World Health Organization critical priority Escherichia coli clone ST648 in magnificent frigatebird (Fregata magnificens) of an uninhabited insular environment

Antimicrobial resistance is an ancient natural phenomenon increasingly pressured by anthropogenic activities. Escherichia coli has been used as markers of environmental contamination and human-related activity. Seabirds may be bioindicators of clinically relevant bacterial pathogens and their antimi...

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Main Authors: Ana Carolina Ewbank, Danny Fuentes-Castillo, Carlos Sacristán, Fernanda Esposito, Bruna Fuga, Brenda Cardoso, Silvia Neri Godoy, Roberta Ramblas Zamana, Marco Aurélio Gattamorta, José Luiz Catão-Dias, Nilton Lincopan
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-08-01
Series:Frontiers in Microbiology
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Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2022.940600/full
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author Ana Carolina Ewbank
Danny Fuentes-Castillo
Danny Fuentes-Castillo
Carlos Sacristán
Fernanda Esposito
Fernanda Esposito
Bruna Fuga
Bruna Fuga
Bruna Fuga
Brenda Cardoso
Brenda Cardoso
Silvia Neri Godoy
Roberta Ramblas Zamana
Marco Aurélio Gattamorta
José Luiz Catão-Dias
Nilton Lincopan
Nilton Lincopan
Nilton Lincopan
author_facet Ana Carolina Ewbank
Danny Fuentes-Castillo
Danny Fuentes-Castillo
Carlos Sacristán
Fernanda Esposito
Fernanda Esposito
Bruna Fuga
Bruna Fuga
Bruna Fuga
Brenda Cardoso
Brenda Cardoso
Silvia Neri Godoy
Roberta Ramblas Zamana
Marco Aurélio Gattamorta
José Luiz Catão-Dias
Nilton Lincopan
Nilton Lincopan
Nilton Lincopan
author_sort Ana Carolina Ewbank
collection DOAJ
description Antimicrobial resistance is an ancient natural phenomenon increasingly pressured by anthropogenic activities. Escherichia coli has been used as markers of environmental contamination and human-related activity. Seabirds may be bioindicators of clinically relevant bacterial pathogens and their antimicrobial resistance genes, including extended-spectrum-beta-lactamase (ESBL) and/or plasmid-encoded AmpC (pAmpC), in anthropized and remote areas. We evaluated cloacal swabs of 20 wild magnificent frigatebirds (Fregata magnificens) of the Alcatrazes Archipelago, the biggest breeding colony of magnificent frigatebirds in the southern Atlantic and a natural protected area with no history of human occupation, located in the anthropized southeastern Brazilian coast. We characterized a highly virulent multidrug-resistant ST648 (O153:H9) pandemic clone, harboring blaCTX–M–2, blaCMY–2, qnrB, tetB, sul1, sul2, aadA1, aac(3)-VIa and mdfA, and virulence genes characteristic of avian pathogenic (APEC) (hlyF, iroN, iss, iutA, and ompT) and other extraintestinal E. coli (ExPEC) (chuA, kpsMII, and papC). To our knowledge, this is the first report of ST648 E. coli co-producing ESBL and pAmpC in wild birds inhabiting insular environments. We suggest this potentially zoonotic and pathogenic lineage was likely acquired through indirect anthropogenic contamination of the marine environment, ingestion of contaminated seafood, or by intra and/or interspecific contact. Our findings reinforce the role of wild birds as anthropization sentinels in insular environments and the importance of wildlife surveillance studies on pathogens of critical priority classified by the World Health Organization.
