Exploring a Possible Link between the Intestinal Microbiota and Feed Efficiency in Pigs

Abstract

Feed efficiency (FE) is critical in pig production for both economic and environmental reasons. As the intestinal microbiota plays an important role in energy harvest, it is likely to influence FE. Therefore, our aim was to characterize the intestinal microbiota of pigs ranked as low, medium, and high residual feed intake ([RFI] a metric for FE), where genetic, nutritional, and management effects were minimized, to explore a possible link between the intestinal microbiota and FE. Eighty-one pigs were ranked according to RFI between weaning and day 126 postweaning, and 32 were selected as the extremes in RFI (12 low, 10 medium, and 10 high). Intestinal microbiota diversity, composition, and predicted functionality were assessed by 16S rRNA gene sequencing. Although no differences in microbial diversity were found, some RFI-associated compositional differences were revealed, principally among members of Firmicutes, predominantly in feces at slaughter (albeit mainly for low-abundance taxa). In particular, microbes associated with a leaner and healthier host (e.g., Christensenellaceae, Oscillibacter, and Cellulosilyticum) were enriched in low RFI (more feed-efficient) pigs. Differences were also observed in the ileum of low RFI pigs; most notably, Nocardiaceae (Rhodococcus) were less abundant. Predictive functional analysis suggested improved metabolic capabilities in these animals, especially within the ileal microbiota. Higher ileal isobutyric acid concentrations were also found in low RFI pigs. Overall, the differences observed within the intestinal microbiota of low RFI pigs compared with that of their high RFI counterparts, albeit relatively subtle, suggest a possible link between the intestinal microbiota and FE in pigs.IMPORTANCE This study is one of the first to show that differences in intestinal microbiota composition, albeit subtle, may partly explain improved feed efficiency (FE) in low residual feed intake (RFI) pigs. One of the main findings is that, although microbial diversity did not differ among animals of varying FE, specific intestinal microbes could potentially be linked with porcine FE. However, as the factors impacting FE are still not fully understood, intestinal microbiota composition may not be a major factor determining differences in FE. Nonetheless, this work has provided a potential set of microbial biomarkers for FE in pigs. Although culturability could be a limiting factor and intervention studies are required, these taxa could potentially be targeted in the future to manipulate the intestinal microbiome so as to improve FE in pigs. If successful, this has the potential to reduce both production costs and the environmental impact of pig production.

Keywords: cecum; feces; ileum; residual feed intake; swine.

FIG 1

Principal-coordinate analysis (PCoA) plot (based on OTUs) according to residual feed intake (RFI) rank and sample type (n = 150). Low RFI: feces (n = 36) and digesta (cecal, n = 12; ileal, n = 9); medium RFI: feces (n = 30) and digesta (ceca, n = 10; ileal, n = 9); high RFI: feces (n = 30) and digesta (cecal, n = 8; ileal, n = 6). Plot is based on the unweighted UniFrac distances. The amount of variance is depicted by the percentages in parentheses on each axis. Ellipses denote clustering according to fecal sample time points and intestinal location.

FIG 2

Median relative abundances (%) of bacterial phyla present in pigs ranked by residual feed intake (RFI) across all fecal time points (n = 96) and both intestinal locations (n = 54). ¹, no blast hits/uncultured; *, significant difference (P ≤ 0.05) (candidate division TM7 in the feces at day 138 postweaning and Fusobacteria in the ileum); †, tendency toward significant differences (Actinobacteria in the ileum; P = 0.06) observed between high and low RFI pigs within each sample type.

FIG 3

Median relative abundance (%) of microbial taxa found to be differentially abundant between pigs ranked with low and high residual feed intake (RFI) (P < 0.05) in feces at weaning (n = 32) (A), feces at day 42 pw (n = 32) (B), feces at day 138 pw (n = 32) (C), cecal digesta (n = 30) (D), and ileal digesta (n = 24) (E). Low RFI: feces (n = 36) and digesta (cecal, n = 12; ileal, n = 9); medium RFI: feces (n = 30) and digesta (cecal, n = 10; ileal, n = 9); high RFI: feces (n = 30) and digesta (cecal, n = 8; ileal, n = 6). F, family; G, genus. Horizontal lines in the plots indicate median values of the distributions. The Fusobacteria phylum was also differentially abundant, and this is illustrated in Fig. 2. Some genus-level differences shown in the plots reflect differences at a higher taxonomic level which are not shown here as follows: ¹, Streptococcaceae family; ², Clostridiaceae family; ³, Christensenellaceae family; ⁴, Bacteroidaceae family; ⁵, candidate division TM7 phylum; ⁶, Nocardiaceae family. Some of the animals for which the highest variance from the median values of the taxa distribution was seen had outlying data for more than one taxon, i.e., one low RFI pig had higher relative abundances than the median values for uncultured Christensenellaceae, Actinobacillus, and Oscillibacter and three high RFI pigs had higher relative abundances than the median value for Rhodococcus and Methanosphaera.

FIG 4

Heatmap showing Spearman correlations between bacterial taxa and physiological measures in pigs ranked by residual feed intake (RFI). Low RFI: feces (n = 36) and digesta (cecal, n = 12; ileal, n = 9); medium RFI: feces (n = 30) and digesta (cecal, n = 10; ileal, n = 9); high RFI: feces (n = 30) and digesta (cecal, n = 8; ileal, n = 6). pw, postweaning. Correlations were examined between bacterial taxa (at both the phylum and genus levels) and physiological measures found to be significantly different between low and high RFI pigs. *, P ≤ 0.05.

FIG 5

Comparison of predicted functional pathways for the fecal and intestinal microbiota of pigs ranked by residual feed intake (RFI). Low RFI: feces (n = 12) and digesta (cecal, n = 12; ileal, n = 9); medium RFI: feces (n = 10) and digesta (cecal, n = 10; ileal, n = 9); high RFI: feces (n = 10) and digesta (cecal, n = 8; ileal, n = 6). Pathways are from the KEGG database and level 3 pathways are presented. Only 11 of 23 differences between all RFI ranks are shown, as 6 were pathways present at <0.001% median relative abundance and another 6 were differences observed for medium RFI pigs. Within each pathway, bars that do not share lowercase letters (a, b, and c) are significantly different (P ≤ 0.05), whereas those that do not share uppercase letters (A, B, and C) tended to be different (P ≤ 0.10).

FIG 6

Flow chart depicting animal management, selection, and sample collection. RFI, residual feed intake; pw, postweaning.