Structure of Dunaliella photosystem II reveals conformational flexibility of stacked and unstacked supercomplexes
- Department of Biochemistry and Molecular Biology, The George S. Wise Faculty of Life Sciences, Tel Aviv University, Israel
- School of Molecular Sciences, Arizona State University, United States
- Biodesign Center for Applied Structural Discovery, Arizona State University, United States
Figures
Figure 1 with 9 supplements
Two conformations of the eukaryotic photosystem II (PSII).
(a) Overall view of the PSII C2S2 map in the compact conformation. One asymmetric unit is coloured in green, and in the other, each chain is coloured individually. PSII is shown from a luminal view …
Figure 1—figure supplement 1
Cryo-EM data collection and processing scheme for unstacked and stacked photosystem II (PSII) complexes.
(a) Sample micrograph collected for the Dunaliella PSII dataset displaying stacked and unstacked PSII particles from multiple views. (b) 2D classes showing stacked and unstacked PSII complexes. (c) …
Figure 1—figure supplement 2
Local resolution and Fourier shell correlation (FSC) of Dunaliella photosystem II (PSII) supercomplexes.
C2S2 local resolution (a) and FSC (b). C2S2 compact local resolution (c) and FSC (d). C2S2 stretched local resolution (e) and FSC (f). C2S local resolution (g) and FSC (h). Stacked C2S2 compact …
Figure 1—figure supplement 3
Map densities of unstacked Dunaliella photosystem II (PSII).
(a) PSII reaction centre chlorophylls (Chls), pheophytins, and quinone. Cryo-EM map shown in panels a–h at is contoured at 4σ unless mentioned otherwise. (b) Cytochrome b559 heme, alpha, and beta …
Figure 1—figure supplement 4
Comparing CP29STR and CP29COMP.
(a and b) CP29STR and CP29COMP backbone, side chains and carotenes, coloured according to their b-factor values, displaying a similar distribution of b-factors in both conformations. (c and d) CP29ST…
Figure 1—figure supplement 5
Comparing CP29 positions between Dunaliella and Chlamydomonas reinhardtii (Cr).
Photosystem II (PSII) from Cr is shown as a molecular surface coloured orange and was superposed on PSIICOMP and PSIISTR using the core subunits (grey tubes). The different orientations of CP29 are …
Figure 1—figure supplement 6
Principal component (PC) analysis of C2S2COMP.
(a) Percent of the variance explained by each of the 12 PCs. (b) The particle distribution along the first six PCs shows continuous heterogeneity in the C2S2COMP. States 1 and 10 are marked with a …
Figure 1—figure supplement 7
Principal component (PC) analysis of C2S2STR.
(a) Percent of the variance explained by each of the 12 PCs. (b) The particle distribution along the first six PCs shows continuous heterogeneity in the C2S2STR. States 1 and 10 are marked with a …
Figure 1—figure supplement 8
Changes in CP29 chlorophyll (Chl) positions between C2S2COMP and C2S2STR.
Several CP29 Chl molecules in C2S2STR are positioned close to light-harvesting complex II (LHCII) and can mediate faster excitation energy transfer (EET) from LHCII to photosystem II (PSII), whereas …
Figure 1—figure supplement 9
Sucrose gradient and sodium dodecyl sulfate–polyacrylamide gel electrophoresis (SDS-PAGE) of Dunaliella photosystem II (PSII) preparation.
(a) Sucrose density gradient of the final Dunaliella PSII preparation. The three fractions collected are marked As, Bs, and Cs. The Bs fraction was used for cryo-EM data collection. (b) SDS-PAGE of …
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Figure 1—figure supplement 9—source data 1
Uncropped gel image of Figure 1—figure supplement 9b.
- https://cdn.elifesciences.org/articles/81150/elife-81150-fig1-figsupp9-data1-v2.pptx
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Figure 1—figure supplement 9—source data 2
Oxygen evolution activity from Figure 1—figure supplement 9c in excel format.
- https://cdn.elifesciences.org/articles/81150/elife-81150-fig1-figsupp9-data2-v2.xlsx
Figure 2
Heterogeneity within photosystem II (PSII) states.
(a) Continuous heterogeneity of C2S2COMP particles distribution along the third principal component (PC) axis. Each PC was divided into 10 states separated by 9% of the particle population along the …
Figure 3 with 2 supplements
Water distribution and channels in eukaryotic photosystem II (PSII).
(a) Water molecules distribution in Dunaliella C2S2COMP structure. The protein scaffold is coloured grey, and water molecules are shown as red spheres. (b) Water molecules distribution in Dunaliella …
Figure 3—figure supplement 1
Sequence alignment of the hydrophobic residues lining the large channel cavity near oxygen-evolving complex (OEC).
(a) Alignment of D1 C-terminus domain, residues 323–344. The hydrophobic residues are marked with black rectangles, together with their conservation score. The organisms used for alignment in panels …
Figure 3—figure supplement 2
Na+ ion and post-translational modifications (PTMs) in Dunaliella photosystem II (PSII).
