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Three-Dimensional Structure of the Rhodobacter sphaeroides RC-LH1-PufX Complex: Dimerization and Quinone Channels Promoted by PufX

Journal Article · · Biochemistry
DOI:https://doi.org/10.1021/bi4011946· OSTI ID:1097031
 [1];  [2];  [3];  [4];  [4];  [4];  [5];  [4];  [4]
  1. Department of Molecular Biology and Biotechnology, University of Sheffield, Western Bank, Firth Court, Sheffield S10 2TN, United Kingdom; Washington University
  2. Institute of Integrative Biology, Biosciences Building, University of Liverpool, Crown Street, Liverpool L69 7ZB, United Kingdom
  3. Department of Molecular Biology and Biotechnology, University of Sheffield, Western Bank, Firth Court, Sheffield S10 2TN, United Kingdom; ChELSI Institute, Department of Chemical and Biological Engineering, University of Sheffield, Mappin Street, Sheffield, S1 3JD, United Kingdom
  4. Department of Molecular Biology and Biotechnology, University of Sheffield, Western Bank, Firth Court, Sheffield S10 2TN, United Kingdom
  5. ChELSI Institute, Department of Chemical and Biological Engineering, University of Sheffield, Mappin Street, Sheffield, S1 3JD, United Kingdom
+ Show Author Affiliations
Reaction center-light harvesting 1 (RC-LH1) complexes are the fundamental units of bacterial photosynthesis, which use solar energy to power the reduction of quinone to quinol prior to the formation of the proton gradient that drives ATP synthesis. The dimeric RC-LH1-PufX complex of Rhodobacter sphaeroides is composed of 64 polypeptides and 128 cofactors, including 56 LH1 bacteriochlorophyll a (BChl a) molecules that surround and donate energy to the two RCs. The 3D structure was determined to 8 Å by X-ray crystallography, and a model was built with constraints provided by electron microscopy (EM), nuclear magnetic resonance (NMR), mass spectrometry (MS), and site-directed mutagenesis. Each half of the dimer complex consists of a RC surrounded by an array of 14 LH1 αβ subunits, with two BChls sandwiched between each αβ pair of transmembrane helices. The N- and C-terminal extrinsic domains of PufX promote dimerization by interacting with the corresponding domains of an LH1 β polypeptide from the other half of the RC-LH1-PufX complex. Close contacts between PufX, an LH1 αβ subunit, and the cytoplasmic domain of the RC-H subunit prevent the LH1 complex from encircling the RC and create a channel connecting the RC QB site to an opening in the LH1 ring, allowing Q/QH2 exchange with the external quinone pool. We also identified a channel that connects the two halves of the dimer, potentially forming a long-range pathway for quinone migration along rows of RC-LH1-PufX complexes in the membrane. The structure of the RC-LH1-PufX complex explains the crucial role played by PufX in dimer formation, and it shows how quinone traffic traverses the LH1 complex as it shuttles between the RC and the cytochrome bc1 complex.
Research Organization:
Washington Univ., St. Louis, MO (United States); Energy Frontier Research Centers (EFRC) (United States). Photosynthetic Antenna Research Center (PARC)
Sponsoring Organization:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
DOE Contract Number:
SC0001035
OSTI ID:
1097031
Report Number(s):
DE-SC0001035-92
Journal Information:
Biochemistry, Journal Name: Biochemistry Journal Issue: 43 Vol. 52; ISSN 0006-2960
Publisher:
American Chemical Society (ACS)
Country of Publication:
United States
Language:
English

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