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Sharing of cmeRABC alleles between C. coli and C. jejuni associated with extensive drug resistance in Campylobacter isolates from infants and poultry in the Peruvian Amazon

Kerry K Cooper Orcid Logo, Evangelos Mourkas Orcid Logo, Francesca Schiaffino Orcid Logo, Craig T Parker Orcid Logo, Tackeshy N Pinedo Vasquez, Paul F Garcia Bardales, Pablo Peñataro Yori, Maribel Paredes Olortegui, Katia Manzanares Villanueva, Lucero Romaina Cachique, Hermann Silva Delgado, Matthew Hitchings Orcid Logo, Steven Huynh, Samuel K Sheppard Orcid Logo, Ben Pascoe Orcid Logo, Margaret N Kosek Orcid Logo

mBio, Start page: e02054-24

Swansea University Author: Matthew Hitchings Orcid Logo

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DOI (Published version): 10.1128/mbio.02054-24

Abstract

Campylobacter is a serious health threat because of the rapid progressive evolution of antimicrobial resistance and efficient transmission from zoonotic as well as human sources. Resistance to fluoroquinolones and macrolides is particularly concerning as this compromises the two most effective oral...

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Published in: mBio
ISSN: 2150-7511
Published: American Society for Microbiology (ASM) 2024
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URI: https://cronfa.swan.ac.uk/Record/cronfa68684
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Resistance to fluoroquinolones and macrolides is particularly concerning as this compromises the two most effective oral antibiotic agents currently available for human campylobacteriosis. Here, we report on the prevalence and worldwide distribution of the operon cmeRABC, which encodes an efflux pump conferring high levels of combined resistance to fluoroquinolones and macrolides in Campylobacter strains isolated from poultry (n = 75) and children (n = 177). These mutations were found to be highly prevalent in isolates from poultry (62.7%) and children (29.4%) in Iquitos, Peru. We investigated the population structure of genes in the cmeRABC operon and identified a potential genetic bottleneck for the cmeA and cmeB genes. While most cmeB alleles segregate by species, alleles associated with high resistance to fluoroquinolones and macrolides were found in both Campylobacter jejuni and Campylobacter coli. We inferred that the likely ancestry of these alleles was from C. jejuni and was later acquired by C. coli through recombination. Publicly accessible global genomic data from 16,120 Campylobacter genomes identified these mutations in approximately 6% of C. jejuni and C. coli isolates globally, with higher prevalence in samples from poultry in many countries, including Peru. 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spelling 2025-01-13T14:41:53.1846767 v2 68684 2025-01-13 Sharing of cmeRABC alleles between C. coli and C. jejuni associated with extensive drug resistance in Campylobacter isolates from infants and poultry in the Peruvian Amazon be98847c72c14a731c4a6b7bc02b3bcf 0000-0002-5527-4709 Matthew Hitchings Matthew Hitchings true false 2025-01-13 MEDS Campylobacter is a serious health threat because of the rapid progressive evolution of antimicrobial resistance and efficient transmission from zoonotic as well as human sources. Resistance to fluoroquinolones and macrolides is particularly concerning as this compromises the two most effective oral antibiotic agents currently available for human campylobacteriosis. Here, we report on the prevalence and worldwide distribution of the operon cmeRABC, which encodes an efflux pump conferring high levels of combined resistance to fluoroquinolones and macrolides in Campylobacter strains isolated from poultry (n = 75) and children (n = 177). These mutations were found to be highly prevalent in isolates from poultry (62.7%) and children (29.4%) in Iquitos, Peru. We investigated the population structure of genes in the cmeRABC operon and identified a potential genetic bottleneck for the cmeA and cmeB genes. While most cmeB alleles segregate by species, alleles associated with high resistance to fluoroquinolones and macrolides were found in both Campylobacter jejuni and Campylobacter coli. We inferred that the likely ancestry of these alleles was from C. jejuni and was later acquired by C. coli through recombination. Publicly accessible global genomic data from 16,120 Campylobacter genomes identified these mutations in approximately 6% of C. jejuni and C. coli isolates globally, with higher prevalence in samples from poultry in many countries, including Peru. Our findings suggest that these extensively drug-resistant Campylobacter strains originated from C. jejuni in poultry. Journal Article mBio 0 e02054-24 American Society for Microbiology (ASM) 2150-7511 Campylobacter, efflux pump, antibiotic resistance, recombination, Iquitos 27 12 2024 2024-12-27 10.1128/mbio.02054-24 COLLEGE NANME Medical School COLLEGE CODE MEDS Swansea University Another institution paid the OA fee This publication made use of the PubMLST website (http://pubmlst.org/) developed by Keith Jolley and Martin Maiden and hosted at the University of Oxford. Funding for this study was provided by the Bill and Melinda Gates Foundation (OPP1066146 and OPP1152146 to M.N.K.) and the National Institutes of Health of the United States (R01AI158576 and R21AI163801 to M.N.K. and C.T.P.; D43TW010913 to M.N.K.; K43TW012298 to F.S.). This research was also supported in part by United States Department of Agriculture–Agricultural Research Service Current Research Information System, project 2030–42000-055-00D (to C.T.P.). 