Resistance Determinants and Their Genetic Context in Enterobacteria from a Longitudinal Study of Pigs Reared under Various Husbandry Conditions

Poulin-Laprade, Dominic; Brouard, Jean-Simon; Gagnon, Nathalie; Turcotte, Annie; Langlois, Alexandra; Matte, J. J.; Carrillo, Catherine D.; Zaheer, Rahat; McAllister, Tim A.; Topp, Edward; Talbot, Guylaine

doi:10.1128/aem.02612-20

Cited by 16 publications

(14 citation statements)

References 92 publications

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“…(39,40). This may explain the extensive background level of resistance to tetracyclines and MLS B antimicrobials in swine gut bacteria even in the absence of exposure to these antimicrobials, as observed here and reported in many previous studies (37,(41)(42)(43). Until relatively recently in North America, antimicrobials were often administered to all pigs in a herd for non-therapeutic purposes, namely for growth promotion (44).…”

Section: Many Of Thesupporting

confidence: 69%

Novel insights into the pig gut microbiome using metagenome-assembled genomes

Holman¹,

Kommadath²,

Tingley

et al. 2022

Preprint

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Pigs are among the most numerous and intensively farmed food-producing animals in the world. The gut microbiome plays an important role in the health and performance of swine and changes rapidly after weaning. Here, fecal samples were collected from pigs at 7 different times points from 7 to 140 days of age. These swine fecal metagenomes were used to assemble 1,150 dereplicated metagenome-assembled genomes (MAGs) that were at least 90% complete and had less than 5% contamination. These MAGs represented 472 archaeal and bacterial species, and the most widely distributed MAGs were the uncultured species Collinsella sp002391315, Sodaliphilus sp004557565, and Prevotella sp000434975. Weaning was associated with a decrease in the relative abundance of 69 MAGs (e.g. Escherichia coli) and an increase in the relative abundance of 140 MAGs (e.g. Clostridium sp000435835, Oliverpabstia intestinalis). Genes encoding for the production of the short-chain fatty acids acetate, butyrate, and propionate were identified in 68.5%, 18.8%, and 8.3% of the MAGs, respectively. Carbohydrate-active enzymes associated with the degradation of arabinose oligosaccharides and mixed-linkage glucans were predicted to be most prevalent among the MAGs. Antimicrobial resistance genes were detected in 327 MAGs, including 59 MAGs with tetracycline resistance genes commonly associated with pigs such as tet(44), tet(Q), and tet(W). Overall, 82% of the MAGs were assigned to species that lack cultured representatives indicating that a large portion of the swine gut microbiome is still poorly characterized. The results here also demonstrate the value of MAGs in adding genomic context to gut microbiomes.ImportanceMany of the bacterial strains found in the mammalian gut are difficult to culture and isolate due to their various growth and nutrient requirements that are frequently unknown. Here, we assembled strain-level genomes from short metagenomic sequences, so-called metagenome-assembled genomes (MAGs), that were derived from fecal samples collected from pigs at multiple time points. The majority of these MAGs represented bacterial species that have yet to be cultured or described thus underlining the need for cultivation studies that isolate and describe novel bacterial species. The genomic context of a number of antimicrobial resistance genes commonly detected in swine was also determined. In addition, our study connected taxonomy with potential metabolic functions such as carbohydrate degradation and short-chain fatty acid production.

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Section: Many Of Thesupporting

confidence: 69%

Novel insights into the pig gut microbiome using metagenome-assembled genomes

Holman¹,

Kommadath²,

Tingley

et al. 2022

Preprint

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“…Another limitation of our study was that we were not able to track AMR profiles beyond the lifecycle of a single cohort of pigs and thus could not make observations about potential multi-generational impacts of the antimicrobial exposures. Such exposures may be important in maintaining ARGs within a continuous flow of pigs [ 100 ]. Multi-generational studies would also help reveal the source and carryover of ARGs within neonatal pigs, which is an important component of understanding ARG ecology within swine herds.…”

Section: Discussionmentioning

confidence: 99%

The impacts of viral infection and subsequent antimicrobials on the microbiome-resistome of growing pigs

