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A structure of the relict phycobilisome from a thylakoid-free cyanobacterium

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Listed:
  • Han-Wei Jiang

    (National Taiwan University)

  • Hsiang-Yi Wu

    (Academia Sinica)

  • Chun-Hsiung Wang

    (Academia Sinica)

  • Cheng-Han Yang

    (Academia Sinica)

  • Jui-Tse Ko

    (National Taiwan University)

  • Han-Chen Ho

    (Tzu Chi University)

  • Ming-Daw Tsai

    (Academia Sinica
    National Taiwan University)

  • Donald A. Bryant

    (The Pennsylvania State University)

  • Fay-Wei Li

    (Boyce Thompson Institute
    Cornell University)

  • Meng-Chiao Ho

    (Academia Sinica
    National Taiwan University
    National Taiwan University)

  • Ming-Yang Ho

    (National Taiwan University
    National Taiwan University)

Abstract

Phycobilisomes (PBS) are antenna megacomplexes that transfer energy to photosystems II and I in thylakoids. PBS likely evolved from a basic, inefficient form into the predominant hemidiscoidal shape with radiating peripheral rods. However, it has been challenging to test this hypothesis because ancestral species are generally inaccessible. Here we use spectroscopy and cryo-electron microscopy to reveal a structure of a “paddle-shaped” PBS from a thylakoid-free cyanobacterium that likely retains ancestral traits. This PBS lacks rods and specialized ApcD and ApcF subunits, indicating relict characteristics. Other features include linkers connecting two chains of five phycocyanin hexamers (CpcN) and two core subdomains (ApcH), resulting in a paddle-shaped configuration. Energy transfer calculations demonstrate that chains are less efficient than rods. These features may nevertheless have increased light absorption by elongating PBS before multilayered thylakoids with hemidiscoidal PBS evolved. Our results provide insights into the evolution and diversification of light-harvesting strategies before the origin of thylakoids.

Suggested Citation

  • Han-Wei Jiang & Hsiang-Yi Wu & Chun-Hsiung Wang & Cheng-Han Yang & Jui-Tse Ko & Han-Chen Ho & Ming-Daw Tsai & Donald A. Bryant & Fay-Wei Li & Meng-Chiao Ho & Ming-Yang Ho, 2023. "A structure of the relict phycobilisome from a thylakoid-free cyanobacterium," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43646-9
    DOI: 10.1038/s41467-023-43646-9
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    References listed on IDEAS

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    1. Kathryn Tunyasuvunakool & Jonas Adler & Zachary Wu & Tim Green & Michal Zielinski & Augustin Žídek & Alex Bridgland & Andrew Cowie & Clemens Meyer & Agata Laydon & Sameer Velankar & Gerard J. Kleywegt, 2021. "Highly accurate protein structure prediction for the human proteome," Nature, Nature, vol. 596(7873), pages 590-596, August.
    2. Jianfei Ma & Xin You & Shan Sun & Xiaoxiao Wang & Song Qin & Sen-Fang Sui, 2020. "Structural basis of energy transfer in Porphyridium purpureum phycobilisome," Nature, Nature, vol. 579(7797), pages 146-151, March.
    3. Lvqin Zheng & Zhenggao Zheng & Xiying Li & Guopeng Wang & Kun Zhang & Peijun Wei & Jindong Zhao & Ning Gao, 2021. "Structural insight into the mechanism of energy transfer in cyanobacterial phycobilisomes," Nature Communications, Nature, vol. 12(1), pages 1-11, December.
    4. Jun Zhang & Jianfei Ma & Desheng Liu & Song Qin & Shan Sun & Jindong Zhao & Sen-Fang Sui, 2017. "Structure of phycobilisome from the red alga Griffithsia pacifica," Nature, Nature, vol. 551(7678), pages 57-63, November.
    5. Lvqin Zheng & Zhengdong Zhang & Hongrui Wang & Zhenggao Zheng & Jiayu Wang & Heyuan Liu & Hailong Chen & Chunxia Dong & Guopeng Wang & Yuxiang Weng & Ning Gao & Jindong Zhao, 2023. "Cryo-EM and femtosecond spectroscopic studies provide mechanistic insight into the energy transfer in CpcL-phycobilisomes," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    6. John Jumper & Richard Evans & Alexander Pritzel & Tim Green & Michael Figurnov & Olaf Ronneberger & Kathryn Tunyasuvunakool & Russ Bates & Augustin Žídek & Anna Potapenko & Alex Bridgland & Clemens Me, 2021. "Highly accurate protein structure prediction with AlphaFold," Nature, Nature, vol. 596(7873), pages 583-589, August.
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