Porcine Feed Efficiency-Associated Intestinal Microbiota and Physiological Traits: Finding Consistent Cross-Locational Biomarkers for Residual Feed Intake

Abstract

Optimal feed efficiency (FE) in pigs is important for economic and environmental reasons. Previous research identified FE-associated bacterial taxa within the intestinal microbiota of growing pigs. This study investigated whether FE-associated bacteria and selected FE-associated physiological traits were consistent across geographic locations (Republic of Ireland [ROI] [two batches of pigs, ROI1 and ROI2], Northern Ireland [NI], and Austria [AT]), where differences in genetic, dietary, and management factors were minimized. Pigs (n = 369) were ranked, within litter, on divergence in residual feed intake (RFI), and 100 extremes were selected (50 with high RFI and 50 with low RFI) across geographic locations for intestinal microbiota analysis using 16S rRNA amplicon sequencing and examination of FE-associated physiological parameters. Microbial diversity varied by geographic location and intestinal sampling site but not by RFI rank, except in ROI2, where more-feed-efficient pigs had greater ileal and cecal diversity. Although none of the 188 RFI-associated taxonomic differences found were common to all locations/batches, Lentisphaerae, Ruminococcaceae, RF16, Mucispirillum, Methanobrevibacter, and two uncultured genera were more abundant within the fecal or cecal microbiota of low-RFI pigs in two geographic locations and/or in both ROI batches. These are major contributors to carbohydrate metabolism, which was reflected in functional predictions. Fecal volatile fatty acids and salivary cortisol were the only physiological parameters that differed between RFI ranks. Despite controlling genetics, diet specification, dietary phases, and management practices in each rearing environment, the rearing environment, encompassing maternal influence, herd health status, as well as other factors, appears to impact intestinal microbiota more than FE.IMPORTANCE Interest in the role of intestinal microbiota in determining FE in pigs has increased in recent years. However, it is not known if the same FE-associated bacteria are found across different rearing environments. In this study, geographic location and intestinal sampling site had a greater influence on the pig gut microbiome than FE. This presents challenges when aiming to identify consistent reliable microbial biomarkers for FE. Nonetheless, seven FE-associated microbial taxa were common across two geographic locations and/or two batches within one location, and these indicated a potentially "healthier" and metabolically more capable microbiota in more-feed-efficient pigs. These taxa could potentially be employed as biomarkers for FE, although bacterial consortia, rather than individual taxa, may be more likely to predict FE. They may also merit consideration for use as probiotics or could be targeted by dietary means as a strategy for improving FE in pigs in the future.

Keywords: feed efficiency; geographic location; intestinal microbiota; pigs.

FIG 1

Alpha diversity of the microbiota within the ileum (A) and cecum (B) of pigs ranked on residual feed intake (RFI¹) from Republic of Ireland batch 2 (ROI2).

FIG 2

Principal-coordinate analysis (PCoA) plots (based on OTUs) by RFI rank (A) and sample type (B).

FIG 3

Principal-coordinate analysis plots (based on OTUs) for feces collected from pigs on day 70 (A) and day 134 (B) of age and in ileal (C) and cecal (D) digesta. ROI, Republic of Ireland; AT, Austria; NI, Northern Ireland.

FIG 4

(A to C) RFI-associated bacterial taxa common to more than one geographic location in feces from pigs at day 70 (A) and day 134 (B) and in cecal digesta (C). Median relative abundances (percent) of these taxa in low-RFI (blue boxes) and high-RFI (red boxes) pigs are also shown. (D) RFI-associated bacterial taxa shared across geographic locations, irrespective of sample type. Only taxa that were significantly different between high- and low-RFI ranks across locations are depicted (P ≤ 0.05). Digesta was not sampled from NI pigs. P, phylum; F, family; G, genus.

FIG 5

Common RFI-associated predicted microbial pathways in low- and high-RFI pigs across geographic locations. Only the predicted pathways that were significantly different between high- and low-RFI ranks across locations are depicted.

FIG 6

Effect of ranking pigs on RFI on volatile fatty acid (VFA) concentrations (millimoles per gram) in feces of ROI1 pigs at day 70 (A) and day 134 (B) of age and in ileal digesta (C) and cecal digesta (D) of ROI1 and AT pigs. VFAs that do not share a superscript letter (a and b) are significantly different from each other (P < 0.05).

FIG 7

Schematic showing pig selection based on RFI and sampling procedure across geographic locations. ¹one common boar was used across the three locations to minimize genetic variation; ²pigs were ranked on RFI at between 70 and 120 days of age; ³pigs were slaughtered at ∼134 days of age, and ileal and cecal digesta were collected; ⁴volatile fatty acids; ⁵lipopolysaccharide.