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Decoding Klebsiella pneumoniae in poultry chain: Unveiling genetic landscape, antibiotic resistance, and biocide tolerance in non-clinical reservoirs

2024-04-12Journal article Open access
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dc.contributor.authorMourão, Joana
dc.contributor.authorMagalhães, Mafalda
dc.contributor.authorRibeiro-Almeida, Marisa
dc.contributor.authorRebelo, Andreia
dc.contributor.authorNovais, Carla
dc.contributor.authorPeixe, Luísa
dc.contributor.authorNovais, Ângela
dc.contributor.authorAntunes, Patrícia
dc.date.accessioned2024-12-16T15:18:47Z
dc.date.available2024-12-16T15:18:47Z
dc.date.issued2024-04-12
dc.description.abstractThe rise of antibiotic resistance in the food chain is influenced by the use of antimicrobial agents, such as antibiotics, metals, and biocides, throughout the entire farm-to-fork continuum. Besides, non-clinical reservoirs potentially contribute to the transmission of critical pathogens such as multidrug-resistant (MDR) Klebsiella pneumoniae. However, limited knowledge exists about the population structure and genomic diversity of K. pneumoniae circulating in conventional poultry production. We conducted a comprehensive characterization of K. pneumoniae across the whole chicken production chain (flocks/environment/meat, 2019-2022), exploring factors beyond antibiotics, like copper and quaternary ammonium compounds (QACs). Clonal diversity and adaptive features of K. pneumoniae were characterized through cultural, molecular (FT-IR), and whole-genome-sequencing (WGS) approaches. All except one flock were positive for K. pneumoniae with a significant increase (p < 0.05) from early to pre-slaughter stages, most persisting in chicken meat batches. Colistin-resistant K. pneumoniae rates were low (4%), while most samples carried MDR strains (67%) and copper-tolerant isolates (63%; sil+pco clusters; MICCuSO4≥16mM), particularly at pre-slaughter. Benzalkonium chloride consistently exhibited activity in K. pneumoniae (MIC/MBC range=4-64mg/L) from diverse and representative strains independently of the presence/absence of genes linked to QACs tolerance. A polyclonal K. pneumoniae population, discriminated by FT-IR and WGS, included various lineages dispersed throughout the chicken’s lifecycle at the farm (ST29-KL124, ST11-KL106, ST15-KL19, ST1228-KL38), until the meat (ST1-KL19, ST11-KL111, ST6405-KL109, and ST6406-CG147-KL111), or over years (ST631-49 KL109, ST6651-KL107, ST6406-CG147-KL111). Notably, some lineages were identical to those from human clinical isolates. WGS also revealed F-type multireplicon plasmids carrying sil+pco (copper) co-located with qacEΔ1±qacF (QACs) and antibiotic resistance genes like those disseminated in humans. In conclusion, chicken farms and their derived meat are significant reservoirs for diverse K. pneumoniae clones enriched in antibiotic resistance and metal tolerance genes, some exhibiting genetic similarities with human clinical strains. Further research is imperative to unravel the factors influencing K. pneumoniae persistence and dissemination within poultry production, contributing to improved food safety risk management. This study underscores the significance of understanding the interplay between antimicrobial control strategies and non-clinical sources to effectively address the spread of antimicrobial resistance.pt_PT
dc.description.versioninfo:eu-repo/semantics/publishedVersionpt_PT
dc.identifier.citationMourão, J., Magalhães, M., Ribeiro-Almeida, M., Rebelo, A., Novais, C., Peixe, L., Novais, Â., & Antunes, P. (2024). Decoding Klebsiella pneumoniae in poultry chain: Unveiling genetic landscape, antibiotic resistance, and biocide tolerance in non-clinical reservoirs. Frontiers in Microbiology, 15. https://doi.org/10.3389/fmicb.2024.1365011pt_PT
dc.identifier.doi10.3389/fmicb.2024.1365011pt_PT
dc.identifier.eissn1664-302X
dc.identifier.urihttp://hdl.handle.net/10400.22/26862
dc.language.isoengpt_PT
dc.peerreviewedyespt_PT
dc.publisherFrontierspt_PT
dc.relationThe author(s) declare financial support was received for the research, authorship, and/or publication of this article. This work was supported by the Applied Molecular Biosciences Unit—UCIBIO which is financed by national funds from FCT—Fundação para a Ciência e a Tecnologia (UIDP/04378/2020 and UIDB/04378/2020), by the Associate Laboratory Institute for Health and Bioeconomy-i4HB (LA/P/0140/2020), by the AgriFood XXI I&D&I project (NORTE-01-0145-FEDER-000041) co-financed by the European Regional Development Fund (ERDF) through NORTE 2020 (Programa Operacional Regional do Norte 2014/2020) and by the University of Porto and Soja de Portugal (grant no IJUP-Empresas-2021-14). JM and ÂN were supported by national funds through FCT/MCTES in the context of the Scientific Employment Stimulus (2021.03416.CEECIND and 2021.02252.CEECIND, respectively). MR-A and AR were supported by PhD fellowships from FCT (SFRH/BD/146405/2019 and SFRH/BD/137100/2018, respectively). The authors are greatly indebted to all the financing sources.pt_PT
dc.relation.publisherversionhttps://www.frontiersin.org/journals/microbiology/articles/10.3389/fmicb.2024.1365011/fullpt_PT
dc.rights.urihttp://creativecommons.org/licenses/by/4.0/pt_PT
dc.subjectKlebsiella pneumoniaept_PT
dc.subjectAntibiotic resistancept_PT
dc.subjectMetalspt_PT
dc.subjectChicken productionpt_PT
dc.subjectEnvironmentpt_PT
dc.subjectMeatpt_PT
dc.subjectWGSpt_PT
dc.subjectPlasmidspt_PT
dc.titleDecoding Klebsiella pneumoniae in poultry chain: Unveiling genetic landscape, antibiotic resistance, and biocide tolerance in non-clinical reservoirspt_PT
dc.typejournal article
dspace.entity.typePublication
oaire.citation.endPage15pt_PT
oaire.citation.startPage1pt_PT
oaire.citation.titleFrontiers in Microbiologypt_PT
oaire.citation.volume15pt_PT
person.familyNameRebelo
person.givenNameAndreia
person.identifier.ciencia-idA81C-7A59-ECAD
person.identifier.orcid0000-0003-2218-6005
person.identifier.ridT-9024-2017
rcaap.rightsopenAccesspt_PT
rcaap.typearticlept_PT
relation.isAuthorOfPublication913dc5cd-9e92-456d-88f5-419571a87f85
relation.isAuthorOfPublication.latestForDiscovery913dc5cd-9e92-456d-88f5-419571a87f85

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