Gut Microbiota Influence Lipid Metabolism of Skeletal Muscle in Pigs

Abstract

Gut microbiota is recognized as a strong determinant of host physiology including fat metabolism and can transfer obesity-associated phenotypes from donors to recipients. However, the relationship between gut microbiota and intramuscular fat (IMF) is still largely unknown. Obese Jinhua pigs (JP) have better meat quality that is associated with higher IMF content than lean Landrace pigs (LP). The present study was conducted to test the contribution of gut microbiota to IMF properties by transplanting fecal microbiota of adult JP and LP to antibiotics-treated mice. Similar to JP donors, the mice receiving JP's microbiota (JM) had elevated lipid and triglyceride levels and the lipoprotein lipase activity, as well as reduced mRNA level of angiopoietin-like 4 (ANGPTL4) in the gastrocnemius muscles, compared to those in mice receiving LP's microbiota (LM). High-throughput 16S rRNA sequencing confirmed that transplantation of JP and LP feces differently reconstructed the gut microbiota in both jejunum and colon of mouse recipients. In colonic samples, we observed an elevated ratio of Firmicutes to Bacteroidetes and increased abundance of genus Romboutsia in JM, which were positively correlated with obesity. Furthermore, the abundance of Akkermansia decreased in JM, which is positively correlated with lean. Colonic concentrations of acetate (P = 0.047) and butyrate (P = 0.014) were significantly lower in JM than in LM, and consistently, the terminal genes for butyrate synthesis, butyryl CoA: acetate CoA transferase were less abundant in colonic microbiota of JM. Taken together, these gut microbiota of obese JP intrinsically promotes IMF accumulation and can transfer the properties to mouse recipients. Manipulation of intestinal microbiota will, therefore, have the potential to improve the meat quality and flavor of pigs and even to ameliorate the metabolic syndrome in human.

Comparison of Digestive Enzyme Activities and Expression of Small Intestinal Transporter Genes in Jinhua and Landrace Pigs

“…The earlier the weaning time, the longer the time required for chymotrypsin activity to return to normal levels in the gastrointestinal tract of weaned piglets, suggesting that chymotrypsin activity may be affected by diet and stress ( Lindemann et al, 1986 ). In our study, the trypsin activity in the small intestine of Jinhua pigs was significantly lower than that in Landrace pigs except for the jejunal mucosa, which indicates that the Jinhua pig, as a local fat-type pig ( Xiao et al, 2018 ; Wu et al, 2021 ), may have a weaker ability to digest protein than the exotic lean-type pig such as the Landrace. The chymotrypsin activity of Jinhua pigs was higher than that in Landrace pigs, indicating that there was a difference in chymotrypsin activity among different species, which may be related to the degree of protein decomposition.…”

The Impact of Genetics on Gut Microbiota of Growing and Fattening Pigs under Moderate N Restriction

“…Other authors have already found slightly higher levels of Lactobacillus genus in high quality meat breeds [36,44]. Moreover, several studies also observed that Clostridium is found in higher proportion in fattier pigs than in their lean counterparts [9,33]. Duroc pigs also harbored higher abundance of Streptococcus and Bifidobacterium genera, which were also higher in Jinhua pigs [35] than in Landrace.…”

“…Together with management (nutrition, biosecurity, vaccination) and genetic plans, implementation of new production strategies should also consider the animal's physiology [2,6]. In this regard, it has been evidenced that gut microbiota plays important roles in promoting immune system development [7], regulating host nutrient metabolism [8,9], modulating phenotypic traits [9,10] and producing beneficial substances [11]. Gut microbiota consists of a complex ecosystem that is established through a sequence of dynamic successions of the dominant microbial groups.…”

“…Since there is high potential to modulate gut microbiome in different managing scenarios [13], it would be possible to reshape the community structure to achieve different productive goals [9]. For this purpose, a further understanding of the factors affecting gut microbiota and their interactions seems essential.…”

Intestinal Microbiota Regulate Certain Meat Quality Parameters in Chicken

“…Native breeds of livestock have superior meat quality and capacity for fat deposition, compared to commercial breeds ( 33 , 34 ). Recently, numerous studies have demonstrated the important role of gut microbiota in regulating skeletal muscle synthesis and development ( 26 , 35 , 36 ). The gut microbiota-muscle axis has been identified ( 37 , 38 ) and, to the best of our knowledge, this is the first report on the intestinal microbiota profile of the Beijing-You broilers by FMT.…”