Intrauterine growth restriction alters growth performance, plasma hormones, and small intestinal microbial communities in growing-finishing pigs

Abstract

Background: The interaction of the gut microbiota with key metabolic and physiological processes may be associated with poor growth outcomes in animals born with intrauterine growth restriction (IUGR).

Results: Growth performance, plasma hormone concentrations, and intestinal microbiota composition were analyzed in IUGR pigs and in normal birth weight (NBW) pigs when the NBW pigs reached 25, 50, and 100 kg of body weight (BW). Compared to NBW pigs, IUGR pigs had lower initial, weaned, and final BW, and lower average daily gain and average daily feed intake in all the considered time points. In the 25 kg BW group, IUGR pigs had higher concentrations of plasma ghrelin and pancreatic polypeptide (PP), but lower insulin concentration than NBW pigs, while the situation was reversed in the 50 kg BW group. As compared to NBW pigs, IUGR pigs had higher microbial alpha diversity in the jejunum and ileum; in the 50 and 100 kg BW groups, IUGR pigs had higher Firmicutes abundance but lower Proteobacteria abundance in the jejunum, and lower Lactobacillus abundance in the jejunum and ileum; in the 25 kg BW group, IUGR pigs showed higher unclassified Ruminococcaceae abundance in the ileum; and in 25 and 50 kg BW groups, IUGR pigs showed lower Ochrobactrum abundance in the jejunum. Spearman's correlation revealed that Lactobacillus was negatively correlated with growth performance, while unclassified Ruminococcaceae was positively correlated. Predictive metagenomic analysis detected significantly different expression of genes in the intestinal microbiota between IUGR and NBW pigs, suggesting different metabolic capabilities between the two groups.

Conclusions: Growing-finishing IUGR pigs showed lower growth performance, higher microbial alpha diversity, and differences in plasma hormone concentrations compared to NBW pigs. Alterations in the abundance of Firmicutes, Proteobacteria, Ruminococcaceae, Lactobacillus, and Ochrobactrum in the small intestine may be associated with IUGR, and may therefore serve as a future target for gut microbiota intervention in growing-finishing IUGR pigs.

Keywords: Growing-finishing pigs; Growth performance; Intrauterine growth restriction; Microbial community; Small intestine.

Fig. 1

Microbial alpha diversity in the jejunum and ileum contents of intrauterine growth retardation (IUGR) pigs and normal birth weight (NBW) pigs in the 25, 50, and 100 kg BW groups. The data presented are obtained from 10 animals in each group (n = 10). a ACE index, b Simpson index, c Shannon index, and d Chao1 index. * denotes a significant difference (P < 0.05) among different treatments

Fig. 2

Differences in intestinal microbial community structure between intrauterine growth retardation ( IUGR) pigs and normal birth weight ( NBW) pigs in the 25, 50, and 100 kg BW groups, and each symbol represents the intestinal microbiota of one pig. The data presented are obtained from 10 animals in each group (n = 10). a Principal coordinate analysis (PCoA) along the axes IUGR and NBW. b Partial least square discriminant analysis (PLS-DA) based on an unweighted UniFrac distances score plot of jejunum and ileum microbiota. Each point represents the microbial community of one pig

Fig. 3

Phylum-level microbial community structure in the jejunum (a) and ileum (b) and genus-level structure in the jejunum (c) and ileum (d) in intrauterine growth retardation (IUGR) pigs and normal birth weight (NBW) pigs. The data presented are obtained from 10 animals in each group (n = 10). Relative abundances of microbial phyla with > 0.01% proportion and genera for the top 50 relative abundance are listed. JI and JN represent samples obtained from the jejunum of IUGR pigs and NBW pigs, respectively; II and IN represent samples obtained from the ileum of IUGR pigs and NBW pigs, respectively. Twenty-five, 50, and 100 represent 25, 50, and 100 kg BW groups

Fig. 4

Data for the small intestinal microbial compositions of intrauterine growth retardation (IUGR) pigs and normal birth weight (NBW) pigs at the phylum level were imported into the statistical analysis of metagenomic profiles (STAMP) software for statistical analysis. The data presented are obtained from 10 animals in each group (n = 10). Differences were considered significant at P < 0.05 using the Mann-Whitney U-test. JI and JN represent samples obtained from the jejunum of IUGR pigs and NBW pigs, respectively; II and IN represent samples obtained from the ileum of IUGR pigs and NBW pigs, respectively. Twenty-five, 50, and 100 represent 25, 50, and 100 kg BW groups

Fig. 5

LEfSe analysis of small intestinal microbial compositions of intrauterine growth retardation (IUGR) pigs and normal birth weight (NBW) pigs throughout the trial at genus level. The data presented are obtained from 10 animals in each group (n = 10). Significant differences (LDA score ≥ 3, P < 0.05) for jejunum and ileum in growing-finishing pigs are shown. JI and JN represent samples obtained from the jejunum of IUGR pigs and NBW pigs, respectively; II and IN represent samples obtained from the ileum of IUGR pigs and NBW pigs, respectively. Twenty-five, 50, and 100 represent 25, 50, and 100 kg BW groups

Fig. 6

Correlations between the growth performance and most common 20 genera according to relative abundance in the 25 (a), 50 (b), and 100 (c) kg BW groups in the jejunum; and in the 25 (d), 50 (e), and 100 (f) kg BW groups in the ileum. The data presented are obtained from 10 animals in each group (n = 10). Average daily gain (ADG), initial body weight (BW at birth), weaned BW, and final BW are presented. Red, blue, and white represent significantly positive correlation, negative correlation, and no significant correlation, respectively. * indicates P < 0.05

Fig. 7

Predictive metagenomics showing differences in function between intrauterine growth retardation (IUGR) pigs and normal birth weight (NBW) pigs in the jejunum and ileum using PICRUSt analysis at level 1 (a) and level 2 (b). The data presented are obtained from 10 animals in each group (n = 10). JI and JN represent samples obtained from the jejunum of IUGR pigs and NBW pigs, respectively; II and IN represent samples obtained from the ileum of IUGR pigs and NBW pigs, respectively. Twenty-five, 50, and 100 represent 25, 50, and 100 kg BW groups

Fig. 8

Predictive metagenomics showing differences in function between intrauterine growth retardation (IUGR) and normal birth weight (NBW) pigs in the jejunum using PICRUSt analysis (level 3). The data presented are obtained from 10 animals in each group (n = 10). JI and JN represent samples obtained from the jejunum of IUGR pigs and NBW pigs, respectively; 25, 50, and 100 represent 25, 50, and 100 kg BW groups. LEfSe analysis was utilized to identify potentially enriched pathways. Pathways with LDA scores ≥2 are shown in the 25 kg BW group (a), and pathways with LDA scores ≥3 in the 50 (b) and 100 (c) kg BW groups

Fig. 9

Predictive metagenomics showing differences in function between intrauterine growth retardation (IUGR) pigs and normal birth weight (NBW) pigs in the ileum using PICRUSt analysis (level 3). The data presented are obtained from 10 animals in each group (n = 10). II and IN represent samples obtained from the ileum of IUGR pigs and NBW pigs, respectively. Twenty-five, 50, and 100 represent 25, 50, and 100 kg BW. LEfSe analysis was used to identify potentially enriched pathways. Pathways with LDA scores ≥2 in the 25 kg BW group (a), and LDA scores ≥3 in the 50 (b) and 100 (c) kg BW groups are shown