The long-range organization of a native photosynthetic membrane

  1. Raoul N. Frese*,,,
  2. C. Alistair Siebert§,
  3. Robert A. Niederman,
  4. C. Neil Hunter§,
  5. Cees Otto, and
  6. Rienk van Grondelle*
  1. *Biophysics, Faculty of Sciences, Vrije Universiteit Amsterdam, De Boelelaan 1081, Amsterdam 1081 HV, The Netherlands; Biophysical Techniques Group, Department of Science and Technology, University of Twente, P.O. Box 217, 7500 AE Enschede, The Netherlands; §Department of Molecular Biology and Biotechnology, University of Sheffield, Sheffield S10 2TN, United Kingdom; and Department of Molecular Biology and Biochemistry, Rutgers, The State University of New Jersey, Piscataway, NJ 08854
  1. Edited by Pierre A. Joliot, Institut de Biologie Physico-Chemique, Paris, France, and approved November 17, 2004 (received for review October 1, 2004)

Abstract

Photosynthesis relies on the delicate interplay between a specific set of membrane-bound pigment–protein complexes that harvest and transport solar energy, execute charge separation, and conserve the energy. We have investigated the organization of the light-harvesting (LH) and reaction-center (RC) complexes in native bacterial photosynthetic membranes of the purple bacterium Rhodobacter sphaeroides by using polarized light spectroscopy, linear dichroism (LD) on oriented membranes. These LD measurements show that in native membranes, which contain LH2 as the major energy absorber, the RC–LH1–PufX complexes are highly organized in a way similar to that which we found previously for a mutant lacking LH2. The relative contribution of LH1 and LH2 light-harvesting complexes to the LD spectrum shows that LH2 preferentially resides in highly curved parts of the membrane. Combining the spectroscopic data with our recent atomic force microscopy (AFM) results, we propose an organization for this photosynthetic membrane that features domains containing linear arrays of RC–LH1–PufX complexes interspersed with LH2 complexes and some LH2 found in separate domains. The study described here allows the simultaneous assessment of both global and local structural information on the organization of intact, untreated membranes.

Footnotes

  • To whom correspondence should be addressed. E-mail: raoul{at}nat.vu.nl.

  • Author contributions: R.N.F. designed research; R.N.F., C.A.S., and R.A.N. performed research; R.N.F. analyzed data; C.N.H., C.O., and R.v.G. supervised research; and R.N.F. wrote the paper.

  • This paper was submitted directly (Track II) to the PNAS office.

  • Abbreviations: LH, light-harvesting; RC, reaction center; LD, linear dichroism; AFM, atomic force microscopy; BChl, bacteriochlorophyll; BPheo, bacteriopheophytin; P, primary electron donor; Q, quinone; LH1 and LH2, light-harvesting complex 1 and 2.

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