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 »
- Authors:
-
- Department of Molecular Biology and Biotechnology, University of Sheffield, Sheffield S10 2TN, United Kingdom
- 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
- Bioenergy and Defense Technologies Department, Sandia National Laboratories, Albuquerque, New Mexico 87185
- Division of Molecular Biosciences, Faculty of Natural Sciences, Imperial College London, London SW7 2AZ, United Kingdom
- 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}
}
https://doi.org/10.1105/tpc.17.00071
Web of Science