Maternal probiotic mixture supplementation optimizes the gut microbiota structure of offspring piglets through the gut-breast axis

Delivery and weaning are major stressful events in sows and piglets, adversely affecting production and growth performance and causing economic losses to swine farms. Probiotics as safe antibiotic alternatives have great potential for use across all stages of livestock farming. Here, 18 pregnant sows from clinical farms randomly divided into two groups, one fed a basal diet (CON group) and the other fed a basal diet plus a probiotic mixture [CBB group, CBB-mix containing 2×1011 CFU Lactobacillus johnsonii (CJ21), 2×108 CFU Bacillus subtilis (BS15), and 2×108 CFU Bacillus licheniformis (BL21)], for 20 d before delivery. The effects of maternal CBB-mix supplementation on sow colostrum metabolome and offspring piglets’ clinical performance, immune status, and gut microbiota were investigated. Additionally, 177 piglets were randomly divided into 4 groups, including CC group (piglets and sows fed a basal diet, n=40 from 5 litters), CP group (piglets fed the basal diet plus CBB-mix and sows fed the basal diet, n=38 from 4 litters), PC group (piglets fed the basal diet and sows fed the basal diet plus CBB-mix, n=50 from 4 litters), PP group (both piglets and sows fed the basal diet plus CBB-mix, n=49 from 5 litters). Among that, CP and PP groups were added CBB-mix (7×109 CFU of CJ21, 7×106 CFU of BS15, and 7×106 CFU of BL21) in the creep feed from 11 days of age for 18 d to study the direct effects of CBB-mix on the growth performance of piglets. Maternal CBB-mix supplementation improved sow production performance, including litter size at birth and litter weight at birth (P<0.05). Piglets born from CBB-mix-fed sows exhibited increased litter size at weaning and reduced diarrhea incidence from 1 to 10 days of age (P<0.05). Additionally, systemic immune status and antioxidant capabilities improved in both sows and piglets. Maternal CBB-mix supplementation reconstituted the gut microbiota structure and increased the Sobs index and Shannon index of fecal microbiota in both sows and piglets (P<0.05). The relative abundance of Firmicutes and Clostridium_sensu_stricro_1 in sow feces was decreased after feeding CBB-mix (P<0.05). In piglets, 10-day-old feces had relatively more abundant Lactobacillus but less Escherichia-Shigella than 1-day-old feces (P<0.05), indicating that maternal feeding CBB-mix alone affects the gut microbiota community of offspring piglets via the gut-breast axis. Piglets born from CBB-mix-fed sows had continuously decreased fecal the relative abundance of Escherichia-Shigella at 28 days of age (P<0.05). Consistently, the metabolite profile in sow milk was also changed by CBB-mix. Colostrum metabolome showed that CBB-mix significantly regulated tryptophan metabolism and primary bile acid biosynthesis pathways. Our data demonstrated that maternal CBB-mix supplementation effectively improved the production performance of sows and their offspring’s growth performance. Through the gut-breast axis (interaction between gut microbiota and mammary glands), feeding CBB-mix to sows impacted the gut microbiota of their offspring. This study provides strategy and evidence for maternal probiotic supplementation to improve immune status and gut microbiota homeostasis in response to delivery and weaning.