Time-Course and Tissue-Specific Molecular Responses to Acute Thermal Stress in Japanese Mantis Shrimp Oratosquilla oratoria

Abstract

Current understanding of adaptability to high temperatures is increasingly important as extreme weather events that can trigger immediate physiological stress in organisms have occurred more frequently. Here, we tracked transcriptomic responses of gills, hepatopancreas, and muscle to acute thermal exposure at 30 °C for 0.5, 6, and 12 h in an economically important crustacean, Oratosquilla oratoria, to gain a preliminary understanding of the tissue-specific and dynamic physiological regulation process under acute heat stress. The unique physiological responses of muscle, hepatopancreas, and gills to acute thermal stress were associated with protein degradation, lipid transport, and energy metabolism in O. oratoria, respectively. Functional enrichment analysis of differentially expressed transcripts and heat-responsive gene clusters revealed a biphasic protective responsiveness of O. oratoria developed from the early responses of signal transduction, immunity, and cytoskeleton reorganization to the responses dominated by protein turnover and energy metabolism at the mid-late stages under acute heat stress. Noteworthy, trend analysis revealed a consistently upregulated expression pattern of high molecular weight heat shock protein (HSP) family members (HSP60, HSP70, and HSP90) during the entire thermal exposure process, highlighting their importance for maintaining heat resistance in O. oratoria. Documenting the whole process of transcriptional responses at fine temporal resolution will contribute to a far-reaching comprehension of plastic responses to acute heat stress in crustaceans, which is critical in the context of a changing climate.