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The native architecture of a photosynthetic membrane

Author

Listed:
  • Svetlana Bahatyrova

    (University of Twente)

  • Raoul N. Frese

    (University of Twente
    Vrije Universiteit Amsterdam, 1081)

  • C. Alistair Siebert

    (University of Sheffield)

  • John D. Olsen

    (University of Sheffield)

  • Kees O. van der Werf

    (University of Twente)

  • Rienk van Grondelle

    (Vrije Universiteit Amsterdam, 1081)

  • Robert A. Niederman

    (Rutgers University)

  • Per A. Bullough

    (University of Sheffield)

  • Cees Otto

    (University of Twente)

  • C. Neil Hunter

    (University of Sheffield)

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.

Suggested Citation

  • Svetlana Bahatyrova & Raoul N. Frese & C. Alistair Siebert & John D. Olsen & Kees O. van der Werf & Rienk van Grondelle & Robert A. Niederman & Per A. Bullough & Cees Otto & C. Neil Hunter, 2004. "The native architecture of a photosynthetic membrane," Nature, Nature, vol. 430(7003), pages 1058-1062, August.
  • Handle: RePEc:nat:nature:v:430:y:2004:i:7003:d:10.1038_nature02823
    DOI: 10.1038/nature02823
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    Cited by:

    1. Kazutoshi Tani & Ryo Kanno & Riku Kikuchi & Saki Kawamura & Kenji V. P. Nagashima & Malgorzata Hall & Ai Takahashi & Long-Jiang Yu & Yukihiro Kimura & Michael T. Madigan & Akira Mizoguchi & Bruno M. H, 2022. "Asymmetric structure of the native Rhodobacter sphaeroides dimeric LH1–RC complex," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    2. Kazutoshi Tani & Kenji V. P. Nagashima & Ryo Kanno & Saki Kawamura & Riku Kikuchi & Malgorzata Hall & Long-Jiang Yu & Yukihiro Kimura & Michael T. Madigan & Akira Mizoguchi & Bruno M. Humbel & Zheng-Y, 2021. "A previously unrecognized membrane protein in the Rhodobacter sphaeroides LH1-RC photocomplex," Nature Communications, Nature, vol. 12(1), pages 1-9, December.
    3. Peng Cao & Laura Bracun & Atsushi Yamagata & Bern M. Christianson & Tatsuki Negami & Baohua Zou & Tohru Terada & Daniel P. Canniffe & Mikako Shirouzu & Mei Li & Lu-Ning Liu, 2022. "Structural basis for the assembly and quinone transport mechanisms of the dimeric photosynthetic RC–LH1 supercomplex," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    4. Emiliano Altamura & Paola Albanese & Pasquale Stano & Massimo Trotta & Francesco Milano & Fabio Mavelli, 2020. "Charge Recombination Kinetics of Bacterial Photosynthetic Reaction Centres Reconstituted in Liposomes: Deterministic Versus Stochastic Approach," Data, MDPI, vol. 5(2), pages 1-15, June.

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