Transcriptomics and metabolomics reveal the regulation of reproductive performance and egg quality of blotched snakehead Channa maculata broodstock induced by a high protein diet

Abstract

To evaluate the effects of dietary protein on reproductive performance, egg quality and larval health of the blotched snakehead Channa maculata, three groups were designed: a high protein group (HP) with 48% protein content, a low protein group (LP) with 44% protein content, and a control group (C) fed with commercial feed containing 40% protein. The results demonstrated that the HP diet significantly enhanced maternal absolute fecundity, egg size and offspring health; however, it had no impact on fertilization rate and hatching rate. The maternal plasma levels of 11-ketotestosterone, 17β-estradiol, and vitellogenin in the HP group were found to be significantly higher compared to those in the C group. Plasma SOD activity and T-AOC capacity in the HP group were significantly higher than those in the C group, while MDA content showed an opposite trend. The trend of T-AOC in 7 days post-hatching larvae exhibited a consistent pattern with that observed in the maternal. Metabolomics and transcriptomics results indirectly indicated that the differences in reproductive and egg quality of the broodstock were associated with the regulation of arachidonic acid metabolism, steroid hormone biosynthesis, cholesterol metabolism, glycerophospholipid metabolism, and glycerolipid metabolism. The expression levels of star, zp3, foxo3, tgf-β, ghr, igf, cyp17a1, and cyp19a1 genes associated with reproduction and were significantly upregulated in the HP group. By depleting the abundance of metabolites in key pathway such as the pentose phosphate pathway, glycolysis/gluconeogenesis, nicotinate and nicotinamide metabolism, vitamin B6 metabolism within the ovary, there is an elevation in arachidonic acid metabolite abundance, thereby facilitating ovarian maturation and regulating egg quality. In conclusion, the high protein diet may affect the reproductive process and egg quality by inducing an upregulation of TGF-beta signaling pathway and ovarian steroidogenesis and arachidonic acid metabolism, leading to increased plasma cholesterol levels and enhanced steroid hormone synthesis.