(a) Na+ binding site close to the oxygen-evolving complex (OEC). The Na+ ion is coordinated by D1 histidine 337, the backbone carbonyls of D1 glutamic acid 333, arginine 334, D2 asparagine 350, and …
Figure 4 with 5 supplements
Heterogeneity, electrostatic interactions, and model for photosystem II (PSII) stacking.
(a) Stacked Dunaliella PSII C2S2COMP maps, and the masks used for multibody refinement. Maps are coloured magenta and grey and masks in green and red. (b) The particle distribution along the first …
Figure 4—figure supplement 1
Principal component (PC) analysis of stacked C2S2COMP.
(a) Percent of the variance explained by each of the 12 PCs. (b) The particle distribution along the first six PCs shows continuous heterogeneity in the C2S2COMP. States 1 and 10 are marked with a …
Figure 4—figure supplement 2
Principal component (PC) analysis of stacked C2S2STR.
(a) Percent of the variance explained by each of the 12 PCs. (b) The particle distribution along the first six PCs shows continuous heterogeneity in the C2S2STR. States 1 and 10 are marked with a …
Figure 4—figure supplement 3
Stromal interactions between photosystem II (PSII) subunits in the stacked configurations.
(a) Structure of stacked Dunaliella C2S2COMP showing a shift in position of each PSII dimer. The region where PSII core subunits are nearest is marked with a blue rectangle. (b) Zoom-in on the …
Figure 4—figure supplement 4
Similar membrane separation in purified and in-vivo detected stacked photosystem II (PSII) complexes.
Panels a, b, and c show Figure 1D from Wietrzynski et al. showing appressed thylakoid membranes in a native state. The stacked PSII dimer (PDBID 7PIN) was back-projected onto the tomogram and is …
Figure 4—figure supplement 5
Light-harvesting complex (LHC) interactions limit stacked photosystem II (PSII) rotation.
(a) In stacked C2S2COMP (right), the rotation is confined by LHCII M3 in state 1 (magenta) and 10 (teal). In both conformations, the rotation extends from LHCII M2 (state 1) to CP26 (state 10), …
Videos
Video 1
Different conformations of Dunaliella C2S2 photosystem II (PSII).
Morph showing the transition from the stretched (magenta) to the compact (green) conformation from a luminal view.
Video 2
Different conformations of Dunaliella C2S2 photosystem II (PSII).
Morph showing the transition from the stretched (magenta) to the compact (green) conformation from a membrane plane view.
Video 3
Continuous heterogeneity in C2S2COMP PC1.
Transition between all states in C2S2COMP (green) PC1 from a luminal view, showing photosystem II (PSII) monomers change in location and orientation along the intermonomer space.
Video 4
Continuous heterogeneity in C2S2COMP PC3.
Transition between all states in C2S2COMP (green) PC3 from a membrane plane view, showing photosystem II (PSII) monomers change in location and orientation along the membrane plane.
Video 5
Continuous heterogeneity in C2S2STR PC1.
Transition between all states in C2S2STR (magenta) PC1 from a luminal view, showing photosystem II (PSII) monomers change in location and orientation along the intermonomer space.
Video 6
Continuous heterogeneity in C2S2STR PC2.
Transition between all states in C2S2STR (magenta) PC2 from a membrane plane view, showing photosystem II (PSII) monomers change in location and orientation along the membrane plane.
Video 7
Continuous heterogeneity in stacked C2S2COMP PC1.
Transition between all states in stacked C2S2COMP (orchid) PC1 from a luminal view, showing the rotation of the upper photosystem II (PSII) dimer compared to the lower dimer.
Video 8
Continuous heterogeneity in stacked C2S2COMP PC2.
Transition between all states in stacked C2S2COMP (orchid) PC2 from a membrane plane view, showing upper photosystem II (PSII) dimer tilting to and from the lower dimer.
Video 9
Continuous heterogeneity in stacked C2S2STR PC1.
Transition between all states in stacked C2S2STR (red) PC1 from a luminal view, showing the rotation of the upper photosystem II (PSII) dimer compared to the lower dimer.
Video 10
Continuous heterogeneity in stacked C2S2STR PC2.
Transition between all states in stacked C2S2STR (red) PC2 from a membrane plane view, showing upper photosystem II (PSII) dimer tilting to and from the lower dimer.
Additional files
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Supplementary file 1
Cryo-EM data collection, refinement, and validation statistics.
- https://cdn.elifesciences.org/articles/81150/elife-81150-supp1-v2.docx
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Supplementary file 2
CP29 chlorophyll composition determined in previous work.
- https://cdn.elifesciences.org/articles/81150/elife-81150-supp2-v2.docx
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Supplementary file 3
Changes in location of CP29 chlorophylls in the compact and stretched conformations principal components (PCs).
Shift in chlorophyll position between states 1 and 10 in the first three PCs of the compact (Comp) and stretched (Str) unstacked PSII. Distances are in Å. The average shift and SD are presented for each component.
- https://cdn.elifesciences.org/articles/81150/elife-81150-supp3-v2.docx
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MDAR checklist
- https://cdn.elifesciences.org/articles/81150/elife-81150-mdarchecklist1-v2.docx
