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Light-driven formation of manganese oxide by today’s photosystem II supports evolutionarily ancient manganese-oxidizing photosynthesis

Author

Listed:
  • Petko Chernev

    (Freie Universität Berlin
    Molecular Biomimetics, Uppsala University)

  • Sophie Fischer

    (Freie Universität Berlin)

  • Jutta Hoffmann

    (Freie Universität Berlin)

  • Nicholas Oliver

    (Freie Universität Berlin)

  • Ricardo Assunção

    (Freie Universität Berlin)

  • Boram Yu

    (Freie Universität Berlin)

  • Robert L. Burnap

    (Oklahoma State University)

  • Ivelina Zaharieva

    (Freie Universität Berlin)

  • Dennis J. Nürnberg

    (Freie Universität Berlin)

  • Michael Haumann

    (Freie Universität Berlin)

  • Holger Dau

    (Freie Universität Berlin)

Abstract

Water oxidation and concomitant dioxygen formation by the manganese-calcium cluster of oxygenic photosynthesis has shaped the biosphere, atmosphere, and geosphere. It has been hypothesized that at an early stage of evolution, before photosynthetic water oxidation became prominent, light-driven formation of manganese oxides from dissolved Mn(2+) ions may have played a key role in bioenergetics and possibly facilitated early geological manganese deposits. Here we report the biochemical evidence for the ability of photosystems to form extended manganese oxide particles. The photochemical redox processes in spinach photosystem-II particles devoid of the manganese-calcium cluster are tracked by visible-light and X-ray spectroscopy. Oxidation of dissolved manganese ions results in high-valent Mn(III,IV)-oxide nanoparticles of the birnessite type bound to photosystem II, with 50-100 manganese ions per photosystem. Having shown that even today’s photosystem II can form birnessite-type oxide particles efficiently, we propose an evolutionary scenario, which involves manganese-oxide production by ancestral photosystems, later followed by down-sizing of protein-bound manganese-oxide nanoparticles to finally yield today’s catalyst of photosynthetic water oxidation.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:11:y:2020:i:1:d:10.1038_s41467-020-19852-0
    DOI: 10.1038/s41467-020-19852-0
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    Cited by:

    1. 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.
    2. 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.

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