Occurrence of Colibacillosis in Broilers and Its Relationship With Avian Pathogenic Escherichia coli (APEC) Population Structure and Molecular Characteristics

Avian pathogenic Escherichia coli (APEC) causes colibacillosis, the disease with the highest economic loss for the broiler industry. However, studies focusing on the prevalence and population structure of APEC in the broiler production pyramid are scarce. Here, we used genotyping and serotyping data...

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Main Authors: Ilias Apostolakos, Andrea Laconi, Lapo Mughini-Gras, Özlem Şahan Yapicier, Alessandra Piccirillo
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-09-01
Series:Frontiers in Veterinary Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fvets.2021.737720/full
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author Ilias Apostolakos
Andrea Laconi
Lapo Mughini-Gras
Lapo Mughini-Gras
Özlem Şahan Yapicier
Alessandra Piccirillo
author_facet Ilias Apostolakos
Andrea Laconi
Lapo Mughini-Gras
Lapo Mughini-Gras
Özlem Şahan Yapicier
Alessandra Piccirillo
author_sort Ilias Apostolakos
collection DOAJ
description Avian pathogenic Escherichia coli (APEC) causes colibacillosis, the disease with the highest economic loss for the broiler industry. However, studies focusing on the prevalence and population structure of APEC in the broiler production pyramid are scarce. Here, we used genotyping and serotyping data to elucidate the APEC population structure and its changes in different broiler production stages along with whole-genome sequencing (WGS) in a subset of APEC isolates to determine transmission patterns amongst dominant APEC sequence types (STs) and characterize them in detail. Comparison of genotypes encountered in both APEC and avian fecal E. coli (AFEC) provided further insights. Overall, APEC-related mortality, as the proportion of the total sampled mortality in the broiler production, was high (35%), while phylogroup C and serogroup O78 were predominant amongst APEC isolates. We found a low (34.0%) and high (53.3%) incidence of colibacillosis in chicks and end-cycle broilers, respectively, which may be related to a shift in APEC genotypes, suggesting a trend from commensalism to pathogenicity across different broiler production stages. Despite considerable APEC genotypic diversity, there was substantial genotype overlap (40.9%, overall) over the production stages and convergence of STs to the four clusters. Within these clusters, WGS data provided evidence of clonal transmission events and revealed an enriched virulence and resistance APEC repertoire. More specifically, sequenced APEC were assigned to defined pathotypes based on their virulence gene content while the majority (86%) was genotypically multi-drug resistant. Interestingly, WGS-based phylogeny showed that a subset of APEC, which are cephalosporin-resistant, may originate directly from cephalosporin-resistant AFEC. Finally, exploration of the APEC plasmidome indicated that the small fraction of the APEC virulome carried by IncF plasmids is pivotal for the manifestation of the APEC pathotype; thus, plasmid exchange can promote pathogenicity in strains that are at the edge of the commensal and pathogenic states.
