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.

氧光合作用的锰钙簇簇引起的水氧化和伴随的双氧形成已经塑造了生物圈，大气层和地圈。据推测，在光合水氧化显着发展之前，从溶解的Mn（2+）离子光驱动形成锰氧化物可能在生物能学中发挥了关键作用，并可能促进了早期地质锰矿床。在这里，我们报告光化学系统形成扩展的氧化锰颗粒的能力的生化证据。菠菜光系统II中不含锰钙簇的光化学氧化还原过程通过可见光和X射线光谱法进行跟踪。溶解的锰离子的氧化产生高价的Mn（III，IV）水钠锰矿类型的氧化物纳米粒子与光系统II结合，每个光系统含50-100个锰离子。已经证明即使当今的光系统II都能有效地形成水钠锰矿型氧化物颗粒，我们提出了一个进化方案，其中涉及由祖先光系统生产氧化锰，随后缩小与蛋白质结合的氧化锰纳米颗粒的尺寸，最终产生当今的光合水氧化的催化剂。