Skip to main content
Biophysical Journal logoLink to Biophysical Journal
. 2000 Aug;79(2):992–1007. doi: 10.1016/S0006-3495(00)76353-3

Decay kinetics and quantum yields of fluorescence in photosystem I from Synechococcus elongatus with P700 in the reduced and oxidized state: are the kinetics of excited state decay trap-limited or transfer-limited?

M Byrdin 1, I Rimke 1, E Schlodder 1, D Stehlik 1, T A Roelofs 1
PMCID: PMC1300995  PMID: 10920029

Abstract

Transfer and trapping of excitation energy in photosystem I (PS I) trimers isolated from Synechococcus elongatus have been studied by an approach combining fluorescence induction experiments with picosecond time-resolved fluorescence measurements, both at room temperature (RT) and at low temperature (5 K). Special attention was paid to the influence of the oxidation state of the primary electron donor P700. A fluorescence induction effect has been observed, showing a approximately 12% increase in fluorescence quantum yield upon P700 oxidation at RT, whereas at temperatures below 160 K oxidation of P700 leads to a decrease in fluorescence quantum yield ( approximately 50% at 5 K). The fluorescence quantum yield for open PS I (with P700 reduced) at 5 K is increased by approximately 20-fold and that for closed PS I (with P700 oxidized) is increased by approximately 10-fold, as compared to RT. Picosecond fluorescence decay kinetics at RT reveal a difference in lifetime of the main decay component: 34 +/- 1 ps for open PS I and 37 +/- 1 ps for closed PS I. At 5 K the fluorescence yield is mainly associated with long-lived components (lifetimes of 401 ps and 1.5 ns in closed PS I and of 377 ps, 1.3 ns, and 4.1 ns in samples containing approximately 50% open and 50% closed PS I). The spectra associated with energy transfer and the steady-state emission spectra suggest that the excitation energy is not completely thermally equilibrated over the core-antenna-RC complex before being trapped. Structure-based modeling indicates that the so-called red antenna pigments (A708 and A720, i.e., those with absorption maxima at 708 nm and 720 nm, respectively) play a decisive role in the observed fluorescence kinetics. The A720 are preferentially located at the periphery of the PS I core-antenna-RC complex; the A708 must essentially connect the A720 to the reaction center. The excited-state decay kinetics turn out to be neither purely trap limited nor purely transfer (to the trap) limited, but seem to be rather balanced.

Full Text

The Full Text of this article is available as a PDF (190.5 KB).

