Multi-omics Uncovers Distinct Microbial Networks Associated with a Blend of Hydrolysable and Condensed Tannins in Weaned Pigs Reared Under Two Different Farming Conditions

Weaning is a critical phase in pig production, often marked by physiological and microbial shifts that can impair growth and health. Tannins are recognized for antimicrobial, antioxidant, and anti-inflammatory properties and may enhance gut health. This study evaluated the effects of a blend of hydrolysable and condensed and tannins coming from chestnut and quebracho (Silvafeed Nutri P, Silvateam, Italy) on growth performance, health status, and fecal metagenomic and metabolomic profiles of weaned pigs raised in two distinct farming environments. A total of 160 pigs (24 ± 2 days old; T0) were assigned to two weaning units classified as high (H) or low (L) performance based on body weight and litter origin. Within each unit, pigs were allocated to a Control group (CON; n = 40) receiving a standard weaning diet or a Treated group (TRT; n = 40) fed the same diet supplemented with 2 g/kg of the tannin blend. Body weight was recorded at 35 (T1), 49 (T2), and 76 (T3) days of age, and fecal samples collected at the same time points for metagenomic profiling and metabolomic analysis (Metabolon, Inc.). Growth performance was analyzed with a linear model including diet (TRT vs. CON) and farming condition (H vs. L). Metabolomic data were analyzed using sparse partial least squares discriminant analysis (sPLS-DA), and microbial species and functions were profiled with a marker gene–based pipelines (MetaPhlAn 4 and HUMAnN 3). At T2, the diarrhea index was significantly lower in the TRT group than in CON within farm L (P = 0.02). Microbial alpha diversity at T2 and T3 was reduced in farm L (P < 0.05) and in TRT compared with CON (P < 0.01). Beta diversity of both species and functions was influenced by the diet × farming condition interaction across all time points (P < 0.05). At T2, sPLS-DA identified urolithin B and isourolithin A as enriched in the TRT group within farm L, which are known metabolites associated with tannin metabolism known for their ant inflammatory and antioxidant property. Weighted gene correlation network analysis revealed a microbial module containing bacteria with urolithin-producing potential, including Ellagibacter isourolithinifaciens and Enterocloster (SGB14313), which were positively correlated with urolithin B (r = 0.4) and isourolithin A (r = 0.5). In conclusion, dietary supplementation with a chestnut–quebracho tannin blend reduced diarrhea under suboptimal sanitary conditions, likely by promoting a microbial network capable of metabolizing tannins and generating metabolites that support gut health.