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1985517720.Pdf JOURNAL OF BACTERIOLOGY, Jan. 2009, p. 347–354 Vol. 191, No. 1 0021-9193/09/$08.00ϩ0 doi:10.1128/JB.01238-08 Copyright © 2009, American Society for Microbiology. All Rights Reserved. Complete Genome Sequence and Comparative Genome Analysis of Enteropathogenic Escherichia coli O127:H6 Strain E2348/69ᰔ† Atsushi Iguchi,1 Nicholas R. Thomson,2 Yoshitoshi Ogura,1,3 David Saunders,2 Tadasuke Ooka,3 Ian R. Henderson,4 David Harris,2 M. Asadulghani,1 Ken Kurokawa,5 Paul Dean,6 Brendan Kenny,6 Michael A. Quail,2 Scott Thurston,2 Gordon Dougan,2 Tetsuya Hayashi,1,3 Julian Parkhill,2 and Gad Frankel7* Division of Bioenvironmental Science, Frontier Science Research Center,1 and Division of Microbiology, Department of Infectious Diseases, Faculty of Medicine,3 University of Miyazaki, Miyazaki, Japan; Pathogen Genomics, The Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge, United Kingdom2; School of Immunity and Infection, University of Downloaded from Birmingham, Birmingham, United Kingdom4; Department of Biological Information, School and Graduate School of Bioscience and Biotechnology, Tokyo Institute of Technology, Kanagawa, Japan5; Institute of Cell and Molecular Biosciences, University of Newcastle, Newcastle upon Tyne, United Kingdom6; and Centre for Molecular Microbiology and Infection, Division of Cell and Molecular Biology, Imperial College London, London, United Kingdom7 Received 5 September 2008/Accepted 15 October 2008 Enteropathogenic Escherichia coli (EPEC) was the first pathovar of E. coli to be implicated in human disease; however, no EPEC strain has been fully sequenced until now. Strain E2348/69 (serotype O127:H6 belonging to E. http://jb.asm.org/ coli phylogroup B2) has been used worldwide as a prototype strain to study EPEC biology, genetics, and virulence. Studies of E2348/69 led to the discovery of the locus of enterocyte effacement-encoded type III secretion system (T3SS) and its cognate effectors, which play a vital role in attaching and effacing lesion formation on gut epithelial cells. In this study, we determined the complete genomic sequence of E2348/69 and performed genomic comparisons with other important E. coli strains. We identified 424 E2348/69-specific genes, most of which are carried on mobile genetic elements, and a number of genetic traits specifically conserved in phylogroup B2 strains irrespective of their pathotypes, including the absence of the ETT2-related T3SS, which is present in E. coli strains belonging to all other phylogroups. The genome analysis revealed the entire gene repertoire related to E2348/69 virulence. Interestingly, E2348/69 contains only 21 intact T3SS effector genes, all of which are carried on prophages and integrative elements, on September 10, 2019 by guest compared to over 50 effector genes in enterohemorrhagic E. coli O157. As E2348/69 is the most-studied pathogenic E. coli strain, this study provides a genomic context for the vast amount of existing experimental data. The unexpected simplicity of the E2348/69 T3SS provides the first opportunity to fully dissect the entire virulence strategy of attaching and effacing pathogens in the genomic context. Escherichia coli is important because it is biology’s premier E. coli has a conserved core of genes common to both com- model organism, is a common commensal of the vertebrate mensal and pathogenic strains. The conserved genome frame- gut, and is a versatile pathogen of humans and animals. Mo- work is decorated with genomic islands and small clusters of lecular epidemiological studies have classified E. coli strains genes that have been acquired by horizontal gene transfer and into a number of phylogroups (phylogroups A, B1, B2, D, and that in pathogenic strains are often associated with virulence E) (13, 42), which are estimated to have diverged in the last 5 (for a review, see reference 32). EPEC strains provide a strik- to 9 million years (37, 42). Commensal E. coli strains are ing example of a pathovar highly adapted to virulence in the beneficial to the host and rarely cause disease. However, sev- human intestine (8, 15), but until now no EPEC strain has been eral clones of E. coli are responsible for a spectrum of diseases, fully sequenced. including urinary tract infection, sepsis/meningitis, and diar- EPEC was the first pathovar of E. coli to be implicated in rhea (for a review, see reference 15). Diarrheagenic E. coli human disease (4) and remains a leading cause of infantile strains are divided into enterotoxigenic E. coli (ETEC), en- diarrhea in developing countries (for a review, see reference teroaggregative E. coli, enteroinvasive E. coli, diffusely adher- 6). However, because EPEC strains were found not to invade ing E. coli, enteropathogenic E. coli (EPEC), and enterohem- cells or release diffusible toxins, doubts about their pathogenic orrhagic E. coli (EHEC) strains (15), which have different potential were raised in the 1960s and 1970s. However, induc- virulence mechanisms. tion of diarrhea in human volunteers (21) provided the decisive Whole-genome sequencing approaches have revealed