IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-40388-6.html
   My bibliography  Save this article

The Ycf48 accessory factor occupies the site of the oxygen-evolving manganese cluster during photosystem II biogenesis

Author

Listed:
  • Ziyu Zhao

    (S. Kensington Campus)

  • Irene Vercellino

    (Institute of Science and Technology Austria
    Forschungszentrum Jülich GmbH, Wilhelm-Johnen-Straße)

  • Jana Knoppová

    (Academy of Sciences of the Czech Republic, Opatovický mlýn)

  • Roman Sobotka

    (Academy of Sciences of the Czech Republic, Opatovický mlýn
    University of South Bohemia)

  • James W. Murray

    (S. Kensington Campus)

  • Peter J. Nixon

    (S. Kensington Campus)

  • Leonid A. Sazanov

    (Institute of Science and Technology Austria)

  • Josef Komenda

    (Academy of Sciences of the Czech Republic, Opatovický mlýn
    University of South Bohemia)

Abstract

Robust oxygenic photosynthesis requires a suite of accessory factors to ensure efficient assembly and repair of the oxygen-evolving photosystem two (PSII) complex. The highly conserved Ycf48 assembly factor binds to the newly synthesized D1 reaction center polypeptide and promotes the initial steps of PSII assembly, but its binding site is unclear. Here we use cryo-electron microscopy to determine the structure of a cyanobacterial PSII D1/D2 reaction center assembly complex with Ycf48 attached. Ycf48, a 7-bladed beta propeller, binds to the amino-acid residues of D1 that ultimately ligate the water-oxidising Mn4CaO5 cluster, thereby preventing the premature binding of Mn2+ and Ca2+ ions and protecting the site from damage. Interactions with D2 help explain how Ycf48 promotes assembly of the D1/D2 complex. Overall, our work provides valuable insights into the early stages of PSII assembly and the structural changes that create the binding site for the Mn4CaO5 cluster.

Suggested Citation

  • Ziyu Zhao & Irene Vercellino & Jana Knoppová & Roman Sobotka & James W. Murray & Peter J. Nixon & Leonid A. Sazanov & Josef Komenda, 2023. "The Ycf48 accessory factor occupies the site of the oxygen-evolving manganese cluster during photosystem II biogenesis," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-40388-6
    DOI: 10.1038/s41467-023-40388-6
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-40388-6
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-40388-6?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Yasufumi Umena & Keisuke Kawakami & Jian-Ren Shen & Nobuo Kamiya, 2011. "Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å," Nature, Nature, vol. 473(7345), pages 55-60, May.
    2. Koji Kato & Ryo Nagao & Tian-Yi Jiang & Yoshifumi Ueno & Makio Yokono & Siu Kit Chan & Mai Watanabe & Masahiko Ikeuchi & Jian-Ren Shen & Seiji Akimoto & Naoyuki Miyazaki & Fusamichi Akita, 2019. "Structure of a cyanobacterial photosystem I tetramer revealed by cryo-electron microscopy," Nature Communications, Nature, vol. 10(1), pages 1-9, December.
    3. Rana Hussein & Mohamed Ibrahim & Asmit Bhowmick & Philipp S. Simon & Ruchira Chatterjee & Louise Lassalle & Margaret Doyle & Isabel Bogacz & In-Sik Kim & Mun Hon Cheah & Sheraz Gul & Casper Lichtenber, 2021. "Structural dynamics in the water and proton channels of photosystem II during the S2 to S3 transition," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
    4. Patrick Jordan & Petra Fromme & Horst Tobias Witt & Olaf Klukas & Wolfram Saenger & Norbert Krauß, 2001. "Three-dimensional structure of cyanobacterial photosystem I at 2.5 Å resolution," Nature, Nature, vol. 411(6840), pages 909-917, June.
    5. Petko Chernev & Sophie Fischer & Jutta Hoffmann & Nicholas Oliver & Ricardo Assunção & Boram Yu & Robert L. Burnap & Ivelina Zaharieva & Dennis J. Nürnberg & Michael Haumann & Holger Dau, 2020. "Light-driven formation of manganese oxide by today’s photosystem II supports evolutionarily ancient manganese-oxidizing photosynthesis," Nature Communications, Nature, vol. 11(1), pages 1-10, December.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. Lin Zhang & Junxiang Ruan & Fudan Gao & Qiang Xin & Li-Ping Che & Lujuan Cai & Zekun Liu & Mengmeng Kong & Jean-David Rochaix & Hualing Mi & Lianwei Peng, 2024. "Thylakoid protein FPB1 synergistically cooperates with PAM68 to promote CP47 biogenesis and Photosystem II assembly," Nature Communications, Nature, vol. 15(1), pages 1-17, December.

