Structure of Dunaliella Photosystem II reveals conformational flexibility of stacked and unstacked supercomplexes

Abstract
Data availability
Article and author information
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Abstract

Photosystem II (PSII) generates an oxidant whose redox potential is high enough to enable water oxidation (Shen 2015; McEvoy and Brudvig 2006), a substrate so abundant that it assures a practically unlimited electron source for life on earth (Barber 2004). Our knowledge on the mechanism of water photooxidation was greatly advanced by high-resolution structures of prokaryotic PSII (Umena et al. 2011; Suga et al. 2019; Kato et al. 2021). Here we show high-resolution cryo-EM structures of eukaryotic PSII from the green alga Dunaliella salina at two distinct conformations. The conformers are also present in stacked PSII, exhibiting flexibility that may relevant to the grana formation in chloroplasts of the green lineage. CP29, one of PSII associated light-harvesting antennae, plays a major role in distinguishing the two conformations of the supercomplex. We also show that the stacked PSII dimer, a form suggested to support the organization of thylakoid membranes (Garab and Mustárdy 2000; Kirchhoff et al. 2007), can appear in many different orientations providing a flexible stacking mechanism for the arrangement of grana stacks in thylakoids. Our findings provide a structural basis for the heterogenous nature of the eukaryotic PSII on multiple levels.

Data availability

Data availability: The atomic coordinates have been deposited in the Protein Data Bank, with accession code 7PI0 (C2S2 COMP ), 7PI5 (C2S2 STR), 7PNK (C2S), 7PIN (stacked C2S2 COMP ) and 7PIW (stacked C2S2 STR ). The cryo-EM maps have been deposited in the Electron Microscopy Data Bank, with accession codes EMD-13429 (C2S2 COMP ), EMD-13430 (C2S2 STR ), EMD-13548 (C2S), EMD-13444 (stacked C2S2 COMP ) and EMD-13455 (stacked C2S2 STR ).

The following data sets were generated

1. Caspy I
2. Fadeeva M
3. Mazor Y
4. Nelson N
(2022) Unstacked compact Dunaliella PSII
PDB, 7PI0.

https://www.rcsb.org/structure/7PI0
1. Caspy I
2. Fadeeva M
3. Mazor Y
4. Nelson N
(2022) Unstacked compact Dunaliella PSII
EMDB, EMD-13429.

https://www.ebi.ac.uk/emdb/EMD-13429
1. Caspy I
2. Fadeeva M
3. Mazor Y
4. Nelson N
(2022) Unstacked stretched Dunaliella PSII
PDB, 7PI5.

https://www.rcsb.org/structure/7PI5
1. Caspy I
2. Fadeeva M
3. Mazor Y
4. Nelson N
(2022) Unstacked stretched Dunaliella PSII
EMDB, EMD-13430.

https://www.ebi.ac.uk/emdb/EMD-13430
1. Caspy I
2. Fadeeva M
3. Mazor Y
4. Nelson N
(2022) Unstacked compact Dunaliella PSII
PDB, 7PNK.

https://www.rcsb.org/structure/7PNK
1. Caspy I
2. Fadeeva M
3. Mazor Y
4. Nelson N
(2022) Unstacked compact Dunaliella PSII
EMDB, EMD-13548.

https://www.ebi.ac.uk/emdb/EMD-13548
1. Caspy I
2. Fadeeva M
3. Mazor Y
4. Nelson N
(2022) Stacked compact Dunaliella PSII
PDB, 7PIN.

https://www.rcsb.org/structure/7PIN
1. Caspy I
2. Fadeeva M
3. Mazor Y
4. Nelson N
(2022) Stacked compact Dunaliella PSII
EMDB, EMD-13444.

https://www.ebi.ac.uk/emdb/EMD-13444
1. Caspy I
2. Fadeeva M
3. Mazor Y
4. Nelson N
(2022) Stacked stretched Dunaliella PSII
PDB, 7PIW.

https://www.rcsb.org/structure/7PIW
1. Caspy I
2. Fadeeva M
3. Mazor Y
4. Nelson N
(2022) Stacked stretched Dunaliella PSII
EMDB, EMD-13455.

https://www.ebi.ac.uk/emdb/EMD-13455

Article and author information

Author details

Ido Caspy

Department of Biochemistry and Molecular Biology, Tel Aviv University, Tel Aviv, Israel

Competing interests
The authors declare that no competing interests exist.
Maria Fadeeva

Department of Biochemistry and Molecular Biology, Tel Aviv University, Tel Aviv, Israel

Competing interests
The authors declare that no competing interests exist.
Yuval Mazor

School of Molecular Sciences, Arizona State University, Tempe, United States

For correspondence
ymazor@asu.edu

Competing interests
The authors declare that no competing interests exist.
Nathan Nelson

Department of Biochemistry and Molecular Biology, Tel Aviv University, Tel Aviv, Israel

For correspondence
nelson@tauex.tau.ac.il

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0003-3588-7265

Funding

Israel Science Foundation (569/17)

Nathan Nelson

Israel Science Foundation (199/21)

Nathan Nelson

German-Israeli Foundation for Scientific Research and Development (G-1483-207/2018)

Nathan Nelson

National Science Foundation (2034021)

Yuval Mazor

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.