Open Access

Chromosomal features of Escherichia coli serotype O2:K2, an avian pathogenic E. coli

  • Steffen L. Jørgensen1,
  • Egle Kudirkiene1,
  • Lili Li2,
  • Jens P. Christensen1,
  • John E. Olsen1,
  • Lisa Nolan3 and
  • Rikke H. Olsen1Email author
Standards in Genomic Sciences201712:33

https://doi.org/10.1186/s40793-017-0245-3

Received: 23 May 2016

Accepted: 27 April 2017

Published: 10 May 2017

Abstract

Escherichia coli causing infection outside the gastrointestinal system are referred to as extra-intestinal pathogenic E. coli. Avian pathogenic E. coli is a subgroup of extra-intestinal pathogenic E. coli and infections due to avian pathogenic E. coli have major impact on poultry production economy and welfare worldwide. An almost defining characteristic of avian pathogenic E. coli is the carriage of plasmids, which may encode virulence factors and antibiotic resistance determinates. For the same reason, plasmids of avian pathogenic E. coli have been intensively studied. However, genes encoded by the chromosome may also be important for disease manifestation and antimicrobial resistance. For the E. coli strain APEC_O2 the plasmids have been sequenced and analyzed in several studies, and E. coli APEC_O2 may therefore serve as a reference strain in future studies. Here we describe the chromosomal features of E. coli APEC_O2. E. coli APEC_O2 is a sequence type ST135, has a chromosome of 4,908,820 bp (plasmid removed), comprising 4672 protein-coding genes, 110 RNA genes, and 156 pseudogenes, with an average G + C content of 50.69%. We identified 82 insertion sequences as well as 4672 protein coding sequences, 12 predicated genomic islands, three prophage-related sequences, and two clustered regularly interspaced short palindromic repeats regions on the chromosome, suggesting the possible occurrence of horizontal gene transfer in this strain. The wildtype strain of E. coli APEC_O2 is resistant towards multiple antimicrobials, however, no (complete) antibiotic resistance genes were present on the chromosome, but a number of genes associated with extra-intestinal disease were identified. Together, the information provided here on E. coli APEC_O2 will assist in future studies of avian pathogenic E. coli strains, in particular regarding strain of E. coli APEC_O2, and aid in the general understanding of the pathogenesis of avian pathogenic E. coli.

Keywords

Avian pathogenic Escherichia coli Genome sequencing Chromosome Colibacillosis Chicken

Introduction

Avian pathogenic Escherichia coli strains are the etiological agent of colibacillosis in birds, which is one of the most significant infectious diseases affecting poultry [6, 33]. In the veterinary field, avian pathogenic E. coli associated diseases implies economic losses in the poultry industry worldwide [27]. Furthermore, avian pathogenic E. coli strains have been reported to represent a zoonotic risk, as the population of avian pathogenic E. coli shares major genomic similarities with the population of human uropathogenic E. coli [22, 44]. Despite importance of this disease, the importance of the genetic features and genome diversity with avian pathogenic E. coli remains to be fully understood. Here we report the full genome sequence and sequence annotation of E. coli APEC_O2. E. coli APEC_O2 is an E coli strain (serotype O2:K2) isolated from the joint of a chicken in 2014 [22]. E. coli APEC_ O2 possesses two large, well-characterized plasmids [22, 23] which have been used in antimicrobial and virulence studies [21, 36], while no characterization of the chromosomal features have been available until now.

Organism information

Classification and features

E. coli is a Gram-negative, non-spore forming, rod-shaped bacteria belonging to the Enterobacteriaceae family [34]. E. coli APEC_O2 is motile by the means of peritrichous flagella (Fig. 1), is non-pigmented, oxidase-negative, facultative anaerobe and is growing with a optimum between 37 and 42 °C. E. coli APEC_O2 is positive for indole production, nitrate reduction, and urease but is hydrogen-sulfide negative. The strain is positive for lysine-decarboxylase and ornithine-decarboxylase activity, and produce acid and gas while fermenting d-glucose. E. coli APEC_O2 fermented d-trehalose, d-sorbitol, d-mannitol, l-rhamnose, d-glucose, d-maltose, and d-arabinose, but does grown on citric acid, inositol or gelatin. Furthermore, the strain does not produce acetoin (Voges–Proskauer negative), and does not utilize malonate.
Fig. 1

Transmission electron micrograph of APEC_O2. The strain is a short to medium rod-shaped bacterium with a length of 1–2 μm. It moves via peritrichous flagella. The magnification rate is 20,000×. The scale bar indicates 1 μm