et al. 2022

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Background Antimicrobials are used in food-producing animals for purposes of preventing, controlling, and/or treating infections. In swine, a major driver of antimicrobial use is porcine reproductive and respiratory syndrome (PRRS), which is caused by a virus that predisposes infected animals to secondary bacterial infections. Numerous antimicrobial protocols are used to treat PRRS, but we have little insight into how these treatment schemes impact antimicrobial resistance (AMR) dynamics within the fecal microbiome of commercial swine. The aim of this study was to determine whether different PRRS-relevant antimicrobial treatment protocols were associated with differences in the fecal microbiome and resistome of growing pigs. To accomplish this, we used a metagenomics approach to characterize and compare the longitudinal wean-to-market resistome and microbiome of pigs challenged with PRRS virus and then exposed to different antimicrobial treatments, and a group of control pigs not challenged with PRRS virus and having minimal antimicrobial exposure. Genomic DNA was extracted from pen-level composite fecal samples from each treatment group and subjected to metagenomic sequencing and microbiome-resistome bioinformatic and statistical analysis. Microbiome-resistome profiles were compared over time and between treatment groups. Results Fecal microbiome and resistome compositions both changed significantly over time, with a dramatic and stereotypic shift between weaning and 9 days post-weaning (dpw). Antimicrobial resistance gene (ARG) richness and diversity were significantly higher at earlier time points, while microbiome richness and diversity were significantly lower. The post-weaning shift was characterized by transition from a Bacteroides-dominated enterotype to Lactobacillus- and Streptococcus-dominated enterotypes. Both the microbiome and resistome stabilized by 44 dpw, at which point the trajectory of microbiome-resistome maturation began to diverge slightly between the treatment groups, potentially due to physical clustering of the pigs. Challenge with PRRS virus seemed to correspond to the re-appearance of many very rare and low-abundance ARGs within the feces of challenged pigs. Despite very different antimicrobial exposures after challenge with PRRS virus, resistome composition remained largely similar between the treatment groups. Differences in ARG abundance between the groups were mostly driven by temporal changes in abundance that occurred prior to antimicrobial exposures, with the exception of ermG, which increased in the feces of treated pigs, and was significantly more abundant in the feces of these pigs compared to the pigs that did not receive post-PRRS antimicrobials. Conclusions The fecal microbiome-resistome of growing pigs exhibited a stereotypic trajectory driven largely by weaning and physiologic aging of the pigs. Events such as viral illness, antimicrobial exposures, and physical grouping of the pigs exerted significant yet relatively minor influence over this trajectory. Therefore, the AMR profile of market-age pigs is the culmination of the life history of the individual pigs and the populations to which they belong. Disease status alone may be a significant driver of AMR in market-age pigs, and understanding the interaction between disease processes and antimicrobial exposures on the swine microbiome-resistome is crucial to developing effective, robust, and reproducible interventions to control AMR.

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“…In addition, excessive intake of meat with antibiotics in the body leads to autoimmune decline and organ disease and thus causes harm to human health . Many countries in the world have clearly stipulated that the use of antibiotic drugs in animal husbandry is strictly prohibited and it is an inevitable trend to completely eliminate antibiotic residues in animal products . Functional feed additives are considered as a potential substitute for antibiotics in feed because of their functions of improving organism sub-health, improving immunity and anti-stress ability, and reducing disease incidences …”

Section: Introductionmentioning

confidence: 99%

“…3 Many countries in the world have clearly stipulated that the use of antibiotic drugs in animal husbandry is strictly prohibited and it is an inevitable trend to completely eliminate antibiotic residues in animal products. 4 Functional feed additives are considered as a potential substitute for antibiotics in feed because of their functions of improving organism sub-health, improving immunity and anti-stress ability, and reducing disease incidences. 5 Selenium (Se) is an essential micronutrient, often added to animal feed to promote animal growth.…”

Section: ■ Introductionmentioning

confidence: 99%

Synthesis, Characterization, Immune Regulation, and Antioxidative Assessment of Yeast-Derived Selenium Nanoparticles in Cyclophosphamide-Induced Rats

Ren

Liang

et al. 2021

ACS Omega

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This article introduces an environmentally friendly and more economical method for preparing red selenium nanoparticles (Se-NPs) with high stability, good biocompatibility, and narrow size using yeast as a bio-reducing agent with high antioxidant, immune regulation, and low toxicity than inorganic and organic Se. The yeast-derived Se-NPs were characterized by scanning electron microscopy, transmission electron microscopy, energy dispersive spectroscopy, Fourier transform infrared spectroscopy, X-ray diffraction, and X-ray photoelectron spectroscopy. The results revealed spherical-shaped particles of Se-NPs with an average diameter of 71.14 ± 18.17 nm, an amorphous structure, and surface enhancement with an organic shell layer, that provide precise geometry and stability in the formation of bio-inert gray or black Se-NPs instead of red Se-NPs. Furthermore, the addition of 0.3−0.8 mg/kg Se-NPs in the feed significantly improved the health of mice. As Se-NPs stimulated the oxidative state of mice, it significantly increased the level of GSH-Px, SOD, and AOC, and decreased the level of MDA. The yeast-derived Se-NPs alleviated the immunosuppression induced by cyclophosphamide, whereas protected the liver, spleen, and kidney of mice, stimulated the humoral immune potential of the mice, and significantly increased the levels of I g M, IgA, and I g G. These results indicated that the yeast-derived Se-NPs, as a trace element feed additive, increased the defense of the animal against oxidative stress and infectious diseases and therefore Se-NPs can be used as a potential antibiotic substitute for animal husbandry.

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Resistance Determinants and Their Genetic Context in Enterobacteria from a Longitudinal Study of Pigs Reared under Various Husbandry Conditions

Cited by 16 publications

References 92 publications

Novel insights into the pig gut microbiome using metagenome-assembled genomes

Novel insights into the pig gut microbiome using metagenome-assembled genomes

The impacts of viral infection and subsequent antimicrobials on the microbiome-resistome of growing pigs

Synthesis, Characterization, Immune Regulation, and Antioxidative Assessment of Yeast-Derived Selenium Nanoparticles in Cyclophosphamide-Induced Rats

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