Spread of multidrug-resistant IncHI1 plasmids carrying ESBL gene blaCTX-M-1 and metabolism operon of prebiotic oligosaccharides in commensal Escherichia coli from healthy horses, France.
Abstract: The objective of the study was to identify the genetic determinants and characteristics of expanded-spectrum cephalosporin (ESC) resistance in commensal Escherichia coli from healthy horses in France in 2015. Faecal samples from 744 adult horses were screened for ESC-resistant E. coli isolates. The extended-spectrum beta-lactamase (ESBL)/AmpC resistance genes were identified using polymerase chain reaction (PCR) and sequencing. ESC phenotypes were horizontally transferred by conjugation or transformation. Plasmids carrying ESBL/AmpC genes were typed by PCR-based replicon typing, restriction fragment length polymorphism (RFLP), and plasmid multilocus sequence typing (pMLST). The ESC-resistant E. coli isolates were typed by XbaI macrorestriction analysis. Sixteen of 41 stables harboured at least one horse carrying ESC-resistant E. coli. The proportion of individually tested horses carrying ESC-resistant E. coli was 8.5% (28/328). Fifty non-redundant ESC-resistant E. coli isolates showing a great diversity of XbaI macrorestriction profiles belonged mainly to phylogroup B1, and were negative for major E. coli virulence genes, indicating they are commensal isolates. ESBL bla genes were dominant (bla, n=34; bla, n=8; bla, n=2) and located on conjugative plasmids belonging to various incompatibility groups (IncHI1, IncI1, IncN, IncY, or non-typeable). Among these, the multidrug-resistant IncHI1-pST9 plasmids were dominant and simultaneously harboured the bla genes and an operon enabling the metabolism of short-chain fructo-oligosaccharides (scFOS). In conclusion, commensal E. coli of French horses displayed a significant distribution of IncHI1-pST9 plasmids carrying both the bla gene and the fos metabolism operon. This finding highlights the risk of co-selection of multidrug-resistant IncHI1 plasmids carrying ESBL genes possibly mediated by the use of scFOS as prebiotic in horses.
Copyright © 2020 Elsevier B.V. and International Society of Chemotherapy. All rights reserved.
Publication Date: 2020-03-07 PubMed ID: 32156619DOI: 10.1016/j.ijantimicag.2020.105936Google Scholar: Lookup
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- Journal Article
Summary
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This research aims to understand the spread of a drug-resistant bacterium called Escherichia coli in healthy horses across France, with a particular focus on specific genetic elements in the bacterium that resist certain antibiotics and can metabolize prebiotic oligosaccharides. The researchers found that drug-resistant E. coli was present in around 8.5% of horses sampled, and that certain forms of resistance-carrying genetic elements, or plasmids, were particularly prevalent.
Research Methods and Goals
- The researchers collected faecal samples from 744 adult horses from 41 stables to examine the presence and characteristics of Escherichia coli resistant to Expanded-spectrum cephalosporin (ESC), a class of antibiotic.
- By using a variety of molecular biology techniques, such as polymerase chain reaction (PCR) and DNA sequencing, specific resistance genes were identified, and the transfer type, namely conjugation (direct transfer between bacteria) or transformation (uptake from the environment), was determined.
- The researchers further classified these E. coli isolates through various typing methods, including PCR-based replicon typing, restriction fragment length polymorphism (RFLP), and plasmid multilocus sequence typing (pMLST).
- The aim was to comprehend the spread and frequency of drug-resistant E. coli in healthy horses and identify the particular genetic determinants responsible for this resistance.
Findings and Implications
- The data showed that around 8.5% of the tested horses carried ESC-resistant E. coli. The E. coli strains were mainly of the B1 phylogroup and did not carry major virulence genes, indicating they are commensal (harmlessly co-existing with the horse).
- The dominant resistance mechanism was through the Extended Spectrum Beta-Lactamase (ESBL) bla genes which were often found on conjugative plasmids – mobile genetic elements that bacteria use to share genes.
- Importantly, the researchers found that these resistance genes were commonly found on the multidrug-resistant IncHI1-pST9 plasmids, which also carried genes for the metabolism of short-chain fructo-oligosaccharides (scFOS), a type of prebiotic.
- This dual presence poses a potential risk if scFOS are used as prebiotics in horse feed, as their consumption could promote the survival and spread of these multidrug-resistant plasmids in the gut microbiota of horses.
- The study thus underscores the need for careful consideration of prebiotic use in managing livestock health to prevent promoting antibiotic resistance among commensal bacteria.
