A One Health approach for the genomic characterization of antibiotic-resistant Campylobacter isolates using Nanopore whole-genome sequencing

In response to the growing threat posed by the spread of antimicrobial resistance in zoonotic Campylobacter, a One Health approach was used to examine the genomic diversity, phylogenomic relationships, and the distribution of genetic determinants of resistance (GDR) in C. jejuni and C. coli isolates...

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Main Authors: Ana Hurtado, Medelin Ocejo, Beatriz Oporto, José Luis Lavín, Ruth Rodríguez, María Ángeles Marcos, Mikel Urrutikoetxea-Gutiérrez, Miriam Alkorta, José María Marimón
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Language:English
Published: Frontiers Media S.A. 2025-01-01
Series:Frontiers in Microbiology
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Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2025.1540210/full
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author Ana Hurtado
Medelin Ocejo
Beatriz Oporto
José Luis Lavín
Ruth Rodríguez
María Ángeles Marcos
Mikel Urrutikoetxea-Gutiérrez
Mikel Urrutikoetxea-Gutiérrez
Miriam Alkorta
Miriam Alkorta
Miriam Alkorta
José María Marimón
José María Marimón
author_facet Ana Hurtado
Medelin Ocejo
Beatriz Oporto
José Luis Lavín
Ruth Rodríguez
María Ángeles Marcos
Mikel Urrutikoetxea-Gutiérrez
Mikel Urrutikoetxea-Gutiérrez
Miriam Alkorta
Miriam Alkorta
Miriam Alkorta
José María Marimón
José María Marimón
author_sort Ana Hurtado
collection DOAJ
description In response to the growing threat posed by the spread of antimicrobial resistance in zoonotic Campylobacter, a One Health approach was used to examine the genomic diversity, phylogenomic relationships, and the distribution of genetic determinants of resistance (GDR) in C. jejuni and C. coli isolates from humans, animals (ruminants, swine, and chickens), and avian food products collected during a regionally (Basque Country, Spain) and temporally (mostly 2021–2022) restricted sampling. Eighty-three C. jejuni and seventy-one C. coli isolates, most exhibiting resistance to ciprofloxacin and/or erythromycin, were whole-genome sequenced using Oxford Nanopore Technologies long-fragment sequencing (ONT). Multilocus sequence typing (MLST) analysis identified a high genomic diversity among isolates. Phylogenomic analysis showed that clustering based on the core genome was aligned with MLST profiles, regardless of the sample source. In contrast, accessory genome content sometimes discriminated isolates within the same STs and occasionally differentiated isolates from different sources. The majority of the identified GDRs were present in isolates from different sources, and a good correlation was observed between GDR distribution and phenotypic susceptibility profiles (based on minimum inhibitory concentrations interpreted according to the EUCAST epidemiological cutoff values). Genotypic resistance profiles were independent of genotypes, indicating no apparent association between resistance and phylogenetic origin. This study demonstrates that ONT sequencing is a powerful tool for molecular surveillance of bacterial pathogens in the One Health framework.
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spelling doaj-art-2fa5ca2fc1d74b67bff9c533f751bc0c2025-01-29T06:45:45ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2025-01-011610.3389/fmicb.2025.15402101540210A One Health approach for the genomic characterization of antibiotic-resistant Campylobacter isolates using Nanopore whole-genome sequencingAna Hurtado0Medelin Ocejo1Beatriz Oporto2José Luis Lavín3Ruth Rodríguez4María Ángeles Marcos5Mikel Urrutikoetxea-Gutiérrez6Mikel Urrutikoetxea-Gutiérrez7Miriam Alkorta8Miriam Alkorta9Miriam Alkorta10José María Marimón11José María Marimón12Animal Health Department, NEIKER – Basque Institute for Agricultural Research and Development, Basque Research and Technology Alliance (BRTA), Bizkaia Science and Technology Park 812L, Derio, Bizkaia, SpainAnimal Health Department, NEIKER – Basque Institute for Agricultural Research and Development, Basque Research and Technology Alliance (BRTA), Bizkaia Science and Technology Park 812L, Derio, Bizkaia, SpainAnimal Health Department, NEIKER – Basque Institute for Agricultural Research and Development, Basque Research and Technology Alliance (BRTA), Bizkaia Science and Technology Park 812L, Derio, Bizkaia, SpainApplied Mathematics Department, NEIKER – Basque Institute for Agricultural Research and Development, Basque Research and Technology Alliance (BRTA), Bizkaia Science and Technology