Maternal Roughage Sources Influence the Gastrointestinal Development of Goat Kids by Modulating the Colonization of Gastrointestinal Microbiota

During pregnancy and lactation, maternal nutrition is linked to the full development of offspring and may have long-term or lifelong effects. However, the influence of the doe’s diet on the gastrointestinal (GI) tract of young kids remains largely unexplored. Therefore, we investigated the effects of doe roughage sources (alfalfa hay, AH, or corn straw, CS) during pregnancy and lactation on kid growth, GI morphology, barrier function, metabolism, immunity, and microbiome composition. The results indicate that, compared with the CS group, does fed an AH diet had significantly higher feed intake (p < 0.01). However, CS-fed does exhibited higher neutral detergent fiber (NDF) digestibility (p < 0.05). There were no significant differences in animal (doe or kid) weight among the groups (p > 0.05). In the rumen of goat kids, the AH group exhibited a higher papillae width and increased levels of interleukin-10 (IL-10) compared with the CS group (p < 0.05). In the jejunum of goat kids, the AH group showed a higher villus-height-to-crypt-depth (VH/CD) ratio, as well as elevated levels of secretory immunoglobulin A (SIgA), immunoglobulin G (IgG), IL-10, acetate, and total volatile fatty acids (TVFAs), when compared with the CS group (p < 0.05). Transcriptome analysis revealed that the source of roughage in does was associated with changes in the GI transcriptome of the kids. Differentially expressed genes (DEGs) in the rumen were mainly associated with tissue development and immune regulation, while the DEGs in the jejunum were mainly associated with the regulation of transferase activity. Spearman correlation analyses indicated significant associations between GI DEGs and phenotypic indicators related to GI development, immunity, and metabolism. LEfSe analysis identified 14 rumen microbial biomarkers and 6 jejunum microbial biomarkers. Notably, these microorganisms were also enriched in the rumen or day 28 milk of the does. Further microbial composition analysis revealed significant correlations between the rumen and milk microbiomes of does and the rumen or jejunum microbiomes of kids. Association analyses indicated that microbial biomarkers interact with host genes, thereby affecting the development and function of the GI system. Additionally, correlation analyses revealed significant association between milk metabolites and the rumen and jejunum microbiomes of kids. This study demonstrated that maternal diet significantly influences the development of microbial ecosystems in offspring by modulating microbial communities and metabolite composition. The early colonization of GI microorganisms is crucial for the structural development, barrier function, immune capacity, and microbial metabolic activity of the GI system.