Early exposure to agricultural soil accelerates the maturation of the early-life pig gut microbiota

Abstract

Reduced microbial exposure in early childhood is postulated to be associated with subsequent immune deficiencies and associated health conditions. This corollary to the "hygiene hypothesis" has grown of popularity in the medical field, but can only be really tested with animal models. Based on previous observation that access to outdoor environment improves piglets' growth performance, we simulated early microbial exposure by providing pigs with topsoil during the lactation phase. Specifically, pigs from 20 litters were assigned to either control treatments (C) or soil treatments (S): pigs exposed to topsoil from day 4 postpartum to the end of lactation. At weaning, five unisex littermates of 10 sows from each treatment were penned together and grew up in the same conditions. Fecal samples were collected at on d 13 (Lactation: L), 21 (Weaning: WT), 35 (Mid-nursery, MNT), 56 (End of Nursery: EONT) and 96 (End of Growth: EGT) for 16s rRNA amplicon high-throughput sequencing. Overall, common trends of gut microbiota maturation, associated with diet switch from maternal milk to plant-based diet, were observed. Bacteroides, Clostridium XIVa and Enterobacteriaceae were most abundant during lactation, while Prevotella, Megasphaera and Blautia became abundant after weaning. Remarkably, exposure to soil resulted in a faster maturation of the piglets gut microbiota at weaning, while a completely distinct phase was observed at day 35 for control piglets. Soil-exposed piglets tened to harbor a more diverse gut microbiota at weaning and day35, however the more significant changes were at those time points in terms of composition. Prevotella, and a wide range of Firmicutes members were significantly enriched in soil-exposed piglets from the lactation to the end of nursery phase. It can be hypothesized that those taxa were either directly transmitted from the soil or stimulated by the presence of plant material in the soil. Those changes were accompanied by depletion in several potentially harmful taxa, as well as improved growth performance between weaning and the end of nursery phase. Our findings suggest that early exposure to soil strongly influences the maturation of the early-life piglets, probably allows for a better adaptation to the plant-based diet, and possibly improves overall health.

Keywords: Agricultural soil; Early-life; Gut microbiota; Hygiene hypothesis.