Integration of energy and electron transfer processes in the photosynthetic membrane of Rhodobacter sphaeroides

Michaël L. Cartron, John D. Olsen, Melih Sener, Philip J. Jackson, Amanda A. Brindley, Pu Qian, Mark J. Dickman, Graham J. Leggett, Klaus Schulten, C. Neil Hunter

Research output: Contribution to journalArticle

Abstract

Photosynthesis converts absorbed solar energy to a protonmotive force, which drives ATP synthesis. The membrane network of chlorophyll-protein complexes responsible for light absorption, photochemistry and quinol (QH 2) production has been mapped in the purple phototrophic bacterium Rhodobacter (Rba.) sphaeroides using atomic force microscopy (AFM), but the membrane location of the cytochrome bc1 (cytbc1) complexes that oxidise QH2 to quinone (Q) to generate a protonmotive force is unknown. We labelled cytbc1 complexes with gold nanobeads, each attached by a Histidine10 (His10)-tag to the C-terminus of cytc1. Electron microscopy (EM) of negatively stained chromatophore vesicles showed that the majority of the cytbc1 complexes occur as dimers in the membrane. The cytbc1 complexes appeared to be adjacent to reaction centre light-harvesting 1-PufX (RC-LH1-PufX) complexes, consistent with AFM topographs of a gold-labelled membrane. His-tagged cytbc1 complexes were retrieved from chromatophores partially solubilised by detergent; RC-LH1-PufX complexes tended to co-purify with cytbc1 whereas LH2 complexes became detached, consistent with clusters of cytbc1 complexes close to RC-LH1-PufX arrays, but not with a fixed, stoichiometric cytbc1-RC-LH1-PufX supercomplex. This information was combined with a quantitative mass spectrometry (MS) analysis of the RC, cytbc1, ATP synthase, cytaa3 and cytcbb3 membrane protein complexes, to construct an atomic-level model of a chromatophore vesicle comprising 67 LH2 complexes, 11 LH1-RC-PufX dimers & 2 RC-LH1-PufX monomers, 4 cytbc 1 dimers and 2 ATP synthases. Simulation of the interconnected energy, electron and proton transfer processes showed a half-maximal ATP turnover rate for a light intensity equivalent to only 1% of bright sunlight. Thus, the photosystem architecture of the chromatophore is optimised for growth at low light intensities.

Original languageEnglish (US)
Pages (from-to)1769-1780
Number of pages12
JournalBiochimica et Biophysica Acta - Bioenergetics
Volume1837
Issue number10
DOIs
StatePublished - Oct 2014

Keywords

  • Atomic force microscopy
  • Bacterial photosynthesis
  • Electron microscopy
  • Membrane modelling
  • Quinone

ASJC Scopus subject areas

  • Biochemistry
  • Biophysics
  • Cell Biology

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  • Cite this

    Cartron, M. L., Olsen, J. D., Sener, M., Jackson, P. J., Brindley, A. A., Qian, P., Dickman, M. J., Leggett, G. J., Schulten, K., & Neil Hunter, C. (2014). Integration of energy and electron transfer processes in the photosynthetic membrane of Rhodobacter sphaeroides. Biochimica et Biophysica Acta - Bioenergetics, 1837(10), 1769-1780. https://doi.org/10.1016/j.bbabio.2014.02.003