Transcriptomic, and metabolic profiling reveals adaptive mechanisms of Auricularia heimuer to temperature stress

Temperature significantly influences the growth and development of edible mushrooms, including the popular Auricularia heimuer. Despite its economic importance, the molecular mechanisms that enable A. heimuer to withstand prolonged temperature stress are poorly characterized. Here, we performed a comprehensive morphologic, transcriptomic, and metabolic analysis of A. heimuer mycelium exposed to different temperatures over a long period of time. Low temperatures (LT) suppressed mycelial growth, while high temperatures (HT) promoted it. Extremely high temperatures (EHT) were highly detrimental, not only inhibiting growth but also potentially leading to mycelial mortality. The production of reactive oxygen species (ROS) and the activities of antioxidant enzymes such as superoxide dismutase (SOD) and catalase (CAT) were significantly altered by temperature. Transcriptomic profiling identified 1,024, 778, and 4,636 differentially expressed genes (DEGs) in LT, HT, and EHT, respectively, compared to normal temperature (NT). The response to LT was found to involve the regulation of protein synthesis and transport. Notably, HT and NT shared the highest degree of similarity, indicating that these two conditions represent a moderate temperature range that places less stress on the mycelium. In contrast, exposure to EHT resulted in the upregulation of genes related to ribosomal biogenesis, suggesting that A. heimuer may increase protein synthesis in response to heat stress. Furthermore, many genes related to carbohydrate metabolism were downregulated under EHT. Enzymatic assays further confirmed that thermal stress profoundly affects the synthesis of metabolic byproducts and the activities of key glycolytic enzymes, suggesting a restructured metabolic landscape under stressful conditions. In summary, our comprehensive analysis of the A. heimuer mycelial transcriptomic and enzymatic responses to sustained temperature fluctuations provides valuable insights into the molecular basis of thermotolerance. This work lays the foundation for future breeding efforts aimed at improving the resilience of cultivated A. heimuer and can serve as the basis for similar initiatives in other fungal species.