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.
Abstract: The relatedness of the equine-associated ST1250 and its single- and double-locus variants (ST1250-SLV/DLV), obtained from horses in Europe, was studied by comparative genome analysis. A total of 54 isolates of ST1250 and ST1250-SLV/DLV from healthy and hospitalized horses across Europe [Czech Republic (n=23), the Netherlands (n=18), Germany (n=9), Denmark (n=3) and France (n=1)] from 2008-2017 were subjected to whole-genome sequencing. An additional 25 draft genome assemblies of ST1250 and ST1250-SLV/DLV were obtained from the public databases. The isolates were compared for genomic features, virulence genes, clade structure and plasmid content. The complete nucleotide sequences of eight IncHI1/ST9 and one IncHI1/ST2 plasmids were obtained using long-read sequencing by PacBio or MinION. In the collection of 79 isolates, only 10 were phylogenetically close (98% similarity) regardless of country of origin and varied only in the structure and integration site of MDR region. ST1250 and ST1250-SLV/DLV are phylogenetically-diverse strains associated with horses. A strong linkage of ST1250 with epidemic multi-drug resistance plasmid lineage IncHI1/ST9 carrying and the operon was identified.
Copyright © 2021 American Society for Microbiology.
Publication Date: 2021-02-22 PubMed ID: 33619063PubMed Central: PMC8092906DOI: 10.1128/AAC.02556-20Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
- Journal Article
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 study investigates the genomic traits of Escherichia coli ST1250 and related strains from various horses all over Europe, and discovers a strong connection with a drug resistance plasmid strain carrying a particular antibiotic resistance gene and a gene cluster for short chain fructooligosaccharide metabolism.
Research Methodology
- The research focuses on comparative genome analysis of the equine-associated E. coli ST1250 and its variants, gathered from horses in Europe across different years (2008-2017). The samples have been collected from both healthy and hospitalized horses.
- A total of 54 original isolates from Czech Republic, the Netherlands, Germany, Denmark and France, and an additional 25 draft genome assemblies of the same strains were obtained from public databases.
- These isolates were subjected ti whole-genome sequencing and studied for various genomic features, virulence genes, clade structure and plasmid content.
Findings and Observations
- A majority of these isolates belonged to phylogroup B1 and carried genes associated with presence of a particular replicon within the corresponding isolates.
- The plasmid content of the isolates was largely dominated by two strains, with the majority containing the first strain. A minority of these isolates also contained an operon for utilizing short chain fructooligosaccharides.
- Upon sequencing, it was found that these plasmids were highly conserved and varied only in structure and MDR region’s integration site, irrespective of the country of origin.
- The E. coli ST1250 and its variants were identified as phylogenetically diverse strains associated with horses.
Significance of the Study
- This study identifies a strong link between E. coli ST1250 and an epidemic multi-drug resistance plasmid lineage carrying specific resistance genes.
- The discovery of this connection can provide valuable insights for creating more efficient treatments for drug-resistant infections in horses.
Cite This Article
APA
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.
(2021).
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, 65(5), e02556-20.
https://doi.org/10.1128/AAC.02556-20 Publication
Researcher Affiliations
- CEITEC VFU, University of Veterinary and Pharmaceutical Sciences Brno, Brno, Czech Republic.
- Department of Biology and Wildlife Diseases, Faculty of Veterinary Hygiene, University of Veterinary and Pharmaceutical Sciences Brno, Brno, Czech Republic.
- CEITEC VFU, University of Veterinary and Pharmaceutical Sciences Brno, Brno, Czech Republic.
- Department of Biology and Wildlife Diseases, Faculty of Veterinary Hygiene, University of Veterinary and Pharmaceutical Sciences Brno, Brno, Czech Republic.
- CEITEC VFU, University of Veterinary and Pharmaceutical Sciences Brno, Brno, Czech Republic.
- Department of Biology and Wildlife Diseases, Faculty of Veterinary Hygiene, University of Veterinary and Pharmaceutical Sciences Brno, Brno, Czech Republic.
- Department of Bacteria, Parasites and Fungi, Statens Serum Institut, Copenhagen, Denmark.
- Department of Microbiology, Faculty of Medicine, and University Hospital in Pilsen, Charles University, Pilsen, Czech Republic.
- Biomedical Center, Faculty of Medicine in Pilsen, Charles University, Pilsen, Czech Republic.
- CEITEC VFU, University of Veterinary and Pharmaceutical Sciences Brno, Brno, Czech Republic.
