scholar]
  9. Butler W. L., Magde D., Berens S. J. Fluorescence lifetimes in the bipartite model of the photosynthetic apparatus with alpha, beta heterogeneity in photosystem II. Proc Natl Acad Sci U S A. 1983 Dec;80(24):7510–7514. doi: 10.1073/pnas.80.24.7510. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Connelly J. P., Müller M. G., Bassi R., Croce R., Holzwarth A. R. Femtosecond transient absorption study of carotenoid to chlorophyll energy transfer in the light-harvesting complex II of photosystem II. Biochemistry. 1997 Jan 14;36(2):281–287. doi: 10.1021/bi962467l. [DOI] [PubMed] [Google Scholar]
  11. Dekker J. P., van Roon H., Boekem E. J. Heptameric association of light-harvesting complex II trimers in partially solubilized photosystem II membranes. FEBS Lett. 1999 Apr 23;449(2-3):211–214. doi: 10.1016/s0014-5793(99)00442-1. [DOI] [PubMed] [Google Scholar]
  12. Gradinaru C. C., Ozdemir S., Gülen D., van Stokkum I. H., 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 Dec;75(6):3064–3077. doi: 10.1016/S0006-3495(98)77747-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Horton P., Ruban A. V., Walters R. G. REGULATION OF LIGHT HARVESTING IN GREEN PLANTS. Annu Rev Plant Physiol Plant Mol Biol. 1996 Jun;47(NaN):655–684. doi: 10.1146/annurev.arplant.47.1.655. [DOI] [PubMed] [Google Scholar]
  14. Jansson S. The light-harvesting chlorophyll a/b-binding proteins. Biochim Biophys Acta. 1994 Feb 8;1184(1):1–19. doi: 10.1016/0005-2728(94)90148-1. [DOI] [PubMed] [Google Scholar]
  15. Jennings R. C., Bassi R., Garlaschi F. M., Dainese P., Zucchelli G. Distribution of the chlorophyll spectral forms in the chlorophyll-protein complexes of photosystem II antenna. Biochemistry. 1993 Apr 6;32(13):3203–3210. doi: 10.1021/bi00064a002. [DOI] [PubMed] [Google Scholar]
  16. Kleima F. J., Gradinaru C. C., Calkoen F., van Stokkum I. H., van Grondelle R., van Amerongen H. Energy transfer in LHCII monomers at 77K studied by sub-picosecond transient absorption spectroscopy. Biochemistry. 1997 Dec 9;36(49):15262–15268. doi: 10.1021/bi9716480. [DOI] [PubMed] [Google Scholar]
  17. Krauss N., Schubert W. D., Klukas O., Fromme P., Witt H. T., Saenger W. Photosystem I at 4 A resolution represents the first structural model of a joint photosynthetic reaction centre and core antenna system. Nat Struct Biol. 1996 Nov;3(11):965–973. doi: 10.1038/nsb1196-965. [DOI] [PubMed] [Google Scholar]
  18. Kudzmauskas S., Valkunas L., Borisov A. Y. A theory of excitation transfer in photosynthetic units. J Theor Biol. 1983 Nov 7;105(1):13–23. doi: 10.1016/0022-5193(83)90421-6. [DOI] [PubMed] [Google Scholar]
  19. Kühlbrandt W., Wang D. N., Fujiyoshi Y. Atomic model of plant light-harvesting complex by electron crystallography. Nature. 1994 Feb 17;367(6464):614–621. doi: 10.1038/367614a0. [DOI] [PubMed] [Google Scholar]
  20. Lavergne J., Trissl H. W. Theory of fluorescence induction in photosystem II: derivation of analytical expressions in a model including exciton-radical-pair equilibrium and restricted energy transfer between photosynthetic units. Biophys J. 1995 Jun;68(6):2474–2492. doi: 10.1016/S0006-3495(95)80429-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Nordlund T. M., Knox W. H. Lifetime of fluorescence from light-harvesting chlorophyll a/b proteins. Excitation intensity dependence. Biophys J. 1981 Oct;36(1):193–201. doi: 10.1016/S0006-3495(81)84723-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Paillotin G. Capture frequency of excitations and energy transfer between photosynthetic units in the photosystem II. J Theor Biol. 1976 May 7;58(1):219–235. doi: 10.1016/0022-5193(76)90149-1. [DOI] [PubMed] [Google Scholar]
  23. Paillotin G., Geacintov N. E., Breton J. A master equation theory of fluorescence induction, photochemical yield, and singlet-triplet exciton quenching in photosynthetic systems. Biophys J. 1983 Oct;44(1):65–77. doi: 10.1016/S0006-3495(83)84278-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Paillotin G., Swenberg C. E., Breton J., Geacintov N. E. Analysis of picosecond laser induced fluorescence phenomena in photosynthetic membranes utilizing a master equation approach. Biophys J. 1979 Mar;25(3):513–533. doi: 10.1016/S0006-3495(79)85320-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Pålsson L. O., Spangfort M. D., Gulbinas V., Gillbro T. Ultrafast chlorophyll b-chlorophyll a excitation energy transfer in the isolated light harvesting complex, LHC II, of green plants. Implications for the organisation of chlorophylls. FEBS Lett. 1994 Feb 14;339(1-2):134–138. doi: 10.1016/0014-5793(94)80400-1. [DOI] [PubMed] [Google Scholar]
