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Applied and environmental microbiology2023; 89(3); e0159022; doi: 10.1128/aem.01590-22

Impacts of Domestication and Veterinary Treatment on Mobile Genetic Elements and Resistance Genes in Equine Fecal Bacteria.

Abstract: Antimicrobial resistance in bacteria is a threat to both human and animal health. We aimed to understand the impact of domestication and antimicrobial treatment on the types and numbers of resistant bacteria, antibiotic resistance genes (ARGs), and class 1 integrons (C1I) in the equine gut microbiome. Antibiotic-resistant fecal bacteria were isolated from wild horses, healthy farm horses, and horses undergoing veterinary treatment, and isolates (9,083 colonies) were screened by PCR for C1I; these were found at frequencies of 9.8% (vet horses), 0.31% (farm horses), and 0.05% (wild horses). A collection of 71 unique C1I isolates (17 and 54 ) was subjected to resistance profiling and genome sequencing. Farm horses yielded mostly C1I (, , , , , ), while vet horses primarily yielded C1I (, , , , , , ); the vet isolates had more extensive resistance and stronger P promoters in the C1Is. All integrons in were flanked by copies of IS, except in , where a novel IS family element (IS) was implicated in mobilization. In the , C1Is were predominantly associated with IS and also IS, Tn, Tn, Tn, and a putative formaldehyde-resistance transposon (Tn). Several large C1I-containing plasmid contigs were retrieved; two of these (plasmid types Y and F) also had extensive sets of metal resistance genes, including a novel copper-resistance transposon (Tn). Both veterinary treatment and domestication increase the frequency of C1Is in equine gut microflora, and each of these anthropogenic factors selects for a distinct group of integron-containing bacteria. There is increasing acknowledgment that a "one health" approach is required to tackle the growing problem of antimicrobial resistance. This requires that the issue is examined from not only the perspective of human medicine but also includes consideration of the roles of antimicrobials in veterinary medicine and agriculture and recognizes the importance of other ecological compartments in the dissemination of ARGs and mobile genetic elements such as C1I. We have shown that domestication and veterinary treatment increase the frequency of occurrence of C1Is in the equine gut microflora and that, in healthy farm horses, the C1I are unexpectedly found in , while in horses receiving antimicrobial veterinary treatments, a taxonomic shift occurs, and the more typical integron-containing are found. We identified several new mobile genetic elements (plasmids, insertion sequences [IS], and transposons) on genomic contigs from the integron-containing equine bacteria.
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Publication Date: 2023-03-07 PubMed ID: 36988354PubMed Central: PMC10057962DOI: 10.1128/aem.01590-22Google Scholar: Lookup
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Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The researchers investigated how domestication and antimicrobial use in horses impact antibiotic resistant bacteria, and the genetic structures that enable this resistance, in the animals’ gut microbiomes. Specifically, they analyzed differences in types and prevalence of these resistant bacteria and their genetic components between wild horses, farm horses, and horses undergoing veterinary treatment.

Method and Findings

  • In this study, the researchers extracted and isolated antibiotic-resistant fecal bacteria from three distinct equine populations: wild horses, healthy domesticated horses, and domestically kept horses currently undergoing veterinary treatment. They gathered a total of 9,083 bacterial colonies across the three groups.
  • They subsequently screened these colonies for class 1 integrons (C1I), a specific type of genetic structure known for their role in antibiotic resistance. They found these structures in the isolated bacteria at differing rates, with the highest prevalence in horses under veterinary treatment (9.8%), followed by farmed horses (0.31%), and wild horses (0.05%).
  • From this array of C1I-positive samples, they isolated 71 unique instances for detailed profiling and genomic sequencing. This detailed analysis allowed better understanding of the types of bacteria carrying these integrons, the specific resistances offered by the integrons, and any other genomic features associated with these bacteria and genetic elements.

