IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-31931-y.html
   My bibliography  Save this article

Post-translational amino acid conversion in photosystem II as a possible origin of photosynthetic oxygen evolution

Author

Listed:
  • Yuichiro Shimada

    (Nagoya University, Furo-cho)

  • Takehiro Suzuki

    (RIKEN Center for Sustainable Resource Science)

  • Takumi Matsubara

    (Nagoya University, Furo-cho)

  • Tomomi Kitajima-Ihara

    (Nagoya University, Furo-cho)

  • Ryo Nagao

    (Nagoya University, Furo-cho
    Okayama University)

  • Naoshi Dohmae

    (RIKEN Center for Sustainable Resource Science)

  • Takumi Noguchi

    (Nagoya University, Furo-cho)

Abstract

Photosynthetic oxygen evolution is performed at the Mn cluster in photosystem II (PSII). The advent of this reaction on ancient Earth changed its environment by generating an oxygenic atmosphere. However, how oxygen evolution originated during the PSII evolution remains unknown. Here, we characterize the site-directed mutants at the carboxylate ligands to the Mn cluster in cyanobacterial PSII. A His residue replaced for D1-D170 is found to be post-translationally converted to the original Asp to recover oxygen evolution. Gln/Asn residues in the mutants at D1-E189/D1-D342 are also converted to Glu/Asp, suggesting that amino-acid conversion is a common phenomenon at the ligand sites of the Mn cluster. We hypothesize that post-translational generation of carboxylate ligands in ancestral PSII could have led to the formation of a primitive form of the Mn cluster capable of partial water oxidation, which could have played a crucial role in the evolutionary process of photosynthetic oxygen evolution.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-31931-y
    DOI: 10.1038/s41467-022-31931-y
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-31931-y
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-022-31931-y?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. Michihiro Suga & Fusamichi Akita & Kunio Hirata & Go Ueno & Hironori Murakami & Yoshiki Nakajima & Tetsuya Shimizu & Keitaro Yamashita & Masaki Yamamoto & Hideo Ago & Jian-Ren Shen, 2015. "Native structure of photosystem II at 1.95 Å resolution viewed by femtosecond X-ray pulses," Nature, Nature, vol. 517(7532), pages 99-103, January.
    2. Joanne S. Boden & Kurt O. Konhauser & Leslie J. Robbins & Patricia Sánchez-Baracaldo, 2021. "Timing the evolution of antioxidant enzymes in cyanobacteria," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    3. Sean A. Crowe & Lasse N. Døssing & Nicolas J. Beukes & Michael Bau & Stephanus J. Kruger & Robert Frei & Donald E. Canfield, 2013. "Atmospheric oxygenation three billion years ago," Nature, Nature, vol. 501(7468), pages 535-538, September.
    4. 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)

    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. 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.
    2. 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.
    3. 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.
    4. Hongping He & Xiao Wu & Haiyang Xian & Jianxi Zhu & Yiping Yang & Ying Lv & Yiliang Li & Kurt O. Konhauser, 2021. "An abiotic source of Archean hydrogen peroxide and oxygen that pre-dates oxygenic photosynthesis," Nature Communications, Nature, vol. 12(1), pages 1-9, December.
    5. Joanne S. Boden & Juntao Zhong & Rika E. Anderson & Eva E. Stüeken, 2024. "Timing the evolution of phosphorus-cycling enzymes through geological time using phylogenomics," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    6. Liuyang Li & Danyue Huang & Yaoxun Hu & Nicola M. Rudling & Daniel P. Canniffe & Fengping Wang & Yinzhao Wang, 2023. "Globally distributed Myxococcota with photosynthesis gene clusters illuminate the origin and evolution of a potentially chimeric lifestyle," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    7. Guo-Wei Qiu & Wen-Can Zheng & Hao-Ming Yang & Yu-Ying Wang & Xing Qi & Da Huang & Guo-Zheng Dai & Huazhong Shi & Neil M. Price & Bao-Sheng Qiu, 2024. "Phosphorus deficiency alleviates iron limitation in Synechocystis cyanobacteria through direct PhoB-mediated gene regulation," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    8. James Andrew M. Leong & Tucker Ely & Everett L. Shock, 2021. "Decreasing extents of Archean serpentinization contributed to the rise of an oxidized atmosphere," Nature Communications, Nature, vol. 12(1), pages 1-11, 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:13:y:2022:i:1:d:10.1038_s41467-022-31931-y. 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.