Selected References

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

  1. Colbow K. Energy transfer in photosynthesis. Biochim Biophys Acta. 1973 Sep 26;314(3):320–327. doi: 10.1016/0005-2728(73)90116-3. [DOI] [PubMed] [Google Scholar]
  2. Croce R., Zucchelli G., Garlaschi F. M., Bassi R., Jennings R. C. Excited state equilibration in the photosystem I-light-harvesting I complex: P700 is almost isoenergetic with its antenna. Biochemistry. 1996 Jul 2;35(26):8572–8579. doi: 10.1021/bi960214m. [DOI] [PubMed] [Google Scholar]
  3. Davis M. S., Forman A., Fajer J. Ligated chlorophyll cation radicals: Their function in photosystem II of plant photosynthesis. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4170–4174. doi: 10.1073/pnas.76.9.4170. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. DiMagno L., Chan C. K., Jia Y., Lang M. J., Newman J. R., Mets L., Fleming G. R., Haselkorn R. Energy transfer and trapping in photosystem I reaction centers from cyanobacteria. Proc Natl Acad Sci U S A. 1995 Mar 28;92(7):2715–2719. doi: 10.1073/pnas.92.7.2715. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Hastings G., Kleinherenbrink F. A., Lin S., Blankenship R. E. Time-resolved fluorescence and absorption spectroscopy of photosystem I. Biochemistry. 1994 Mar 22;33(11):3185–3192. doi: 10.1021/bi00177a007. [DOI] [PubMed] [Google Scholar]
  6. Hastings G., Kleinherenbrink F. A., Lin S., McHugh T. J., Blankenship R. E. Observation of the reduction and reoxidation of the primary electron acceptor in photosystem I. Biochemistry. 1994 Mar 22;33(11):3193–3200. doi: 10.1021/bi00177a008. [DOI] [PubMed] [Google Scholar]
  7. Hastings G., Reed L. J., Lin S., Blankenship R. E. Excited state dynamics in photosystem I: effects of detergent and excitation wavelength. Biophys J. 1995 Nov;69(5):2044–2055. doi: 10.1016/S0006-3495(95)80074-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Holzwarth A. R., Schatz G., Brock H., 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. 1993 Jun;64(6):1813–1826. doi: 10.1016/S0006-3495(93)81552-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Ikegami I. Fluorescence changes related in the primary photochemical reaction in the P-700-enriched particles isolated from spinach chloroplasts. Biochim Biophys Acta. 1976 Nov 9;449(2):245–258. doi: 10.1016/0005-2728(76)90137-7. [DOI] [PubMed] [Google Scholar]
  10. Jia Y., Jean J. M., Werst M. M., Chan C. K., Fleming G. R. Simulations of the temperature dependence of energy transfer in the PSI core antenna. Biophys J. 1992 Jul;63(1):259–273. doi: 10.1016/S0006-3495(92)81589-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Karapetyan N. V., Dorra D., Schweitzer G., Bezsmertnaya I. N., Holzwarth A. R. Fluorescence spectroscopy of the longwave chlorophylls in trimeric and monomeric photosystem I core complexes from the cyanobacterium Spirulina platensis. Biochemistry. 1997 Nov 11;36(45):13830–13837. doi: 10.1021/bi970386z. [DOI] [PubMed] [Google Scholar]
  12. Ke B. The rise time of photoreduction, difference spectrum, and oxidation-reduction potential of P430. Arch Biochem Biophys. 1972 Sep;152(1):70–77. doi: 10.1016/0003-9861(72)90194-4. [DOI] [PubMed] [Google Scholar]
  13. Klukas O., Schubert W. D., Jordan P., Krau N., Fromme P., Witt H. T., Saenger W. Localization of two phylloquinones, QK and QK', in an improved electron density map of photosystem I at 4-A resolution. J Biol Chem. 1999 Mar 12;274(11):7361–7367. doi: 10.1074/jbc.274.11.7361. [DOI] [PubMed] [Google Scholar]
  14. Laible P. D., Zipfel W., Owens T. G. Excited state dynamics in chlorophyll-based antennae: the role of transfer equilibrium. Biophys J. 1994 Mar;66(3 Pt 1):844–860. doi: 10.1016/s0006-3495(94)80861-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Owens T. G., Webb S. P., Mets L., Alberte R. S., Fleming G. R. Antenna size dependence of fluorescence decay in the core antenna of photosystem I: estimates of charge separation and energy transfer rates. Proc Natl Acad Sci U S A. 1987 Mar;84(6):1532–1536. doi: 10.1073/pnas.84.6.1532. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Pålsson L. O., Flemming C., Gobets B., van Grondelle R., Dekker J. P., Schlodder E. Energy transfer and charge separation in photosystem I: P700 oxidation upon selective excitation of the long-wavelength antenna chlorophylls of Synechococcus elongatus. Biophys J. 1998 May;74(5):2611–2622. doi: 10.1016/S0006-3495(98)77967-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Satoh K., Butler W. L. Low temperature spectral properties of subchloroplast fractions purified from spinach. Plant Physiol. 1978 Mar;61(3):373–379. doi: 10.1104/pp.61.3.373. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. 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]
  19. Schlodder E., Falkenberg K., Gergeleit M., Brettel K. Temperature dependence of forward and reverse electron transfer from A1-, the reduced secondary electron acceptor in photosystem I. Biochemistry. 1998 Jun 30;37(26):9466–9476. doi: 10.1021/bi973182r. [DOI] [PubMed] [Google Scholar]
  20. Schubert W. D., Klukas O., Krauss N., Saenger W., Fromme P., Witt H. T. Photosystem I of Synechococcus elongatus at 4 A resolution: comprehensive structure analysis. J Mol Biol. 1997 Oct 10;272(5):741–769. doi: 10.1006/jmbi.1997.1269. [DOI] [PubMed] [Google Scholar]
  21. 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]
  22. Telfer A., Barber J., Heathcote P., Evans M. C. Variable chlorophyll a fluorescence from P-700 enriched photosystem I particles dependent on the redox state of the reaction centre. Biochim Biophys Acta. 1978 Oct 11;504(1):153–164. doi: 10.1016/0005-2728(78)90014-2. [DOI] [PubMed] [Google Scholar]
  23. Trinkunas G., Holzwarth A. R. Kinetic modeling of exciton migration in photosynthetic systems. 2. Simulations of excitation dynamics in two-dimensional photosystem I core antenna/reaction center complexes. Biophys J. 1994 Feb;66(2 Pt 1):415–429. doi: 10.1016/s0006-3495(94)80792-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Trinkunas G., 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. 1996 Jul;71(1):351–364. doi: 10.1016/S0006-3495(96)79233-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Webber A. N., Su H., Bingham S. E., Käss H., Krabben L., Kuhn M., Jordan R., Schlodder E., Lubitz W. Site-directed mutations affecting the spectroscopic characteristics and midpoint potential of the primary donor in photosystem I. Biochemistry. 1996 Oct 1;35(39):12857–12863. doi: 10.1021/bi961198w. [DOI] [PubMed] [Google Scholar]
  26. Werst M., Jia Y., Mets L., Fleming G. R. Energy transfer and trapping in the photosystem I core antenna. A temperature study. Biophys J. 1992 Apr;61(4):868–878. doi: 10.1016/S0006-3495(92)81894-5. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES