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Comparative genomics reveals a lack of evidence for pigeons as a main source of stx(2f)-carrying Escherichia coli causing disease in humans and the common existence of hybrid Shiga toxin-producing and enteropathogenic E. coli pathotypes

BACKGROUND: Wild birds, in particular pigeons are considered a natural reservoir for stx(2f)-carrying E. coli. An extensive comparison of isolates from pigeons and humans from the same region is lacking, which hampers justifiable conclusions on the epidemiology of these pathogens. Over two hundred h...

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Autores principales: van Hoek, Angela H. A. M., van Veldhuizen, Janieke N. J., Friesema, Ingrid, Coipan, Claudia, Rossen, John W. A., Bergval, Indra L., Franz, Eelco
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451237/
https://www.ncbi.nlm.nih.gov/pubmed/30953471
http://dx.doi.org/10.1186/s12864-019-5635-z
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author van Hoek, Angela H. A. M.
van Veldhuizen, Janieke N. J.
Friesema, Ingrid
Coipan, Claudia
Rossen, John W. A.
Bergval, Indra L.
Franz, Eelco
author_facet van Hoek, Angela H. A. M.
van Veldhuizen, Janieke N. J.
Friesema, Ingrid
Coipan, Claudia
Rossen, John W. A.
Bergval, Indra L.
Franz, Eelco
author_sort van Hoek, Angela H. A. M.
collection PubMed
description BACKGROUND: Wild birds, in particular pigeons are considered a natural reservoir for stx(2f)-carrying E. coli. An extensive comparison of isolates from pigeons and humans from the same region is lacking, which hampers justifiable conclusions on the epidemiology of these pathogens. Over two hundred human and pigeon stx(2f)-carrying E. coli isolates predominantly from the Netherlands were analysed by whole genome sequencing and comparative genomic analysis including in silico MLST, serotyping, virulence genes typing and whole genome MLST (wgMLST). RESULTS: Serotypes and sequence types of stx(2f)-carrying E. coli showed a strong non-random distribution among the human and pigeon isolates with O63:H6/ST583, O113:H6/ST121 and O125:H6/ST583 overrepresented among the human isolates and not found among pigeons. Pigeon isolates were characterized by an overrepresentation of O4:H2/ST20 and O45:H2/ST20. Nearly all isolates harboured the locus of enterocyte effacement (LEE) but different eae and tir subtypes were non-randomly distributed among human and pigeon isolates. Phylogenetic core genome comparison demonstrated that the pigeon isolates and clinical isolates largely occurred in separated clusters. In addition, serotypes/STs exclusively found among humans generally were characterized by high level of clonality, smaller genome sizes and lack of several non-LEE-encoded virulence genes. A bundle-forming pilus operon, including bfpA, indicative for typical enteropathogenic E. coli (tEPEC) was demonstrated in 72.0% of the stx(2f)-carrying serotypes but with distinct operon types between the main pigeon and human isolate clusters. CONCLUSIONS: Comparative genomics revealed that isolates from mild human disease are dominated by serotypes not encountered in the pigeon reservoir. It is therefore unlikely that zoonotic transmission from this reservoir plays an important role in the contribution to the majority of human disease associated with stx(2f)-producing E. coli in the Netherlands. Unexpectedly, this study identified the common occurrence of STEC(2f)/tEPEC hybrid pathotype in various serotypes and STs. Further research should focus on the possible role of human-to-human transmission of Stx2f-producing E. coli. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-019-5635-z) contains supplementary material, which is available to authorized users.
