CaltechAUTHORS
Published October 3, 2022 | Version public
Journal Article Metadata-only

Molecular asymmetry of a photosynthetic supercomplex from green sulfur bacteria

Creators

  • 1. ROR icon Arizona State University
  • 2. ROR icon California Institute of Technology
  • 3. ROR icon Washington University in St. Louis

Abstract

The photochemical reaction center (RC) features a dimeric architecture for charge separation across the membrane. In green sulfur bacteria (GSB), the trimeric Fenna-Matthews-Olson (FMO) complex mediates the transfer of light energy from the chlorosome antenna complex to the RC. Here we determine the structure of the photosynthetic supercomplex from the GSB Chlorobaculum tepidum using single-particle cryogenic electron microscopy (cryo-EM) and identify the cytochrome c subunit (PscC), two accessory protein subunits (PscE and PscF), a second FMO trimeric complex, and a linker pigment between FMO and the RC core. The protein subunits that are assembled with the symmetric RC core generate an asymmetric photosynthetic supercomplex. One linker bacteriochlorophyll (BChl) is located in one of the two FMO-PscA interfaces, leading to differential efficiencies of the two energy transfer branches. The two FMO trimeric complexes establish two different binding interfaces with the RC cytoplasmic surface, driven by the associated accessory subunits. This structure of the GSB photosynthetic supercomplex provides mechanistic insight into the light excitation energy transfer routes and a possible evolutionary transition intermediate of the bacterial photosynthetic supercomplex from the primitive homodimeric RC.

Additional Information

© The Author(s) 2022. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/. We thank Chihiro Azai, Patricia Baker, and Hila Toporik for advising us on the procedure for culture growth. We very much appreciate Robert Blankenship and Kevin Redding for fruitful scientific discussion. We thank Dewight Williams and David Lowry for the EM assistance in the Eyring Materials Center (EMC) at Arizona State University (ASU). We acknowledge using the Titan Krios TEM at the EMC and the funding for the instrumentation by NSF MRI 1531991. A portion of this research was supported by NIH grant U24GM129547 and performed at the Pacific Northwest Center for Cryo-EM (PNCC) at Oregon Health & Science University (OHSU), Portland, OR, and accessed through EMSL (grid.436923.9), a DOE Office of Science User Facility sponsored by the Office of Biological and Environmental Research (PNCC proposal number: 160074). We thank Omar Davulcu for the EM assistance at the PNCC site. We acknowledge the funding support by Army Research Office (ARO) (W911NF2010321) to P.-L.C., the support by the DOE, Office of Basic Energy Sciences, Photosynthetic Systems Program (DE-FG02-07ER15902) to H.L., and the GPU device support by the NVIDIA GPU Grant Program to P.-L.C. We especially thank John C.H. Spence for initiating the idea for the quantum biology project, and we missed the days discussing sciences and making discoveries together. Author contributions. R.P., C.D.T., K.S., and Y.-P.P. performed cell culture and protein purification. R.P. and C.D.T. prepared frozen specimens for cryo-EM data collection. S.C. and K.-Y.C. performed the characterization of purified protein complexes. S.L., K.-W.C., T.-Y.W., H.L., and T.-F.C. performed mass spectrometric experiments and analyses. P.-L.C. processed cryo-EM image data and performed structural modeling, analyses, and interpretations. Y.M. performed the calculations to analyze possible excitation energy transfer pathways. R.P., Y.-P.P., and P.-L.C. prepared figures. B.N. and P.-L.C. initiated and supervised the project. R.P., Y.M., B.N., and P.-L.C. wrote the manuscript with input from all the authors. Data availability. Cryo-EM density maps (MRC format) of the RC-FMO2 and RC-FMO1 protein complexes determined in this study were deposited in the Electron Microscopy Data Bank (EMDB) under accession numbers EMD-26471 (RC-FMO₂) and EMD-26469 (RC-FMO₁). Model coordinates were deposited in the Protein Data Bank (PDB) under accession numbers 7UEB (RC-FMO2; 10.2210/pdb7ueb/pdb) and 7UEA (RC-FMO1; 10.2210/pdb7uea/pdb). All the data are available in the EMDB and wwPDB databases or from the corresponding author upon request. The authors declare no competing interests.

Additional details

Identifiers

PMCID
PMC9529944
Eprint ID
117493
Resolver ID
CaltechAUTHORS:20221019-343672700.6

Funding

NSF
MRI-1531991
NIH
U24GM129547
Army Research Office (ARO)
W911NF2010321
Department of Energy (DOE)
DE-FG02-07ER15902

Dates

Created
2022-10-27
Created from EPrint's datestamp field
Updated
2023-07-06
Created from EPrint's last_modified field

Caltech Custom Metadata

Caltech groups
Division of Biology and Biological Engineering (BBE)