The photosystem I supercomplex from a primordial green alga Ostreococcus tauri harbors three light-harvesting complex trimers

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Abstract

As a ubiquitous picophytoplankton in the ocean and an early-branching green alga, Ostreococcus tauri is a model prasinophyte species for studying the functional evolution of the light-harvesting systems in photosynthesis. Here, we report the structure and function of the O. tauri photosystem I (PSI) supercomplex in low light conditions, where it expands its photon-absorbing capacity by assembling with the light-harvesting complexes I (LHCI) and a prasinophyte-specific light-harvesting complex (Lhcp). The architecture of the supercomplex exhibits hybrid features of the plant-type and the green algal-type PSI supercomplexes, consisting of a PSI core, a Lhca1-Lhca4-Lhca2-Lhca3 belt attached on one side and a Lhca5-Lhca6 heterodimer associated on the other side between PsaG and PsaH. Interestingly, nine Lhcp subunits, including one Lhcp1 monomer with a phosphorylated amino-terminal threonine and eight Lhcp2 monomers, oligomerize into three trimers and associate with PSI on the third side between Lhca6 and PsaK. The Lhcp1 phosphorylation and the light-harvesting capacity of PSI were subjected to reversible photoacclimation, suggesting that the formation of OtPSI-LHCI-Lhcp supercomplex is likely due to a phosphorylation-dependent mechanism induced by changes in light intensity. Notably, this supercomplex did not exhibit far-red peaks in the 77 K fluorescence spectra, which is possibly due to the weak coupling of the chlorophyll a603-a609 pair in OtLhca1-4.

Data availability

The atomic coordinates of the OtPSI-LHCI-Lhcp supercomplex have been deposited in the Protein Data Bank (PDB) with accession code 7YCA. The cryo-EM map of the supercomplex has been deposited in the Electron Microscopy Data Bank (EMDB) with accession code EMD-33737. The local maps and corresponding models of the three individual Lhcp trimers have also been deposited in the EMDB and PDB under accession codes of EMD-34733 and 8HG3, EMD-34735 and 8HG5, EMD-34736 and 8HG6.

The following data sets were generated

1. Shan J
2. Sheng X
3. Ishii A
4. Watanabe A
5. Song C
6. Murata K
7. Minagawa J
8. Liu Z
(2022) Cryo-EM structure of the PSI-LHCI-Lhcp supercomplex from Ostreococcus tauri
Protein Data Bank, 7YCA.

https://cdn.elifesciences.org/articles/84488/https:www.rcsb.org/structure/7YCA
1. Shan J
2. Sheng X
3. Ishii A
4. Watanabe A
5. Song C
6. Murata K
7. Minagawa J
8. Liu Z
(2023) Cryo-EM structure of the Lhcp complex from Ostreococcus tauri
Protein Data Bank, 8HG3.

https://www.rcsb.org/structure/8HG3
1. Shan J
2. Sheng X
3. Ishii A
4. Watanabe A
5. Song C
6. Murata K
7. Minagawa J
8. Liu Z
(2023) Cryo-EM structure of the prasinophyte-specific light-harvesting complex (Lhcp)from Ostreococcus tauri
Protein Data Bank, 8HG5.

https://www.rcsb.org/structure/8HG5
1. Shan J
2. Sheng X
3. Ishii A
4. Watanabe A
5. Song C
6. Murata K
7. Minagawa J
8. Liu Z
(2023) Cryo-EM structure of the prasinophyte-specific light-harvesting complex (Lhcp)from Ostreococcus tauri
Protein Data Bank, 8HG6.

https://www.rcsb.org/structure/8HG6
1. Shan J
2. Sheng X
3. Ishii A
4. Watanabe A
5. Song C
6. Murata K
7. Minagawa J
8. Liu Z
(2022) Cryo-EM structure of the PSI-LHCI-Lhcp supercomplex from Ostreococcus tauri
Electron Microscopy Data Bank, EMD-33737.

