Integrated mRNA-Seq and miRNA-Seq analysis reveals the microRNAs-transcription factor-mRNA regulatory network of pearl gentian grouper under acute hypoxia

Pearl gentian grouper (Epinephelus lanceolatus ♂ × Epinephelus fuscoguttatus ♀) is a hybrid fish with high commercial value and it has the highest yield among groupers farmed along the southeastern coast of China. However, hypoxia is not only a key factor to limit the healthy growth and survival of the grouper under high-density and intensive farming, but also hinders the rapid development of its aquaculture industry. In this study, we analyzed the transcriptomic characteristics of pearl gentian grouper under acute hypoxic stress (DO 0.5 mg/L) for 1 h, 3 h, 6 h, and 9 h and normoxic condition (DO 5.5 mg/L) to determine the biological processes and molecular regulatory mechanisms underlying the response to hypoxia. By an integrated analysis of mRNA and miRNA sequencing data, we constructed a microRNA-transcription factor-mRNA regulatory network containing 52 miRNAs, 17 transcription factors, and 72 genes. During acute hypoxic stress, these key molecules were involved in several important biological processes. The activation of anaerobic glycolysis and fatty acid metabolism, cell cycle arrest contributed to grouper survival under hypoxia. Based on analyses of gene expression profiles, hypoxic stress for 3–6 h and 9 h were identified as two critical periods with significantly altered physiologic and metabolic responses in pearl gentian grouper (e.g., the transformation of energy metabolism patterns and severe oxidative stress). These results indicate that intervention measures should be implemented within 6 h of acute hypoxia in high-density and intensive farming of the grouper. Thus, our study contributes to a deeper understanding of the molecular regulatory mechanism of pearl gentian grouper adaption to acute hypoxia and provide an important scientific basis for the management of hypoxia in high-density and intensive farming practices.