The primary habitat of E. coli is in the gastrointestinal tract (GIT) of humans, many of the warm blooded animals as well as poultry [24]. Most strains of E. coli are considered commensal strains of the GIT, however, certain pathovars of E. coli may cause intestinal disease, while other cause disease when entering the extra-intestinal compartments of the body [30]. Avian pathogenic E. coli is an important agent of extra-intestinal diseases in poultry, including respiratory, hematogenous, ascending and skin infections, collectively called colibacillosis [33]. E. coli APEC_O2 was obtained from a joint of chicken with arthritis in 2014 (Table 1), and has subsequently been used in different scientific studies [22, 23, 36]. The serotype of E. coli APEC_O2 is O2:K2 [22], which is one of the most common serotypes among avian pathogenic Escherichia coli worldwide [33].
Table 1

Classification and general features of the E. coli APEC_ O2 strain

MIGS ID

Property

Term

Evidence codea

 

Classification

Domain Bacteria

TAS [41]

  

Phylum Proteobacteria

TAS [16]

  

Class Gammaproteobacteria

TAS [40]

  

Order’ Enterobacteriales”

TAS [16, 40]

  

Family Enterobacteriaceae

TAS [8]

  

Genus Escherichia

TAS [13]

  

Species Escherichia coli

TAS [13]

 

Gram stain

Negative

TAS [39]

 

Cell shape

Rod

TAS [39]

 

Motility

Motile

TAS [39]

 

Sporulation

None-sporeforming

TAS [39]

 

Temperature range

Mesophile

TAS [39]

 

Optimum temperature

37 °C

TAS [39]

 

pH range; Optimum

5.5–8.0; 7.0

TAS [39]

 

Carbon source

Carbohdrates, salicin, sorbitol, mannitol, indole, peptides

TAS [39]

MIGS-6

Habitat

Host-associated

TAS [14]

MIGS-6.3

Salinity

Not reported

 

MIGS-22

Oxygen requirement

Aerobe and facultative anaerobe

TAS [39]

MIGS-15

Biotic relationship

Parasitism

TAS [6, 14]

MIGS-14

Pathogenicity

Pathogenic

TAS [6, 14]

MIGS-4

Geographic location

USA

NAS

MIGS-5

Sample collection

2014

 

MIGS-4.1

Latitude

Not reported

 

MIGS-4.2

Longitude

Not reported

 

MIGS-4.4

Altitude

Not reported

 

a Evidence codes - TAS: Traceable Author Statement (i.e., a direct report exists in the literature); NAS: Non-traceable Author Statement (i.e., not directly observed for the living, isolated sample, but based on a generally accepted property for the species, or anecdotal evidence). These evidence codes are from the Gene Ontology project [2]

A Maximum Likelihood method phylogenetic tree based on the concatenated seven housekeeping genes of E. coli , were made in MEGA (version 7) [37], with 500 bootstrap (Fig. 2). Housekeeping gene sequences from the following strains were used to construct the phylogenetic tree: E. coli str. K-12 str. MG1655, NC_000913.3, E. coli APEC O1, NC_008563.1, E. coli UTI89, NC_007946.1, E. coli S88, CU928161.2, E. coli CFT073, NC_004431.1, E. coli APEC O78, NC_020163.1, E. coli ST131 strain EC958, Z_HG941718.1, E. coli strain SF-468, NZ_CP012625.1, E. coli APEC IMT5155, NZ_CP005930.1, E. coli O83:H1 str. NRG 857C, CP001855.1, E. coli DSM 30083, NZ_KK583188.1, and Escherichia fergusonii ATCC 35469, NC_011740.1.
Fig. 2

Maximum likehood tree of APEC_O2 relative to other closely related strains. The phylogenetic tree was constructed from the concatenated seven housekeeping genes (adk, fumC, gyrB, icd, mdh, purA, and recA) in MEGA software version 7. Escherichia fergusonii (ATCC35469) was used as an out-group. Bootstrap values of 500 replicates are indicated at the nodes. The scale bar indicates nucleotide diversity between the strains

Two large plasmids of APEC_O2 (pAPEC-O2-ColV and pAPEC-O2-R) have previously been described in details [22, 23]. Various antibiotic resistance and virulence associated genes of APEC_O2 have been identified on these two plasmids. The plasmid pAPEC-O2-ColV has been reported to be co-transferred with plasmid pAPEC-O2-R into the non-virulent E. coli DH5α strain, resulting in an increase in antibiotic resistance and virulence of the recipient strain [21].

Genome sequencing information

Genome project history

The strain of E. coli APEC_O2 was selected for whole genome sequencing at the Department of Veterinary Disease Biology, Denmark, because information regarding the chromosomal background of the strains was lacking. Sequence assembly and annotation were completed in December 2015, and the draft genome sequence was deposited in GenBank under accession number LSZR00000000. A summary of the project information and its association with “Minimum Information about a Genome Sequence” according to Field et al. [15] is provided in Table 2.
Table 2

Project information

MIGS ID

Property

Term

MIGS 31

Finishing quality

Drafted

MIGS-28

Libraries used

Paired-end Nextera XT DNA

MIGS 29

Sequencing platforms

Illumina MiSeq

MIGS 31.2

Fold coverage

33.0x

MIGS 30

Assemblers

CLC NGS Cell v. 7.0.4

MIGS 32

Gene calling method

GeneMarkS+

 