Cite This Article
APA
de Lagarde M, Larrieu C, Praud K, Lallier N, Trotereau A, Sallé G, Fairbrother JM, Schouler C, Doublet B.
(2020).
Spread of multidrug-resistant IncHI1 plasmids carrying ESBL gene blaCTX-M-1 and metabolism operon of prebiotic oligosaccharides in commensal Escherichia coli from healthy horses, France.
Int J Antimicrob Agents, 55(6), 105936.
https://doi.org/10.1016/j.ijantimicag.2020.105936 Publication
Researcher Affiliations
- OIE Reference Laboratory for Escherichia coli, Faculty of Veterinary Medicine, Université de Montréal, Saint-Hyacinthe, QC, Canada.
- INRAE, Université de Tours, ISP, Nouzilly, France.
- INRAE, Université de Tours, ISP, Nouzilly, France.
- INRAE, Université de Tours, ISP, Nouzilly, France.
- INRAE, Université de Tours, ISP, Nouzilly, France.
- INRAE, Université de Tours, ISP, Nouzilly, France.
- OIE Reference Laboratory for Escherichia coli, Faculty of Veterinary Medicine, Université de Montréal, Saint-Hyacinthe, QC, Canada.
- INRAE, Université de Tours, ISP, Nouzilly, France.
- INRAE, Université de Tours, ISP, Nouzilly, France. Electronic address: benoit.doublet@inrae.fr.
MeSH Terms
- Animals
- Anti-Bacterial Agents / pharmacology
- Bacterial Proteins / genetics
- Cephalosporins / pharmacology
- Conjugation, Genetic
- Drug Resistance, Multiple, Bacterial / genetics
- Escherichia coli / drug effects
- Escherichia coli / genetics
- Escherichia coli / metabolism
- Feces / microbiology
- France / epidemiology
- Horses / microbiology
- Multilocus Sequence Typing
- Oligosaccharides / metabolism
- Operon
- Phylogeny
- Plasmids / genetics
- Prebiotics / microbiology
- beta-Lactamases / genetics
Citations
This article has been cited 6 times.- Nohejl T, Palkovicova J, Nesporova K, Valcek A, Lausova J, Dolejska M. Broad-Host Dissemination of Plasmids Coharboring the fos Operon for Fructooligosaccharide Metabolism with Antibiotic Resistance Genes.. Appl Environ Microbiol 2023 Aug 30;89(8):e0037123.
- Banerjee J, Bhattacharyya D, Habib M, Chaudhary S, Biswas S, Maji C, Nanda PK, Das AK, Dandapat P, Samanta I, Lorenzo JM, Dutt T, Bandyopadhyay S. Antimicrobial Resistance Pattern, Clustering Mechanisms and Correlation Matrix of Drug-Resistant Escherichia coli in Black Bengal Goats in West Bengal, India.. Antibiotics (Basel) 2022 Oct 1;11(10).
- Goodman-Davis R, Figurska M, Cywinska A. Gut Microbiota Manipulation in Foals-Naturopathic Diarrhea Management, or Unsubstantiated Folly?. Pathogens 2021 Sep 4;10(9).
- Reshadi P, Heydari F, Ghanbarpour R, Bagheri M, Jajarmi M, Amiri M, Alizade H, Badouei MA, Sahraei S, Adib N. Molecular characterization and antimicrobial resistance of potentially human-pathogenic Escherichia coli strains isolated from riding horses.. BMC Vet Res 2021 Mar 25;17(1):131.
- Valcek A, Sismova P, Nesporova K, Overballe-Petersen S, Bitar I, Jamborova I, Kant A, Hrabak J, Wagenaar JA, Madec JY, Damborg P, van Duijkeren E, Ewers C, Hordijk J, Hasman H, Brouwer MSM, Dolejska M. Horsing around: Escherichia coli ST1250 of equine origin harbouring epidemic IncHI1/ST9 plasmid with bla (CTX-M-1) and an operon for short-chain fructooligosaccharides metabolism.. Antimicrob Agents Chemother 2023 May 1;65(5).
- Zong G, Zhong C, Fu J, Zhang Y, Zhang P, Zhang W, Xu Y, Cao G, Zhang R. The carbapenem resistance gene bla(OXA-23) is disseminated by a conjugative plasmid containing the novel transposon Tn6681 in Acinetobacter johnsonii M19.. Antimicrob Resist Infect Control 2020 Nov 9;9(1):182.
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