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mBio2019; 10(5); e02260-19; doi: 10.1128/mBio.02260-19

Clonal Confinement of a Highly Mobile Resistance Element Driven by Combination Therapy in Rhodococcus equi.

Abstract: Antibiotic use has been linked to changes in the population structure of human pathogens and the clonal expansion of multidrug-resistant (MDR) strains among healthcare- and community-acquired infections. Here we present a compelling example in a veterinary pathogen, , the causative agent of a severe pulmonary infection affecting foals worldwide. We show that the (46) gene responsible for emerging macrolide resistance among equine isolates in the United States is part of a 6.9-kb transposable element, Tn, actively mobilized by an IS family transposase. Tn is carried on an 87-kb conjugative plasmid, pRErm46, transferable between strains at frequencies up to 10 The (46) gene becomes stabilized in by pRErm46's apparent fitness neutrality and wholesale Tn transposition onto the host genome. This includes the conjugally exchangeable pVAPA virulence plasmid, enabling the possibility of cotransfer of two essential traits for survival in macrolide-treated foals in a single mating event. Despite its high horizontal transfer potential, phylogenomic analyses show that (46) is paradoxically confined to a specific clone, 2287. 2287 also carries a unique mutation conferring high-level resistance to rifampin, systematically administered together with macrolides against rhodococcal pneumonia on equine farms. Our data illustrate that under sustained combination therapy, several independent "founder" genetic events are concurrently required for resistance, limiting not only its emergence but also, crucially, horizontal spread, ultimately determining multiresistance clonality. MDR clades arise upon acquisition of resistance traits, but the determinants of their clonal expansion remain largely undefined. Taking advantage of the unique features of infection control in equine farms, involving the same dual antibiotic treatment since the 1980s (a macrolide and rifampin), this study sheds light into the determinants of multiresistance clonality and the importance of combination therapy in limiting the dissemination of mobile resistance elements. Clinically effective therapeutic alternatives against foal pneumonia are currently lacking, and the identified macrolide-rifampin MDR clone 2287 has serious implications. Still at early stages of evolution and local spread, 2287 may disseminate globally, posing a significant threat to the equine industry and, also, public health due to the risk of zoonotic transmission. The characterization of the 2287 clone and its resistance determinants will enable targeted surveillance and control interventions to tackle the emergence of MDR .
Copyright © 2019 Álvarez-Narváez et al.
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Publication Date: 2019-10-15 PubMed ID: 31615959PubMed Central: PMC6794481DOI: 10.1128/mBio.02260-19Google 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.

This research investigates the antibiotic resistance in Rhodococcus equi, a veterinary pathogen causing severe lung infection in foals. The study reveals that the gene responsible for emerging antibiotic resistance in the US equine R. equi population is part of the mobile genetic element, Tn. It further explores how combination therapy can limit the spread of this resistance.

Resistance Element in Rhodococcus equi

  • The researchers identify the errm(46) gene as the key player in the observed antibiotic resistance. This gene is located on a mobile genetic element, Tn, and is easily transferable between R. equi strains.
  • The protein encoded by the errm(46) gene confers the bacterium resistance to macrolide, a category of antibiotics commonly used against R. equi infections.

Role of Conjugative Plasmid

  • The errm(46) gene resides on a 6.9kb transposable element, Tn, which is mobilized by a specific enzyme, an IS family transposase.
  • The Tn element is carried by an 87-kb conjugative plasmid, pRErm46, which allows the spread of the errm(46) gene between R. equi strains. This study shows that pRErm46 has a high transfer frequency.
  • Once acquired by a new strain, the errm(46) gene becomes stable due to the plasmid’s apparent fitness neutrality and Tn’s ability to transpose onto the host genome.

Confinement to Specific R. equi Clone

  • Despite the high mobility of the errm(46) gene, it is found confined to a specific R. equi clone, 2287, resulting in the clonal spread of this antibiotic resistance.
  • The 2287 clone also carries a unique mutation that provides additional resistance to rifampin, another antibiotic used in combination with macrolides against R. equi infection. The concurrent requirement for multiple genetic changes for resistance under dual drug therapy significantly limits the emergence and spread of antibiotic resistance among R. equi strains.

Implications and Threats

  • This study underscores the risks associated with the potential global spread of R. equi clone 2287, given its dual-antibiotic resistance. This could pose a substantial threat not only to the equine industry but also to public health because of possible transmission to humans.
  • The lack of clinically effective alternatives to fight R. equi pneumonia in foals makes the emergence of multidrug-resistant clones like 2287 a serious problem. Therefore, characterizing the 2287 clone and its resistance determinants can guide surveillance and control measures effectively.

Cite This Article

APA
Álvarez-Narváez S, Giguère S, Anastasi E, Hearn J, Scortti M, Vázquez-Boland JA. (2019). Clonal Confinement of a Highly Mobile Resistance Element Driven by Combination Therapy in Rhodococcus equi. mBio, 10(5), e02260-19. https://doi.org/10.1128/mBio.02260-19

Publication

mBio
ISSN: 2150-7511
NlmUniqueID: 101519231
Country: United States
Language: English
Volume: 10
Issue: 5
PII: e02260-19

Researcher Affiliations

Álvarez-Narváez, Sonsiray
  • Microbial Pathogenesis Group, Infection Medicine, Edinburgh Medical School (Biomedical Sciences), University of Edinburgh, Edinburgh, United Kingdom.
Giguère, Steeve
  • Department of Large Animal Medicine, University of Georgia, Athens, Georgia, USA.
Anastasi, Elisa
  • Microbial Pathogenesis Group, Infection Medicine, Edinburgh Medical School (Biomedical Sciences), University of Edinburgh, Edinburgh, United Kingdom.
Hearn, Jack
  • Institute of Evolutionary Biology, University of Edinburgh, Edinburgh, United Kingdom.
Scortti, Mariela
  • Microbial Pathogenesis Group, Infection Medicine, Edinburgh Medical School (Biomedical Sciences), University of Edinburgh, Edinburgh, United Kingdom.
Vázquez-Boland, José A
  • Microbial Pathogenesis Group, Infection Medicine, Edinburgh Medical School (Biomedical Sciences), University of Edinburgh, Edinburgh, United Kingdom v.boland@ed.ac.uk.

MeSH Terms

  • Anti-Bacterial Agents / pharmacology
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism
  • Drug Resistance, Bacterial / genetics
  • Macrolides / pharmacology
  • Microbial Sensitivity Tests
  • Rhodococcus equi / drug effects
  • Rhodococcus equi / genetics
  • Virulence / genetics

Grant Funding

  • BB/J004227/1 / Biotechnology and Biological Sciences Research Council

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