skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

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. Univ. of Sheffield (United Kingdom). Dept. of Molecular Biology and Biotechnology
  2. Univ. of Illinois, Urbana-Champaign, IL (United States). Beckman Inst. for Advanced Science and Technology, and Dept. of Physics
  3. Sandia National Lab. (SNL-NM), Albuquerque, NM (United States). Bioenergy and Defense Technologies Dept.
  4. Imperial College, London (United Kingdom). Division of Molecular Biosciences, Faculty of Natural Sciences
  5. Univ. of Illinois, Urbana-Champaign, IL (United States). Beckman Inst. for Advanced Science and Technology, and Center for Biophysics and Computational Biology, and Dept. of Physics
Publication Date:
Research Org.:
Sandia National Lab. (SNL-NM), Albuquerque, NM (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22); USDOE National Nuclear Security Administration (NNSA)
OSTI Identifier:
1429809
Report Number(s):
SAND-2017-7776J
Journal ID: ISSN 1040-4651; 655583
Grant/Contract Number:
AC04-94AL85000; SC0001035; MCB1157615; PHY0822613; P41GM104601; 5R01GM09824302
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Plant Cell
Additional Journal Information:
Journal Volume: 29; Journal Issue: 5; Journal ID: ISSN 1040-4651
Publisher:
American Society of Plant Biologists
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. 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, and Hunter, C. Neil. Fri . "Lateral Segregation of Photosystem I in Cyanobacterial Thylakoids". United States. doi:10.1105/tpc.17.00071. https://www.osti.gov/servlets/purl/1429809.
@article{osti_1429809,
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 = {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

Citation Metrics:
Cited by: 2works
Citation information provided by
Web of Science

Save / Share: