Antibiotic resistance gene sharing networks and the effect of dietary nutritional content on the canine and feline gut resistome

Abstract

Background: As one of the most densely populated microbial communities on Earth, the gut microbiota serves as an important reservoir of antibiotic resistance genes (ARGs), referred to as the gut resistome. Here, we investigated the association of dietary nutritional content with gut ARG diversity and composition, using publicly available shotgun metagenomic sequence data generated from canine and feline fecal samples. Also, based on network theory, we explored ARG-sharing patterns between gut bacterial genera by identifying the linkage structure between metagenomic assemblies and their functional genes obtained from the same data. Results: In both canine and feline gut microbiota, an increase in protein and a reduction in carbohydrate in the diet were associated with increased ARG diversity. ARG diversity of the canine gut microbiota also increased, but less strongly, after a reduction in protein and an increase in carbohydrate in the diet. The association between ARG and taxonomic composition suggests that diet-induced changes in the gut microbiota may be responsible for changes in ARG composition, supporting the links between protein metabolism and antibiotic resistance in gut microbes. In the analysis of the ARG-sharing patterns, 22 ARGs were shared among 46 genera in the canine gut microbiota, and 11 ARGs among 28 genera in the feline gut microbiota. Of these ARGs, the tetracycline resistance gene tet(W) was shared among the largest number of genera, predominantly among Firmicutes genera. Bifidobacterium, a genus extensively used in the fermentation of dairy products and as probiotics, shared tet(W) with a wide variety of other genera. Finally, genera from the same phylum were more likely to share ARGs than with those from different phyla. Conclusions: Our findings show that dietary nutritional content, especially protein content, is associated with the gut resistome and suggest future research to explore the impact of dietary intervention on the development of antibiotic resistance in clinically-relevant gut microbes. Our network analysis also reveals that the genetic composition of bacteria acts as an important barrier to the horizontal transfer of ARGs. By capturing the underlying gene-sharing relationships between different bacterial taxa from metagenomes, our network approach improves our understanding of horizontal gene transfer dynamics.

Metagenomic analysis revealed a wide distribution of antibiotic resistance genes and biosynthesis of antibiotics in the gut of giant pandas

“…The genes abundant in juvenile included those that are involved in fatty acid biosynthesis, phenylalanine metabolism, purine metabolism, glutathione metabolism, antibiotic resistance, and biosynthesis of streptomycin in the shooting stage [ 4 ]. The dietary nutritional content, especially protein content, was previously found associated with the abundance of ARGs in the gut [ 25 ]. Besides milk, bamboo shoots are a good protein source with protein content ranging from 1.49 g/100 g to 4.04 g/100 g in fresh bamboo shoots [ 64 , 65 ].…”

“…Diet is an essential factor that may influence the gut microbiome [ 20 – 24 ]. Increased antibiotic resistance genes (ARGs) have been observed with a high protein diet in a recent study [ 25 ]. Another study revealed a varying rate of expression of genes involved in phenylalanine metabolism, fatty acid biosynthesis, purine metabolism, glutathione metabolism, antibiotic resistance, and streptomycin biosynthesis in the gut of juvenile GPs that were fed with bamboo leaves and shoot as diet and the more genes were found in shooting stage [ 4 ].…”

A review of the resistome within the digestive tract of livestock

“…According to a recent review, β-lactams such as amoxicillin are the most commonly used antimicrobials for dogs and cats in European countries including UK, Italy, and four Nordic countries [ 221 ]. A recent study investigated the profiles of resistome in the digestive tract of dogs and cats and found that tetracycline and aminoglycoside resistance genes were the most abundant among the 23 classes of ARGs, indicating that the gut microbiota of dogs and cats is also a reservoir of ARGs [ 222 ]. We thus speculate that there could be many shared ARGs between these companion and food-producing animals living together in farms considering the similarity of the profiles of predominant ARGs (e.g.…”

Unveiling the Gut Microbiota and Resistome of Wild Cotton Mice, Peromyscus gossypinus , from Heavy Metal- and Radionuclide-Contaminated Sites in the Southeastern United States

“…This selective pressure can enrich antimicrobial resistance genes (ARGs), which can be rapidly disseminated and exchanged between bacteria via horizontal gene transfer of mobile genetic elements (MGEs) or through de novo mutations that are positively selected ( 16 – 18 ). In the intestinal tract of humans and animals, there is evidence that antibiotic use can enrich multiple ARGs in not only gut pathogens, but also commensals ( 4 , 19 – 22 ).…”