Screening of Microbes Associated With Swine Growth and Fat Deposition Traits Across the Intestinal Tract

Abstract

Pigs, as one of the most common livestock species worldwide, are expected to have a fast growth rate and lower subcutaneous fatness but higher intramuscular fat ("marbling meat"). Nowadays, it is believed that not only host genetics but also its gut microbiomes can modulate farm animal phenotypes, however, many of the mechanisms remain elusive. We measured the body weight (BW), average daily gain (ADG), backfat thickness (BFT), and intramuscular fatness (IMF) of 91 Enshi pigs at 260 days of age, then genotyped each one individually using a 50K single nucleotide polymorphism array and performed 16S ribosomal RNA gene sequencing on 455 microbial samples from the jejunum, ileum, cecum, colon, and rectum. The microbial diversity showed notable spatial variation across the entire intestinal tract, with the cecum and colon having the highest α-diversity. The cecal and colonic microbiotas made greater contributions to BW and ADG and accounted for 22-37% of the phenotypic variance. The jejunal and cecal microbiotas contributed more (13-31%) to the BFT and IMF than the other segments. Finally, from cecum, colon, and jejunum, we identified eight microbial taxa that were significantly correlated with the target traits. The genera Alloprevotella and Ruminococcaceae UCG-005 were highly positively correlated with BW and ADG. The genera Prevotellaceae UCG-001 and Alistipes in the cecum and Clostridium sensu stricto 1 in the jejunum were highly positively correlated with BFT and IMF. The genera Stenotrophomonas, Sphaerochaeta, and Desulfovibrio were negatively associated with the mentioned traits. These findings could aid in developing strategies for manipulating the gut microbiota to alter production performance in pigs.

Keywords: 16S RNA; intestinal gut segment; meat qualities; microbiota; pig.

FIGURE 1

Spatial variations of the microbial composition and diversity across the intestinal tract. (A) Venn plot of the OTU numbers in each gut segment. (B) Principal coordinate analysis plot based on Bray–Curtis dissimilarities. (C) α-Diversity comparison based on the Shannon diversity index, with ANOVA to determine significant differences (^∗∗p < 0.01). (D) Relative abundances in the dominant phyla across the intestinal tract. (E) Relative abundances of dominant genera across the intestinal tract. Only the genera with an abundance of > 1.0% in any segment are plotted.

FIGURE 2

Description of functional capacities of the gut microbiota in each gut segment. (A) Overlap of the top 50 predictions across the five gut segments. (B) Description of the top 20 functional classifications. y-axis lists the functional classifications. x-axis shows the sum abundance of microbes in the corresponding function classification. Colored squares indicate different Kyoto Encyclopedia of Genes and Genomes pathways; colored circles indicate the subclassifications in the Kyoto Encyclopedia of Genes and Genomes pathway of metabolism.

FIGURE 3

Contribution of host genetics and gut microbiota to target traits. From top to bottom, the figures describe the heritability and microbiability of body weight, average daily gain, backfat thickness, and intramuscular fatness.

FIGURE 4

Microbial detections via Wilcoxon rank-sum tests between divergent groups and their distributions. (A) Volcano plots for differentially presented microbes in the cecum, colon, and jejunum for BW, ADG, BFT, and IMF. Red points represent upregulated microbes with a log2 (fold change) > 1 and p < 0.05; blue points represent downregulated microbes with a log2 (fold change) < -1 and p_adj < 0.05; gray points represent microbes with no significant difference. Fold change = normalized microbial abundance in the highest 20% group/lowest 20% group. (B) Distributions of significant microbes on phyla and traits. (C–E) Major families to which the significant microbes belong within the phyla of Firmicutes, Bacteroidetes, and Proteobacteria.

FIGURE 5

Candidate microorganisms for growth and fat-related traits. (A) Correlation coefficients for the BW, ADG, BFT, IMF, and eight microbial genera. Upper and lower diagonals indicate the Pearson and Spearman correlations, respectively. Diagonal shows the traits and gut segments (JE: jejunum, CE: cecum, and CO: colon). (B) Detection rate of these seven microbial genera across the intestinal tract. (C) Differences in BW, ADG, BFT, and IMF between the top and bottom abundances of Ruminococcaceae UCG 005, Prevotellaceae UCG 001, Stenotrophomonas, and Desulfovibrio.