Locus Tag

AZE29

 

Genbank ID

LSZR00000000

 

GenBank Date of Release

2016/04/14

 

BIOPROJECT

PRJNA312653

BioSample Accession

SAMN04503534

MIGS 13

Source Material Identifier

APEC_O2

 

Project relevance

Pathogenic bacterium, biotechnological

Growth conditions and genomic DNA preparation

One colony of E. coli APEC_O2 cultured on agar plates (Blood agar base, Oxoid, Roskilde, Denmark), supplement with 5% bovine blood was inoculated in 10 mL Brain and Heart Infusion (BHI) broth for 18 h yielding a final density of 109 colony forming units per mL BHI broth. DNA from 1 mL of the APEC_O2 inoculated was extracted using DNeasy Blood & Tissue Kit (Qiagen, USA). The quantity (127 ng/μl) and quality of DNA (ratio of light absorption at wavelengths 260/280 was 1.81 and 1.99 at wavelengths 260/230) was assessed using Nanodrop (Thermo Scientific, USA).

Genome sequencing and assembly

Genome sequencing was performed using the MiSeq instrument (Illumina) at a 300-bp paired-end-read format. CLC Genomic Workbench 6.5.1 software package (CLC, Denmark) was used to perform adapter trimming and quality assessment of the reads. Sequencing reads were de novo assembled using the SPAdes v.3.5.0 [5]. The quality of the assembly was evaluated with QUAST v.2.3 [18]. The run yielded 981,795 high quality filtered reads containing 5,166,016 bases, which provided an average of 33-fold coverage of the genome. The assembly resulted in 304 contigs ranging from 216 to 192,013 bp in size. The contigs were aligned with two previously published E. coli APEC_O2 plasmids ColV and R (R) using the progressive Mauve algorithm in Mauve 2.3.1 [11], and those corresponding to the plasmid sequences were removed. The final E. coli APEC_O2 chromosomal genome had the size of 4.9 Mbp, and was assembled into 261 contigs. The relative large number of contigs is most likely due to a high number of mobile elements found in draft genome of E. coli APEC_O2 (please see result section). Genes in internal clusters were detected using CD-HIT v4.6 with thresholds of 50% covered length and 50% sequence identity [9].

Genome annotation

The draft genome sequence of E. coli APEC_O2 was analyzed using Glimmer 3.0 and GeneMark for gene prediction [7, 12, 25]. Ribosomal RNA identification was performed using RNAmmer 1.2 [26]. The predicted protein coding sequences were annotated and protein features were predicted by BASys analysis using the NCBI database [38].

Genome properties

The complete draft genome of E. coli APEC_O2 consists of one circular chromosome of 4,908,820 bp with an average G + C content is 50.69%. In addition E. coli APEC_O2 contains two plasmids: pAPEC-O2-ColV and pAPEC-O2-R, which are not included in the analysis or features descripted in the present study (Table 3). In total, 4938 genes were predicted on the chromosomal genome, of which 110 coded for RNA related genes, 4672 were protein coding genes, and 156 were pseudogenes (Table 4). In total, 4099 genes were assigned in COG functional categories and listed in Table 5.
Table 3

Summary of APEC_O2 genome: one chromosome and two plasmids

Label

Size (Mb)

Topology

INSDC identifier

RefSeq ID

Chromosome

4,908,820

Circular

GenBank

GCA_001620375.1

pAPEC-O2-ColV

0.18

Circular

GenBank

AY545598.5

pAPEC-O2-R

0.1

Circular

GenBank

AY214164.3

Table 4

Genome statistics

Attribute

Value

% of Total

Genome size (bp)

4,908,820

100.00

DNA coding (bp)

4,320,149

88.01

DNA G + C (bp)

