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Investigating the host specificity of Campylobacter jejuni and Campylobacter coli by sequencing gyrase subunit A

BACKGROUND: Surveillance and field investigations of Campylobacter infections require molecular tools with genetic markers appropriate for tracing purposes, i.e. based on the principle that some Campylobacter lineages acquire a host signature under adaptive selection pressure. We developed a sequenc...

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Autores principales: Ragimbeau, Catherine, Colin, Stephanie, Devaux, Anthony, Decruyenaere, Frédéric, Cauchie, Henry-Michel, Losch, Serge, Penny, Christian, Mossong, Joël
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4156964/
https://www.ncbi.nlm.nih.gov/pubmed/25163418
http://dx.doi.org/10.1186/s12866-014-0205-7
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author Ragimbeau, Catherine
Colin, Stephanie
Devaux, Anthony
Decruyenaere, Frédéric
Cauchie, Henry-Michel
Losch, Serge
Penny, Christian
Mossong, Joël
author_facet Ragimbeau, Catherine
Colin, Stephanie
Devaux, Anthony
Decruyenaere, Frédéric
Cauchie, Henry-Michel
Losch, Serge
Penny, Christian
Mossong, Joël
author_sort Ragimbeau, Catherine
collection PubMed
description BACKGROUND: Surveillance and field investigations of Campylobacter infections require molecular tools with genetic markers appropriate for tracing purposes, i.e. based on the principle that some Campylobacter lineages acquire a host signature under adaptive selection pressure. We developed a sequence-based method targeting the quinolone resistance determining region within the subunit A of DNA gyrase (gyrA). Host specificity was evaluated by characterizing two collections of Campylobacter jejuni (N = 430) and Campylobacter coli (N = 302) originating from surface waters, domestic mammals and poultry. RESULTS: Based on nucleotide identity, a total of 80 gyrA alleles were observed. Thirty nine alleles assigned to C. coli encoding two peptides fell into three clades: two associated with surface waters and one associated with domestic mammals and poultry. The variability in GC content generated by synonymous mutations suggested that surface waters isolates originated from two distinct ecological niches. A total of 42 alleles were recorded from C. jejuni strains and encoded 8 peptides including one lying in a distinct lineage associated with wildlife. Seven of the 23 alleles encoding peptide #1 displayed the synonymous mutation G408A not identified in poultry isolates. By contrast, the substitution Ser22Gly observed in 4 different peptide groups was significantly associated with domestic birds (P = 0.001). The change in amino acid sequences Thr86Ile conferring resistance to quinolones was significantly associated with poultry (P < 0.001) in both C. jejuni and C. coli with 38.7% and 67.9% of quinolone-resistant strains, respectively. CONCLUSIONS: The gyrA typing method presented here is an informative tool as sequences appear to be predictive of particular ecological niches. Combined with multi-locus sequence typing, it could increase the resolution of source attribution, and combined with porA/flaA typing it could be suitable for detecting temporal clusters of human cases. All gyrA alleles identified were deposited in the freely accessible online database http://pubmlst.org/campylobacter. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12866-014-0205-7) contains supplementary material, which is available to authorized users.
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spelling pubmed-41569642014-09-08 Investigating the host specificity of Campylobacter jejuni and Campylobacter coli by sequencing gyrase subunit A Ragimbeau, Catherine Colin, Stephanie Devaux, Anthony Decruyenaere, Frédéric Cauchie, Henry-Michel Losch, Serge Penny, Christian Mossong, Joël BMC Microbiol Research Article BACKGROUND: Surveillance and field investigations of Campylobacter infections require molecular tools with genetic markers appropriate for tracing purposes, i.e. based on the principle that some Campylobacter lineages acquire a host signature under adaptive selection pressure. We developed a sequence-based method targeting the quinolone resistance determining region within the subunit A of DNA gyrase (gyrA). Host specificity was evaluated by characterizing two collections of Campylobacter jejuni (N = 430) and Campylobacter coli (N = 302) originating from surface waters, domestic mammals and poultry. RESULTS: Based on nucleotide identity, a total of 80 gyrA alleles were observed. Thirty nine alleles assigned to C. coli encoding two peptides fell into three clades: two associated with surface waters and one associated with domestic mammals and poultry. The variability in GC content generated by synonymous mutations suggested that surface waters isolates originated from two distinct ecological niches. A total of 42 alleles were recorded from C. jejuni strains and encoded 8 peptides including one lying in a distinct lineage associated with wildlife. Seven of the 23 alleles encoding peptide #1 displayed the synonymous mutation G408A not identified in poultry isolates. By contrast, the substitution Ser22Gly observed in 4 different peptide groups was significantly associated with domestic birds (P = 0.001). The change in amino acid sequences Thr86Ile conferring resistance to quinolones was significantly associated with poultry (P < 0.001) in both C. jejuni and C. coli with 38.7% and 67.9% of quinolone-resistant strains, respectively. CONCLUSIONS: The gyrA typing method presented here is an informative tool as sequences appear to be predictive of particular ecological niches. Combined with multi-locus sequence typing, it could increase the resolution of source attribution, and combined with porA/flaA typing it could be suitable for detecting temporal clusters of human cases. All gyrA alleles identified were deposited in the freely accessible online database http://pubmlst.org/campylobacter. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12866-014-0205-7) contains supplementary material, which is available to authorized users. BioMed Central 2014-08-28 /pmc/articles/PMC4156964/ /pubmed/25163418 http://dx.doi.org/10.1186/s12866-014-0205-7 Text en © Ragimbeau et al.; licensee BioMed Central Ltd. 2014 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Ragimbeau, Catherine
Colin, Stephanie
Devaux, Anthony
Decruyenaere, Frédéric
Cauchie, Henry-Michel
Losch, Serge
Penny, Christian
Mossong, Joël
Investigating the host specificity of Campylobacter jejuni and Campylobacter coli by sequencing gyrase subunit A
title Investigating the host specificity of Campylobacter jejuni and Campylobacter coli by sequencing gyrase subunit A
title_full Investigating the host specificity of Campylobacter jejuni and Campylobacter coli by sequencing gyrase subunit A
title_fullStr Investigating the host specificity of Campylobacter jejuni and Campylobacter coli by sequencing gyrase subunit A
title_full_unstemmed Investigating the host specificity of Campylobacter jejuni and Campylobacter coli by sequencing gyrase subunit A
title_short Investigating the host specificity of Campylobacter jejuni and Campylobacter coli by sequencing gyrase subunit A
title_sort investigating the host specificity of campylobacter jejuni and campylobacter coli by sequencing gyrase subunit a
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4156964/
https://www.ncbi.nlm.nih.gov/pubmed/25163418
http://dx.doi.org/10.1186/s12866-014-0205-7
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