The effects of antibiotic use on the dynamics of the microbiome and resistome in pigs

Abstract

Antibiotics are widely used in pig farming across the world which has led to concerns about the potential impact on human health through the selection of antibiotic resistant pathogenic bacteria. This worry has resulted in the development of a production scheme known as pigs Raised Without Antibiotics (RWA), in which pigs are produced in commercial farms, but are ear-tagged as RWA until slaughter unless they receive treatment, thus allowing the farmer to sell the pigs either as premium priced RWA or as conventional meat. Development of antibiotic resistance in pig farming has been studied in national surveys of antibiotic usage and resistance, as well as in experimental studies of groups of pigs, but not in individual pigs followed longitudinally in a commercial pig farm. In this study, a cohort of RWA designated pigs were sampled at 10 time points from birth until slaughter along with pen-mates treated with antibiotics at the same farm. From these samples, the microbiome, determined using 16S sequencing, and the resistome, as determined using qPCR for 82 resistance genes, was investigated, allowing us to examine the difference between RWA pigs and antibiotic treated pigs. We furthermore included 176 additional pigs from six different RWA farms which were sampled at the slaughterhouse as an endpoint to substantiate the cohort as well as for evaluation of intra-farm variability. The results showed a clear effect of age in both the microbiome and resistome composition from early life up until slaughter. As a function of antibiotic treatment, however, we observed a small but significant divergence between treated and untreated animals in their microbiome composition immediately following treatment, which disappeared before 8 weeks of age. The effect on the resistome was evident and an effect of treatment could still be detected at week 8. In animals sampled at the slaughterhouse, we observed no difference in the microbiome or the resistome as a result of treatment status but did see a strong effect of farm origin. Network analysis of co-occurrence of microbiome and resistome data suggested that some resistance genes may be transferred through mobile genetic elements, so we used Hi-C metagenomics on a subset of samples to investigate this. We conclude that antibiotic treatment has a differential effect on the microbiome vs. the resistome and that although resistance gene load is increased by antibiotic treatment load, this effect disappears before slaughter. More studies are needed to elucidate the optimal way to rear pigs without antibiotics.

Transmission of antimicrobial resistance in the gut microbiome of gregarious cockroaches: the importance of interaction between antibiotic exposed and non-exposed populations

“…This suggests that the gregarious behavior of P. surinamensis facilitates the transmission of bacteria between individuals ( 70 , 71 ) and by extension the transmission of their resistomes. A similar observation has been made among pigs reared together, where the resistomes of treated and untreated individuals converged ( 5 ). However, in that study, the cause of convergence was a reduction in ARG abundance in the treated individuals, and not an increase in ARG abundance in the untreated individuals, as in our study.…”

“…The tet (M) and tet(S/M) genes have wide host ranges, which is attributed to their association with broad host range conjugative transposons and plasmids ( 73 – 76 ), while tet(O) and tet (Q) have been found associated both with the chromosome of some bacterial species and in connection with conjugative transposons and plasmids ( 72 , 73 , 77 , 78 ). Unfortunately, without high-quality metagenomic assemblies or long-read sequences, it is not possible to confirm the location of these genes of interest on the chromosomes or the plasmids ( 5 , 79 ). The wide host range and the association with conjugative transposons could point to horizontal gene transfer during the experiment, which has been recorded before in other cockroaches (e.g.,see reference 80 ).…”

Improvements of weaned pigs barn hygiene to reduce the spread of antimicrobial resistance

“…This suggests a widespread ampicillin resistance, might be related to previous colonization (before arrival) or possibly due to the use of the drug (Dupamox; amoxicillin derivatives) against rare bacterial infections in individual piglets on the studied farm, particularly in experimental groups ( Supplementary Table S1 ). Antibiotic treatment of individual diseased pigs resulted in increased E. coli resistance that can last up to some weeks ( Sali et al, 2021 ; Tams et al, 2023 ). On the other hand, ampicillin is also an old antibiotic widely used in humans and animals and therefore has been heavily exposed to Enterobacteriaceae for many years, resulting in a high basic rate of resistance and the according resistance genes, particularly bla TEM-1 ( Tran-Dien et al, 2018 ).…”

“…Frontiers in Microbiology 08 frontiersin.org experimental groups (Supplementary Table S1). Antibiotic treatment of individual diseased pigs resulted in increased E. coli resistance that can last up to some weeks (Sali et al, 2021;Tams et al, 2023). On the other hand, ampicillin is also an old antibiotic widely used in humans and animals and therefore has been heavily exposed to Enterobacteriaceae for many years, resulting in a high basic rate of resistance and the according resistance genes, particularly bla TEM-1 (Tran-Dien et al, 2018).…”