2,488,281

50.69

DNA scaffold

261

-

Total genes

4938

100

Protein coding genes

4672

94.61

RNA genes

110

2.22

Pseudo genes

156

3.16

Genes in internal clusters

252

5.1

Genes with function prediction

4209

85.24

Genes assigned to COGs

4099

83.00

Genes with Pfam domains

4713

95.44

Genes with signal peptides

550

11.14

Genes with transmembrane helices

1107

22.42

CRISPR repeats

2

 
Table 5

Number of genes associated with general COG functional categories

Code

Value

% age

Description

J

200

4.06

Translation, ribosomal structure and biogenesis

A

0

0.00

RNA processing and modification

K

319

6.47

Transcription

L

231

4.67

Replication, recombination and repair

B

0

0.00

Chromatin structure and dynamics

D

35

0.71

Cell cycle control, Cell division, chromosome partitioning

V

0

0.00

Defense mechanisms

T

161

3.26

Signal transduction mechanisms

M

270

5.47

Cell wall/membrane biogenesis

N

143

2.89

Cell motility

U

0

0.00

Intracellular trafficking and secretion

O

163

3.31

Posttranslational modification, protein turnover, chaperones

C

327

6.61

Energy production and conversion

G

471

9.53

Carbohydrate transport and metabolism

E

384

7.78

Amino acid transport and metabolism

F

109

2.21

Nucleotide transport and metabolism

H

156

3.16

Coenzyme transport and metabolism

I

119

2.41

Lipid transport and metabolism

P

221

4.47

Inorganic ion transport and metabolism

Q

61

1.24

Secondary metabolites biosynthesis, transport and catabolism

R

393

7.95

General function prediction only

S

336

6.81

Function unknown

-

734

14.86

Not in COGs

The total is based on the total number of protein coding genes in the genome

MLST finder 1.8 [28] was used to identify the sequence type of E. coli APEC_O2 as ST135, while SeroTypeFinder [20] was used to confirm the serotype of E. coli APEC_O2 as O2:K2 as published by others [22].

VirulenceFinder 1.5 and ResFinder 2.1 were used for identification of intrinsic genes associated with virulence and antibiotic resistance, respectively [19, 42]. Clustered regularly interspaced short palindromic repeat sequences were detected using CRISPR-finder [17]. IS-finder and PHAST were used for identification and location of insertion sequences and phages [35, 43].

BLAST ring image generator (BRIG) [1] was applied to the compare the genome of E. coli APEC_O2 with APEC O78 (CP004009.1), three isolates of human urinary pathogenic E. coli isolates (CFT073 (NC_004431.1), UTI89 (NC_007946.1) and UTI536 (NC_008253.01)), three intestinal pathogenic E. coli ( E. coli HUS (PRJNA68275), E. coli O127 (PRJNA204937), E. coli _O157:H7 (GCA_000008865.1) and AIEC (GCA_000183345.1), a non-pathogenic E. coli ( E. coli _K12 (GCA_000005845.2) (Fig. 3).
Fig. 3

Genomic comparison of APEC_O2 with other strains of Escherichia coli. Genome wide comparison of APEC_O2 with the complete genomes of another Avian pathogenic E. coli, APECO78 (CP004009.1), three isolates of human urinary pathogenic E. coli (CFT073(NC_004431.1), UTI89 (NC_007946.1) and UTI536 (NC_008253.01), three isolates of intestinal pathogenic E. coli (E. coli HUS (PRJNA68275), E. coli O127 (PRJNA204937), E. coli O157:H7 (GCA_000008865.1) and AIEC (GCA_000183345.1), respectively) and a non-pathogenic E. coli (E. coli_K12 (GCA_000005845.2). Solid color of concentric rings indicated genomic areas also present in APEC_O2 (inner black circle), whereas absence of color in a ring indicates absence of the region

BRIG was also used to examine the genome of E. coli APEC_O2 for the presence of selected virulence genes. The sequences of sixty-two genes related to extra-intestinal virulence were extracted from the Virulence Factor Database [10] and blasted against the genome of E. coli APEC_O2. The virulence genes included six adhesins (bma, ecp, pap, fim, foc, and sfa), five toxins (astA, cnf1, vat, cdt,, hlyF), six auto-transporters (aat, ehaB, pic, upaG, tsh,sat), two invasion genes (ibeA, tia), 14 iron acquisition genes (chuA, eitB, sitA, sitB, sitC, irp2, fyuA, ompT,iroN, iutA, iucA, iucB, iucC, iucD), one gene of the type VI secretion system (T6SS) and four miscellaneous genes (iss, cvaC, traT, malX) (Fig. 4). The RAST server [4] was used to identify subsystem features in E. coli APEC_O2 and the type strain of E. coli ( E. coli DMS 30038). In silico DNA-DNA hybridization (dDDH)similarities between the E. coli APEC_ O2 strain and the 12 strains used for the Maximum likelihood analysis, were calculated using the Genome-to-Genome Distance Calculator v. 2.1 [3].
Fig. 4

Screening for the presence of selected virulence genes. The presence or absence of 65 genes related to extra-intestinal disease in APEC_O2. For comparison reasons the genomes of two plasmids of the wildtype of APEC_O2 (pAPEC ColV(NC_007675.1) and APEC-R (AY214164)), in addition to the genomes of CFT073(NC_004431.1, UTI89 (NC_007946.1), E. coli HUS (PRJNA68275), E. coli O127 (PRJNA204937), E. coli O157:H7 (GCA_000008865.1) and E. coli_K12 (GCA_000005845.2), respectively, were also included in the analysis. All genomic sequences of the virulence genes were obtained from the online Virulence Factor Database (http://www.mgc.ac.cn/VFs/main.htm)

Insights from the genome sequence

Here we present the draft genome sequencing and annotation of the chromosome of the E. coli strain APEC_O2. Four thousand six hundred seventy two protein-coding sequences accounting for 94.61% of the total number of 4938 genes identified. This analysis predicted 82 insertion sequences and three phage associated sequences.

