The extremophile Chlamydomonas acidophila PM01 survives high manganese contamination by restricting non-vacuolar intracellular content

Abstract

Acidophilic and metallotolerant microalgae represent an indispensable element of strategies to exploit or revive acid mine drainage ponds and similar systems with high levels of dissolved metal ions. The selection of an optimal strain for a specific application depends on the capacity to tolerate selected metal(s) and on the mechanisms of tolerance. Herein we examined the tolerance to manganese by Chlamydomonas acidophila PM01, an extremophilic strain that lives under acidic conditions and high concentrations of iron and other metals in its anthropogenic aquatic habitat. PM01 survived an extremely high Mn concentration of 50 mM (2.75 g/L). At 20 mM, cells kept intracellular Mn concentrations at a low level probably through binding to the cell wall, and vacuolization and excretion of Mn from the cell. Mn²⁺ was sequestrated by oxygen ligands, including phosphates, in octahedral geometry, in vacuoles and the cell wall. Energy challenges induced by Mn excess are met by the consumption of starch and lipid reserves, and improved photosynthetic performance. The exposure to Mn excess was related to decreased abundance of Fe-metalloenzymes and mild oxidative stress. The tolerance to Fe is coincident to tolerance to Mn. Acidophilic microalgae may be used for commercialization of metal-infested waters through biomass and biofuels production avoiding the need to use freshwaters and reducing contamination by other organisms. Finally, our study points out a novel low-intracellular Mn retention tolerance model that may be specific to acidophilic eukaryotic microalgae and enable superior survival tolerance. However, such strategy of tolerance is not optimal for bioremediation.