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The native architecture of a photosynthetic membrane

Nature volume 430, pages 10581062 (26 August 2004) | Download Citation

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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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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.

Author information

Author notes

    • Svetlana Bahatyrova
    •  & Raoul N. Frese

    These authors contributed equally to this work

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, de Boelelaan 1081, 1081 HV, The Netherlands

    • Raoul N. Frese
    •  & Rienk van Grondelle
  3. Department of Molecular Biology and Biotechnology, University of Sheffield, Sheffield S10 2TN, UK

    • C. Alistair Siebert
    • , John D. Olsen
    • , Per A. Bullough
    •  & C. Neil Hunter
  4. Rutgers University, Department of Molecular Biology and Biochemistry, Piscataway, New Jersey 08854, USA

    • Robert A. Niederman

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Competing interests

The authors declare that they have no competing financial interests.

Corresponding author

Correspondence to C. Neil Hunter.

Supplementary information

PDF files

  1. 1.

    Supplementary Figure 1

    Presents a gallery of additional images showing the arrangement of photosynthetic complexes in several membrane patches.

  2. 2.

    Supplementary Figure 2

    Demonstrates the very low lateral mobility of photosynthetic complexes in the membrane patches observed by AFM.

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DOI

https://doi.org/10.1038/nature02823

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