E. coli APEC_O2 was interestingly found to belong to sequence type ST135, which previously only sparsely have been associated with pathogenicity [32].

E. coli APEC_O2 is phylogenetically closely related to E. coli strain EC958, belonging to ST131, which is recognized as a leading contributor to human urinary tract infections, and to an adherent invasive E. coli strain (NRG EC958), which originally were isolated from a terminal patient suffering from Chron’s disease. The latter was quite unexpected, as intestinal and extra-intestinal pathogenic E. coli are believed to constitute two different pathotypes [24], however, other studies have suggested that there might be a phylogenetic relationship between adherent invasive E. coli and extra-intestinal pathogenic E. coli [29]. Adding to the suggested close relationship between adherent invasive E. coli and extra-intestinal pathogenic E. coli , in this case E. coli APEC_O2, was the finding of a dDDH estimate of 96.50% between the two strains, which is higher than the similarities to any of the other strains included in the phylogenetic analysis (Fig. 1, Table 6). Moreover, the similarity to E. coli strain EC958 were almost 10% lower, and the probability that E. coli APEC_O2 belong to the same subspecies (estimated by dDDH > 79%) were below 60%. (Table 6).
Table 6

DNA:DNA-hybridization (dDDH) of APEC_O2 to selected E. coli strains

 

DDH estimate (GLM-based)

Probability that DDH > 70%

Probability that DDH > 79%

APEC_O2 versus:

E. coli 1655 (NZCP005930.1)

74.80% [71.8–77.6%]

85.53%

37.84%

APEC01 (NC008563.1)

90.60% [88.3–92.4%]

95.98%

66.14%

E. coli APECO78 (NC020163.1)

74.70% [71.6–77.5%]

85.33%

37.53%

E. coli CFT073 (NC004431.1)

91.00% [88.8–92.8%]

96.13%

66.89%

E.coli_ST131_strain_EC958 (NZHG941718.1)

86.60% [84–88.8%]

94.48%

59.67%

E.coli_O83H1_strain_NRG_857C (CP001855.1)

96.50% [95.3–97.5%]

95.55%

74.94%

E. fergusonii ATCC 35469 (NC011740.1)a

40.30% [37.8–42.8%]

2.9%

0.73%

E. coli IMT5155 (NZCP005930.1)

90.90% [88.7–92.7%]

96.1%

66.7%

E. coli S88 (CU928161.2)

89.90% [87.6–91.8%]

95.77%

65.12%

E. coli SF/468 (NZCP012625.1)

90.50% [88.2–92.3%]

95.95%

65.89%

E. coli DMS 30083 (NZKK583188.1)

90.30% [88–92.2%]

95.89%

65.72%

E. coli UTI89 (NC004431.1)

91.10% [89–92.9%]

96.17%

67.05%

a E. fergusonii ATCC 35469 (NC011740.1) was included to represent an out-group strain

For comparison, the dDDH estimate between the type strain of E. coli ( E. coli DSM) [31] and avian pathogenic E. coli were around 90%. The differences might be due to the considerably higher numbers of phage- and prophage regions in the type strain compared to E. coli APEC_O2 (Fig. 5). Besides difference in this feature, distribution of subsystem feature counts was highly similar between the two strains.
Fig. 5

Subsystem feature counts in APEC_O2 and E. coli DMS 30083 (NZKK583188.1)

Conclusions

In this study, we present the draft genome sequence of the chicken-derived E. coli isolate APEC_O2. The genome of E. coli APEC_O2 consists of a 4,908,820 bp long chromosome, containing 4672 protein coding genes. E. coli APEC_O2 furthermore contains two transferable plasmids, which carry several virulence and antibiotic resistance genes.

Previous studies have demonstrated close genetic resemblance between avian pathogenic E. coli and extra-intestinal pathogenic E. coli strains, and suggested poultry as a reservoir of extra-intestinal pathogenic E. coli strains associated with disease in humans, and as a possible route of transmission. In the present study full genomic comparison of genomes did not reveal closer genomic relationship between E. coli APEC_O2 and human extra-intestinal pathogenic E. coli strains than to human E. coli strains of other pathotypes similarities. Nevertheless, the chromosomal contents of APEC_O2 did harbor genes of importance for extra-intestinal disease. In addition, dDDH similarities indicated that APEC_O2 had equally high similarity to strains uropathogenic strains as to other avian pathogenic E. coli strain and the type strain of E. coli .

More surprising, E. coli APEC_O2 had the highest dDDH similarity to an adherent invasive E. coli , as intestinal E. coli original were considered to constitute a pathotype very different from extra-intestinal pathogenic E. coli .

Conclusively, the draft genome sequence and annotation of the pathogenic avian pathogenic E. coli strain APEC_O2 provides new information, which may add for future studies of the pathogenesis, transmission and zoonotic risk related to avian pathogenic E. coli .

