Spread of avian pathogenic Escherichia coli ST117 O78:H4 in Nordic broiler production

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Abstract

Background

Escherichia coli infections known as colibacillosis constitute a considerable challenge to poultry farmers worldwide, in terms of decreased animal welfare and production economy. Colibacillosis is caused by avian pathogenic E. coli (APEC). APEC strains are extraintestinal pathogenic E. coli and have in general been characterized as being a genetically diverse population. In the Nordic countries, poultry farmers depend on import of Swedish broiler breeders which are part of a breeding pyramid. During 2014 to 2016, an increased occurrence of colibacillosis on Nordic broiler chicken farms was reported. The aim of this study was to investigate the genetic diversity among E. coli isolates collected on poultry farms with colibacillosis issues, using whole genome sequencing.

Methods

Hundred and fourteen bacterial isolates from both broilers and broiler breeders were whole genome sequenced. The majority of isolates were collected from poultry with colibacillosis on Nordic farms. Subsequently, comparative genomic analyses were carried out. This included in silico typing (sero- and multi-locus sequence typing), identification of virulence and resistance genes and phylogenetic analyses based on single nucleotide polymorphisms.

Results

In general, the characterized poultry isolates constituted a genetically diverse population. However, the phylogenetic analyses revealed a major clade of 47 closely related ST117 O78:H4 isolates. The isolates in this clade were collected from broiler chickens and breeders with colibacillosis in multiple Nordic countries. They clustered together with a human ST117 isolate and all carried virulence genes that previously have been associated with human uropathogenic E. coli.

Conclusions

The investigation revealed a lineage of ST117 O78:H4 isolates collected in different Nordic countries from diseased broilers and breeders. The data indicate that the closely related ST117 O78:H4 strains have been transferred vertically through the broiler breeding pyramid into distantly located farms across the Nordic countries.

Electronic supplementary material

The online version of this article (doi:10.1186/s12864-016-3415-6) contains supplementary material, which is available to authorized users.

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Most cited references 28

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Fast algorithms for large-scale genome alignment and comparison.

Arthur L. Delcher, Adam Phillippy, Jane Carlton … (2002)

We describe a suffix-tree algorithm that can align the entire genome sequences of eukaryotic and prokaryotic organisms with minimal use of computer time and memory. The new system, MUMmer 2, runs three times faster while using one-third as much memory as the original MUMmer system. It has been used successfully to align the entire human and mouse genomes to each other, and to align numerous smaller eukaryotic and prokaryotic genomes. A new module permits the alignment of multiple DNA sequence fragments, which has proven valuable in the comparison of incomplete genome sequences. We also describe a method to align more distantly related genomes by detecting protein sequence homology. This extension to MUMmer aligns two genomes after translating the sequence in all six reading frames, extracts all matching protein sequences and then clusters together matches. This method has been applied to both incomplete and complete genome sequences in order to detect regions of conserved synteny, in which multiple proteins from one organism are found in the same order and orientation in another. The system code is being made freely available by the authors.

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Avian pathogenic, uropathogenic, and newborn meningitis-causing Escherichia coli: how closely related are they?

S. Kiessling, Hartmut Steinrück, Ines Diehl … (2007)

Avian pathogenic Escherichia coli (APEC), uropathogenic E. coli (UPEC), and newborn meningitis-causing E. coli (NMEC) establish infections in extraintestinal habitats (extraintestinal pathogenic E. coli; ExPEC) of different hosts. As diversity, epidemiological sources, and evolutionary origins of ExPEC are so far only partially defined, we screened a collection of 526 strains of medical and veterinary origin of various O-types for assignment to E. coli reference collection (ECOR) group and virulence gene patterns. Results of ECOR typing confirmed that human ExPEC strains mostly belong to groups B2, followed by group D. Although a considerable portion of APEC strains did also fell into ECOR group B2 (35.1%), a higher amount (46.1%) belonged to group A, which has previously been described to also harbour strains with a high pathogenic potential for humans. The number of virulence-associated genes of single strains ranged from 5 to 26 among 33 genes tested and high numbers were rather related to K1-positive and ECOR B2 strains than to a certain pathotype. With a few exceptions (iha, afa/draB, sfa/foc, and hlyA), which were rarely present in APEC strains, most chromosomally located genes were widely distributed among all ExPEC strains irrespective of host and pathotype. However, prevalence of invasion genes (ibeA and gimB) and K1 capsule-encoding gene neuC indicated a closer relationship between APEC and NMEC strains. Genes associated with ColV plasmids (tsh, iss, and the episomal sit locus) were in general more prevalent in APEC than in UPEC and NMEC strains, indicating that APEC could be a source of ColV-located genes or complete plasmids for other ExPEC strains. Our data support the hypothesis that (a) poultry may be a vehicle or even a reservoir for human ExPEC strains, (b) APEC potentially serve as a reservoir of virulence-associated genes for UPEC and NMEC, (c) some ExPEC strains, although of different pathotypes, may share common ancestors, and (d) as a conclusion certain APEC subgroups have to be considered potential zoonotic agents. The finding of different evolutionary clusters within these three pathotypes implicates an independently and parallel evolution, which should be resolved in the future by thorough phylogenetic typing.

