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Title: Lateral Segregation of Photosystem I in Cyanobacterial Thylakoids

Abstract

Photosystem I (PSI) is the dominant photosystem in cyanobacteria and it plays a pivotal role in cyanobacterial metabolism. Despite its biological importance, the native organization of PSI in cyanobacterial thylakoid membranes is poorly understood. Here, we use atomic force microscopy (AFM) to show that ordered, extensive macromolecular arrays of PSI complexes are present in thylakoids from Thermosynechococcus elongatus, Synechococcus sp PCC 7002, and Synechocystis sp PCC 6803. Hyperspectral confocal fluorescence microscopy and three-dimensional structured illumination microscopy of Synechocystis sp PCC 6803 cells visualize PSI domains within the context of the complete thylakoid system. Crystallographic and AFM data were used to build a structural model of a membrane landscape comprising 96 PSI trimers and 27,648 chlorophyll a molecules. Rather than facilitating intertrimer energy transfer, the close associations between PSI primarily maximize packing efficiency; short-range interactions with Complex I and cytochrome b6f are excluded from these regions of the membrane, so PSI turnover is sustained by long-distance diffusion of the electron donors at the membrane surface. Elsewhere, PSI-photosystem II contact zones provide sites for docking phycobilisomes and the formation of megacomplexes. Finally, PSI-enriched domains in cyanobacteria might foreshadow the partitioning of PSI into stromal lamellae in plants, similarly sustained by long-distance diffusionmore » of electron carriers.« less

Authors:
 [1];  [2]; ORCiD logo [1];  [1];  [3]; ORCiD logo [4];  [4]; ORCiD logo [3];  [5]; ORCiD logo [1]
  1. Department of Molecular Biology and Biotechnology, University of Sheffield, Sheffield S10 2TN, United Kingdom
  2. Beckman Institute for Advanced Science and Technology, University of Illinois at Urbana-Champaign, Urbana, Illinois 61801, Department of Physics, University of Illinois at Urbana-Champaign, Urbana, Illinois 61801
  3. Bioenergy and Defense Technologies Department, Sandia National Laboratories, Albuquerque, New Mexico 87185
  4. Division of Molecular Biosciences, Faculty of Natural Sciences, Imperial College London, London SW7 2AZ, United Kingdom
  5. Beckman Institute for Advanced Science and Technology, University of Illinois at Urbana-Champaign, Urbana, Illinois 61801, Department of Physics, University of Illinois at Urbana-Champaign, Urbana, Illinois 61801, Center for Biophysics and Computational Biology, University of Illinois at Urbana-Champaign, Urbana, Illinois 61801
Publication Date:
Research Org.:
Sandia National Lab. (SNL-NM), Albuquerque, NM (United States); Energy Frontier Research Centers (EFRC) (United States). Photosynthetic Antenna Research Center (PARC)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES); USDOE National Nuclear Security Administration (NNSA)
OSTI Identifier:
1670238
Alternate Identifier(s):
OSTI ID: 1429809
Report Number(s):
SAND-2017-7776J
Journal ID: ISSN 1040-4651; /plantcell/29/5/1119.atom
Grant/Contract Number:  
SC 0001035; 338895; AC04-94AL85000; SC0001035; MCB1157615; PHY0822613; P41GM104601; 5R01GM09824302
Resource Type:
Published Article
Journal Name:
The Plant Cell
Additional Journal Information:
Journal Name: The Plant Cell Journal Volume: 29 Journal Issue: 5; Journal ID: ISSN 1040-4651
Publisher:
Oxford University Press
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

MacGregor-Chatwin, Craig, Sener, Melih, Barnett, Samuel F. H., Hitchcock, Andrew, Barnhart-Dailey, Meghan C., Maghlaoui, Karim, Barber, James, Timlin, Jerilyn A., Schulten, Klaus, and Hunter, C. Neil. Lateral Segregation of Photosystem I in Cyanobacterial Thylakoids. United States: N. p., 2017. Web. doi:10.1105/tpc.17.00071.
MacGregor-Chatwin, Craig, Sener, Melih, Barnett, Samuel F. H., Hitchcock, Andrew, Barnhart-Dailey, Meghan C., Maghlaoui, Karim, Barber, James, Timlin, Jerilyn A., Schulten, Klaus, & Hunter, C. Neil. Lateral Segregation of Photosystem I in Cyanobacterial Thylakoids. United States. https://doi.org/10.1105/tpc.17.00071
MacGregor-Chatwin, Craig, Sener, Melih, Barnett, Samuel F. H., Hitchcock, Andrew, Barnhart-Dailey, Meghan C., Maghlaoui, Karim, Barber, James, Timlin, Jerilyn A., Schulten, Klaus, and Hunter, C. Neil. Fri . "Lateral Segregation of Photosystem I in Cyanobacterial Thylakoids". United States. https://doi.org/10.1105/tpc.17.00071.
@article{osti_1670238,
title = {Lateral Segregation of Photosystem I in Cyanobacterial Thylakoids},
author = {MacGregor-Chatwin, Craig and Sener, Melih and Barnett, Samuel F. H. and Hitchcock, Andrew and Barnhart-Dailey, Meghan C. and Maghlaoui, Karim and Barber, James and Timlin, Jerilyn A. and Schulten, Klaus and Hunter, C. Neil},
abstractNote = {Photosystem I (PSI) is the dominant photosystem in cyanobacteria and it plays a pivotal role in cyanobacterial metabolism. Despite its biological importance, the native organization of PSI in cyanobacterial thylakoid membranes is poorly understood. Here, we use atomic force microscopy (AFM) to show that ordered, extensive macromolecular arrays of PSI complexes are present in thylakoids from Thermosynechococcus elongatus, Synechococcus sp PCC 7002, and Synechocystis sp PCC 6803. Hyperspectral confocal fluorescence microscopy and three-dimensional structured illumination microscopy of Synechocystis sp PCC 6803 cells visualize PSI domains within the context of the complete thylakoid system. Crystallographic and AFM data were used to build a structural model of a membrane landscape comprising 96 PSI trimers and 27,648 chlorophyll a molecules. Rather than facilitating intertrimer energy transfer, the close associations between PSI primarily maximize packing efficiency; short-range interactions with Complex I and cytochrome b6f are excluded from these regions of the membrane, so PSI turnover is sustained by long-distance diffusion of the electron donors at the membrane surface. Elsewhere, PSI-photosystem II contact zones provide sites for docking phycobilisomes and the formation of megacomplexes. Finally, PSI-enriched domains in cyanobacteria might foreshadow the partitioning of PSI into stromal lamellae in plants, similarly sustained by long-distance diffusion of electron carriers.},
doi = {10.1105/tpc.17.00071},
journal = {The Plant Cell},
number = 5,
volume = 29,
place = {United States},
year = {Fri Mar 31 00:00:00 EDT 2017},
month = {Fri Mar 31 00:00:00 EDT 2017}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1105/tpc.17.00071

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Cited by: 48 works
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Figures / Tables:

Figure 1 Figure 1: AFM Imaging and Analysis of a Thylakoid Membrane Patch from T. elongatus That Contains Ordered Arrays of Trimeric Complexes. (A) AFM topograph of a membrane patch. (B)Zoom to a single complex, with the positions of three height profiles shown (red, pink, and green dashed lines), taken across themore » approximate positions of maximum height. (C) Height profiles corresponding to the lines in (B), with lateral distances shown. (D) Structure of the cytoplasmic face of the PSI complex taken from PDB:1JB0. The dashed yellow lines are drawn between proline 29 of the PsaC subunit on each monomer, shown in green, and represent a distance of 9.1 nm.« less

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