- Department of Bacteriology and Epidemiology, Wageningen Bioveterinary Research, Lelystad, The Netherlands.
- Department of Microbiology, Faculty of Medicine, and University Hospital in Pilsen, Charles University, Pilsen, Czech Republic.
- Biomedical Center, Faculty of Medicine in Pilsen, Charles University, Pilsen, Czech Republic.
- Department of Bacteriology and Epidemiology, Wageningen Bioveterinary Research, Lelystad, The Netherlands.
- Department of Infectious Diseases and Immunology, Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands.
- Université de Lyon-ANSES, Unité Antibiorésistance et Virulence Bactériennes, Lyon, France.
- Department of Veterinary and Animal Sciences, Faculty of Health and Medical Sciences, University of Copenhagen, Frederiksberg, Denmark.
- Center for Infectious Disease Control, National Institute for Public Health and the Environment, Bilthoven, The Netherlands.
- Institute of Hygiene and Infectious Diseases of Animals, Justus-Liebig-University Giessen, 35392 Giessen, Germany.
- Department of Infectious Diseases and Immunology, Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands.
- Department of Bacteria, Parasites and Fungi, Statens Serum Institut, Copenhagen, Denmark.
- Department of Bacteriology and Epidemiology, Wageningen Bioveterinary Research, Lelystad, The Netherlands.
- CEITEC VFU, University of Veterinary and Pharmaceutical Sciences Brno, Brno, Czech Republic monika.dolejska@gmail.com.
- Department of Biology and Wildlife Diseases, Faculty of Veterinary Hygiene, University of Veterinary and Pharmaceutical Sciences Brno, Brno, Czech Republic.
References
This article includes 54 references
- Ewers C, Bethe A, Semmler T, Guenther S, Wieler LH. Extended-spectrum β-lactamase-producing and AmpC-producing Escherichia coli from livestock and companion animals, and their putative impact on public health: a global perspective.. Clin Microbiol Infect 2012 Jul;18(7):646-55.
- El Salabi A, Walsh TR, Chouchani C. Extended spectrum β-lactamases, carbapenemases and mobile genetic elements responsible for antibiotics resistance in Gram-negative bacteria.. Crit Rev Microbiol 2013 May;39(2):113-22.
- McNulty CAM, Lecky DM, Xu-McCrae L, Nakiboneka-Ssenabulya D, Chung KT, Nichols T, Thomas HL, Thomas M, Alvarez-Buylla A, Turner K, Shabir S, Manzoor S, Smith S, Crocker L, Hawkey PM. CTX-M ESBL-producing Enterobacteriaceae: estimated prevalence in adults in England in 2014.. J Antimicrob Chemother 2018 May 1;73(5):1368-1388.
- Teklu DS, Negeri AA, Legese MH, Bedada TL, Woldemariam HK, Tullu KD. Extended-spectrum beta-lactamase production and multi-drug resistance among Enterobacteriaceae isolated in Addis Ababa, Ethiopia.. Antimicrob Resist Infect Control 2019;8:39.
- Dolejska M, Duskova E, Rybarikova J, Janoszowska D, Roubalova E, Dibdakova K, Maceckova G, Kohoutova L, Literak I, Smola J, Cizek A. Plasmids carrying blaCTX-M-1 and qnr genes in Escherichia coli isolates from an equine clinic and a horseback riding centre.. J Antimicrob Chemother 2011 Apr;66(4):757-64.
- Dolejska M, Villa L, Minoia M, Guardabassi L, Carattoli A. Complete sequences of IncHI1 plasmids carrying blaCTX-M-1 and qnrS1 in equine Escherichia coli provide new insights into plasmid evolution.. J Antimicrob Chemother 2014 Sep;69(9):2388-93.
- Damborg P, Marskar P, Baptiste KE, Guardabassi L. Faecal shedding of CTX-M-producing Escherichia coli in horses receiving broad-spectrum antimicrobial prophylaxis after hospital admission.. Vet Microbiol 2012 Jan 27;154(3-4):298-304.
- Jakobsen L, Bortolaia V, Bielak E, Moodley A, Olsen SS, Hansen DS, Frimodt-Møller N, Guardabassi L, Hasman H. Limited similarity between plasmids encoding CTX-M-1 β-lactamase in Escherichia coli from humans, pigs, cattle, organic poultry layers and horses in Denmark.. J Glob Antimicrob Resist 2015 Jun;3(2):132-136.
