Genomic insight into Campylobacter jejuni isolated from commercial turkey flocks in Germany using whole-genome sequencing analysis

Campylobacter (C.) jejuni is a zoonotic bacterium of public health significance. The present investigation was designed to assess the epidemiology and genetic heterogeneity of C. jejuni recovered from commercial turkey farms in Germany using whole-genome sequencing. The Illumina MiSeq® technology wa...

Full description

Bibliographic Details
Main Authors: Hosny El-Adawy, Helmut Hotzel, Silvia García-Soto, Herbert Tomaso, Hafez M. Hafez, Stefan Schwarz, Heinrich Neubauer, Jörg Linde
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-02-01
Series:Frontiers in Veterinary Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fvets.2023.1092179/full
_version_ 1797904976467460096
author Hosny El-Adawy
Hosny El-Adawy
Helmut Hotzel
Silvia García-Soto
Herbert Tomaso
Hafez M. Hafez
Stefan Schwarz
Stefan Schwarz
Heinrich Neubauer
Jörg Linde
author_facet Hosny El-Adawy
Hosny El-Adawy
Helmut Hotzel
Silvia García-Soto
Herbert Tomaso
Hafez M. Hafez
Stefan Schwarz
Stefan Schwarz
Heinrich Neubauer
Jörg Linde
author_sort Hosny El-Adawy
collection DOAJ
description Campylobacter (C.) jejuni is a zoonotic bacterium of public health significance. The present investigation was designed to assess the epidemiology and genetic heterogeneity of C. jejuni recovered from commercial turkey farms in Germany using whole-genome sequencing. The Illumina MiSeq® technology was used to sequence 66 C. jejuni isolates obtained between 2010 and 2011 from commercial meat turkey flocks located in ten German federal states. Phenotypic antimicrobial resistance was determined. Phylogeny, resistome, plasmidome and virulome profiles were analyzed using whole-genome sequencing data. Genetic resistance markers were identified with bioinformatics tools (AMRFinder, ResFinder, NCBI and ABRicate) and compared with the phenotypic antimicrobial resistance. The isolates were assigned to 28 different sequence types and 11 clonal complexes. The average pairwise single nucleotide-polymorphisms distance of 14,585 SNPs (range: 0–26,540 SNPs) revealed a high genetic distinction between the isolates. Thirteen virulence-associated genes were identified in C. jejuni isolates. Most of the isolates harbored the genes flaA (83.3%) and flaB (78.8%). The wlaN gene associated with the Guillain–Barré syndrome was detected in nine (13.6%) isolates. The genes for resistance to ampicillin (blaOXA), tetracycline [tet(O)], neomycin [aph(3')-IIIa], streptomycin (aadE) and streptothricin (sat4) were detected in isolated C. jejuni using WGS. A gene cluster comprising the genes sat4, aph(3′)-IIIa and aadE was present in six isolates. The single point mutation T86I in the housekeeping gene gyrA conferring resistance to quinolones was retrieved in 93.6% of phenotypically fluoroquinolone-resistant isolates. Five phenotypically erythromycin-susceptible isolates carried the mutation A103V in the gene for the ribosomal protein L22 inferring macrolide resistance. An assortment of 13 β-lactam resistance genes (blaOXA variants) was detected in 58 C. jejuni isolates. Out of 66 sequenced isolates, 28 (42.4%) carried plasmid-borne contigs. Six isolates harbored a pTet-like plasmid-borne contig which carries the tet(O) gene. This study emphasized the potential of whole-genome sequencing to ameliorate the routine surveillance of C. jejuni. Whole-genome sequencing can predict antimicrobial resistance with a high degree of accuracy. However, resistance gene databases need curation and updates to revoke inaccuracy when using WGS-based analysis pipelines for AMR detection.
first_indexed 2024-04-10T09:58:49Z
format Article
id doaj.art-5eddc65ad0ab4e4dafb111e9c5665f35
institution Directory Open Access Journal
issn 2297-1769
language English
last_indexed 2024-04-10T09:58:49Z
publishDate 2023-02-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Veterinary Science
spelling doaj.art-5eddc65ad0ab4e4dafb111e9c5665f352023-02-16T11:35:50ZengFrontiers Media S.A.Frontiers in Veterinary Science2297-17692023-02-011010.3389/fvets.2023.10921791092179Genomic insight into Campylobacter jejuni isolated from commercial turkey flocks in Germany using whole-genome sequencing analysisHosny El-Adawy0Hosny El-Adawy1Helmut Hotzel2Silvia García-Soto3Herbert Tomaso4Hafez M. Hafez5Stefan Schwarz6Stefan Schwarz7Heinrich Neubauer8Jörg Linde9Institute of Bacterial Infections and Zoonoses, Friedrich-Loeffler-Institut, Jena, GermanyFaculty of Veterinary Medicine, Kafrelsheikh University, Kafr El-Sheikh, EgyptInstitute of Bacterial Infections and Zoonoses, Friedrich-Loeffler-Institut, Jena, GermanyInstitute of Bacterial Infections and Zoonoses, Friedrich-Loeffler-Institut, Jena, GermanyInstitute of Bacterial Infections and Zoonoses, Friedrich-Loeffler-Institut, Jena, GermanyInstitute of Poultry Diseases, Free University Berlin, Berlin, GermanyInstitute of Microbiology and Epizootics, Centre for Infection Medicine, Department of Veterinary Medicine, Freie Universität Berlin, Berlin, GermanyVeterinary Centre of Resistance Research (TZR), Freie Universität Berlin, Berlin, GermanyInstitute of Bacterial Infections and Zoonoses, Friedrich-Loeffler-Institut, Jena, GermanyInstitute of Bacterial Infections and Zoonoses, Friedrich-Loeffler-Institut, Jena, GermanyCampylobacter (C.) jejuni is a zoonotic bacterium of public health significance. The present investigation was designed to assess the epidemiology and genetic heterogeneity of C. jejuni recovered from commercial turkey farms in Germany using whole-genome sequencing. The Illumina MiSeq® technology was used to sequence 66 C. jejuni isolates obtained between 2010 and 2011 from commercial meat turkey flocks located in ten German federal states. Phenotypic antimicrobial resistance was determined. Phylogeny, resistome, plasmidome and virulome profiles were analyzed using whole-genome sequencing data. Genetic resistance markers were identified with bioinformatics tools (AMRFinder, ResFinder, NCBI and ABRicate) and compared with the phenotypic antimicrobial resistance. The isolates were assigned to 28 different sequence types and 11 clonal complexes. The average pairwise single nucleotide-polymorphisms distance of 14,585 SNPs (range: 0–26,540 SNPs) revealed a high genetic distinction between the isolates. Thirteen virulence-associated genes were identified in C. jejuni isolates. Most of the isolates harbored the genes flaA (83.3%) and flaB (78.8%). The wlaN gene associated with the Guillain–Barré syndrome was detected in nine (13.6%) isolates. The genes for resistance to ampicillin (blaOXA), tetracycline [tet(O)], neomycin [aph(3')-IIIa], streptomycin (aadE) and streptothricin (sat4) were detected in isolated C. jejuni using WGS. A gene cluster comprising the genes sat4, aph(3′)-IIIa and aadE was present in six isolates. The single point mutation T86I in the housekeeping gene gyrA conferring resistance to quinolones was retrieved in 93.6% of phenotypically fluoroquinolone-resistant isolates. Five phenotypically erythromycin-susceptible isolates carried the mutation A103V in the gene for the ribosomal protein L22 inferring macrolide resistance. An assortment of 13 β-lactam resistance genes (blaOXA variants) was detected in 58 C. jejuni isolates. Out of 66 sequenced isolates, 28 (42.4%) carried plasmid-borne contigs. Six isolates harbored a pTet-like plasmid-borne contig which carries the tet(O) gene. This study emphasized the potential of whole-genome sequencing to ameliorate the routine surveillance of C. jejuni. Whole-genome sequencing can predict antimicrobial resistance with a high degree of accuracy. However, resistance gene databases need curation and updates to revoke inaccuracy when using WGS-based analysis pipelines for AMR detection.https://www.frontiersin.org/articles/10.3389/fvets.2023.1092179/fullCampylobacter jejuniturkeysgenetic diversityWGSMLSTresistome
spellingShingle Hosny El-Adawy
Hosny El-Adawy
Helmut Hotzel
Silvia García-Soto
Herbert Tomaso
Hafez M. Hafez
Stefan Schwarz
Stefan Schwarz
Heinrich Neubauer
Jörg Linde
Genomic insight into Campylobacter jejuni isolated from commercial turkey flocks in Germany using whole-genome sequencing analysis
Frontiers in Veterinary Science
Campylobacter jejuni
turkeys
genetic diversity
WGS
MLST
resistome
title Genomic insight into Campylobacter jejuni isolated from commercial turkey flocks in Germany using whole-genome sequencing analysis
title_full Genomic insight into Campylobacter jejuni isolated from commercial turkey flocks in Germany using whole-genome sequencing analysis
title_fullStr Genomic insight into Campylobacter jejuni isolated from commercial turkey flocks in Germany using whole-genome sequencing analysis
title_full_unstemmed Genomic insight into Campylobacter jejuni isolated from commercial turkey flocks in Germany using whole-genome sequencing analysis
title_short Genomic insight into Campylobacter jejuni isolated from commercial turkey flocks in Germany using whole-genome sequencing analysis
title_sort genomic insight into campylobacter jejuni isolated from commercial turkey flocks in germany using whole genome sequencing analysis
topic Campylobacter jejuni
turkeys
genetic diversity
WGS
MLST
resistome
url https://www.frontiersin.org/articles/10.3389/fvets.2023.1092179/full
work_keys_str_mv AT hosnyeladawy genomicinsightintocampylobacterjejuniisolatedfromcommercialturkeyflocksingermanyusingwholegenomesequencinganalysis
AT hosnyeladawy genomicinsightintocampylobacterjejuniisolatedfromcommercialturkeyflocksingermanyusingwholegenomesequencinganalysis
AT helmuthotzel genomicinsightintocampylobacterjejuniisolatedfromcommercialturkeyflocksingermanyusingwholegenomesequencinganalysis
AT silviagarciasoto genomicinsightintocampylobacterjejuniisolatedfromcommercialturkeyflocksingermanyusingwholegenomesequencinganalysis
AT herberttomaso genomicinsightintocampylobacterjejuniisolatedfromcommercialturkeyflocksingermanyusingwholegenomesequencinganalysis
AT hafezmhafez genomicinsightintocampylobacterjejuniisolatedfromcommercialturkeyflocksingermanyusingwholegenomesequencinganalysis
AT stefanschwarz genomicinsightintocampylobacterjejuniisolatedfromcommercialturkeyflocksingermanyusingwholegenomesequencinganalysis
AT stefanschwarz genomicinsightintocampylobacterjejuniisolatedfromcommercialturkeyflocksingermanyusingwholegenomesequencinganalysis
AT heinrichneubauer genomicinsightintocampylobacterjejuniisolatedfromcommercialturkeyflocksingermanyusingwholegenomesequencinganalysis
AT jorglinde genomicinsightintocampylobacterjejuniisolatedfromcommercialturkeyflocksingermanyusingwholegenomesequencinganalysis