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Avian colibacillosis: still many black holes.

Rodrigo Guabiraba, Catherine Schouler (2015)

Avian pathogenic Escherichia coli (APEC) strains cause severe respiratory and systemic diseases, threatening food security and avian welfare worldwide. Intensification of poultry production and the quick expansion of free-range production systems will increase the incidence of colibacillosis through greater exposure of birds to pathogens and stress. Therapy is mainly based on antibiotherapy and current vaccines have poor efficacy. Serotyping remains the most frequently used diagnostic method, only allowing the identification of a limited number of APEC strains. Several studies have demonstrated that the most common virulence factors studied in APEC are all rarely present in the same isolate, showing that APEC strains constitute a heterogeneous group. Different isolates may harbor different associations of virulence factors, each one able to induce colibacillosis. Despite its economical relevance, pathogenesis of colibacillosis is poorly understood. Our knowledge on the host response to APEC is based on very descriptive studies, mostly restricted to bacteriological and histopathological analysis of infected organs such as lungs. Furthermore, only a small number of APEC isolates have been used in experimental studies. In the present review, we discuss current knowledge on APEC diversity and virulence, including host response to infection and the associated inflammatory response with a focus on pulmonary colibacillosis.

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Author and article information

Contributors

Troels Ronco:

ORCID: http://orcid.org/0000-0001-7873-2816

troro@vet.dtu.dk

Marc Stegger: mtg@ssi.dk

Rikke Heidemann Olsen: cava@sund.ku.dk

Camilla Sekse: camilla.sekse@vetinst.no

Anne Bang Nordstoga: anne.nordstoga@vetinst.no

Tarja Pohjanvirta: Tarja.Pohjanvirta@evira.fi

Berit Lilje: beli@ssi.dk

Ulrike Lyhs: ully@vet.dtu.dk

Paal Skytt Andersen: psa@ssi.dk

Karl Pedersen: kape@vet.dtu.dk

Journal

Journal ID (nlm-ta): BMC Genomics

Journal ID (iso-abbrev): BMC Genomics

Title: BMC Genomics

Publisher: BioMed Central (London )

ISSN (Electronic): 1471-2164

Publication date (Electronic): 3 January 2017

Publication date PMC-release: 3 January 2017

Publication date Collection: 2017

Volume: 18

Electronic Location Identifier: 13

Affiliations

[1 ]National Veterinary Institute, Technical University of Denmark, Bülowsvej 27, 1870 Frederiksberg C, Denmark

[2 ]Statens Serum Institut, Department of Microbiology and Infection Control, Artillerivej 5, 2300 Copenhagen S, Denmark

[3 ]Department of Veterinary Disease Biology, University of Copenhagen, Stigbøjlen 4, 1870 Frederiksberg C, Denmark

[4 ]Norwegian Veterinary Institute, Ullevaalsveien 68, 0454 Oslo, Norway

[5 ]Finnish Food Safety Authority, Veterinary Bacteriology, Neulaniementie 4, FI-70210 Kuopio, Finland

Author information

Troels Ronco http://orcid.org/0000-0001-7873-2816

Article

Publisher ID: 3415

DOI: 10.1186/s12864-016-3415-6

PMC ID: 5210278

PubMed ID: 28049430

SO-VID: e2e6dad4-0cf8-48eb-84ec-e4cf3d0e6698

License:

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.

History

Date received : 14 September 2016

Date accepted : 12 December 2016

Funding

Funded by: Danish Poultry Levy Fond

Custom metadata

ScienceOpen disciplines: Genetics

Keywords: apec,colibacillosis,comparative genomics,phylogenetic analysis,virulence factors

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ScienceOpen disciplines: Genetics

Keywords: apec, colibacillosis, comparative genomics, phylogenetic analysis, virulence factors

Spread of avian pathogenic Escherichia coli ST117 O78:H4 in Nordic broiler production

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Abstract

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Animal Welfare

Most cited references 28

Fast algorithms for large-scale genome alignment and comparison.

Avian pathogenic, uropathogenic, and newborn meningitis-causing Escherichia coli: how closely related are they?

Avian colibacillosis: still many black holes.

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