Craig MacGregor-Chatwin, Melih Sener, Samuel F.H. Barnett, Andrew Hitchcock,
Meghan C. Barnhart-Dailey, Karim Maghlaoui, James Barber, Jerilyn A. Timlin,
Klaus Schulten, and C. Neil Hunter.
Lateral segregation of Photosystem I in cyanobacterial
thylakoid.
Plant Cell, 29:1119-1136, 2017.
(PMC: PMC5466035)
MACG2017
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. 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.
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