2025-01-13T14:41:53.1846767 2025-01-13T14:25:44.8280427 Faculty of Medicine, Health and Life Sciences Swansea University Medical School - Biomedical Science Kerry K Cooper 0000-0003-4541-1324 1 Evangelos Mourkas 0000-0002-7411-4743 2 Francesca Schiaffino 0000-0002-5796-5116 3 Craig T Parker 0000-0002-7719-8882 4 Tackeshy N Pinedo Vasquez 5 Paul F Garcia Bardales 6 Pablo Peñataro Yori 7 Maribel Paredes Olortegui 8 Katia Manzanares Villanueva 9 Lucero Romaina Cachique 10 Hermann Silva Delgado 11 Matthew Hitchings 0000-0002-5527-4709 12 Steven Huynh 13 Samuel K Sheppard 0000-0001-6901-3203 14 Ben Pascoe https://orcid.org/0000-0001-6376-5121 15 Margaret N Kosek 0000-0001-6340-4852 16
title Sharing of cmeRABC alleles between C. coli and C. jejuni associated with extensive drug resistance in Campylobacter isolates from infants and poultry in the Peruvian Amazon
spellingShingle Sharing of cmeRABC alleles between C. coli and C. jejuni associated with extensive drug resistance in Campylobacter isolates from infants and poultry in the Peruvian Amazon
Matthew Hitchings
title_short Sharing of cmeRABC alleles between C. coli and C. jejuni associated with extensive drug resistance in Campylobacter isolates from infants and poultry in the Peruvian Amazon
title_full Sharing of cmeRABC alleles between C. coli and C. jejuni associated with extensive drug resistance in Campylobacter isolates from infants and poultry in the Peruvian Amazon
title_fullStr Sharing of cmeRABC alleles between C. coli and C. jejuni associated with extensive drug resistance in Campylobacter isolates from infants and poultry in the Peruvian Amazon
title_full_unstemmed Sharing of cmeRABC alleles between C. coli and C. jejuni associated with extensive drug resistance in Campylobacter isolates from infants and poultry in the Peruvian Amazon
title_sort Sharing of cmeRABC alleles between C. coli and C. jejuni associated with extensive drug resistance in Campylobacter isolates from infants and poultry in the Peruvian Amazon
author_id_str_mv be98847c72c14a731c4a6b7bc02b3bcf
author_id_fullname_str_mv be98847c72c14a731c4a6b7bc02b3bcf_***_Matthew Hitchings
author Matthew Hitchings
author2 Kerry K Cooper
Evangelos Mourkas
Francesca Schiaffino
Craig T Parker
Tackeshy N Pinedo Vasquez
Paul F Garcia Bardales
Pablo Peñataro Yori
Maribel Paredes Olortegui
Katia Manzanares Villanueva
Lucero Romaina Cachique
Hermann Silva Delgado
Matthew Hitchings
Steven Huynh
Samuel K Sheppard
Ben Pascoe
Margaret N Kosek
format Journal article
container_title mBio
container_volume 0
container_start_page e02054-24
publishDate 2024
institution Swansea University
issn 2150-7511
doi_str_mv 10.1128/mbio.02054-24
publisher American Society for Microbiology (ASM)
college_str Faculty of Medicine, Health and Life Sciences
hierarchytype
hierarchy_top_id facultyofmedicinehealthandlifesciences
hierarchy_top_title Faculty of Medicine, Health and Life Sciences
hierarchy_parent_id facultyofmedicinehealthandlifesciences
hierarchy_parent_title Faculty of Medicine, Health and Life Sciences
department_str Swansea University Medical School - Biomedical Science{{{_:::_}}}Faculty of Medicine, Health and Life Sciences{{{_:::_}}}Swansea University Medical School - Biomedical Science
document_store_str 0
active_str 0
description Campylobacter is a serious health threat because of the rapid progressive evolution of antimicrobial resistance and efficient transmission from zoonotic as well as human sources. Resistance to fluoroquinolones and macrolides is particularly concerning as this compromises the two most effective oral antibiotic agents currently available for human campylobacteriosis. Here, we report on the prevalence and worldwide distribution of the operon cmeRABC, which encodes an efflux pump conferring high levels of combined resistance to fluoroquinolones and macrolides in Campylobacter strains isolated from poultry (n = 75) and children (n = 177). These mutations were found to be highly prevalent in isolates from poultry (62.7%) and children (29.4%) in Iquitos, Peru. We investigated the population structure of genes in the cmeRABC operon and identified a potential genetic bottleneck for the cmeA and cmeB genes. While most cmeB alleles segregate by species, alleles associated with high resistance to fluoroquinolones and macrolides were found in both Campylobacter jejuni and Campylobacter coli. We inferred that the likely ancestry of these alleles was from C. jejuni and was later acquired by C. coli through recombination. Publicly accessible global genomic data from 16,120 Campylobacter genomes identified these mutations in approximately 6% of C. jejuni and C. coli isolates globally, with higher prevalence in samples from poultry in many countries, including Peru. Our findings suggest that these extensively drug-resistant Campylobacter strains originated from C. jejuni in poultry.
published_date 2024-12-27T14:39:30Z
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score 11.048042

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