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Mobility of photosynthetic complexes in thylakoid membranes

Nature volume 390, pages 421–424 (1997)Cite this article

Abstract

The structures of many photosynthetic pigment–protein complexes have now been determined1,2,3,4,5,6, but a real understanding of the photosynthetic membrane at the molecular level will also require knowledge of the organization and dynamics of these complexes in the intact membrane. Using fluorescence recovery after photobleaching (FRAP)7 and a scanning confocal microscope, we have made direct measurements in vivo of the lateral diffusion of light-harvesting complexes and reaction centres in the thylakoid membranes of the cyanobacterium Dactylococcopsis salina8. We find that the phycobilisomes (the accessory light-harvesting complexes of cyanobacteria) diffuse quite rapidly, but that photosystem II is immobile on the timescale of the measurement, indicating that the linkage between phycobilisomes and photosystem II is unstable. We propose that the lateral diffusion of phycobilisomes is involved in regulation of photosynthetic light-harvesting (state 1–state 2 transitions). The mobility of the phycobilisomes may also be essential to allow the synthesis and repair of thylakoid membrane components.

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Figure 1: The geometry of our one-dimensional FRAP measurements.
Figure 2: Selected fluorescence images from typical sequences recorded before bleaching, immediately after bleaching, and at various times thereafter.
Figure 3: Selected one-dimensional bleaching profiles derived from the sequences of fluorescence images shown in Fig. 2 .
Figure 4: Calculation of the diffusion coefficient D for phycobilisomes from the time-dependence of the maximum bleach depth, C y = 0, t in the measurement series shown in Figs 2a and 3a .

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References

  1. Krauss, N. et al . Photosystem I at 4-å resolution represents the first structural model of a joint photosynthetic reaction centre and core antenna system. Nature Struct. Biol. 3, 965–973 (1996).

    Article  CAS  Google Scholar 

  2. Sidler, W. A. in The Molecular Biology of Cyanobacteria(ed. Bryant, D. A.) 139–216 (Kluwer Academic, Dordrecht, (1994)).

    Book  Google Scholar 

  3. McDermott, G. et al . Crystal structure of an integral membrane light-harvesting complex from photosynthetic bacteria. Nature 374, 517–521 (1995).

    Article  ADS  CAS  Google Scholar 

  4. Kühlbrandt, W., Wang, D. N. & Fijiyoshi, Y. Atomic model of plant light-harvesting complex by electron crystallography. Nature 367, 614–621 (1994).

    Article  ADS  Google Scholar 

  5. Holzenburg, A., Bewley, M. C., Wilson, F. H., Nicholson, W. V. & Ford, R. C. Three-dimensional structure of photosystem II. Nature 363, 470–473 (1993).

    Article  ADS  CAS  Google Scholar 

  6. Boekema, E. J. et al . Supramolecular structure of the photosystem II complex from green plants and cyanobacteria. Proc. Natl Acad. Sci. USA 92, 175–179 (1995).

    Article  ADS  CAS  Google Scholar 

  7. Thomas, J. & Webb, W. W. in Non-invasive Techniques in Cell Biology 129–152 (Wiley–Liss, New York, (1990)).

    Google Scholar 

  8. Walsby, A. E., van Rijn, J. & Cohen, Y. The biology of a new gas-vacuolate cyanobacterium, Dactylococcopsis salina sp. nov. in Solar Lake. Proc. R. Soc. Lond. B 217, 417–447 (1983).

    Article  ADS  Google Scholar 

  9. Zhang, F., Lee, G. M. & Jacobson, K. Protein lateral mobility as a reflection of membrane microstructure. BioEssays 15, 579–588 (1993).

    Article  CAS  Google Scholar 

  10. Kubitscheck, U., Wedekind, P. & Peters, R. Lateral diffusion measurement at high spatial resolution by scanning microphotolysis in a confocal microscope. Biophys. J. 67, 948–956 (1994).

    Article  ADS  CAS  Google Scholar 

  11. Drepper, F., Carlberg, I., Andersson, B. & Haehnel, W. Lateral diffusion of an integral membrane protein: Monte Carlo analysis of the migration of phosphorylated light-harvesting complex II in the thylakoid membrane. Biochemistry 32, 11915–11922 (1993).

    Article  CAS  Google Scholar 

  12. Barber, J. & Andersson, B. Revealing the blueprint of photosynthesis. Nature 370, 31–34 (1994).

    Article  ADS  CAS  Google Scholar 

  13. Holzwarth, A. R. Fluorescence lifetimes in photosynthetic systems. Photochem. Photobiol. 43, 707–725 (1986).

    Article  CAS  Google Scholar 

  14. Bald, D., Kruip, J. & Rögner, M. Supramolecular architecture of cyanobacterial thylakoid membranes: how is the phycobilisome connected with the photosystems? Photosynth. Res. 49, 103–118 (1996).

    Article  CAS  Google Scholar 

  15. Giddings, T. H., Wasmann, C. & Staehelin, L. A. Structure of the thylakoids and envelope membranes of the cyanelles of Cyanophora paradoxa . Plant Physiol. 71, 409–419 (1983).

    Article  CAS  Google Scholar 

  16. Mustardy, L., Cunningham, F. X. & Gantt, E. Photosynthetic membrane topography: quantitative in situ localisation of photosystems I and II. Proc. Natl Acad. Sci. USA 89, 10021–10025 (1992).

    Article  ADS  CAS  Google Scholar 

  17. Adir, N., Shochat, S. & Ohad, I. Light-dependent D1 protein synthesis and translocation is regulated by reaction centre II. J. Biol. Chem. 265, 12563–12568 (1990).

    CAS  PubMed  Google Scholar 

  18. Allen, J. F. Protein phosphorylation in regulation of photosynthesis. Biochim. Biophys. Acta 1098, 275–335 (1992).

    Article  CAS  Google Scholar 

  19. Soitamo, A. J. et al . Overproduction of the D1:2 protein makes Synechococcus cells more tolerant to photoinhibition of photosystem II. Plant Mol. Biol. 30, 467–478 (1996).

    Article  CAS  Google Scholar 

  20. Mullineaux, C. W., Bittersmann, E., Allen, J. F. & Holzwarth, A. R. Picosecond time-resolved fluorescence emission spectra indicate decreased excitation energy transfer from the phycobilisome to photosystem II in the cyanobacterium Synechococcus 6301. Biochim. Biophys. Acta 1015, 231–242 (1990).

    Article  CAS  Google Scholar 

  21. Mullineaux, C. W. Excitation energy transfer from phycobilisomes to photosystem I in a cyanobacterial mutant lacking photosystem II. Biochim. Biophys. Acta 1184, 71–77 (1994).

    Article  CAS  Google Scholar 

  22. van der Oord, C. J. R. et al . High-resolution confocal microscopy using synchrotron radiation. J. Microsc. 182, 217–224 (1996).

    Article  CAS  Google Scholar 

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Acknowledgements

We thank A. E. Walsby for discussion and for the culture of Dactylococcopsis salina .

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Authors and Affiliations

  1. Department of Biology, University College London, Darwin Building, Gower Street, London, WC1E 6BT, UK

    Conrad W. Mullineaux

  2. CLRC Daresbury Laboratory, Daresbury, Warrington, WA4 4AD, Cheshire, UK

    Mark J. Tobin & Gareth R. Jones

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Correspondence to Conrad W. Mullineaux.

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Mullineaux, C., Tobin, M. & Jones, G. Mobility of photosynthetic complexes in thylakoid membranes. Nature 390, 421–424 (1997). https://doi.org/10.1038/37157

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