Dietary carbohydrates influence muscle texture of olive flounder Paralichthys olivaceus through impacting mitochondria function and metabolism of glycogen and protein

Wenbing Zhang,Jiahuan Liu,Kangyu Deng,Kangsen Mai,Mingzhu Pan,Dong Huang,Jing Wu,Mengxi Yang,Guangxia Liu

doi:10.1038/s41598-020-76255-3

Abstract

The present study was conducted to estimate the effects of dietary carbohydrates on muscle quality and the underlying mechanisms. Six isonitrogenous and isolipidic diets were formulated to contain graded levels of carbohydrates (0%, 8%, 12%, 16%, 20% and 24%, respectively). These diets were named as C0, C8, C12, C16, C20 and C24, respectively. After a 10-week feeding trial, results showed that the muscle pH, liquid holding capacity (LHC) and hardness were significantly decreased by the increasing dietary carbohydrate levels. Dietary carbohydrates significantly decreased the muscle fibre diameter, and the highest value was found in the C0 group. Accumulated glycogen and degenerated mitochondrial cristae were observed in the C24 group. Significantly higher contents of protein carbonyls were observed in the C20 group and C24 group (P < 0.05). There was a significant decrease of mtDNA copy number in the C24 group compared with that in the C0 and C8 groups. The AMP/ATP ratio in muscle decreased first and then increased with the increasing dietary carbohydrate levels. The dietary incorporation of carbohydrate significantly reduced the expression of opa1, pygm and genes involved in myogenesis (myf5 and myog). Meanwhile, proteolysis-related genes (murf-1, mafbx, capn2 and ctsl), pro-inflammatory cytokines (il-6 and tnf-α) and mstn were significantly up-regulated. In the C24 group, significant increase of phosphorylation of AMPK (Thr172), up-regulation of PGC-1α and GLUT4 were observed, while the phosphorylation level of S6 (Ser235/236) was significantly decreased. It was concluded that excessive dietary carbohydrate level (24%) had negative impacts on mitochondria function and promoted glycogen accumulation, and thereafter influenced the muscle quality of olive flounder. The activation of AMPK as well as the upregulation of PGC-1α and GLUT4 was the key mechanism.

Highlights

The present study was conducted to estimate the effects of dietary carbohydrates on muscle quality and the underlying mechanisms
Previous studies have identified some genes associated with the muscle cellularity of fish, such as insulin-like growth factors (IGFs), myostatin and myogenic regulatory factors (MRFs)[15,16,17]
Previous studies in Atlantic salmon (Salmo salar)[40,41] and cod (Gadus morhua)[42] suggested that the glycogen level in muscle is the principal determinant of post-mortem pH due to its anaerobic glycolysis to lactic a cid[43]

Summary

Introduction

The present study was conducted to estimate the effects of dietary carbohydrates on muscle quality and the underlying mechanisms. In the C24 group, significant increase of phosphorylation of AMPK (Thr172), up-regulation of PGC-1α and GLUT4 were observed, while the phosphorylation level of S6 (Ser235/236) was significantly decreased. Higher dietary carbohydrate levels (44.1% vs 30.9%) increased the glycogen concentration together with postmortem glycolytic potential in muscle by influencing glycolytic enzymes activities and myofibre transformation[23,26,27]. It led to lower pH, higher drip loss, tender texture and paler color of pig muscle[23,25]. The mechanism of effects of dietary carbohydrate on the muscle growth and quality is still not clarified in fish

Methods

Results

Discussion

Conclusion