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, high acidity, 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 information is important for understanding the evolution of microorganisms in the early stages of life on Earth because these extreme environments are similar. By analyzing the remodeling of the global transcriptome upon long-term exposure of C. merolae to extremely high concentrations of nickel, the key adaptive metabolic pathways and associated molecular components were identified. Our work shows that long-term Ni exposure of C. merolae cells leads to the lagged metabolic switch demonstrated by transcriptional upregulation of the metabolic pathways critical for cell survival such as DNA replication, cell cycle, and protein quality control with the concomitant downregulation 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 the development of the rational approaches for bioremediation of contaminated aquatic environments by modifying expression of the critical molecular components identified here. Overall design: C. merolae was exposed to 0, 1 and 3mM and Nickel and cultivated for 5 and 10 days.

红色微藻（Cyanidioschyzon merolae）栖息于高温、高酸且富含高浓度重金属与亚硫酸盐的极端环境中，这类环境对绝大多数其他生命形式均具有致死性。然而，目前关于这类极端微生物（extremophile）适应此类严苛环境的精准调控机制的相关研究信息仍较为匮乏。获取此类研究信息，对于解析地球早期生命演化阶段的微生物演化历程具有重要意义——因为这类极端环境与地球早期的环境特征高度相似。本研究通过分析该微藻长期暴露于极高浓度镍离子环境下的全球转录组重塑特征，成功鉴定出其关键适应性代谢通路及相关分子组分。研究结果显示，该微藻长期暴露于镍离子环境后会出现延迟性代谢转换：与细胞存活密切相关的代谢通路（如DNA复制、细胞周期调控及蛋白质质量控制）的转录水平显著上调，而能量消耗较高的生理过程（包括光合装置组装与脂质生物合成）则伴随出现转录水平下调。本研究为光合自养生物（phototrophs）的非生物胁迫适应分子机制的多组学研究，以及通过调控本研究鉴定出的关键分子组分来开发污染水环境的理性生物修复方案，奠定了重要基础。整体实验设计：将该微藻暴露于0、1和3 mM镍离子环境中，分别培养5天与10天。