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spelling pubmed-64512372019-04-16 Comparative genomics reveals a lack of evidence for pigeons as a main source of stx(2f)-carrying Escherichia coli causing disease in humans and the common existence of hybrid Shiga toxin-producing and enteropathogenic E. coli pathotypes van Hoek, Angela H. A. M. van Veldhuizen, Janieke N. J. Friesema, Ingrid Coipan, Claudia Rossen, John W. A. Bergval, Indra L. Franz, Eelco BMC Genomics Research Article BACKGROUND: Wild birds, in particular pigeons are considered a natural reservoir for stx(2f)-carrying E. coli. An extensive comparison of isolates from pigeons and humans from the same region is lacking, which hampers justifiable conclusions on the epidemiology of these pathogens. Over two hundred human and pigeon stx(2f)-carrying E. coli isolates predominantly from the Netherlands were analysed by whole genome sequencing and comparative genomic analysis including in silico MLST, serotyping, virulence genes typing and whole genome MLST (wgMLST). RESULTS: Serotypes and sequence types of stx(2f)-carrying E. coli showed a strong non-random distribution among the human and pigeon isolates with O63:H6/ST583, O113:H6/ST121 and O125:H6/ST583 overrepresented among the human isolates and not found among pigeons. Pigeon isolates were characterized by an overrepresentation of O4:H2/ST20 and O45:H2/ST20. Nearly all isolates harboured the locus of enterocyte effacement (LEE) but different eae and tir subtypes were non-randomly distributed among human and pigeon isolates. Phylogenetic core genome comparison demonstrated that the pigeon isolates and clinical isolates largely occurred in separated clusters. In addition, serotypes/STs exclusively found among humans generally were characterized by high level of clonality, smaller genome sizes and lack of several non-LEE-encoded virulence genes. A bundle-forming pilus operon, including bfpA, indicative for typical enteropathogenic E. coli (tEPEC) was demonstrated in 72.0% of the stx(2f)-carrying serotypes but with distinct operon types between the main pigeon and human isolate clusters. CONCLUSIONS: Comparative genomics revealed that isolates from mild human disease are dominated by serotypes not encountered in the pigeon reservoir. It is therefore unlikely that zoonotic transmission from this reservoir plays an important role in the contribution to the majority of human disease associated with stx(2f)-producing E. coli in the Netherlands. Unexpectedly, this study identified the common occurrence of STEC(2f)/tEPEC hybrid pathotype in various serotypes and STs. Further research should focus on the possible role of human-to-human transmission of Stx2f-producing E. coli. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-019-5635-z) contains supplementary material, which is available to authorized users. BioMed Central 2019-04-05 /pmc/articles/PMC6451237/ /pubmed/30953471 http://dx.doi.org/10.1186/s12864-019-5635-z Text en © The Author(s). 2019 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. 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
van Hoek, Angela H. A. M.
van Veldhuizen, Janieke N. J.
Friesema, Ingrid
Coipan, Claudia
Rossen, John W. A.
Bergval, Indra L.
Franz, Eelco
Comparative genomics reveals a lack of evidence for pigeons as a main source of stx(2f)-carrying Escherichia coli causing disease in humans and the common existence of hybrid Shiga toxin-producing and enteropathogenic E. coli pathotypes
title Comparative genomics reveals a lack of evidence for pigeons as a main source of stx(2f)-carrying Escherichia coli causing disease in humans and the common existence of hybrid Shiga toxin-producing and enteropathogenic E. coli pathotypes
title_full Comparative genomics reveals a lack of evidence for pigeons as a main source of stx(2f)-carrying Escherichia coli causing disease in humans and the common existence of hybrid Shiga toxin-producing and enteropathogenic E. coli pathotypes
title_fullStr Comparative genomics reveals a lack of evidence for pigeons as a main source of stx(2f)-carrying Escherichia coli causing disease in humans and the common existence of hybrid Shiga toxin-producing and enteropathogenic E. coli pathotypes
title_full_unstemmed Comparative genomics reveals a lack of evidence for pigeons as a main source of stx(2f)-carrying Escherichia coli causing disease in humans and the common existence of hybrid Shiga toxin-producing and enteropathogenic E. coli pathotypes
title_short Comparative genomics reveals a lack of evidence for pigeons as a main source of stx(2f)-carrying Escherichia coli causing disease in humans and the common existence of hybrid Shiga toxin-producing and enteropathogenic E. coli pathotypes
title_sort comparative genomics reveals a lack of evidence for pigeons as a main source of stx(2f)-carrying escherichia coli causing disease in humans and the common existence of hybrid shiga toxin-producing and enteropathogenic e. coli pathotypes
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6451237/
https://www.ncbi.nlm.nih.gov/pubmed/30953471
http://dx.doi.org/10.1186/s12864-019-5635-z
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