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spelling doaj.art-45878c0242be4e85898da607452e22462022-12-22T03:43:24ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2022-08-011310.3389/fmicb.2022.940600940600World Health Organization critical priority Escherichia coli clone ST648 in magnificent frigatebird (Fregata magnificens) of an uninhabited insular environmentAna Carolina Ewbank0Danny Fuentes-Castillo1Danny Fuentes-Castillo2Carlos Sacristán3Fernanda Esposito4Fernanda Esposito5Bruna Fuga6Bruna Fuga7Bruna Fuga8Brenda Cardoso9Brenda Cardoso10Silvia Neri Godoy11Roberta Ramblas Zamana12Marco Aurélio Gattamorta13José Luiz Catão-Dias14Nilton Lincopan15Nilton Lincopan16Nilton Lincopan17Laboratory of Wildlife Comparative Pathology, Department of Pathology, School of Veterinary Medicine and Animal Sciences, University of São Paulo, São Paulo, BrazilDepartamento de Patología y Medicina Preventiva, Facultad de Ciencias Veterinarias, Universidad de Concepción, Chillán, ChileOne Health Brazilian Resistance Project (OneBR), São Paulo, BrazilCentro de Investigación en Sanidad Animal (CISA-INIA), CSIC, Valdeolmos-Alalpardo, SpainOne Health Brazilian Resistance Project (OneBR), São Paulo, BrazilDepartment of Clinical Analysis, School of Pharmacy, University of São Paulo, São Paulo, BrazilOne Health Brazilian Resistance Project (OneBR), São Paulo, BrazilDepartment of Clinical Analysis, School of Pharmacy, University of São Paulo, São Paulo, BrazilDepartment of Microbiology, Institute of Biomedical Sciences, University of São Paulo, São Paulo, BrazilOne Health Brazilian Resistance Project (OneBR), São Paulo, BrazilDepartment of Clinical Analysis, School of Pharmacy, University of São Paulo, São Paulo, BrazilRefúgio de Vida Silvestre do Arquipélago de Alcatrazes – Instituto Chico Mendes de Conservação da Biodiversidade, São Paulo, BrazilLaboratory of Wildlife Comparative Pathology, Department of Pathology, School of Veterinary Medicine and Animal Sciences, University of São Paulo, São Paulo, BrazilLaboratory of Wildlife Comparative Pathology, Department of Pathology, School of Veterinary Medicine and Animal Sciences, University of São Paulo, São Paulo, BrazilLaboratory of Wildlife Comparative Pathology, Department of Pathology, School of Veterinary Medicine and Animal Sciences, University of São Paulo, São Paulo, BrazilOne Health Brazilian Resistance Project (OneBR), São Paulo, BrazilDepartment of Clinical Analysis, School of Pharmacy, University of São Paulo, São Paulo, BrazilDepartment of Microbiology, Institute of Biomedical Sciences, University of São Paulo, São Paulo, BrazilAntimicrobial resistance is an ancient natural phenomenon increasingly pressured by anthropogenic activities. Escherichia coli has been used as markers of environmental contamination and human-related activity. Seabirds may be bioindicators of clinically relevant bacterial pathogens and their antimicrobial resistance genes, including extended-spectrum-beta-lactamase (ESBL) and/or plasmid-encoded AmpC (pAmpC), in anthropized and remote areas. We evaluated cloacal swabs of 20 wild magnificent frigatebirds (Fregata magnificens) of the Alcatrazes Archipelago, the biggest breeding colony of magnificent frigatebirds in the southern Atlantic and a natural protected area with no history of human occupation, located in the anthropized southeastern Brazilian coast. We characterized a highly virulent multidrug-resistant ST648 (O153:H9) pandemic clone, harboring blaCTX–M–2, blaCMY–2, qnrB, tetB, sul1, sul2, aadA1, aac(3)-VIa and mdfA, and virulence genes characteristic of avian pathogenic (APEC) (hlyF, iroN, iss, iutA, and ompT) and other extraintestinal E. coli (ExPEC) (chuA, kpsMII, and papC). To our knowledge, this is the first report of ST648 E. coli co-producing ESBL and pAmpC in wild birds inhabiting insular environments. We suggest this potentially zoonotic and pathogenic lineage was likely acquired through indirect anthropogenic contamination of the marine environment, ingestion of contaminated seafood, or by intra and/or interspecific contact. Our findings reinforce the role of wild birds as anthropization sentinels in insular environments and the importance of wildlife surveillance studies on pathogens of critical priority classified by the World Health Organization.https://www.frontiersin.org/articles/10.3389/fmicb.2022.940600/fullpAmpCESBLantimicrobial resistanceislandwildlifeOne Health
spellingShingle Ana Carolina Ewbank
Danny Fuentes-Castillo
Danny Fuentes-Castillo
Carlos Sacristán
Fernanda Esposito
Fernanda Esposito
Bruna Fuga
Bruna Fuga
Bruna Fuga
Brenda Cardoso
Brenda Cardoso
Silvia Neri Godoy
Roberta Ramblas Zamana
Marco Aurélio Gattamorta
José Luiz Catão-Dias
Nilton Lincopan
Nilton Lincopan
Nilton Lincopan
World Health Organization critical priority Escherichia coli clone ST648 in magnificent frigatebird (Fregata magnificens) of an uninhabited insular environment
Frontiers in Microbiology
pAmpC
ESBL
antimicrobial resistance
island
wildlife
One Health
title World Health Organization critical priority Escherichia coli clone ST648 in magnificent frigatebird (Fregata magnificens) of an uninhabited insular environment
title_full World Health Organization critical priority Escherichia coli clone ST648 in magnificent frigatebird (Fregata magnificens) of an uninhabited insular environment
title_fullStr World Health Organization critical priority Escherichia coli clone ST648 in magnificent frigatebird (Fregata magnificens) of an uninhabited insular environment
title_full_unstemmed World Health Organization critical priority Escherichia coli clone ST648 in magnificent frigatebird (Fregata magnificens) of an uninhabited insular environment
title_short World Health Organization critical priority Escherichia coli clone ST648 in magnificent frigatebird (Fregata magnificens) of an uninhabited insular environment
title_sort world health organization critical priority escherichia coli clone st648 in magnificent frigatebird fregata magnificens of an uninhabited insular environment
topic pAmpC
ESBL
antimicrobial resistance
island
wildlife
One Health
url https://www.frontiersin.org/articles/10.3389/fmicb.2022.940600/full
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