Comparative proteomic responses of Paranosema locustae spores to desiccation and ultraviolet irradiation

ABSTRACT Environmental persistence is essential for the efficacy of the microsporidian parasite Paranosema locustae ( P. locustae ), yet the molecular mechanisms underlying its tolerance to desiccation and ultraviolet (UV) stress remain poorly understood. Here, we employed data-independent acquisition (DIA)-based quantitative proteomics to characterize the global proteomic responses of P. locustae spores subjected to desiccation and UV irradiation. Spores were exposed either to desiccation at 40°C and ≤30% relative humidity for 5 days or to UV irradiation (≥100 μW/cm²) for 24 h, followed by comparative proteomic analyses against untreated controls. In total, 187 proteins were identified across all treatments. Desiccation stress resulted in 22 upregulated and 8 downregulated proteins, whereas UV irradiation induced 31 upregulated and 12 downregulated proteins. Functional enrichment analyses revealed that differentially expressed proteins were predominantly associated with vacuolar/endosomal trafficking (KEGG sce04145/spo04145), transmembrane transport, and protein homeostasis, while proteins involved in biosynthetic metabolism were generally downregulated. Under desiccation, the proteomic response was characterized by upregulation of vacuolar-trafficking and transmembrane transport proteins together with downregulation of biosynthetic pathways, consistent with entry into a metabolically repressed, dormancy-like state. In contrast, UV irradiation triggered a coordinated stress-response program characterized by enhanced protein processing in the endoplasmic reticulum, proteasomal activity, and the integrated stress response, accompanied by repression of energetically costly processes such as translation and biosynthesis. Together, these findings demonstrate that P. locustae deploys distinct, stress-specific molecular responses to desiccation and UV stress. IMPORTANCE Environmental persistence is essential for Paranosema locustae as a biocontrol agent, with desiccation adaptation helping to elucidate its underlying mechanism; our results demonstrate that desiccation helps maintain P. locustae in a dormant state characterized by transcriptional remodeling but suppressed metabolism, while ultraviolet (UV) exposure activates proteostasis and antioxidant pathways and downregulates energy-intensive biosynthesis, thereby providing insights for optimizing microsporidian biocontrol strategies in pest management.