https://www.ebi.ac.uk/emdb/EMD-33737
1. Shan J
2. Sheng X
3. Ishii A
4. Watanabe A
5. Song C
6. Murata K
7. Minagawa J
8. Liu Z
(2023) Cryo-EM structure of the Lhcp complex from Ostreococcus tauri
Electron Microscopy Data Bank, EMD-34733.

https://www.ebi.ac.uk/emdb/EMD-34733
1. Shan J
2. Sheng X
3. Ishii A
4. Watanabe A
5. Song C
6. Murata K
7. Minagawa J
8. Liu Z
(2023) Cryo-EM structure of the prasinophyte-specific light-harvesting complex (Lhcp)from Ostreococcus tauri
Electron Microscopy Data Bank, EMD-34735.

https://www.ebi.ac.uk/emdb/EMD-34735
1. Shan J
2. Sheng X
3. Ishii A
4. Watanabe A
5. Song C
6. Murata K
7. Minagawa J
8. Liu Z
(2023) Cryo-EM structure of the prasinophyte-specific light-harvesting complex (Lhcp)from Ostreococcus tauri
Electron Microscopy Data Bank, EMD-34736.

https://www.ebi.ac.uk/emdb/EMD-34736

Article and author information

Author details

Asako Ishii

Division of Environmental Photobiology, National Institute for Basic Biology, Okazaki, Japan

Competing interests
No competing interests declared.
Jianyu Shan

National Laboratory of Biomacromolecules, Chinese Academy of Sciences, Beijing, China

Competing interests
No competing interests declared.
Xin Sheng

National Laboratory of Biomacromolecules, Chinese Academy of Sciences, Beijing, China

Competing interests
Xin Sheng, is affiliated with Shenzhen Jingtai Technology Co. Ltd. The author has no financial interests to declare.
Eunchul Kim

Division of Environmental Photobiology, National Institute for Basic Biology, Okazaki, Japan

Competing interests
No competing interests declared.
Akimasa Watanabe

Division of Environmental Photobiology, National Institute for Basic Biology, Okazaki, Japan

Competing interests
No competing interests declared.

"This ORCID iD identifies the author of this article:" 0000-0001-6068-1328
Makio Yokono

Division of Environmental Photobiology, National Institute for Basic Biology, Okazaki, Japan

Competing interests
No competing interests declared.
Chiyo Noda

Division of Environmental Photobiology, National Institute for Basic Biology, Okazaki, Japan

Competing interests
No competing interests declared.
Chihong Song

National Institute for Physiological Sciences, National Institutes of Natural Sciences, Okazaki, Japan

Competing interests
No competing interests declared.
Kazuyoshi Murata

National Institute for Physiological Sciences, National Institutes of Natural Sciences, Okazaki, Japan

Competing interests
No competing interests declared.

"This ORCID iD identifies the author of this article:" 0000-0001-9446-3652
Zhenfeng Liu

Institute of Biophysics, Chinese Academy of Sciences, Beijing, China

For correspondence
liuzf@ibp.ac.cn

Competing interests
No competing interests declared.

"This ORCID iD identifies the author of this article:" 0000-0001-5502-9474
Jun Minagawa

Division of Environmental Photobiology, National Institute for Basic Biology, Okazaki, Japan

For correspondence
minagawa@nibb.ac.jp

Competing interests
No competing interests declared.

"This ORCID iD identifies the author of this article:" 0000-0002-3028-3203

Funding

Japan Society for the Promotion of Science (21H04778)

Jun Minagawa

Japan Society for the Promotion of Science (21H05040)

Jun Minagawa

National Natural Science Foundation of China (31925024)

Zhenfeng Liu

Chinese Academy of Sciences (XDB37020101)

Zhenfeng Liu

Chinese Academy of Sciences (YSBR-015)

Zhenfeng Liu

National Key Research and Development Program of China (2017YFA0503702)

Zhenfeng Liu

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

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