Diet shapes the gut microbiome of pigs during nursing and weaning

Abstract

Background: The newborn mammal is rapidly colonized by a complex microbial community, whose importance for host health is becoming increasingly clear. Understanding the forces that shape the early community, especially during the nursing period, is critical to gain insight into how this consortium of microbes is assembled. Pigs present an attractive model for nursing humans, given physiological and compositional similarity of pig and human milk and the utility of pigs in experimental studies. However, there is a paucity of data examining the gut microbiome in nursing pigs from birth through weaning using modern molecular methods and fewer experimental studies that examine the impact of diet on these microbial communities.

Results: We characterized the fecal microbiome of pigs from birth through 7 weeks of age, during which the animals were transitioned from an exclusive diet of sow milk to a starter diet composed of plant and animal-based components. Microbial communities were clearly distinguishable based on diet, being relatively stable absent dietary changes. Metagenomic sequencing was used to characterize a subset of animals before and after weaning, which identified glycan degradation pathways differing significantly between diets. Predicted enzymes active on milk-derived glycans that are otherwise indigestible to the host animal were enriched in the microbial metagenome of milk-fed animals. In contrast, the bacterial metagenome of weaned animals was enriched in functional pathways involved in plant glycan deconstruction and consumption.

Conclusions: The gut microbiome in young pigs is dramatically shaped by the composition of dietary glycans, reflected by the different functional capacities of the microbiome before and after weaning.

Fig. 1

Pig fecal alpha diversity (phylogenetic distance, PD), measured in rarified samples, compared between diets (a) and over time (b). Bars are colored by diet, nursing (blue) or weaned (red). Bars are shown ± SEM

Fig. 2

Principal component analysis plots of pig fecal microbiota colored by diet (a nursing, blue; weaned, red), day (b day 1, dark red; day 3, red; day 5, orange; day 7, yellow; day 14, green; day 21, dark green; day 28, blue; day 35, dark blue; day 42, purple), or litter (c litter 1, red; litter 2, yellow; litter 3, blue)

Fig. 3

Stacked bar plots showing average percentage of bacterial populations in pig feces over time, from left to right, at day 1, 3, 5, 7, 14, 21, 28, 35, and 42. Colored bars below plot indicate diet (blue, nursing; red, weaned)

Fig. 4

Extended error bar plot identifying significant differences between mean proportions of bacterial taxa in nursing (blue) and weaned (red) samples. Corrected p values are shown at right

Fig. 5

Metagenomic sequencing of pig fecal samples analyzed using PCA (a), and bar charts comparing normalized abundances of individual predicted genes involved in lactose utilization (b) and plant-derived glycans (c). All differences between diets shown (blue, nursing; red, weaned) were significant (p < 0.01), unless indicated with an asterisk, where p < 0.05

Fig. 6

Distribution of metagenomic reads from pig fecal samples annotated as key catabolic enzymes in (a) nursing or (b) weaned animals