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The native architecture of a photosynthetic membrane

Nature volume 430, pages 1058–1062 (2004)Cite this article

Abstract

In photosynthesis, the harvesting of solar energy and its subsequent conversion into a stable charge separation are dependent upon an interconnected macromolecular network of membrane-associated chlorophyll–protein complexes. Although the detailed structure of each complex has been determined1,2,3,4, the size and organization of this network are unknown. Here we show the use of atomic force microscopy to directly reveal a native bacterial photosynthetic membrane. This first view of any multi-component membrane shows the relative positions and associations of the photosynthetic complexes and reveals crucial new features of the organization of the network: we found that the membrane is divided into specialized domains each with a different network organization and in which one type of complex predominates. Two types of organization were found for the peripheral light-harvesting LH2 complex. In the first, groups of 10–20 molecules of LH2 form light-capture domains that interconnect linear arrays of dimers of core reaction centre (RC)–light-harvesting 1 (RC–LH1–PufX) complexes; in the second they were found outside these arrays in larger clusters. The LH1 complex is ideally positioned to function as an energy collection hub, temporarily storing it before transfer to the RC where photochemistry occurs: the elegant economy of the photosynthetic membrane is demonstrated by the close packing of these linear arrays, which are often only separated by narrow ‘energy conduits’ of LH2 just two or three complexes wide.

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Figure 1: AFM of native photosynthetic membranes.
Figure 2: Membrane patches showing two types of arrangement of photosynthetic complexes.
Figure 3: Three-dimensional representation of a small region of membrane showing RC–LH1–PufX core complex dimers and monomers with associated LH2 complexes.

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References

  1. Deisenhofer, J., Epp, O., Miki, K., Huber, R. & Michel, H. Structure of the protein subunits in the photosynthetic reaction centre of Rhodopseudomonas viridis at 3 Å resolution. Nature 318, 618–624 (1985)

    Article  ADS  CAS  Google Scholar 

  2. Allen, J. P., Feher, G., Yeates, T. O., Komiya, H. & Rees, D. C. Structure of the reaction center from Rhodobacter sphaeroides R26: The protein subunits. Proc. Natl Acad. Sci. USA 84, 6162–6166 (1987)

    Article  ADS  CAS  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. Roszak, A. W. et al. Crystal structure of the RC-LH1 core complex from Rhodopseudomonas palustris. Science 302, 1969–1972 (2003)

    Article  ADS  CAS  Google Scholar 

  5. Walz, T., Jamieson, S. J., Bowers, C. M., Bullough, P. A. & Hunter, C. N. Projection structures of three photosynthetic complexes from Rhodobacter sphaeroides: LH2 at 6 Å, LH1 and RC-LH1 at 25 Å. J. Mol. Biol. 282, 833–845 (1998)

    Article  CAS  Google Scholar 

  6. Jamieson, S. J. et al. Projection structure of the photosynthetic reaction centre-antenna complex of Rhodospirillum rubrum at 8.5 Å resolution. EMBO J. 21, 3927–3935 (2002)

    Article  CAS  Google Scholar 

  7. Bahatyrova, S. et al. Flexibility and size heterogeneity of the LH1 light harvesting complex revealed by atomic force microscopy: functional significance for bacterial photosynthesis. J. Biol. Chem. 279, 21327–21333 (2004)

    Article  CAS  Google Scholar 

  8. Fotiadis, D. et al. Structural analysis of the RC-LH1 photosynthetic core complex of Rhodospirillum rubrum using atomic force microscopy. J. Biol. Chem. 279, 2063–2068 (2004)

    Article  CAS  Google Scholar 

  9. Siebert, C. A. et al. Molecular architecture of photosynthetic membranes in Rhodobacter sphaeroides: the role of PufX. EMBO J. 23, 690–700 (2004)

    Article  CAS  Google Scholar 

  10. Vos, M. H., van Dorssen, R. J., Amesz, J., van Grondelle, R. & Hunter, C. N. The organisation of the photosynthetic apparatus of Rhodobacter sphaeroides: studies of antenna mutants using singlet-singlet quenching. Biochim. Biophys. Acta 933, 132–140 (1988)

    Article  CAS  Google Scholar 

  11. Aagaard, J. & Siström, W. R. Control of synthesis of reaction centre bacteriochlorophyll in photosynthetic bacteria. Photochem. Photobiol. 15, 209–225 (1972)

    Article  CAS  Google Scholar 

  12. Monger, T. & Parson, W. W. Singlet-triplet fusion in Rhodopseudomonas sphaeroides. Biochim. Biophys. Acta 460, 393–407 (1977)

    Article  CAS  Google Scholar 

  13. Hunter, C. N., Kramer, H. J. M. & van Grondelle, R. Linear dichroism and fluorescence emission of antenna complexes during photosynthetic unit assembly in Rhodopseudomonas sphaeroides. Biochim. Biophys. Acta 807, 44–51 (1985)

    Article  CAS  Google Scholar 

  14. Visscher, K. J., Bergström, H., Sundström, V., Hunter, C. N. & van Grondelle, R. Temperature-dependence of energy-transfer from the long wavelength antenna BChl-896 to the reaction centre in Rhodospirillum rubrum, Rhodobacter sphaeroides (w.t. and M21 mutant) from 77 to 177K, studied by picosecond absorption spectroscopy. Photosyn. Res. 22, 211–217 (1989)

