Structures of PSI-FCPI from Thalassiosira pseudonana grown under high light provide evidence for convergent evolution and light-adaptive strategies in diatom FCPIs

doi:10.1111/jipb.13816

J Integr Plant Biol. ›› 2025, Vol. 67 ›› Issue (4): 949-966.DOI: 10.1111/jipb.13816

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Structures of PSI-FCPI from Thalassiosira pseudonana grown under high light provide evidence for convergent evolution and light-adaptive strategies in diatom FCPIs

Yue Feng^1,2†, Zhenhua Li^1,2†, Yang Yang^1,3, Lili Shen^1,2, Xiaoyi Li^1,4, Xueyang Liu^1,2, Xiaofei Zhang⁵, Jinyang Zhang^1,2, Fei Ren^1,2, Yuan Wang^1,2, Cheng Liu^1,4,6, Guangye Han^1,4, Xuchu Wang^3,7, Tingyun Kuang^1,4, Jian-Ren Shen^1,8,*, Wenda Wang^1,4,6,*

1. Key Laboratory of Photobiology, Photosynthesis Research Center, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China;
2. University of Chinese Academy of Sciences, Beijing 100049, China;
3. Laboratory for Ecology of Tropical Islands, Ministry of Education, College of Life Sciences, Hainan Normal University, Haikou 571158, China;
4. China National Botanical Garden, Beijing 100093, China;
5. Department of Chemistry and Center of Artificial Photosynthesis for Solar Fuels, School of Science, Westlake University, Hangzhou, Zhejiang 310024, China;
6. Academician Workstation of Agricultural High-Tech Industrial Area of the Yellow River Delta, National Center of Technology Innovation for Comprehensive Utilization of Saline-Alkali Land, Dongying 257300, China;
7. Key Laboratory of Plant Resources Conservation and Germplasm Innovation in Mountainous Region, Ministry of Education, College of Life Sciences, Guizhou University, Guiyang 550025, China;
8. Research Institute for Interdisciplinary Science, Graduate School of Environmental, Life, Natural Science and Technology, Okayama University, Okayama 700-8530, Japan

Received:2024-06-16 Accepted:2024-11-15 Online:2024-12-13 Published:2025-04-01
Contact: *Jian-Ren Shen (shen@cc.okayama-u.ac.jp); Wenda Wang (wdwang@ibcas.ac.cn, Dr. Wang is fully responsible for the distribution of all materials associated with this article)
About author:^†These authors contributed equally to this work.
Supported by:
National Key R&D Program of China (2021YFA1300403), the Youth Innovation Promotion Association of CAS (2020081), the CAS Project for Young Scientists in Basic Research (YSBR-093), the National Natural Science Foundation of China (32222007), the Innovation Platform for Academicians of Hainan Province (2022YSCXTD0005), and the Science & Technology Specific Project in Agricultural High-Tech Industrial Demonstration Area of the Yellow River Delta (2022SZX12).

Abstract

Abstract: Diatoms rely on fucoxanthin chlorophyll a/c-binding proteins (FCPs) for light harvesting and energy quenching under marine environments. Here we report two cryo-electron microscopic structures of photosystem I (PSI) with either 13 or five fucoxanthin chlorophyll a/c-binding protein Is (FCPIs) at 2.78 and 3.20 Å resolutions from Thalassiosira pseudonana grown under high light (HL) conditions. Among them, five FCPIs are stably associated with the PSI core, these include Lhcr3, RedCAP, Lhcq8, Lhcf10, and FCP3. The eight additional Lhcr-type FCPIs are loosely associated with the PSI core and detached under the present purification conditions. The pigments of this centric diatom showed a higher proportion of chlorophylls a, diadinoxanthins, and diatoxanthins; some of the chlorophyll as and diadinoxanthins occupy the locations of fucoxanthins found in the huge PSI-FCPI from another centric diatom Chaetoceros gracilis grown under low-light conditions. These additional chlorophyll as may form more energy transfer pathways and additional diadinoxanthins may form more energy dissipation sites relying on the diadinoxanthin-diatoxanthin cycle. These results reveal the assembly mechanism of FCPIs and corresponding light-adaptive strategies of T. pseudonana PSI-FCPI, as well as the convergent evolution of the diatom PSI-FCPI structures.

Key words: cryo-EM, diatom, FCPI, light-adaptive strategies, photosynthesis, PSI

Yue Feng, Zhenhua Li, Yang Yang, Lili Shen, Xiaoyi Li, Xueyang Liu, Xiaofei Zhang, Jinyang Zhang, Fei Ren, Yuan Wang, Cheng Liu, Guangye Han, Xuchu Wang, Tingyun Kuang, Jian-Ren Shen, Wenda Wang. Structures of PSI-FCPI from Thalassiosira pseudonana grown under high light provide evidence for convergent evolution and light-adaptive strategies in diatom FCPIs[J]. J Integr Plant Biol., 2025, 67(4): 949-966.

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Structures of PSI-FCPI from Thalassiosira pseudonana grown under high light provide evidence for convergent evolution and light-adaptive strategies in diatom FCPIs

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