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Single-molecule in vivo imaging of bacterial respiratory complexes indicates delocalized oxidative phosphorylation

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Author(s)

  • Isabel Llorente-Garcia
  • Tchern Lenn
  • Heiko Erhardt
  • Oliver L Harriman
  • Lu-Ning Liu
  • Alex Robson
  • Sheng-Wen Chiu
  • Sarah Matthews
  • Nicky J Willis
  • Christopher D Bray
  • Sang-Hyuk Lee
  • Jae Yen Shin
  • Carlos Bustamante
  • Jan Liphardt
  • Thorsten Friedrich
  • Conrad W Mullineaux
  • Mark C Leake

Department/unit(s)

Publication details

JournalBiochimica et Biophysica Acta. Bioenergetics
DateE-pub ahead of print - 7 Feb 2014
DatePublished (current) - Jun 2014
Issue number6
Volume1837
Number of pages14
Pages (from-to)811-824
Early online date7/02/14
Original languageEnglish

Abstract

Chemiosmotic energy coupling through oxidative phosphorylation (OXPHOS) is crucial to life, requiring coordinated enzymes whose membrane organization and dynamics are poorly understood. We quantitatively explore localization, stoichiometry, and dynamics of key OXPHOS complexes, functionally fluorescent protein-tagged, in Escherichia coli using low-angle fluorescence and superresolution microscopy, applying single-molecule analysis and novel nanoscale co-localization measurements. Mobile 100-200nm membrane domains containing tens to hundreds of complexes are indicated. Central to our results is that domains of different functional OXPHOS complexes do not co-localize, but ubiquinone diffusion in the membrane is rapid and long-range, consistent with a mobile carrier shuttling electrons between islands of different complexes. Our results categorically demonstrate that electron transport and proton circuitry in this model bacterium are spatially delocalized over the cell membrane, in stark contrast to mitochondrial bioenergetic supercomplexes. Different organisms use radically different strategies for OXPHOS membrane organization, likely depending on the stability of their environment.

Bibliographical note

© 2014 The Authors. Published by Elsevier B.V. This is an open access article under a Creative Commons Attribution (CC BY) licence.

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