- Apostolakos I, Franz E, van Hoek AHAM, Florijn A, Veenman C, Sloet-van Oldruitenborgh-Oosterbaan MM, Dierikx C, van Duijkeren E. Occurrence and molecular characteristics of ESBL/AmpC-producing Escherichia coli in faecal samples from horses in an equine clinic.. J Antimicrob Chemother 2017 Jul 1;72(7):1915-1921.
- Hordijk J, Farmakioti E, Smit LAM, Duim B, Graveland H, Theelen MJP, Wagenaar JA. Fecal Carriage of Extended-Spectrum-β-Lactamase/AmpC-Producing Escherichia coli in Horses.. Appl Environ Microbiol 2020 Apr 1;86(8).
- Isgren CM, Edwards T, Pinchbeck GL, Winward E, Adams ER, Norton P, Timofte D, Maddox TW, Clegg PD, Williams NJ. Emergence of carriage of CTX-M-15 in faecal Escherichia coli in horses at an equine hospital in the UK; increasing prevalence over a decade (2008-2017).. BMC Vet Res 2019 Jul 29;15(1):268.
- Ewers C, Bethe A, Stamm I, Grobbel M, Kopp PA, Guerra B, Stubbe M, Doi Y, Zong Z, Kola A, Schaufler K, Semmler T, Fruth A, Wieler LH, Guenther S. CTX-M-15-D-ST648 Escherichia coli from companion animals and horses: another pandemic clone combining multiresistance and extraintestinal virulence?. J Antimicrob Chemother 2014 May;69(5):1224-30.
- Kaspar U, von Lützau K, Schlattmann A, Rösler U, Köck R, Becker K. Zoonotic multidrug-resistant microorganisms among non-hospitalized horses from Germany.. One Health 2019 Jun;7:100091.
- Lupo A, Haenni M, Saras E, Gradin J, Madec JY, Börjesson S. Is bla(CTX-M-1) Riding the Same Plasmid Among Horses in Sweden and France?. Microb Drug Resist 2018 May 24;.
- Sadikalay S, Reynaud Y, Guyomard-Rabenirina S, Falord M, Ducat C, Fabre L, Le Hello S, Talarmin A, Ferdinand S. High genetic diversity of extended-spectrum β-lactamases producing Escherichia coli in feces of horses.. Vet Microbiol 2018 Jun;219:117-122.
- de Lagarde M, Larrieu C, Praud K, Lallier N, Trotereau A, Sallé G, Fairbrother JM, Schouler C, Doublet B. Spread of multidrug-resistant IncHI1 plasmids carrying ESBL gene bla(CTX-M-1) and metabolism operon of prebiotic oligosaccharides in commensal Escherichia coli from healthy horses, France.. Int J Antimicrob Agents 2020 Jun;55(6):105936.
- Schouler C, Taki A, Chouikha I, Moulin-Schouleur M, Gilot P. A genomic island of an extraintestinal pathogenic Escherichia coli Strain enables the metabolism of fructooligosaccharides, which improves intestinal colonization.. J Bacteriol 2009 Jan;191(1):388-93.
- Respondek F, Myers K, Smith TL, Wagner A, Geor RJ. Dietary supplementation with short-chain fructo-oligosaccharides improves insulin sensitivity in obese horses.. J Anim Sci 2011 Jan;89(1):77-83.
- Sonnenborn U, Schulze J. The non-pathogenic Escherichia coli strain Nissle 1917 — features of a versatile probiotic. Microb Ecol Health Dis 21:122–158.
- Qi B, Han M. Microbial Siderophore Enterobactin Promotes Mitochondrial Iron Uptake and Development of the Host via Interaction with ATP Synthase.. Cell 2018 Oct 4;175(2):571-582.e11.
- Girón JA, Torres AG, Freer E, Kaper JB. The flagella of enteropathogenic Escherichia coli mediate adherence to epithelial cells.. Mol Microbiol 2002 Apr;44(2):361-79.
- Qin X, Hu F, Wu S, Ye X, Zhu D, Zhang Y, Wang M. Comparison of adhesin genes and antimicrobial susceptibilities between uropathogenic and intestinal commensal Escherichia coli strains.. PLoS One 2013;8(4):e61169.
- Talmi-Frank D, Altboum Z, Solomonov I, Udi Y, Jaitin DA, Klepfish M, David E, Zhuravlev A, Keren-Shaul H, Winter DR, Gat-Viks I, Mandelboim M, Ziv T, Amit I, Sagi I. Extracellular Matrix Proteolysis by MT1-MMP Contributes to Influenza-Related Tissue Damage and Mortality.. Cell Host Microbe 2016 Oct 12;20(4):458-470.