Abbreviations

BHI: 

Brain and Heart Infusion

BRIG: 

BLAST Ring Image Generator

CRISPR: 

Clustered Regularly Interspaced Short Palindromic Repeats

dDDH: 

DNA-DNA hybridization

E. coli

Escherichia coli

GIT: 

Gastrointestinal tract

IS: 

Insertion sequences

MLST: 

Multi Locus Sequence typing

PHAST: 

PHAge Search Tool

ST: 

Sequence type

Declarations

Acknowledgements

The core facility for Integrated Microscopy (CFIM) at Panum, Denmark, is thanked for skillful preparation of the sample for transmission electron microscopy.

Funding

This project has received funding from the Danish Council of Independent Research, grant agreement no. 4184-00512.

Authors’ contributions

SLJ, RHO and LL conducted the phylogenetic studies. SLJ, RHO, EK, LL, JEO, LN and JPC drafted the manuscript. RHO and LL performed the laboratory experiments. EK, RHO, SLJ and LL, sequenced, assembled and annotated the genome. All authors read and approved the final manuscript.

Competing interests

The authors declare that they have no competing interests.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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.

Authors’ Affiliations

(1)
Department of Veterinary and Animal Sciences, Faculty of Health and Medical Sciences, University of Copenhagen
(2)
College of Light Industry and Food Sciences, South China University of Technology
(3)
Department of Veterinary Microbiology and Preventive Medicine, College of Veterinary Medicine, Iowa State University