    Article  CAS  Google Scholar 

  15. Beekman, L. M. et al. Trapping kinetics in mutants of the photosynthetic purple bacterium Rhodobacter sphaeroides: influence of the charge separation rate and consequences for the rate-limiting step in the light-harvesting process. Biochemistry 33, 3143–3147 (1994)

    Article  CAS  Google Scholar 

  16. Frese, R. N. et al. The long-range supraorganization of the bacterial photosynthetic unit: A key role for PufX. Proc. Natl Acad. Sci. USA 97, 5197–5202 (2000)

    Article  ADS  CAS  Google Scholar 

  17. Scheuring, S. et al. Nanodissection and high-resolution imaging of the Rhodopseudomonas viridis photosynthetic core complex in native membranes by AFM. Proc. Natl Acad. Sci. USA 100, 1690–1693 (2003)

    Article  ADS  CAS  Google Scholar 

  18. Hess, S. et al. Temporally and spectrally resolved subpicosecond energy transfer within the peripheral antenna complex (LH2) and from LH2 to the core antenna complex in photosynthetic purple bacteria. Proc. Natl Acad. Sci. USA 92, 12333–12337 (1995)

    Article  ADS  CAS  Google Scholar 

  19. Scheuring, S. et al. AFM characterization of tilt and intrinsic flexibility of Rhodobacter sphaeroides light harvesting complex 2 (LH2). J. Mol. Biol. 325, 569–580 (2003)

    Article  CAS  Google Scholar 

  20. Katona, G., Andreasson, U., Landau, E. M., Andreasson, L. E. & Neutze, R. Lipidic cubic phase crystal structure of the photosynthetic reaction centre from Rhodobacter sphaeroides at 2.35 angstrom resolution. J. Mol. Biol. 331, 681–692 (2003)

    Article  CAS  Google Scholar 

  21. Scheuring, S. et al. Structural role of PufX in the dimerization of the photosynthetic core-complex of Rhodobacter sphaeroides. J. Biol. Chem. 279, 3620–3626 (2004)

    Article  CAS  Google Scholar 

  22. Sturgis, J. N. & Niederman, R. A. The effect of different levels of the B800–850 light-harvesting complex on intracytoplasmic membrane development in Rhodobacter sphaeroides. Arch. Microbiol. 165, 235–242 (1996)

    Article  CAS  Google Scholar 

  23. Müller, D. J. et al. Observing membrane protein diffusion at subnanometer resolution. J. Mol. Biol. 327, 925–930 (2003)

    Article  Google Scholar 

  24. Berry, E. A. et al. X-ray structure of Rhodobacter capsulatus cytochrome bc1: Comparison with its mitochondrial and chloroplast counterparts. Photosyn. Res. (in the press)

  25. Feniouk, B. A., Cherepanov, D. A., Voskoboynikova, N. E., Mulkidjanian, A. Y. & Junge, W. Chromatophore vesicles of Rhodobacter capsulatus contain on average one FoF1-ATP synthase each. Biophys. J. 82, 1115–1122 (2002)

    Article  CAS  Google Scholar 

  26. 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. 301, 1123–1133 (2000)

    Article  CAS  Google Scholar 

  27. Niederman, R. A., Mallon, D. E. & Parks, L. C. Membranes of Rhodopseudomonas sphaeroides. VI. Isolation of a fraction enriched in newly synthesized bacteriochlorophyll α-protein complexes. Biochim. Biophys. Acta 555, 210–220 (1979)

    Article  CAS  Google Scholar 

  28. Van der Werf, K. O. et al. Compact stand-alone atomic force microscope. Rev. Sci. Instrum. 64, 2892–2897 (1993)

    Article  ADS  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by grants from the BBSRC (UK) and the Netherlands Organisation for Scientific Research (NWO). This paper is dedicated to the memory of Prof. Dr. Bart de Grooth.

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Author notes

  1. Svetlana Bahatyrova and Raoul N. Frese: These authors contributed equally to this work

Authors and Affiliations

  1. Biophysical Techniques Group, Department of Science & Technology, BMTI, MESA, University of Twente, P.O. Box 217, 7500 AE, Enschede, The Netherlands

    Svetlana Bahatyrova, Raoul N. Frese, Kees O. van der Werf & Cees Otto

  2. Biophysics, Faculty of Sciences, Vrije Universiteit Amsterdam, 1081, 1081 HV, de Boelelaan, The Netherlands

    Raoul N. Frese & Rienk van Grondelle

  3. Department of Molecular Biology and Biotechnology, University of Sheffield, S10 2TN, Sheffield, UK

    C. Alistair Siebert, John D. Olsen, Per A. Bullough & C. Neil Hunter

  4. Department of Molecular Biology and Biochemistry, Rutgers University, Piscataway, New Jersey, 08854, USA

    Robert A. Niederman

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  1. Svetlana Bahatyrova
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Correspondence to C. Neil Hunter.

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Supplementary information

Supplementary Figure 1

Presents a gallery of additional images showing the arrangement of photosynthetic complexes in several membrane patches. (PDF 1278 kb)

Supplementary Figure 2

Demonstrates the very low lateral mobility of photosynthetic complexes in the membrane patches observed by AFM. (PDF 1019 kb)

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Bahatyrova, S., Frese, R., Siebert, C. et al. The native architecture of a photosynthetic membrane. Nature 430, 1058–1062 (2004). https://doi.org/10.1038/nature02823

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