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

Petko Chernev, Sophie Fischer, Jutta Hoffmann, Nicholas Oliver, Ricardo Assunção, Boram Yu, Robert L. Burnap, Ivelina Zaharieva, Dennis J. Nürnberg, Michael Haumann and Holger Dau ()
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Petko Chernev: Freie Universität Berlin
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

Nature Communications, 2020, vol. 11, issue 1, 1-10

Abstract: 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.

Date: 2020
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DOI: 10.1038/s41467-020-19852-0

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