Characterization of the Pig Gut Microbiome and Antibiotic Resistome in Industrialized Feedlots in China

Abstract

To characterize the diversity and richness and explore the function and structure of swine gut microbiome and resistome in common pig-farming feedlots, we sampled and metagenomic sequenced the feces of pigs from four different industrialized feedlots located in four distant provinces across China. Surprisingly, more than half of the nonredundant genes (1,937,648, 54.3%) in the current catalogue were newly found compared with the previously published reference gene catalogue (RGC) of the pig gut microbiome. Additionally, 16 high-completeness draft genomes were obtained by analyzing the dominant species on each feedlot. Notably, seven of these species often appeared in the human body sites. Despite a smaller number of nonredundant genes, our study identified more antibiotic resistance genes than those available in the RGC. Tetracycline, aminoglycoside, and multidrug resistance genes accounted for nearly 70% of the relative abundance in the current catalogue. Slightly higher sharing ratios were shown between the industrialized feedlot pig gut microbiomes and human gut microbiomes than that between the RGC and human counterpart (14.7% versus 12.6% in genes and 94.1% versus 87.7% in functional groups, respectively). Furthermore, a remarkably high number of the antibiotic resistance proteins (n =141) were identified to be shared by the pig, human, and mouse resistome, indicating the potential for horizontal transfer of resistance genes. Of the antibiotic resistance proteins shared by pigs and humans, 50 proteins were related to tetracycline resistance, and 49 were related to aminoglycoside resistance.IMPORTANCE The gut microbiota is believed to be closely related to many important physical functions in the host. Comprehensive data on mammalian gut metagenomes has facilitated research on host-microbiome interaction mechanisms, but less is known about pig gut microbiome, especially the gut microbiome in industrialized feedlot pigs, compared with human microbiome. On the other hand, pig production, as an important source of food, is believed to exacerbate the antibiotic resistance in humans due to the abuse of antibiotics in pig production in various parts of the world. This study delineates an intricate picture of swine gut microbiome and antibiotic resistome in industrialized feedlots and may provide insight for the pig producing industry.

Keywords: antibiotic resistance gene; antibiotic resistome; gene catalogue; industrialized feedlot; pig gut microbiome.

FIG 1

Characterization of pig gut gene catalogue in industrialized feedlots. (a) Rarefaction analysis of pig gut microbiome on each feedlot. The number of observed genes in different feedlots was calculated based on a randomly selected specific numbers of reads (per million) with 20 replacements, and the median was plotted. (b) Gene sharing relationship of four feedlots. (c) Comparison of genes between the IFGC and RGC catalogues, with 54.3% unique nonredundant genes in the IFGC that were not overlapped by RGC.

FIG 2

Phylogenetic and functional composition of the pig gut microbiome in industrialized feedlots. (a) Relative abundance of the pig gut microbiome at the genus level in each feedlot. (b) Relative abundance of the pig gut microbiome at the species level in each feedlot. (c) Functional composition of the pig gut microbiome, with functional pathways annotated via the KEGG pathway databases at level B.

FIG 3

Pig gut antibiotic resistome analysis. (a) Composition of AR genes in the pig gut microbiome in industrialized feedlots. (b) Comparison of AR genes between the IFGC and RGC catalogues. (c) Relative abundance of antibiotic resistance genes in each feedlot.

FIG 4

Comparison of the gut antibiotic resistome of pig, human, and mouse. (a) Two nonredundant gene catalogues, the IFGC and RGC, were compared with the integrated human gut gene catalogue (16), and their overlapping rates in genes and functional groups were shown. (b) Comparison of AR types and number of AR genes in the pig, human, and mouse gut resistomes. (c) Pairwise overlap of gut resistomes in pig, human, and mouse.