Park 812L, Derio, Bizkaia, SpainLaboratorio de Salud Pública en Gipuzkoa, Donostia-San Sebastián, Gipuzkoa, SpainLaboratorio de Salud Pública en Gipuzkoa, Donostia-San Sebastián, Gipuzkoa, SpainClinical Microbiology Service, Basurto University Hospital, Organización Sanitaria Integrada Bilbao-Basurto, Bilbao, Bizkaia, SpainBiobizkaia Health Research Institute, Microbiology and Infection Control, Barakaldo, Bizkaia, SpainInfectious Diseases Area, Microbiology Department, Biogipuzkoa Health Research Institute, Donostia-San Sebastián, Gipuzkoa, SpainDonostialdea Integrated Health Organization, Donostia University Hospital, Donostia-San Sebastián, Gipuzkoa, SpainFaculty of Medicine, University of the Basque Country, UPV/EHU, Donostia-San Sebastián, Gipuzkoa, SpainInfectious Diseases Area, Microbiology Department, Biogipuzkoa Health Research Institute, Donostia-San Sebastián, Gipuzkoa, SpainDonostialdea Integrated Health Organization, Donostia University Hospital, Donostia-San Sebastián, Gipuzkoa, SpainIn response to the growing threat posed by the spread of antimicrobial resistance in zoonotic Campylobacter, a One Health approach was used to examine the genomic diversity, phylogenomic relationships, and the distribution of genetic determinants of resistance (GDR) in C. jejuni and C. coli isolates from humans, animals (ruminants, swine, and chickens), and avian food products collected during a regionally (Basque Country, Spain) and temporally (mostly 2021–2022) restricted sampling. Eighty-three C. jejuni and seventy-one C. coli isolates, most exhibiting resistance to ciprofloxacin and/or erythromycin, were whole-genome sequenced using Oxford Nanopore Technologies long-fragment sequencing (ONT). Multilocus sequence typing (MLST) analysis identified a high genomic diversity among isolates. Phylogenomic analysis showed that clustering based on the core genome was aligned with MLST profiles, regardless of the sample source. In contrast, accessory genome content sometimes discriminated isolates within the same STs and occasionally differentiated isolates from different sources. The majority of the identified GDRs were present in isolates from different sources, and a good correlation was observed between GDR distribution and phenotypic susceptibility profiles (based on minimum inhibitory concentrations interpreted according to the EUCAST epidemiological cutoff values). Genotypic resistance profiles were independent of genotypes, indicating no apparent association between resistance and phylogenetic origin. This study demonstrates that ONT sequencing is a powerful tool for molecular surveillance of bacterial pathogens in the One Health framework.https://www.frontiersin.org/articles/10.3389/fmicb.2025.1540210/fullCampylobacter jejuniCampylobacter coliantimicrobial resistancewhole-genome sequencingNanopore long-fragment sequencingone health
spellingShingle Ana Hurtado
Medelin Ocejo
Beatriz Oporto
José Luis Lavín
Ruth Rodríguez
María Ángeles Marcos
Mikel Urrutikoetxea-Gutiérrez
Mikel Urrutikoetxea-Gutiérrez
Miriam Alkorta
Miriam Alkorta
Miriam Alkorta
José María Marimón
José María Marimón
A One Health approach for the genomic characterization of antibiotic-resistant Campylobacter isolates using Nanopore whole-genome sequencing
Frontiers in Microbiology
Campylobacter jejuni
Campylobacter coli
antimicrobial resistance
whole-genome sequencing
Nanopore long-fragment sequencing
one health
title A One Health approach for the genomic characterization of antibiotic-resistant Campylobacter isolates using Nanopore whole-genome sequencing
title_full A One Health approach for the genomic characterization of antibiotic-resistant Campylobacter isolates using Nanopore whole-genome sequencing
title_fullStr A One Health approach for the genomic characterization of antibiotic-resistant Campylobacter isolates using Nanopore whole-genome sequencing
title_full_unstemmed A One Health approach for the genomic characterization of antibiotic-resistant Campylobacter isolates using Nanopore whole-genome sequencing
title_short A One Health approach for the genomic characterization of antibiotic-resistant Campylobacter isolates using Nanopore whole-genome sequencing
title_sort one health approach for the genomic characterization of antibiotic resistant campylobacter isolates using nanopore whole genome sequencing
topic Campylobacter jejuni
Campylobacter coli
antimicrobial resistance
whole-genome sequencing
Nanopore long-fragment sequencing
one health
url https://www.frontiersin.org/articles/10.3389/fmicb.2025.1540210/full
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