- Francetic O, Pugsley AP. The cryptic general secretory pathway (gsp) operon of Escherichia coli K-12 encodes functional proteins.. J Bacteriol 1996 Jun;178(12):3544-9.
- Francetic O, Belin D, Badaut C, Pugsley AP. Expression of the endogenous type II secretion pathway in Escherichia coli leads to chitinase secretion.. EMBO J 2000 Dec 15;19(24):6697-703.
- Bébien M, Kirsch J, Méjean V, Verméglio A. Involvement of a putative molybdenum enzyme in the reduction of selenate by Escherichia coli.. Microbiology (Reading) 2002 Dec;148(Pt 12):3865-3872.
- Minazzato G, Gasparrini M, Amici A, Cianci M, Mazzola F, Orsomando G, Sorci L, Raffaelli N. Functional Characterization of COG1713 (YqeK) as a Novel Diadenosine Tetraphosphate Hydrolase Family.. J Bacteriol 2020 Apr 27;202(10).
- Frederix M, Hütter K, Leu J, Batth TS, Turner WJ, Rüegg TL, Blanch HW, Simmons BA, Adams PD, Keasling JD, Thelen MP, Dunlop MJ, Petzold CJ, Mukhopadhyay A. Development of a native Escherichia coli induction system for ionic liquid tolerance.. PLoS One 2014;9(7):e101115.
- Jenkins LS, Nunn WD. Regulation of the ato operon by the atoC gene in Escherichia coli.. J Bacteriol 1987 May;169(5):2096-102.
- Seeger C, Poulsen C, Dandanell G. Identification and characterization of genes (xapA, xapB, and xapR) involved in xanthosine catabolism in Escherichia coli.. J Bacteriol 1995 Oct;177(19):5506-16.
- Koga M, Otsuka Y, Lemire S, Yonesaki T. Escherichia coli rnlA and rnlB compose a novel toxin-antitoxin system.. Genetics 2011 Jan;187(1):123-30.
- Cain AK, Hall RM. Evolution of IncHI1 plasmids: two distinct lineages.. Plasmid 2013 Sep;70(2):201-8.
- Smith H, Bossers A, Harders F, Wu G, Woodford N, Schwarz S, Guerra B, Rodríguez I, van Essen-Zandbergen A, Brouwer M, Mevius D. Characterization of epidemic IncI1-Iγ plasmids harboring ambler class A and C genes in Escherichia coli and Salmonella enterica from animals and humans.. Antimicrob Agents Chemother 2015 Sep;59(9):5357-65.
- Wang Y, Tong MK, Chow KH, Cheng VC, Tse CW, Wu AK, Lai RW, Luk WK, Tsang DN, Ho PL. Occurrence of Highly Conjugative IncX3 Epidemic Plasmid Carrying bla (NDM) in Enterobacteriaceae Isolates in Geographically Widespread Areas.. Front Microbiol 2018;9:2272.
- Ho PL, Wang Y, Liu MC, Lai EL, Law PY, Cao H, Chow KH. IncX3 Epidemic Plasmid Carrying bla(NDM-5) in Escherichia coli from Swine in Multiple Geographic Areas in China.. Antimicrob Agents Chemother 2018 Mar;62(3).
- Chouikha I, Germon P, Brée A, Gilot P, Moulin-Schouleur M, Schouler C. A selC-associated genomic island of the extraintestinal avian pathogenic Escherichia coli strain BEN2908 is involved in carbohydrate uptake and virulence.. J Bacteriol 2006 Feb;188(3):977-87.
- CLSI. 2018. Performance standards for antimicrobial susceptibility testing; twenty-eighth informational supplement. CLSI document M100-S28. Clinical and Laboratory Standards Institute, Wayne, PA.
- Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data.. Bioinformatics 2014 Aug 1;30(15):2114-20.
- Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing.. J Comput Biol 2012 May;19(5):455-77.
- Chin CS, Alexander DH, Marks P, Klammer AA, Drake J, Heiner C, Clum A, Copeland A, Huddleston J, Eichler EE, Turner SW, Korlach J. Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data.. Nat Methods 2013 Jun;10(6):563-9.
- Wick RR, Judd LM, Gorrie CL, Holt KE. Unicycler: Resolving bacterial genome assemblies from short and long sequencing reads.. PLoS Comput Biol 2017 Jun;13(6):e1005595.