References

  1. Alikhan NF, Petty NK, Ben Zakour NL, Beatson SA. BLAST Ring Generator (BRIG): simple prokaryote genome comparisons. BMC Genomics. 2011;12:402.View ArticlePubMedPubMed CentralGoogle Scholar
  2. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet. 2000;25:25–9.View ArticlePubMedPubMed CentralGoogle Scholar
  3. Auch AF, Klenk HP, Goker M. Standard operating procedure for calculating genome-to-genome distances based on high-scoring segment pairs. Stand Genomic Sci. 2010;2:142–8.View ArticlePubMedPubMed CentralGoogle Scholar
  4. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM, Kubal M, Meyer F, Olsen GJ, Olson R, Osterman AL, Overbeek RA, McNeil LK, Paarmann D, Paczian T, Parrello B, Pusch GD, Reich C, Stevens R, Vassieva O, Vonstein V, Wilke A, Zagnitko O. The RAST Server: rapid annotations using subsystems technology. BMC Genomics. 2008;9:75.View ArticlePubMedPubMed CentralGoogle Scholar
  5. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol. 2012;19:455–77.View ArticlePubMedPubMed CentralGoogle Scholar
  6. Barnes HJ, Nolan LK, Vaillancourt JF. Colibacilliosis. In: Saif YM, Fadly AM, editors. Diseases of poultry. Ames, Iowa: Blackwell Publishing; 2008. p. 691–732.Google Scholar
  7. Besemer J, Lomsadze A, Borodovsky M. GeneMarkS: a self-training method for prediction of gene starts in microbial genomes. Implications for finding sequence motifs in regulatory regions. Nucleic Acids Res. 2001;29:2607–18.View ArticlePubMedPubMed CentralGoogle Scholar
  8. Brenner D, Family I. Enterobacteriaceae Rahn 1937, Nom. fam. con. Opin. 15. Com 1958, 73; Ewing, Famer, and Brenner 1980, 674; Judical Commission 1981, 104. In: Krieg N, Holt J, editors. Bergey’s Manual of Systematic Bacteriology. Baltimore: The Williams & Wilkins Co; 1984. p. 408–20.Google Scholar
  9. CD-HIT. http://weizhongli-lab.org/cd-hit/ref.php. 2016.
  10. Chen L, Yang J, Yu J, Yao Z, Sun L, Shen Y, Jin Q. VFDB: a reference database for bacterial virulence factors. Nucleic Acids Res. 2005;33:D325–8.View ArticlePubMedGoogle Scholar
  11. Darling AE, Mau B, Perna NT. progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS One. 2010;5:e11147.View ArticlePubMedPubMed CentralGoogle Scholar
  12. Delcher AL, Harmon D, Kasif S, White O, Salzberg SL. Improved microbial gene identification with GLIMMER. Nucleic Acids Res. 1999;27:4636–41.View ArticlePubMedPubMed CentralGoogle Scholar
  13. Escherich T. Die Darmbakterien des Säuglings und ihre Beziehungen zur Physiologie der Varsauung., Stuttgart: 1886: 63–74Google Scholar
  14. Ewers C, Li GW, Wilking H, Kiessling S, Alt K, Antao EM, Laturnus C, Diehl I, Glodde S, Homeier T, Bohnke U, Steinruck H, Philipp HC, Wieler LH. Avian pathogenic, uropathogenic, and newborn meningitis-causing Escherichia coli: How closely related are they? Int J Med Microbiol. 2007;297:163–76.View ArticlePubMedGoogle Scholar
  15. Field D, Garrity G, Gray T, Morrison N, Selengut J, Sterk P, Tatusova T, Thomson N, Allen MJ, Angiuoli SV, Ashburner M, Axelrod N, Baldauf S, Ballard S, Boore J, Cochrane G, Cole J, Dawyndt P, De VP, DePamphilis C, Edwards R, Faruque N, Feldman R, Gilbert J, Gilna P, Glockner FO, Goldstein P, Guralnick R, Haft D, Hancock D, Hermjakob H, Hertz-Fowler C, Hugenholtz P, Joint I, Kagan L, Kane M, Kennedy J, Kowalchuk G, Kottmann R, Kolker E, Kravitz S, Kyrpides N, Leebens-Mack J, Lewis SE, Li K, Lister AL, Lord P, Maltsev N, Markowitz V, Martiny J, Methe B, Mizrachi I, Moxon R, Nelson K, Parkhill J, Proctor L, White O, Sansone SA, Spiers A, Stevens R, Swift P, Taylor C, Tateno Y, Tett A, Turner S, Ussery D, Vaughan B, Ward N, Whetzel T, San GI, Wilson G, Wipat A. The minimum information about a genome sequence (MIGS) specification. Nat Biotechnol. 2008;26:541–7.View ArticlePubMedPubMed CentralGoogle Scholar
  16. Garrity G, Bell J, Lilburn T. Class III. Gammaproteobacteria class. nov. In: Garrity G, Brenner D, Krieg N, Staley J, editors. Bergey’s Manual of Systematic Bacteriology. New York: Springer; 2005.Google Scholar
  17. Grissa I, Vergnaud G, Pourcel C. CRISPRFinder: a web tool to identify clustered regularly interspaced short palindromic repeats. Nucleic Acids Res. 2007;35:W52–7.View ArticlePubMedPubMed CentralGoogle Scholar
  18. Gurevich A, Saveliev V, Vyahhi N, Tesler G. QUAST: quality assessment tool for genome assemblies. Bioinformatics. 2013;29:1072–5.View ArticlePubMedPubMed CentralGoogle Scholar
  19. Joensen KG, Scheutz F, Lund O, Hasman H, Kaas RS, Nielsen EM, Aarestrup FM. Real-time whole-genome sequencing for routine typing, surveillance, and outbreak detection of verotoxigenic Escherichia coli. J Clin Microbiol. 2014;52:1501–10.View ArticlePubMedPubMed CentralGoogle Scholar
  20. Joensen KG, Tetzschner AM, Iguchi A, Aarestrup FM, Scheutz F. Rapid and easy in silico serotyping of Escherichia coli isolates by use of whole-genome sequencing data. J Clin Microbiol. 2015;53:2410–26.View ArticlePubMedPubMed CentralGoogle Scholar
  21. Johnson TJ, Giddings CW, Horne SM, Gibbs PS, Wooley RE, Skyberg J, Olah P, Kercher R, Sherwood JS, Foley SL, Nolan LK. Location of increased serum survival gene and selected virulence traits on a conjugative R plasmid in an avian Escherichia coli isolate. Avian Dis. 2002;46:342–52.View ArticlePubMedGoogle Scholar
