Prevotella copri increases fat accumulation in pigs fed with formula diets

Congying Chen,Jun Gao,Shaoming Fang,Hao Fu,Lusheng Huang,Jinyuan Wu,Maozhang He,Hong Wei,Xinwei Xiong,Yunyan Zhou,Hui Yang

doi:10.1186/s40168-021-01110-0

Congying Chen, Jun Gao + Show 9 more

Open Access

https://doi.org/10.1186/s40168-021-01110-0

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Abstract

BackgroundExcessive fat accumulation of pigs is undesirable, as it severely affects economic returns in the modern pig industry. Studies in humans and mice have examined the role of the gut microbiome in host energy metabolism. Commercial Duroc pigs are often fed formula diets with high energy and protein contents. Whether and how the gut microbiome under this type of diet regulates swine fat accumulation is largely unknown.ResultsIn the present study, we systematically investigated the correlation of gut microbiome with pig lean meat percentage (LMP) in 698 commercial Duroc pigs and found that Prevotella copri was significantly associated with fat accumulation of pigs. Fat pigs had significantly higher abundance of P. copri in the gut. High abundance of P. copri was correlated with increased concentrations of serum metabolites associated with obesity, e.g., lipopolysaccharides, branched chain amino acids, aromatic amino acids, and the metabolites of arachidonic acid. Host intestinal barrier permeability and chronic inflammation response were increased. A gavage experiment using germ-free mice confirmed that the P. copri isolated from experimental pigs was a causal species increasing host fat accumulation and altering serum metabolites. Colon, adipose tissue, and muscle transcriptomes in P. copri-gavaged mice indicated that P. copri colonization activated host chronic inflammatory responses through the TLR4 and mTOR signaling pathways and significantly upregulated the expression of the genes related to lipogenesis and fat accumulation, but attenuated the genes associated with lipolysis, lipid transport, and muscle growth.ConclusionsTaken together, the results proposed that P. copri in the gut microbial communities of pigs fed with commercial formula diets activates host chronic inflammatory responses by the metabolites through the TLR4 and mTOR signaling pathways, and increases host fat deposition significantly. The results provide fundamental knowledge for reducing fat accumulation in pigs through regulating the gut microbial composition.8i_LmNceHRNfJRY2rW1K4pVideo

Highlights

Excessive fat accumulation of pigs is undesirable, as it severely affects economic returns in the modern pig industry
The CAG3 containing the Operational taxonomic unit (OTU) mostly annotated to Prevotella, especially P. copri, were negatively correlated with the lean meat percentage (LMP), while the CAG8 that contained the OTUs annotated to F. prausnitzii and R. flavefaciens showed strongly positive correlations with the LMP, suggesting the central roles of these co-abundance groups (CAGs) in the functional guilds of gut microbiota related to the LMP (Fig. 1a)
We identified 17 Kyoto Encyclopedia of Genes and Genomes (KEGG) pathways having significantly higher abundance in the gut microbiomes of fat pigs, including lipopolysaccharide biosynthesis and arachidonic acid metabolism involved in mediating inflammatory reactions [11, 18]; FoxO signaling pathway, insulin resistance, branch chain amino acids (BCAAs) biosynthesis, and metabolism of aromatic amino acids related to obesity and insulin resistance [12, 15], [19, 20] along with a two-component system, bacterial chemotaxis, flagellar assembly, and carbohydrate digestion and absorption associated with increased capacity for energy harvest from bacteria [6, 21]

Summary

Introduction

Excessive fat accumulation of pigs is undesirable, as it severely affects economic returns in the modern pig industry. Commercial Duroc pigs are often fed formula diets with high energy and protein contents. Whether and how the gut microbiome under this type of diet regulates swine fat accumulation is largely unknown. Fatness traits such as backfat thickness and lean meat percentage (LMP) are economically important traits that affect the efficiency and return of modern pig production. In the modern pig industry, to obtain rapid body weight gain, commercial formula diets with high concentrations of proteins and energy have often been provided to production pig herds. Whether and how the gut microbiome regulates swine fat accumulation (e.g., LMP) is largely unknown

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