Early life administration of milk fat globule membrane promoted SCFA-producing bacteria colonization, intestinal barriers and growth performance of neonatal piglets

Abstract

Milk fat globule membrane (MFGM) possesses various nutritional and biological benefits for mammals, whereas its effects on neonatal gut microbiota and barrier integrity remained unclear. This study investigated the effects of MFGM administration on microbial compositions and intestinal barrier functions of neonatal piglets. Sixteen newborn piglets were randomly allocated into a CON group or MFGM group, orally administered with saline or MFGM solution (1 g/kg body weight) respectively during the first postnatal week, and all piglets were breastfed during the whole neonatal period. The present study found that the MFGM oral administration during the first postnatal week increased the plasma immunoglobulin (Ig) G level, body weight and average daily gain of piglets (P < 0.05) on 21 d. Additionally, MFGM administration enriched fecal SCFA-producing bacteria (Ruminococ aceae_UCG-002, Ruminococ aceae_UCG-010, Ruminococ aceae_UCG-004, Ruminococ aceae_UCG-014 and [Ruminococcus]_gauvrearuii_group), SCFA concentrations (acetate, propionate and butyrate; P < 0.05) and their receptor (G-protein coupled receptor 41, GPR41). Furthermore, MFGM administration promoted intestinal villus morphology (P < 0.05) and barrier functions by upregulating genes of tight junctions (E-cadherin, claudin-1, occludin and zonula occludin 1 [ZO-1]), mucins (mucin-13 and mucin-20) and interleukin (IL)-22 (P < 0.05). Positive correlation was found between the beneficial microbes and SCFA levels pairwise with the intestinal barrier genes (P < 0.05). In conclusion, orally administrating MFGM during the first postnatal week stimulated SCFA-producing bacteria colonization and SCFA generation, enhanced intestinal barrier functions and consequently improved growth performance of neonatal piglets on 21 d. Our findings will provide new insights about MFGM intervention for microbial colonization and intestinal development of neonates during their early life.

Keywords: Gut microbiota; Intestinal barrier; Milk fat globule membrane; Piglet; SCFA.

Fig. 1

Effects of milk fat globule membrane (MFGM) administration on intestinal morphological structure of the neonatal piglets on 21 d. Light microscopy (100×) of the intestinal morphology of duodenum, jejunum and ileum in piglets. CON, piglets fed with saline; MFGM, piglets fed with MFGM.

Fig. 2

Effects of milk fat globule membrane administration on fecal microbiota composition of the neonatal piglets on 21 d. Venn diagram (A); beta-diversity of PCoA based on Unweighted Unifrac distances (B); microbial composition at the phylum and genus levels (C, D); differential microbial composition based on Wilconxon rank sum test (E). CON, piglets fed with saline; MFGM, piglets fed with milk fat globule membrane. ∗P < 0.05.

Fig. 3

Effects of milk fat globule membrane (MFGM) administration on functional prediction of microbial community of the neonatal piglets on 21 d. Differential abundances of KEGG pathways. KEGG = Kyoto Encyclopedia of Genes and Genomes. CON, piglets fed with saline; MFGM, piglets fed with MFGM. ∗P < 0.05; ∗∗P < 0.01.

Fig. 4

Effects of milk fat globule membrane administration on fecal SCFA concentrations and intestinal GPR genes of the neonatal piglets on 21 d. The concentrations of SCFA in colonic content (A); the gene expressions of GPRs in colonic mucosa (B). CON, piglets fed with saline; MFGM, piglets fed with milk fat globule membrane. GPR41 = G-protein coupled receptor 41; GPR43 = G-protein coupled receptor 43; GPR119 = G-protein coupled receptor 119; GPR120 = G-protein coupled receptor 120. ∗P < 0.05.

Fig. 5

Effects of milk fat globule membrane administration on intestinal barrier functions associated genes of the neonatal piglets on 21 d. Gene expressions of tight junctions, mucins, cytokines and Reg3γ in ileal mucosa (A to C) and colonic mucosa (D to F). CON, piglets fed with saline; MFGM, piglets fed with milk fat globule membrane. ZO-1 = zonula occludin 1; TNF-α = tumor necrosis factor α; IFN-γ = interferon γ; IL-1β = interleukin 1β; IL-10 = interleukin 10; IL-22 = interleukin 22; Reg3γ = regenerating gene 3γ. ∗P < 0.05.

Fig. 6

Spearman correlation analysis between microbiota and SCFA concentrations, intestinal barrier functions associated gene expressions. The correlation heatmap of microbiota and SCFA levels in feces (A), as well as intestinal barrier genes (B). ∗P < 0.05, ∗∗P < 0.01, ∗∗∗P < 0.001.