Photochemical conversion in oxygenic photosynthesis takes place in two large protein–pigment complexes named photosystem II and photosystem I (PSII and PSI, respectively). Photosystems associate with antennae in vivo to increase the size of photosynthetic units to hundreds or thousands of pigments. Regulation of the interactions between antennae and photosystems allows photosynthetic organisms to adapt to their environment. In low-iron environments, cyanobacteria express IsiA, a PSI antenna, critical to their survival. Here we describe the structure of the PSI–IsiA complex isolated from the mesophilic cyanobacterium Synechocystis sp. PCC 6803. This 2-MDa photosystem–antenna supercomplex structure reveals more than 700 pigments coordinated by 51 subunits, as well as the mechanisms facilitating the self-assembly and association of IsiA with multiple PSI assemblies.
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The final model (PDB 6NWA) and map (EMD 0524) were deposited in the Protein Databank and Electro-Magnetic Database, respectively. All other data are available from the authors upon reasonable request.
Dipole orientation values were calculated using an R script available from the author upon reasonable request.
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We would like to thank N. Nelson and P. Fromme for critical reading of the manuscript, and O. Rog for many discussions. We would like to acknowledge the use of the Titan Krios at the Erying Materials Center at Arizona State University, and the funding of this instrument by the National Science Foundation (No. MRI 1531991). This study is funded by a startup grant from Arizona State University.
The authors declare no competing interests.
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Integrated supplementary information
A. Sucrose gradients (10% – 60% sucrose) of IsiA-containing complexes showing that at our growth conditions there is one major fraction of PSI – IsiA. B. An SDS-PAGE gel showing the subunit composition of the main chlorophyll containing fraction from the first (I) and second (II) sucrose gradient showing the presence of IsiA. The same subunit composition is shown for the sample used for the cryo-EM experiments (Grid). C. Flow chart describing the workflow of image processing. D. A representative micrograph together with the power spectrum and CTF fit. In vitreous ice, PSI – IsiA particles are visible in different orientations as projections (a subset is surrounded by a red ring). E. Representative 2D class averages generated from unsupervised 2D classification. F. Top and side views, respectively, of the Euler angle distributions of particles obtained in the final refinement with C3 symmetry.
A, B, C and D: The final 3D map colored according to the local resolution estimates obtained from ResMap, seen from the Lumen ‘A’, Stroma ‘B’, membrane ‘C’ and membrane section with surface capping along the dashed line ‘D’ orientations. E. Plots of Fourier shell correlation (FSC) against resolution. F. Representative map sections showing transmembrane helices, carotenoids, chlorophylls and lipids from PSI – IsiA. The identity of each one is indicated above.
A. The orientation of IsiA monomers in PSI-IsiA. Only transmembrane segments are shown. Subunits are colored as in Fig. 1 in the main text. The six IsiA transmembrane helices are marked in position ‘a’. B. A detailed view of the E loop and two IsiA unique chlorophylls together with their coordinating residues, Gln 316 for chlorophyll 8 and the backbone carbonyl of Ile 282 for chlorophyll 17. C. The orientation of CP43 and D1 compared with that of the IsiA dimer. The figure shows the transmembrane helices of the respective subunits (labeled according to sequence position). D. Comparing the chlorophylls and carotenoids of IsiA and CP43 shows the position of two new chlorophylls (numbered 8 and 17) as well as a new carotenoid (B1) in addition to the three similar positions in CP43.