Effects of alpha-(1,2)-fucosyltransferase genotype variants on plasma metabolome, immune responses and gastrointestinal bacterial enumeration of pigs pre- and post-weaning

Abstract

In pigs, the alpha-(1,2) fucosyltransferase (FUT1) gene has been highlighted for its properties in controlling the intestinal expression of enterotoxigenic E. coli (ETEC) F18 receptors; a pathogen causing edema disease and post-weaning diarrhoea. In this study, we hypothesized that pigs with different genotypes (ETEC F18 resistant (FUT1AA) versus susceptible (FUT1AG)) differed in following systemic and enteric responses: growth performance, plasma metabolic profiles, expression of candidate genes for intestinal mucosal homeostasis and immunity, number of selected bacteria and the concentration of short-chain fatty acids (SCFA) in faeces and digesta in piglets pre and post-weaning, and on the ETEC F18 adherence ex vivo. Genotype had the strongest impact on plasma metabolomic profile on day 7 and 28 of age. FUT1AG piglets had higher level of N-methyl-2-pyrrolidinone, hippuric acid, oxindole, and 3-oxo-5-beta-chol-7-en-24-oic acid on day 7, and a higher level of guanosine on day 28 than that in the FUT1AA piglets. FUT1AA piglets had a higher level of betaine on day 7 and 3-methylguanine on day 28. On day 34 of age, the FUT1AA pigs had higher levels of S-2-hydroxyglutarate, L-phenylalanine, tauroursodeoxycholic acid and an undetermined PC/LysoPC, while Ile Glu Phe Gly peptide and genistein 5-O-glucuronide, and PC (18:0/0:0) were at higher levels in the FUT1AG piglets. FUT1 genotype did not affect the growth performance and expression of candidate genes. FUT1AG piglets had a higher number of haemolytic bacteria in faeces and in digesta than that in FUT1AA at 34 days of age. The colonic acetic acid concentration was highest in FUT1AG piglets. FUT1 genotype may influence not only the expression of E. coli F18 receptors but could potentially impact the gut homeostasis and metabotype of piglets pre and post-weaning. Further investigations on the relation between FUT1 genotype and these aspects including the intestinal commensal microbiota will expand the knowledge on factors affecting the intestinal ecosystem.

Effect of Mucine 4 and Fucosyltransferase 1 genetic variants on gut homoeostasis of growing healthy pigs

“…Little information is reported on the FUT1 effect on intestinal microbiota. However, our results reinforce the observations reported by Poulsen et al () in which FUT1 AG ETEC F18 susceptible piglets showed a higher number of non‐beneficial bacteria, including haemolytic bacteria, both in faeces and in digesta, and of Enterobacteriaceae in digesta than FUT1 AA piglets, even without the presences of diarrhoea. Thus, our results suggest that FUT1 genotype is not only associated with ETEC F18 resistance but can also play a role in the modulation of the commensal gut bacteria in healthy pigs.…”

“…Those differences in the intestinal characteristics can, therefore, concur to determine differences in piglets’ metabolism (Poulsen et al, ) and in piglet nutritional requirement (Trevisi et al, ) and result in different growth performance as already reported by Fontanesi et al. () for MUC4 and by Bao et al () for FUT1 in adult pigs.…”

“…The role of FUT1 in the glycosylation in the gut and on the modulation of gut microbiota could also explain the variation in the plasma metabolic profile that we observed in our study. Previous observation showed the influence of FUT1 genotypes in modulating the plasma metabolome and some specific plasma metabolites related with gut microbial metabolism (hippuric acid, oxindole, betaine) and inflammation (guanosine) (Poulsen et al, ). Since different techniques were applied in our and Poulsen et al () studies, and no univocal metabolites were detected, results cannot directly be compared.…”

“…Previous observation showed the influence of FUT1 genotypes in modulating the plasma metabolome and some specific plasma metabolites related with gut microbial metabolism (hippuric acid, oxindole, betaine) and inflammation (guanosine) (Poulsen et al, ). Since different techniques were applied in our and Poulsen et al () studies, and no univocal metabolites were detected, results cannot directly be compared. Here, we detected a higher amount of several phosphatidylcholines in the FUT1 GG genotype than in the FUT1 AA genotype.…”

“…Studies suggested that MUC4 and FUT1 genotypes are not only associated with piglets susceptibility to PWD but can also influence the intestinal homoeostasis. For instance, healthy piglets with different MUC4 and FUT1 genotypes are known to differ for their intestinal microbial profile ( MUC4 , Messori, Trevisi, Simongiovanni, Priori, & Bosi, ; FUT1 , Poulsen et al, ) and for their intestinal protein glycosylation (Hesselager, Everest‐Dass, Thaysen‐Andersen, Bendixen, & Packer, ). Furthermore, the intestinal mucosa of piglets with the susceptible genotype ( MUC4 CG/GG ) had an up‐regulation of genes related to antimicrobial peptide and immune function such as lipopolysaccharide binding protein ( LBPI ) and regenerating islet‐derived 3 gamma ( REG3G) compared to pigs with a resistant genotype (Trevisi et al, ).…”