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Ryo Nagao & Koji Kato & Tasuku Hamaguchi & Yoshifumi Ueno & Naoki Tsuboshita & Shota Shimizu & Miyu Furutani & Shigeki Ehira & Yoshiki Nakajima & Keisuke Kawakami & Takehiro Suzuki & Naoshi Dohmae & S, 2023. "Structure of a monomeric photosystem I core associated with iron-stress-induced-A proteins from Anabaena sp. PCC 7120," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    2. Koji Kato & Ryo Nagao & Yoshifumi Ueno & Makio Yokono & Takehiro Suzuki & Tian-Yi Jiang & Naoshi Dohmae & Fusamichi Akita & Seiji Akimoto & Naoyuki Miyazaki & Jian-Ren Shen, 2022. "Structure of a tetrameric photosystem I from a glaucophyte alga Cyanophora paradoxa," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    3. Shishang Dong & Guoqiang Huang & Changhui Wang & Jiajia Wang & Sen-Fang Sui & Xiaochun Qin, 2022. "Structure of the Acidobacteria homodimeric reaction center bound with cytochrome c," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    4. Futing Zhang & Zuozhu Wen & Shanlin Wang & Weiyi Tang & Ya-Wei Luo & Sven A. Kranz & Haizheng Hong & Dalin Shi, 2022. "Phosphate limitation intensifies negative effects of ocean acidification on globally important nitrogen fixing cyanobacterium," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    5. Shivam Yadav & Martin Centola & Mathilda Glaesmann & Denys Pogoryelov & Roman Ladig & Mike Heilemann & L. C. Rai & Özkan Yildiz & Enrico Schleiff, 2022. "Cyclophilin anaCyp40 regulates photosystem assembly and phycobilisome association in a cyanobacterium," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    6. Ryan Puskar & Chloe Truong & Kyle Swain & Saborni Chowdhury & Ka-Yi Chan & Shan Li & Kai-Wen Cheng & Ting Yu Wang & Yu-Ping Poh & Yuval Mazor & Haijun Liu & Tsui-Fen Chou & Brent L. Nannenga & Po-Lin , 2022. "Molecular asymmetry of a photosynthetic supercomplex from green sulfur bacteria," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    7. Rana Hussein & Mohamed Ibrahim & Asmit Bhowmick & Philipp S. Simon & Ruchira Chatterjee & Louise Lassalle & Margaret Doyle & Isabel Bogacz & In-Sik Kim & Mun Hon Cheah & Sheraz Gul & Casper Lichtenber, 2021. "Structural dynamics in the water and proton channels of photosystem II during the S2 to S3 transition," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
    8. Lin Zhang & Junxiang Ruan & Fudan Gao & Qiang Xin & Li-Ping Che & Lujuan Cai & Zekun Liu & Mengmeng Kong & Jean-David Rochaix & Hualing Mi & Lianwei Peng, 2024. "Thylakoid protein FPB1 synergistically cooperates with PAM68 to promote CP47 biogenesis and Photosystem II assembly," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    9. Yu Guo & Lanlan He & Yunxuan Ding & Lars Kloo & Dimitrios A. Pantazis & Johannes Messinger & Licheng Sun, 2024. "Closing Kok’s cycle of nature’s water oxidation catalysis," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    10. Xuelei Pan & Mengyu Yan & Qian Liu & Xunbiao Zhou & Xiaobin Liao & Congli Sun & Jiexin Zhu & Callum McAleese & Pierre Couture & Matthew K. Sharpe & Richard Smith & Nianhua Peng & Jonathan England & Sh, 2024. "Electric-field-assisted proton coupling enhanced oxygen evolution reaction," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    11. Zhiyuan Mao & Xingyue Li & Zhenhua Li & Liangliang Shen & Xiaoyi Li & Yanyan Yang & Wenda Wang & Tingyun Kuang & Jian-Ren Shen & Guangye Han, 2024. "Structure and distinct supramolecular organization of a PSII-ACPII dimer from a cryptophyte alga Chroomonas placoidea," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    12. Xing Zhang & Yanan Xiao & Xin You & Shan Sun & Sen-Fang Sui, 2024. "In situ structural determination of cyanobacterial phycobilisome–PSII supercomplex by STAgSPA strategy," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    13. Yusuke Yoneda & Eric A. Arsenault & Shiun-Jr Yang & Kaydren Orcutt & Masakazu Iwai & Graham R. Fleming, 2022. "The initial charge separation step in oxygenic photosynthesis," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    14. Yuichiro Shimada & Takehiro Suzuki & Takumi Matsubara & Tomomi Kitajima-Ihara & Ryo Nagao & Naoshi Dohmae & Takumi Noguchi, 2022. "Post-translational amino acid conversion in photosystem II as a possible origin of photosynthetic oxygen evolution," Nature Communications, Nature, vol. 13(1), pages 1-8, December.
    15. Ganesh, Ibram, 2015. "Solar fuels vis-à-vis electricity generation from sunlight: The current state-of-the-art (a review)," Renewable and Sustainable Energy Reviews, Elsevier, vol. 44(C), pages 904-932.
    16. Joseph T Snow & Despo Polyviou & Paul Skipp & Nathan A M Chrismas & Andrew Hitchcock & Richard Geider & C Mark Moore & Thomas S Bibby, 2015. "Quantifying Integrated Proteomic Responses to Iron Stress in the Globally Important Marine Diazotroph Trichodesmium," PLOS ONE, Public Library of Science, vol. 10(11), pages 1-24, November.
    17. Xiaojing Lin & Zhaojie Wang & Shoufu Cao & Yuying Hu & Siyuan Liu & Xiaodong Chen & Hongyu Chen & Xingheng Zhang & Shuxian Wei & Hui Xu & Zhi Cheng & Qi Hou & Daofeng Sun & Xiaoqing Lu, 2023. "Bioinspired trimesic acid anchored electrocatalysts with unique static and dynamic compatibility for enhanced water oxidation," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    18. Vincenzo Mascoli & Ahmad Farhan Bhatti & Luca Bersanini & Herbert Amerongen & Roberta Croce, 2022. "The antenna of far-red absorbing cyanobacteria increases both absorption and quantum efficiency of Photosystem II," Nature Communications, Nature, vol. 13(1), pages 1-8, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-40388-6. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.