Exosomal microRNAs regulate the heat stress response in sea cucumber Apostichopus japonicus

Exosomes are small extracellular vesicles that contain nucleic acids such as microRNAs and may participate in important biological processes. We made the initial report of exosomes from sea cucumber Apostichopus japo-nicus, that were classically cup-shaped and had an average size of 74.65 nm, and identified specific exosome biomarkers (HSP70, TSG101, and CD9). We explored changes in the global expression of microRNAs in exosomes from the commercially important A. japonicus under normal conditions and heat-stressed conditions for 3 and 7 d. We found that heat stress increased exosome production and modified the expression profiles of the micro-RNAs that they contained. Novel_mir31, novel_mir132, novel_mir26, miR-92_1, and novel_mir27 were commonly found to be differentially expressed in three comparison groups, indicating their importance in the heat stress response. The microRNA expression levels were validated by qPCR. Function analysis of the target genes of these microRNAs indicated they were involved mainly in replication and repair in the initial response of A. japonicus to heat stress exposure. Conversely, during acclimation to the high temperature conditions, the target genes of the differentially expressed microRNAs were primarily involved in metabolism adjustments. Our results will contribute to a better understanding of the regulatory roles of exosomes in sea cucumber, and provide insights into the functions of sea cucumber exosome-shuttled microRNAs against environmental stresses exacerbated by global warming.

Automated summary

This study reported exosomes secreted by sea cucumber Apostichopus japonicus, which were cup-shaped and had an average size of 74.65 nm, and identified specific exosome biomarkers (HSP70, TSG101, and CD9). The global expression of microRNAs in exosomes from normal and heat-stressed A. japonicus was analyzed, revealing increased exosome production and altered expression profiles of microRNAs under heat stress. Several differentially expressed microRNAs were commonly found, indicating their importance in the heat stress response. Target gene analysis revealed their involvement in replication and repair during the initial response and metabolism adjustments during acclimation to high temperature conditions. These findings provide insights into the regulatory roles of exosomes and microRNAs in sea cucumber's response to environmental stresses exacerbated by global warming.