Differences Between Equine Populations

  • The analysis showed varied carriage of C1I among different equine populations. Farm horses were found to primarily carry a certain type of bacteria armed with C1Is, the specific details of which are omitted from the summary. Contrastingly, horses under veterinary treatment largely contained a different type of bacteria carrying C1Is.
  • Furthermore, the bacteria isolated from horses undergoing veterinary treatment demonstrated more extensive resistance profiles and contained stronger promoter sequences within the C1Is, indicating a higher potential for dissemination and expression of these resistance elements.

    • Discovered Genetic Components

    • In the course of their study, the researchers identified a variety of mobile genetic elements, such as plasmids, insertion sequences, and transposons, which are structures that can move around within the genome. These components are known to be important tools for bacterial adaptation and survival, including the acquisition of antibiotic resistance.
    • They found that many of these elements were linked or associated with the C1Is they had initially screened for, likely playing a role in the spread and stability of these resistance elements across the equine gut microbiota. Notably, they identified a number of novel genes and structures indicating resistance to various pressures, including metals like copper and formaldehyde.

      • Conclusion and Implications

      • This study concluded that both the process of domestication and the use of antimicrobials are contributing factors to the increased prevalence of antibiotic resistance genes and associated genetic elements such as C1Is in equine gut flora.
      • The researchers stress the importance of a “One Health” approach in tackling growing antimicrobial resistance issues, calling for a global effort that considers the roles of human, animal health, and environmental impacts on the spread of resistance. In this context, the work completed here expands our knowledge of how anthropogenic factors contribute to the development and propagation of resistance from a veterinary perspective.

Cite This Article

APA
Mitchell SW, Moran RA, Elbourne LDH, Chapman B, Bull M, Muscatello G, Coleman NV. (2023). Impacts of Domestication and Veterinary Treatment on Mobile Genetic Elements and Resistance Genes in Equine Fecal Bacteria. Appl Environ Microbiol, 89(3), e0159022. https://doi.org/10.1128/aem.01590-22

Publication

Applied and environmental microbiology
ISSN: 1098-5336
NlmUniqueID: 7605801
Country: United States
Language: English
Volume: 89
Issue: 3
Pages: e0159022
PII: e01590-22

Researcher Affiliations

Mitchell, Scott W
  • School of Life and Environmental Sciences, University of Sydney, Sydney, New South Wales, Australia.
Moran, Robert A
  • Institute of Microbiology and Infection, School of Medical and Dental Sciences, University of Birmingham, Birmingham, United Kingdom.
Elbourne, Liam D H
  • School of Natural Sciences, Macquarie University, Sydney, New South Wales, Australia.
Chapman, Belinda
  • Quantal Bioscience Pty Ltd, Carlingford, New South Wales, Australia.
Bull, Michelle
  • Quantal Bioscience Pty Ltd, Carlingford, New South Wales, Australia.
Muscatello, Gary
  • School of Life and Environmental Sciences, University of Sydney, Sydney, New South Wales, Australia.
Coleman, Nicholas V
  • School of Life and Environmental Sciences, University of Sydney, Sydney, New South Wales, Australia.

MeSH Terms

  • Horses
  • Animals
  • Humans
  • Domestication
  • DNA Transposable Elements
  • Plasmids
  • Integrons / genetics
  • Bacteria / genetics
  • Anti-Bacterial Agents / pharmacology

Conflict of Interest Statement

The authors declare no conflict of interest.

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Citations

This article has been cited 2 times.
  1. Salem S, Abdelsalam NA, Shata AH, Mouftah SF, Cobo-Díaz JF, Osama D, Atteya R, Elhadidy M. Unveiling the microevolution of antimicrobial resistance in selected Pseudomonas aeruginosa isolates from Egyptian healthcare settings: A genomic approach. Sci Rep 2024 Jul 5;14(1):15500.
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  2. Harmer CJ, Hall RM. IS26 and the IS26 family: versatile resistance gene movers and genome reorganizers. Microbiol Mol Biol Rev 2024 Jun 27;88(2):e0011922.
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