A three-step process of manganese acquisition and storage in the microalga Chlorella sorokiniana

Metabolism of metals in microalgae and the adaptation to metal excess are of significant environmental importance. We report here a three-step mechanism that the green microalga Chlorella sorokiniana activates during the acquisition of and adaptation to manganese (Mn), which is both, an essential trace metal and a pollutant of waters. In the early stage, Mn 2+ was mainly bound to membrane phospholipids and phosphates in released mucilage. The outer cell wall was reorganized, and lipids were accumulated with a relative increase in lipid saturation. Intracellular redox settings were rapidly altered in the presence of Mn excess, with increased production of reactive oxygen species that resulted in lipid peroxidation and a decrease in the level of thiols. In the later stage, Mn 2+ was chelated by polyphosphates and accumulated in the cells. The structure of the inner cell wall was modified and the redox milieu established a new balance. Polyphosphates serve as a transient Mn 2+ storage ligand, as proposed previously. At the final stage, Mn was stored in multi-valent Mn clusters that resemble the structure of tetramanganese-calcium core of the oxygen-evolving complex. The present findings elucidate bioinorganic chemistry and metabolism of Mn in microalgae, and may shed new light on water-splitting Mn clusters.