Integrated multiple-omics reveals the regulatory mechanism underlying the effects of artificial feed and grass feeding on growth and muscle quality of grass carp (Ctenopharyngodon idellus)

The muscle quality of farmed fish has attracted widespread public attention. To understand a comprehensive molecular mechanism underlying the effects of artificial formula feed- (AF) and grass-feeding (GF) on muscle quality and growth of grass carp ( Ctenopharyngodon idellus ), muscular transcriptomics and proteomics of GF and AF C. idellus were characterized. A total of 834 DEGs (484 up-, 350 down-regulated genes) and 487 DEPs (271 up- and 216 down-regulations) were identified between groups. Then, the functional enrichment analysis of DEGs & DEPs (DEs) and the integration of multiple-Omics (SDFs), further reflected that the stronger myofiber differentiation and protein synthesis capacities are likely the main strategy of more muscle mass gain in AF C. idellus , while the muscle growth in GF C. idellus is consequent to the stronger muscle cell proliferation and hypertrophy. Secondly, there was a significant difference in muscle fiber types between GF and AF groups, this has a noticeable effect on muscle tenderness and quality. In combination with previously metabolic results, we established DEG-DEP-SDM interaction network, which validated that the slow-MyHC-I fiber, dense in AF C. idellus muscles, accumulated more glycogen and exhibited more powerful glycolytic activity. Meanwhile, the suppressed activity of eIF2α in AF C. idellus muscles promoted protein synthesis, the “Ubiquitin mediated proteolysis” was simultaneously restrained. However, the activities of TCA cycle and fatty acid oxidation were significantly enhanced in GF muscles (rich in fast-MyHC-IIb). Accordingly, the up-regulated ACSL1, ACADS, ppara , etc. were quantified in GF C. idellus samples with stronger fatty acids β-oxidation activity, then led to the reduction of cellular triglycerides and lipid droplet formation. Additionally, our results also provide key information for further understanding of the molecular mechanisms (e.g. MAPK and PI3K signaling pathways, Necroptosis and so on) of C. idellus under dietary treatments. In summary, the grass-feeding could effectively alleviate the negative effects of AF on fish, namely, reducing fat deposition, improving nutrients, flavor and texture of muscle, relieving insulin resistance and stress tolerance, finally lead to better nourishing and healthy C. idellus . • The muscle growth of GF C. idellus is triggered by cell proliferation and hypertrophy. • The grass-feeding could inspire the muscle fiber-type switching (type I → type IIb). • The GF C. idellus displayed stronger TCA cycle and fatty acid β-oxidation activities.