Maternal probiotic supplementation at different reproductive statuses enhances sow performance by shaping sow-offspring gut microbiota colonization

<title>Abstract</title> <p> Background Perinatal gut microbiota dynamics crucially impact maternal and fetal metabolism and can be modulated by probiotics. Although <italic>Bacillus coagulans</italic> C56 ( <bold>C56</bold> ) is a promising probiotic, its stage-specific effects in sow production remain unexplored. This study investigated how 0.03% C56 supplementation during late gestation or lactation affects reproductive performance, offspring health, and vertically transmitted microbiota. Results Eighty sows (90 days gestation) were assigned to four groups (n = 20): Con-Con (unsupplemented), C56-Con (late gestation supplementation), Con-C56 (lactation supplementation), and C56-C56 (supplemented during both periods). C56 significantly increased lactating sows' average daily feed intake ( <italic>P</italic>  &lt; 0.05) without altering backfat loss. While late gestation supplementation alone minimally affected litter performance, lactation supplementation increased weaned piglet number and weight ( <italic>P</italic>  &lt; 0.05), milk lactose ( <italic>P</italic>  &lt; 0.05), and decreased urea nitrogen ( <italic>P</italic>  &lt; 0.01). Maternal C56 supplementation alleviated perinatal constipation ( <italic>P</italic>  &lt; 0.05), reduced the Firmicutes/Bacteroidota ratio and <italic>Escherichia-Shigella</italic> abundance ( <italic>P</italic>  &lt; 0.05), and decreased fecal endotoxin levels ( <italic>P</italic>  &lt; 0.05). It also elevated antioxidant indices ( <bold>GSH-Px</bold> , <bold>T-SOD</bold> ) ( <italic>P</italic>  &lt; 0.05), coinciding with increased short-chain fatty acids ( <bold>SCFAs</bold> ) and decreased pathogen-associated quorum-sensing signal autoinducer-2 ( <bold>AI-2</bold> ) ( <italic>P</italic>  &lt; 0.05). Furthermore, maternal C56 vertically delivered <italic>Bacillus</italic> and <italic>Bifidobacterium</italic> to piglets via feces, milk, and skin ( <italic>P</italic>  &lt; 0.05), reducing intestinal <italic>E. coli</italic> colonization ( <italic>P</italic>  &lt; 0.01) and upregulating plasma IgM and IGF-1 ( <italic>P</italic>  &lt; 0.05). Conclusions Lactation is the critical intervention window for C56. By remodeling maternal gut microbiota, enhancing antioxidant capacity, and regulating key metabolites (SCFAs, AI-2), C56 optimizes the gut-mammary axis, promoting beneficial microbial colonization in offspring and superior lactation performance. </p>