Impact of Intestinal Microbiota on Growth Performance of Suckling and Weaned Piglets

Abstract

Small-scale studies investigating the relationship between pigs' intestinal microbiota and growth performance have generated inconsistent results. We hypothesized that on farms under favorable environmental conditions (e.g., promoting sow nest-building behavior, high colostrum production, low incidence of diseases and minimal use of antimicrobials), the piglet gut microbiota may develop toward a population that promotes growth and reduces pathogenic bacteria. Using 16S rRNA gene amplicon sequencing, we sampled and profiled the fecal microbiota from 170 individual piglets throughout suckling and postweaning periods (in total 670 samples) to track gut microbiota development and its potential association with growth. During the suckling period, the dominant genera were Lactobacillus and Bacteroides, the latter being gradually replaced by Clostridium sensu scricto 1 as piglets aged. The gut microbiota during the nursery stage, not the suckling period, predicted the average daily growth (ADG) of piglets. The relative abundances of SCFA-producing genera, in particular Faecalibacterium, Megasphaera, Mitsuokella, and Subdoligranulum, significantly correlated with high ADG of weaned piglets. In addition, the succession of the gut microbiota in high-ADG piglets occurred faster and stabilized sooner upon weaning, whereas the gut microbiota of low-ADG piglets continued to mature after weaning. Overall, our findings suggest that weaning is the major driver of gut microbiota variation in piglets with different levels of overall growth performance. This calls for further research to verify if promotion of specific gut microbiota, identified here at weaning transition, is beneficial for piglet growth. IMPORTANCE The relationship between pigs' intestinal microbiota and growth performance is of great importance for improving piglets' health and reducing antimicrobial use. We found that gut microbiota variation is significantly associated with growth during weaning and the early nursery period. Importantly, transitions toward a mature gut microbiota enriched with fiber-degrading bacteria mostly complete upon weaning in piglets with better growth. Postponing the weaning age may therefore favor the development of fiber degrading gut bacteria, conferring the necessary capacity to digest and harvest solid postweaning feed. The bacterial taxa associated with piglet growth identified herein hold potential to improve piglet growth and health.

Keywords: NGS sequencing; SCFA; fiber degrading bacteria; growth; gut microbiota; pig; weaning.

FIG 1

Longitudinal gut microbiota profiles from all piglets and sows’ gut microbiota profiles (A) Principal coordinate analysis (PCoA) plot of microbiota variation based on the Bray-Curtis dissimilarity matrix. Sampling time explained 33% of the microbiota variation, while farm type explained only 1% of the microbiota variation (P = 0.001, PERMANOVA, [farm type 1 = farm 1; farm type 2 = farms 2, 3, and 4]). (B) Violin plots (a combination of the box plot with a kernel density plot) showing microbiota α-diversity (richness and Shannon diversity) at each sampling time in comparison to the sow gut microbiota. The center line denotes the median, the boxes cover the 25th and 75th percentiles, and the whiskers extend to the most extreme data point, which is no more than 1.5 times the length of the box away from the box. Points outside the whiskers represent outlier samples. Significance was calculated using the Wilcoxon rank-sum test. ****, P < 0.0001; ***, P < 0.001; **, P < 0.01; *, P < 0.05; “ns” P > 0.05. (C) Stacked bar plots showing the average relative abundance of dominant bacterial genera (>1%).

FIG 2

Explained variance of select microbiota covariates at various sampling times modeled by envfit. Horizontal bars show the degree of variance (R-squared) explained by each covariate in the model using microbiota profiles at the genus level. The covariates not applicable for the given sampling time are denoted with NA. Nonsignificant covariates are denoted with NS.

FIG 3

Associations between the gut microbiota and overall piglet growth or growth during specific periods. (A) Bar plots showing significant associations (FDR-P < 0.05) between individual bacterial genera and overall ADG. Bacterial genera are colored according to their respective phyla (Bacteroidetes in yellow, Proteobacteria in gray, and Firmicutes in blue). (B) Bar plots showing the predictive power (R-squared) of the gut microbiota at sampling point 1, 2, and 3 for the ADG of its succeeding period (i.e., the growth between sampling point 1 to 2, 2 to 3, and 3 to 4) and the overall ADG.

FIG 4

Microbiota development and maturity and their associations with piglet growth. (A) Heat map showing the relative abundances of the 25 most dominant bacterial genera per Dirichlet multinomial mixtures (DMM) cluster. DMM clustering using the entire piglet data set formed eight distinct clusters. (B) Transitions between DMM clusters throughout sampling time points in the high (N = 157) or low (N = 158) ADG group. The sizes of nodes and edges are scaled by the number of included samples; nodes are colored according to DMM clusters and edges by the transition frequency. Transition frequency was determined by dividing the number of transitions toward a given DMM cluster by the total number of transitions within each time window. Single edges (transitions) are not shown. (C) Microbiota-by-age Z-scores (MAZ), reflecting microbiota maturity, throughout four sampling times in the high-ADG (black line) and low-ADG (blue line) group as modeled using the Loess regression. Gray areas represent the 95% confidence intervals.

FIG 5

ADG group-specific enrichment or depletion of bacterial genera in the gut microbiota during weaning. Heat map showing the 14 bacterial genera with increased or decreased relative abundances, calculated by log₂ fold change, during weaning (sampling time 2 to 3) statistically significant only in high- or low-ADG group (FDR-P < 0.05, log₂ fold change > 1). ***, FDR-P < 0.001; **, FDR-P < 0.01; *, FDR-P < 0.05.