Liver transcriptome analysis reveals changes in energy metabolism, oxidative stress, and apoptosis in pearl gentian grouper exposed to acute hypoxia

Pearl gentian grouper is an important new breed of high-density farmed fish with high commercial value on the coast of southeast China. However, frequent hypoxia could suppress growth and increase the mortality of high-density farmed pearl gentian grouper, limiting the application and scope of this farming mode and obstructing the rapid development of grouper aquaculture. Thus, this study investigated liver transcriptional changes in pearl gentian grouper exposed to hypoxic conditions (dissolved oxygen: 0.5 ± 0.05 mg/L) for different durations (0 h, 1 h, 3 h, 6 h, and 9 h) using Illumina RNA-Seq technology. Based on a differential expression analysis, short time-series expression miner (STEM) clustering, and weighted gene co-expression network analysis (WGCNA), 2383 differentially expressed genes (DEGs), two gene sets (profiles 0 and 18) with obvious expression trends, and three hypoxia-specific modules (lightcyan1, tan, and antiquewhite4) were screened, respectively. Genes involved in glycolysis (SLC2A3, PFKP, ALDOB, TPI1, GAPDH, PK, and LDHA) and fatty acid β-oxidation (ACSL1, ACOX1, and EHHADH) were all up-regulated, whereas genes involved in aerobic glycolysis (PC) and fatty acid synthesis (ACACB, FASN, FADS2) were down-regulated during hypoxic exposure. The CHAC1, GGCT, and OPLAH genes, involved in glutathione decomposition, were up-regulated. Additionally, the PXMP4, MPV17, SOD1, and CAT genes, involved in peroxisome antioxidation, were up-regulated. Moreover, the up-regulation of apoptosis-related genes (AIFM1, ENDOG, TNFRSF10A, and MCL1) was also detected. The results revealed that anaerobic glycolysis, fatty acid β-oxidation, glutathione metabolism, peroxisome antioxidation, and apoptosis played crucial roles in the transcriptomic responses of pearl gentian grouper towards hypoxia. These findings provide an essential basis for understanding the molecular mechanism by which this grouper adapts to profound changes in dissolved oxygen, thereby reducing damage caused by acute hypoxia during high-density farming. [Display omitted] •Hypoxic adaptation in pearl gentian grouper was explored at the transcriptome level.•Anaerobic glycolysis and fatty acid β-oxidation were the main energy sources.•GSH activity was inhibited but peroxisome antioxidant capacity was enhanced.•Hypoxia activated the apoptosis, including mitochondrial pathway and external death receptor pathway.