  22. Johnson TJ, Siek KE, Johnson SJ, Nolan LK. DNA sequence and comparative genomics of pAPEC-O2-R, an avian pathogenic Escherichia coli transmissible R plasmid. Antimicrob Agents Chemother. 2005;49:4681–8.View ArticlePubMedPubMed CentralGoogle Scholar
  23. Johnson TJ, Siek KE, Johnson SJ, Nolan LK. DNA sequence of a ColV plasmid and prevalence of selected plasmid-encoded virulence genes among avian Escherichia coli strains. J Bacteriol. 2006;188:745–58.View ArticlePubMedPubMed CentralGoogle Scholar
  24. Kaper JB. Pathogenic Escherichia coli. Int J Med Microbiol. 2005;295:355–6.View ArticlePubMedGoogle Scholar
  25. Kelley DR, Liu B, Delcher AL, Pop M, Salzberg SL. Gene prediction with Glimmer for metagenomic sequences augmented by classification and clustering. Nucleic Acids Res. 2012;40:e9.View ArticlePubMedGoogle Scholar
  26. Lagesen K, Hallin P, Rodland EA, Staerfeldt HH, Rognes T, Ussery DW. RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res. 2007;35:3100–8.View ArticlePubMedPubMed CentralGoogle Scholar
  27. Landman WJ, van Eck JH. The incidence and economic impact of the Escherichia coli peritonitis syndrome in Dutch poultry farming. Avian Pathol. 2015;44:370–8.View ArticlePubMedGoogle Scholar
  28. Larsen MV, Cosentino S, Rasmussen S, Friis C, Hasman H, Marvig RL, Jelsbak L, Sicheritz-Ponten T, Ussery DW, Aarestrup FM, Lund O. Multilocus sequence typing of total-genome-sequenced bacteria. J Clin Microbiol. 2012;50:1355–61.View ArticlePubMedPubMed CentralGoogle Scholar
  29. Martinez-Medina M, Mora A, Blanco M, Lopez C, Alonso MP, Bonacorsi S, Nicolas-Chanoine MH, Darfeuille-Michaud A, Garcia-Gil J, Blanco J. Similarity and divergence among adherent-invasive Escherichia coli and extraintestinal pathogenic E. coli strains. J Clin Microbiol. 2009;47:3968–79.View ArticlePubMedPubMed CentralGoogle Scholar
  30. Maturana VG, de PF, Carlos C, Mistretta PM, de CT A, Nakazato G, Guedes SE, Logue CM, Nolan LK, da SW D. Subpathotypes of Avian Pathogenic Escherichia coli (APEC) exist as defined by their syndromes and virulence traits. Open Microbiol J. 2011;5:55–64.View ArticlePubMedPubMed CentralGoogle Scholar
  31. Meier-Kolthoff JP, Hahnke RL, Petersen J, Scheuner C, Michael V, Fiebig A, Rohde C, Rohde M, Fartmann B, Goodwin LA, Chertkov O, Reddy T, Pati A, Ivanova NN, Markowitz V, Kyrpides NC, Woyke T, Goker M, Klenk HP. Complete genome sequence of DSM 30083(T), the type strain (U5/41(T)) of Escherichia coli, and a proposal for delineating subspecies in microbial taxonomy. Stand Genomic Sci. 2014;9:2.View ArticlePubMedPubMed CentralGoogle Scholar
  32. MLST Database at UoW. http://mlst.warwick.ac.uk/mlst/.
  33. Rodriguez-Siek KE, Giddings CW, Doetkott C, Johnson TJ, Nolan LK. Characterizing the APEC pathotype. Vet Res. 2005;36:241–56.View ArticlePubMedGoogle Scholar
  34. Scheutz F, Stockbine NA. Genus I. Escherichia Castellani and Chalmers 1919. In: Brenner DJ, Krieg NR, Staley JT, editors. Bergey’s Manual of Systematic Bacteriology. New York: Springer; 2005. p. 607–24.Google Scholar
  35. Siguier P, Perochon J, Lestrade L, Mahillon J, Chandler M. ISfinder: the reference centre for bacterial insertion sequences. Nucleic Acids Res. 2006;34:D32–6.View ArticlePubMedGoogle Scholar
  36. Skyberg JA, Johnson TJ, Johnson JR, Clabots C, Logue CM, Nolan LK. Acquisition of avian pathogenic Escherichia coli plasmids by a commensal E. coli isolate enhances its abilities to kill chicken embryos, grow in human urine, and colonize the murine kidney. Infect Immun. 2006;74:6287–92.View ArticlePubMedPubMed CentralGoogle Scholar
  37. Tamura K, Dudley J, Nei M, Kumar S. MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol. 2007;24:1596–9.View ArticlePubMedGoogle Scholar
  38. Van Domselaar GH, Stothard P, Shrivastava S, Cruz JA, Guo A, Dong X, Lu P, Szafron D, Greiner R, Wishart DS. BASys: a web server for automated bacterial genome annotation. Nucleic Acids Res. 2005;33:W455–9.View ArticlePubMedPubMed CentralGoogle Scholar
  39. Welch R. The Genus Escherichia. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K, Stackebrant E, editors. The Prokaryotes. Berlin: Springer; 2005.Google Scholar
  40. Williams KP, Kelly DP. Proposal for a new class within the phylum Proteobacteria, Acidithiobacillia classis nov., with the type order Acidithiobacillales, and emended description of the class Gammaproteobacteria Int J Syst Evol Microbiol. 2013;63:2901–906.Google Scholar
  41. Woese CR, Kandler O, Wheelis ML. Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci U S A. 1990;87:4576–9.View ArticlePubMedPubMed CentralGoogle Scholar
  42. Zankari E, Hasman H, Cosentino S, Vestergaard M, Rasmussen S, Lund O, Aarestrup FM, Larsen MV. Identification of acquired antimicrobial resistance genes. J Antimicrob Chemother. 2012;67:2640–4.View ArticlePubMedPubMed CentralGoogle Scholar
  43. Zhou Y, Liang Y, Lynch KH, Dennis JJ, Wishart DS. PHAST: a fast phage search tool. Nucleic Acids Res. 2011;39:W347–52.View ArticlePubMedPubMed CentralGoogle Scholar
  44. Zhu GX, Jiang J, Pan Z, Hu L, Wang S, Wang H, Leung FC, Dai J, Fan H. Comparative genomic analysis shows that avian pathogenic Escherichia coli isolate IMT5155 (O2:K1:H5; ST complex 95, ST140) shares close relationship with ST95 APEC O1:K1 and human ExPEC O18:K1 strains. PLoS One. 2014;9:e112048.View ArticleGoogle Scholar

Copyright

© The Author(s). 2017