The energy-saving metabolic switch underlies survival of extremophilic red microalgae in extremely high nickel levels

The red microalga Cyanidioschyzon merolae inhabits extreme environments of high temperature (40-56{degrees}C), high acidity (pH 0.05-4), and the presence of high concentrations of heavy metals and sulphites that are lethal to most other forms of life. However, information is scarce on the precise adaptation mechanisms of this extremophile to such hostile conditions. Gaining such knowledge is important for understanding the evolution of microorganisms in the early stages of life on Earth characterized by such extreme environments. By analyzing the re-programming of the global transcriptome upon long-term (up to 15 days) exposure of C. merolae to extremely high concentrations of nickel (1 and 3 mM), the key adaptive metabolic pathways and associated molecular components were identified. Our work shows that long-term Ni exposure of C. merolae leads to the lagged metabolic switch demonstrated by the transcriptional upregulation of the metabolic pathways critical for cell survival. DNA replication, cell cycle, and protein quality control processes were upregulated while downregulation occurred of energetically costly processes including assembly of the photosynthetic apparatus and lipid biosynthesis. This study paves the way for the multi-omic studies of the molecular mechanisms of abiotic stress adaptation in phototrophs, as well as future development of the rational approaches for bioremediation of contaminated aquatic environments. ImportanceThis study provides the first comprehensive analysis of the global transcriptome re-programming in the extremophilic red microalga Cyanidioschyzon merolae during its long-term adaptation to heavy metals. We show that the lagged metabolic switch, demonstrated by the transcriptional upregulation of the metabolic pathways critical for cell survival, underlies the long-term Ni adaptation of this model extremophile. The transcriptomic results shed light on how life may have adapted to some of the harshest abiotic stresses on Earth including high temperatures, extreme acidity, and high levels heavy metals that are prohibitive to most other organisms. Additionally, the differentially regulated genes identified in this work provide important clues on the rational development of effective bioremediation strategies of removing heavy metals from the heavily contaminated aquatic environments.