  26. Roelofs T. A., Lee C. H., Holzwarth A. R. Global target analysis of picosecond chlorophyll fluorescence kinetics from pea chloroplasts: A new approach to the characterization of the primary processes in photosystem II alpha- and beta-units. Biophys J. 1992 May;61(5):1147–1163. doi: 10.1016/s0006-3495(92)81924-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Savikhin S., Xu W., Soukoulis V., Chitnis P. R., Struve W. S. Ultrafast primary processes in photosystem I of the cyanobacterium Synechocystis sp. PCC 6803. Biophys J. 1999 Jun;76(6):3278–3288. doi: 10.1016/S0006-3495(99)77480-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Savikhin S., van Amerongen H., Kwa S. L., van Grondelle R., Struve W. S. Low-temperature energy transfer in LHC-II trimers from the Chl a/b light-harvesting antenna of photosystem II. Biophys J. 1994 May;66(5):1597–1603. doi: 10.1016/S0006-3495(94)80951-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Schödel R., Hillmann F., Schrötter T., Voigt J., Irrgang K. D., Renger G. Kinetics of excited states of pigment clusters in solubilized light-harvesting complex II: photon density-dependent fluorescence yield and transmittance. Biophys J. 1996 Dec;71(6):3370–3380. doi: 10.1016/S0006-3495(96)79530-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Simidjiev I., Barzda V., Mustárdy L., Garab G. Isolation of lamellar aggregates of the light-harvesting chlorophyll a/b protein complex of photosystem II with long-range chiral order and structural flexibility. Anal Biochem. 1997 Aug 1;250(2):169–175. doi: 10.1006/abio.1997.2204. [DOI] [PubMed] [Google Scholar]
  31. Somsen O. J., Valkunas L., van Grondelle R. A perturbed two-level model for exciton trapping in small photosynthetic systems. Biophys J. 1996 Feb;70(2):669–683. doi: 10.1016/S0006-3495(96)79607-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Somsen O. J., van Mourik F., van Grondelle R., Valkunas L. Energy migration and trapping in a spectrally and spatially inhomogeneous light-harvesting antenna. Biophys J. 1994 May;66(5):1580–1596. doi: 10.1016/S0006-3495(94)80950-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Sonneveld A., Rademaker H., Duysens L. N. Chlorophyll a fluorescence as a monitor of nanosecond reduction of the photooxidized primary donor P-680 Of photosystem II. Biochim Biophys Acta. 1979 Dec 6;548(3):536–551. doi: 10.1016/0005-2728(79)90063-x. [DOI] [PubMed] [Google Scholar]
  34. Sonneveld A., Rademaker H., Duysens L. N. Transfer and trapping of excitation energy in photosystem II as studied by chlorophyll alpha 2 fluorescence quenching by dinitrobenzene and carotenoid triplet. The matrix model. Biochim Biophys Acta. 1980 Dec 3;593(2):272–289. doi: 10.1016/0005-2728(80)90065-1. [DOI] [PubMed] [Google Scholar]
  35. Valkunas L., Akesson E., Pullerits T., Sundström V. Energy migration in the light-harvesting antenna of the photosynthetic bacterium Rhodospirillum rubrum studied by time-resolved excitation annihilation at 77 K. Biophys J. 1996 May;70(5):2373–2379. doi: 10.1016/S0006-3495(96)79804-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Valkunas L., Trinkunas G., Liuolia V., van Grondelle R. Nonlinear annihilation of excitations in photosynthetic systems. Biophys J. 1995 Sep;69(3):1117–1129. doi: 10.1016/S0006-3495(95)79986-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Vasil'ev S., Irrgang K. D., Schrötter T., Bergmann A., Eichler H. J., Renger G. Quenching of chlorophyll a fluorescence in the aggregates of LHCII: steady state fluorescence and picosecond relaxation kinetics. Biochemistry. 1997 Jun 17;36(24):7503–7512. doi: 10.1021/bi9625253. [DOI] [PubMed] [Google Scholar]

Articles from Biophysical Journal are provided here courtesy of The Biophysical Society

RESOURCES