The present study aimed to investigate the impacts of dietary standardized ileal digestible lysine to net energy (SID Lys:NE) ratio on lipid metabolism in pigs fed high-wheat diets. Thirty-six crossbred growing barrows (65.20 ± 0.38 kg) were blocked into two treatment groups, fed high-wheat diets with either a high SID Lys:NE ratio (HR) or a low SID Lys:NE ratio (LR). Each treatment group consisted of three replicates, with six pigs per pen in each replicate. The diminishing dietary SID Lys:NE ratio exhibited no adverse impacts on the carcass trait (
p > 0.05) but increased the marbling score of the longissimus dorsi muscle (
p < 0.05). Meanwhile, LR diets tended to increase the serum triglyceride concentration (
p < 0.1). LR diets upregulated fatty acid transport protein 4 and acetyl-coA carboxylase α expression levels and downregulated the expression level of adipose triglyceride lipase (
p < 0.05). LR diets improved energy metabolism via decreasing the expression levels of AMP-activated protein kinase (AMPK) α1, sirtuin 1 (SIRT1), and peroxisome proliferator-activated receptor-γ coactivator-1α (PGC-1α) (
p < 0.05). Additionally, LR diets stimulated hepatic bile acid synthesis via upregulating the expression levels of cytochrome P450 family 7 subfamily A member 1 and cytochrome P450 family 27 subfamily A member 1, and downregulating farnesol X receptor (FXR) and small heterodimer partner (SHP) expression levels (
p < 0.05). A lowered SID Lys:NE ratio affected the colonic microbial composition, characterized by increased relative abundances of
YRC22,
Parabacteroides,
Sphaerochaeta, and
Bacteroides, alongside a decreased in the proportion of
Roseburia,
f_Lachnospiraceae_g_Clostridium,
Enterococcus,
Shuttleworthia,
Exiguobacterium,
Corynebacterium,
Subdoligranulum,
Sulfurospirillum, and
Marinobacter (
p < 0.05). The alterations in microbial composition were accompanied by a decrease in colonic butyrate concentration (
p < 0.1). The metabolomic analysis revealed that LR diets affected primary bile acid synthesis and AMPK signaling pathway (
p < 0.05). And the mantel analysis indicated that
Parabacteroides,
Sphaerochaeta,
f_Lachnospiraceae_g_Clostridium,
Shuttleworthia, and
Marinobacter contributed to the alterations in body metabolism. A reduced dietary SID Lys:NE ratio improves energy metabolism, stimulates lipogenesis, and inhibits lipolysis in finishing pigs by regulating the AMPKα/SIRT1/PGC-1α pathway and the FXR/SHP pathway.
Parabacteroides and
Sphaerochaeta benefited bile acids synthesis, whereas
f_Lachnospiraceae_g_Clostridium,
Shuttleworthia, and
Marinobacter may contribute to the activation of the AMPK signaling pathway. Overall, body metabolism and colonic microbiota collectively controlled the lipid metabolism in finishing pigs.
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