Thermal acclimation and nitrogen deprivation drive distinct transcriptomic reprogramming toward a shared lipid...

Polar microalgae possess unique mechanisms that enable them to thrive in extreme environments; however, their molecular responses remain poorly explored in biotechnological contexts. This study presents the physiological and transcriptomic responses of Chlamydomonas malina RCC2488 under two key environmental conditions: Thermal acclimation (8 vs 4 °C) and nitrogen deprivation (-N vs +N). Through de novo RNA-seq assembly (46,536 transcripts; 20,993 annotated), 1696 and 1296 differentially expressed genes were identified under thermal acclimation and nitrogen deprivation, respectively. Both conditions induced the accumulation of triacylglycerols (TAGs) enriched in polyunsaturated fatty acids (PUFAs) and repression of photosynthesis-related genes. However, the underlying regulatory mechanisms differed substantially. Thermal acclimation significantly reduced the growth rate (from 1.707 to 0.324 d⁻¹) and activated the de novo fatty acid and TAG biosynthesis pathway through upregulation of key genes including ACCase, KAS, KAR, HD, DGAT and G3PDH. In contrast, nitrogen deprivation halted cell division and triggered prioritized metabolic reprogramming characterized by the activation of critical lipogenic enzymes (PDH, ACCase, HD, G3PDH, and DGAT), transcriptional maintenance of nitrogen transporters and assimilation enzymes (NR, NRT2) in an alert state, and repression of non-essential growth-associated pathways such as amino acid and nucleotide metabolism, translation, cell division and protein degradation. The identification of shared differentially expressed genes between both conditions suggests the existence of a common transcriptomic core associated with cellular homeostasis and resource optimization. Collectively, these findings demonstrate that two distinct environmental perturbations converge toward the same lipid phenotype through differentiated regulatory programs, revealing an adaptive strategy oriented toward resource economy and energy storage in dynamic polar environments. This study positions Chlamydomonas malina RCC2488 as a relevant model for understanding metabolic plasticity in polar microalgae and as a promising platform for sustainable TAG and PUFA production under suboptimal conditions.