- Brettin T, Davis JJ, Disz T, Edwards RA, Gerdes S, Olsen GJ, Olson R, Overbeek R, Parrello B, Pusch GD, Shukla M, Thomason JA 3rd, Stevens R, Vonstein V, Wattam AR, Xia F. RASTtk: a modular and extensible implementation of the RAST algorithm for building custom annotation pipelines and annotating batches of genomes.. Sci Rep 2015 Feb 10;5:8365.
- Zankari E, Hasman H, Cosentino S, Vestergaard M, Rasmussen S, Lund O, Aarestrup FM, Larsen MV. Identification of acquired antimicrobial resistance genes.. J Antimicrob Chemother 2012 Nov;67(11):2640-4.
- Liu B, Zheng D, Jin Q, Chen L, Yang J. VFDB 2019: a comparative pathogenomic platform with an interactive web interface.. Nucleic Acids Res 2019 Jan 8;47(D1):D687-D692.
- Carattoli A, Zankari E, García-Fernández A, Voldby Larsen M, Lund O, Villa L, Møller Aarestrup F, Hasman H. In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing.. Antimicrob Agents Chemother 2014 Jul;58(7):3895-903.
- Ingle DJ, Valcanis M, Kuzevski A, Tauschek M, Inouye M, Stinear T, Levine MM, Robins-Browne RM, Holt KE. In silico serotyping of E. coli from short read data identifies limited novel O-loci but extensive diversity of O:H serotype combinations within and between pathogenic lineages.. Microb Genom 2016 Jul;2(7):e000064.
- Beghain J, Bridier-Nahmias A, Le Nagard H, Denamur E, Clermont O. ClermonTyping: an easy-to-use and accurate in silico method for Escherichia genus strain phylotyping.. Microb Genom 2018 Jul;4(7).
- Seemann T. Prokka: rapid prokaryotic genome annotation.. Bioinformatics 2014 Jul 15;30(14):2068-9.
- Page AJ, Cummins CA, Hunt M, Wong VK, Reuter S, Holden MT, Fookes M, Falush D, Keane JA, Parkhill J. Roary: rapid large-scale prokaryote pan genome analysis.. Bioinformatics 2015 Nov 15;31(22):3691-3.
- Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models.. Bioinformatics 2006 Nov 1;22(21):2688-90.
- Letunic I, Bork P. Interactive Tree Of Life (iTOL) v4: recent updates and new developments.. Nucleic Acids Res 2019 Jul 2;47(W1):W256-W259.
- Zhou Z, Alikhan NF, Sergeant MJ, Luhmann N, Vaz C, Francisco AP, Carriço JA, Achtman M. GrapeTree: visualization of core genomic relationships among 100,000 bacterial pathogens.. Genome Res 2018 Sep;28(9):1395-1404.
- Darling AE, Mau B, Perna NT. progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement.. PLoS One 2010 Jun 25;5(6):e11147.
- Alikhan NF, Petty NK, Ben Zakour NL, Beatson SA. BLAST Ring Image Generator (BRIG): simple prokaryote genome comparisons.. BMC Genomics 2011 Aug 8;12:402.
Citations
This article has been cited 4 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.
- Ma J, Wang J, Yang H, Su M, Li R, Bai L, Feng J, Huang Y, Yang Z, Tang B. IncHI1 plasmids mediated the tet(X4) gene spread in Enterobacteriaceae in porcine.. Front Microbiol 2023;14:1128905.
- Elankumuran P, Browning GF, Marenda MS, Kidsley A, Osman M, Haenni M, Johnson JR, Trott DJ, Reid CJ, Djordjevic SP. Identification of genes influencing the evolution of Escherichia coli ST372 in dogs and humans.. Microb Genom 2023 Feb;9(2).
- Cormier AC, Chalmers G, Zamudio R, Mulvey MR, Mather AE, Boerlin P. Diversity of blaCTX-M-1-carrying plasmids recovered from Escherichia coli isolated from Canadian domestic animals.. PLoS One 2022;17(3):e0264439.
Use Nutrition Calculator
Check if your horse's diet meets their nutrition requirements with our easy-to-use tool Check your horse's diet with our easy-to-use tool
Talk to a Nutritionist
Discuss your horse's feeding plan with our experts over a free phone consultation Discuss your horse's diet over a phone consultation
Submit Diet Evaluation
Get a customized feeding plan for your horse formulated by our equine nutritionists Get a custom feeding plan formulated by our nutritionists