that evidence that EPEC is a true human pathogen. As a result of this study, one of the strains tested, E2348/69 (serotype O127: H6), isolated in Taunton, United Kingdom, in 1969, became * Corresponding author. Mailing address: Flowers Building, Impe- the prototype strain used globally to study EPEC biology and rial College London, London SW7 2AZ, United Kingdom. Phone: 44 disease. Indeed, E2348/69 is probably the most-studied patho- 20 7954 5253. Fax: 44 20 7594 3069. E-mail: [email protected]. † Supplemental material for this article may be found at http://jb genic E. coli strain, and until now it was impossible to place the .asm.org/. vast amount of biological data in a genomic context. ᰔ Published ahead of print on 24 October 2008. Typical EPEC strains, which belong to a limited number of 347 348 IGUCHI ET AL. J. BACTERIOL. O serogroups, contain the EPEC adherence factor plasmid RESULTS AND DISCUSSION that encodes the bundle-forming pilus (BFP) (10) and also General genomic features of E2348/69. The genome of contain the gene regulator locus per (for a review, see refer- E2348/69 comprises a circular chromosome (4,965,553 bp), the ence 6). Typical EPEC strains are further divided into four EPEC adherence factor plasmid (pMAR2; 97,978 bp), and a distinct lineages, EPEC lineages 1 to 4 (18); E2348/69 belongs small drug-resistant plasmid (pE2348-2; 6,147 bp) (Fig. 1 and to EPEC lineage 1 and to the B2 phylogroup. Table 1; see Table S1 in the supplemental material). The The hallmark of EPEC infection is formation of distinct chromosome contains 4,703 predicted protein-encoding genes attaching and effacing (A/E) lesions, which are characterized (including 145 pseudogenes), 92 tRNA genes (including two by effacement of the brush border microvilli and intimate bac- pseudogenes), and seven rRNA operons. The pMAR2 plasmid terial attachment (for reviews, see references 6 and 8). The is nearly identical to pMAR7, a previously sequenced pMAR2 ability to induce A/E lesions is encoded on a pathogenicity derivative (5), but we identified three single-nucleotide poly- island termed the locus of enterocyte effacement (LEE), which morphisms and two single-base indels in intergenic regions is also present in O157 and non-O157 EHEC strains and the that differentiate these two plasmids (see Fig. S2 in the sup- Downloaded from mouse pathogen Citrobacter rodentium (24, 25; for a review, see plemental material). pMAR2 carries an additional copy of the reference 9). The LEE encodes the adhesin intimin, the struc- insertion sequence (IS) element ISEc21, which is not present tural components of a type III secretion system (T3SS) in- in pMAR7. pE2348-2 is distantly related to the ColE1 plasmid volved in translocation of effector proteins into the mammalian family and carries the strAB operon encoding streptomycin host cell, gene regulators, chaperones, translocators, and seven resistance. effector proteins (EspB, EspF, EspG, EspH, EspZ, Map, and Mobile genetic elements. A comparison of the E2348/69 se- Tir) (for a review, see reference 9). Recent studies have shown quence (phylogroup B2) with the genomes of eight sequenced that the EPEC strain E2348/69 genome encodes several addi- E. coli strains, including K-12 strain MG1655 (phylogroup A), http://jb.asm.org/ tional non-LEE effectors, including EspJ (23), EspG2, and EHEC strain Sakai (phylogroup E), three uropathogenic E. EspI/NleA, as well as NleB, NleC, NleD, NleE, and NleH (for coli (UPEC) strains (UTI89, CFT073, and 536), an avian a review, see reference 9). Additional putative virulence fac- pathogenic E. coli (APEC) strain (O1) (phylogroup B2), an tors include the autotransporter protein EspC (26), lymphos- ETEC strain (E24377A) (phylogroup B1), and a commensal tatin (LifA) (17), and several fimbrial operons. Here we report strain (HS) (phylogroup A) (Table 1; see Fig. S3 in the sup- the genome sequence of E2348/69, describe a bioinformatics plemental material), showed that the chromosomes of these survey of this strain’s virulence factors, and present the results organisms are remarkably conserved and display a high degree of overall synteny (Fig. 2). We found no evidence of large of comprehensive comparative studies performed with com- on September 10, 2019 by guest mensal and other pathogenic E. coli strains. chromosome inversions or translocations in E2348/69. How- ever, scattered between the conserved regions in E2348/69 are many strain-specific sequences (about 23 and 21% of the chro- MATERIALS AND METHODS mosome compared to E. coli K-12 [3] and EHEC strain Sakai Bacterial strain and sequencing. EPEC serotype O127:H6 strain E2348/69 was [12], respectively [Table 1]), which are mainly mobile genetic isolated in Taunton, United Kingdom, in 1969 during an outbreak of infantile elements. diarrhea. The sequenced strain was obtained from the original stock kept at the Within the E2348/69-specific sequences we identified 13 Health Protection Agency in Colindale, United Kingdom, and was subjected to prophages (PPs) (PP1 to PP13) and eight integrative elements minimal laboratory passages.
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