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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
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    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.
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