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.

A Correction to this paper has been published: https://doi.org/10.1038/s41467-020-20868-9

Nature Com.: Abstract approximately 150 words)Water oxidation and concomitant O2-formation by the Mn4Ca 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, photosynthetic formation of Mn oxides from dissolved Mn(2+) ions may have played a key role in bioenergetics and possibly facilitated early geological manganese deposits. The biochemical evidence for the ability of photosystems to form extended Mn oxide particles, lacking until now, is provided herein. We tracked the light-driven redox processes in spinach photosystem II (PSII) particles devoid of the Mn4Ca clusters by UV-vis and X-ray spectroscopy. We find that oxidation of aqueous Mn(2+) ions results in PSII-bound Mn(III,IV)-oxide nanoparticles of the birnessite type comprising 50-100 Mn ions per PSII. Having shown that even today's photosystem-II can form birnessite-type oxide particles efficiently, we propose an evolutionary scenario, which involves Mn-oxide production by ancestral photosystems, later followed by down-sizing of protein-bound Mn-oxide nanoparticles to finally yield today's Mn4CaO5 cluster of photosynthetic water oxidation.Sample preparation for XAS. Powder samples of manganese reference compounds (Mn oxides) were prepared from commercially available chemicals (MnCl2, Mn oxides) or from material (buserite, birnessite) that was kindly provided by the group of P. Kurz (Uni. Freiburg, Germany), diluted by grinding with boron-nitride (BN) to a level, which resulted in <15 % absorption at the K-edge maximum to avoid flattening effects in fluorescence-detected XAS spectra, loaded into Kapton-covered acrylic-glass holders, and frozen in liquid nitrogen. Aqueous MnCl2 (20 mM) samples were prepared at pH 7.0. Unless otherwise specified, PSII samples were prepared as follows: Mn-depleted PSII samples (3 mL) were prepared similar to the samples for optical absorption spectroscopy (see above), the pH was adjusted to the desired value, and samples were illuminated for 3 min at 1000 µE m -2 s -1 or kept in the dark as a control after addition of 240 µM MnCl2 and 60 µM PPBQ ox (pH 7.5). Thereafter, the cuvette volume was rapidly mixed with ice-cold MES buffer (7 mL, pH 7.5, see above for ingredients) on ice in the dark, the pH was measured using a pH electrode and, if necessary, readjusted to the desired value (+/-0.1 pH units), the PSII membranes were pelleted by centrifugation (10 min, 20000 g, 2 °C), and kept on ice. Several of these sample types were rapidly merged on ice in the dark by loading (~30 µL) into XAS holders, which were immediately frozen in liquid nitrogen. Native PSII samples were prepared by pelleting of dark-adapted O2-evolving PSII membrane particles (~8 mg chlorophyll mL -1 , pH 6.3), loading of the pellet material into XAS holders, and freezing in liquid nitrogen 73 . The shown XAS data for the electrodeposited Mn oxides has been collected in the context of earlier studies (16-18) a...