From mother to piglet: the lasting influence of the maternal microbiome.

Abstract

Background: Given their crucial roles in agriculture and biomedical research, promoting pig health is essential. A balanced gut microbiota is vital for immune development, metabolism and pathogen resistance, and requires optimal initial colonization by beneficial bacteria. This becomes particularly evident during early life stages, like suckling and weaning, where disruptions can lead to long-term health issues. Understanding the factors influencing microbiome development during these phases is fundamental for enhancing pig health. On these basis, rectal swab samples from eighteen sow-piglet pairs were collected at multiple time points from 7 days after birth to 10 days post-weaning, and analyzed through 16S rRNA gene sequencing. This study aims to understand the maternal influence on piglet microbiota development during the suckling-weaning period, exploring microbial diversity, composition and additional influencing factors such as age, piglet and weaning.

Results: α diversity significantly increased with piglet age (p < 0.001) and stabilized upon weaning, with maternal influence and differences between individual piglet affecting variability before weaning. Post-weaning α diversity was influenced by the pen environment (contributing to 14.5-16% of the variability between piglets) rather than age. Both the sow (~ 9.6%) and age of the piglets (20-30%) had a significant impact on the microbial β diversity over the entire timeframe. Moreover, at 10 days post-weaning a significant influence of the cage mates on piglets microbial β diversity was observed (~ 24.6%). Source-tracking analysis revealed a significant maternal contribution to piglet microbiome at 7 days (31.68%), which decreased over time but remained at 13.33% post-weaning. Piglet microbiome exhibited consistency across time, with 22.55-61.23% of bacteria retained from previous stages. Cage mates contributed 53.54% to the microbiome at 10 days post-weaning. Additionally, 68.32% of piglets microbiome at 7 days was derived from sources not included in the study, decreasing to 37.6% by 10 days post-weaning. ASV-level analysis showed that the majority of maternally transmitted ASVs pre-weaning persisted until the last time point, with both beneficial bacteria and pathobionts being transmitted.

Conclusions: This study highlights the significant influence of maternal microbiota on piglet gut microbiome development, affecting both diversity and composition. Beneficial bacteria are transmitted from mothers to offspring and persist through early developmental stages, thereby emphasizing the long-lasting impact of maternal microbiome and the importance of early microbial colonization for piglet health.