Molecular mechanisms of heavy metal adaptation of an extremophilic red alga Cyanidioschyzon merolae

The order of Cyanidiales comprise seven acido-thermophilic red microalgal species thriving in hot springs of volcanic origin characterized by extremely low pH, moderately high temperatures and the presence of elevated concentrations of sulphites and heavy metals that are prohibitive for most other organisms. Little is known about the molecular mechanisms of Cyanidiales long-term adaptation to such hostile environments, in particular to heavy metals, yet elucidation of these processes is important for understanding the evolution of the metabolic pathways underlying heavy metal detoxification for developing rational strategies for heavy metal bioremediation. Here, we investigated the long-term adaptive responses of Cyanidioschyzon merolae cells, a member of Cyanidiales, to extremely high nickel concentrations. Through complementary approaches based on physiological, microscopic and elemental analyses we dissect several molecular mechanisms underlying the long-term adaptation of this model extremophilic microalga to high Ni exposure. These include: (i) extrusion of Ni from the cells and lack of significant Ni accumulation inside the cells; (ii) maintenance of efficient photoprotective responses including non-photochemical quenching and state transitions; (iii) dynamic remodeling of the chloroplast ultrastructure such as formation of metabolically active prolamellar bodies and plastoglobuli together with loosening of the thylakoid membranes; (iv) activation of ROS amelioration metabolic pathways; and (v) preservation of the efficient respiratory chain functionality. All the dynamically regulated processes identified in this study underlie the remarkable adaptability of C. merolae to extremely high Ni levels that exceed by several orders of magnitude the levels of this heavy metal found in the natural environment of this extremophile.