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spelling doaj.art-2244ee37cbe4424ea4eb0e48240475532022-12-21T21:26:03ZengFrontiers Media S.A.Frontiers in Veterinary Science2297-17692021-09-01810.3389/fvets.2021.737720737720Occurrence of Colibacillosis in Broilers and Its Relationship With Avian Pathogenic Escherichia coli (APEC) Population Structure and Molecular CharacteristicsIlias Apostolakos0Andrea Laconi1Lapo Mughini-Gras2Lapo Mughini-Gras3Özlem Şahan Yapicier4Alessandra Piccirillo5Department of Comparative Biomedicine and Food Science, University of Padua, Legnaro, ItalyDepartment of Comparative Biomedicine and Food Science, University of Padua, Legnaro, ItalyCenter for Infectious Disease Control, National Institute for Public Health and the Environment (RIVM), Bilthoven, NetherlandsFaculty of Veterinary Medicine, Utrecht University, Utrecht, NetherlandsRepublic of Turkey Ministry of Agriculture and Forestry Veterinary Control, Central Research Institute, Bacteriology Diagnostic Laboratory, Ankara, TurkeyDepartment of Comparative Biomedicine and Food Science, University of Padua, Legnaro, ItalyAvian pathogenic Escherichia coli (APEC) causes colibacillosis, the disease with the highest economic loss for the broiler industry. However, studies focusing on the prevalence and population structure of APEC in the broiler production pyramid are scarce. Here, we used genotyping and serotyping data to elucidate the APEC population structure and its changes in different broiler production stages along with whole-genome sequencing (WGS) in a subset of APEC isolates to determine transmission patterns amongst dominant APEC sequence types (STs) and characterize them in detail. Comparison of genotypes encountered in both APEC and avian fecal E. coli (AFEC) provided further insights. Overall, APEC-related mortality, as the proportion of the total sampled mortality in the broiler production, was high (35%), while phylogroup C and serogroup O78 were predominant amongst APEC isolates. We found a low (34.0%) and high (53.3%) incidence of colibacillosis in chicks and end-cycle broilers, respectively, which may be related to a shift in APEC genotypes, suggesting a trend from commensalism to pathogenicity across different broiler production stages. Despite considerable APEC genotypic diversity, there was substantial genotype overlap (40.9%, overall) over the production stages and convergence of STs to the four clusters. Within these clusters, WGS data provided evidence of clonal transmission events and revealed an enriched virulence and resistance APEC repertoire. More specifically, sequenced APEC were assigned to defined pathotypes based on their virulence gene content while the majority (86%) was genotypically multi-drug resistant. Interestingly, WGS-based phylogeny showed that a subset of APEC, which are cephalosporin-resistant, may originate directly from cephalosporin-resistant AFEC. Finally, exploration of the APEC plasmidome indicated that the small fraction of the APEC virulome carried by IncF plasmids is pivotal for the manifestation of the APEC pathotype; thus, plasmid exchange can promote pathogenicity in strains that are at the edge of the commensal and pathogenic states.https://www.frontiersin.org/articles/10.3389/fvets.2021.737720/fullavian pathogenic E. coli (APEC)broiler-chickenWGS (whole genome sequencing)antimicrobial resistance (AMR)avian fecal Escherichia coli (AFEC)ST11689
spellingShingle Ilias Apostolakos
Andrea Laconi
Lapo Mughini-Gras
Lapo Mughini-Gras
Özlem Şahan Yapicier
Alessandra Piccirillo
Occurrence of Colibacillosis in Broilers and Its Relationship With Avian Pathogenic Escherichia coli (APEC) Population Structure and Molecular Characteristics
Frontiers in Veterinary Science
avian pathogenic E. coli (APEC)
broiler-chicken
WGS (whole genome sequencing)
antimicrobial resistance (AMR)
avian fecal Escherichia coli (AFEC)
ST11689
title Occurrence of Colibacillosis in Broilers and Its Relationship With Avian Pathogenic Escherichia coli (APEC) Population Structure and Molecular Characteristics
title_full Occurrence of Colibacillosis in Broilers and Its Relationship With Avian Pathogenic Escherichia coli (APEC) Population Structure and Molecular Characteristics
title_fullStr Occurrence of Colibacillosis in Broilers and Its Relationship With Avian Pathogenic Escherichia coli (APEC) Population Structure and Molecular Characteristics
title_full_unstemmed Occurrence of Colibacillosis in Broilers and Its Relationship With Avian Pathogenic Escherichia coli (APEC) Population Structure and Molecular Characteristics
title_short Occurrence of Colibacillosis in Broilers and Its Relationship With Avian Pathogenic Escherichia coli (APEC) Population Structure and Molecular Characteristics
title_sort occurrence of colibacillosis in broilers and its relationship with avian pathogenic escherichia coli apec population structure and molecular characteristics
topic avian pathogenic E. coli (APEC)
broiler-chicken
WGS (whole genome sequencing)
antimicrobial resistance (AMR)
avian fecal Escherichia coli (AFEC)
ST11689
url https://www.frontiersin.org/articles/10.3389/fvets.2021.737720/full
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