Escherichia coli Serotype O55:H7 Diversity Supports Parallel Acquisition of Bacteriophage at Shiga Toxin Phage Insertion Sites during Evolution of the O157:H7 Lineage

Kyle, Jennifer L.; Cummings, Craig; Parker, Craig T.; Quiñones, Beatriz; Vatta, Paolo; Newton, Elizabeth M.; Huynh, Steven; Swimley, Michelle; Degoricija, Lovorka; Barker, Melissa; Fontanoz, Samar; Nguyen, Kimberly; Patel, Ronak; Fang, Rixun; Tebbs, Robert S.; Petrauskene, Olga V.; Furtado, Manohar R.; Mandrell, Robert E.

doi:10.1128/jb.00120-12

Cited by 59 publications

(71 citation statements)

References 81 publications

(107 reference statements)

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“…We did not observe prophages with high sequence similarity to Sp11 and Sp12 in the corresponding genomic region of E. coli O55:H7 (see Fig. S4), the predecessor of O157:H7 (19,(44)(45)(46). These observations collectively highlighted the dynamic changes within this region that have occurred during the course of O157:H7 evolution.…”

Section: Discussionsupporting

confidence: 54%

“…Although in silico analysis suggested that many of these prophages are defective, Asadulghani et al (15) demonstrated that some can be induced or packaged and may even transduce other E. coli strains. The constant loss and acquisition of prophages are identified as the major mechanisms in the evolution of this pathogen (11,12,15,(18)(19)(20). In addition to integrase-mediated phage integration and excision, homologous recombination between related prophages can also contribute to the genomic instability of E. coli O157:H7 (9,11).…”

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confidence: 99%

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Identification and Characterization of Spontaneous Deletions within the Sp11-Sp12 Prophage Region of Escherichia coli O157:H7 Sakai

Chun

Lewis

Goswami

et al. 2013

Appl Environ Microbiol

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bProphages make up 12% of the enterohemorrhagic Escherichia coli genome and play prominent roles in the evolution and virulence of this food-borne pathogen. Acquisition and loss of and rearrangements within prophage regions are the primary causes of differences in pulsed-field gel electrophoresis (PFGE) patterns among strains of E. coli O157:H7. Sp11 and Sp12 are two tandemly integrated and putatively defective prophages carried by E. coli O157:H7 strain Sakai. In this study, we identified 3 classes of deletions that occur within the Sp11-Sp12 region, at a frequency of ca. 7.74 ؋ 10 ؊4 . One deletion resulted in a precise excision of Sp11, and the other two spanned the junction of Sp11 and Sp12. All deletions resulted in shifts in the XbaI fragment pattern observed by PFGE. We sequenced the inducible prophage pool of Sakai but did not identify any mature phage particles corresponding to either Sp11 or Sp12. Deletions containing pchB and psrC, which are Sp11-carried genes encoding proteins known or suspected to regulate type III secretion, did not affect the secretion levels of the EspA or EspB effector. Alignment of the Sp11-Sp12 DNA sequence with its corresponding regions in other E. coli O157:H7 and O55:H7 strains suggested that homologous recombination rather than integrase-mediated excision is the mechanism behind these deletions. Therefore, this study provides a mechanism behind the previously observed genetic instability of this genomic region of E. coli O157:H7.

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Section: Discussionsupporting

confidence: 54%

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confidence: 99%

Identification and Characterization of Spontaneous Deletions within the Sp11-Sp12 Prophage Region of Escherichia coli O157:H7 Sakai

Chun

Lewis

Goswami

et al. 2013

Appl Environ Microbiol

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“…We found no similarities between this sequence and those of any other replication proteins from known Inc group plasmids (33,45). GenBank analysis showed that RCS47 RepA is present in only the genomes of phages, such as pO111_2 (46) and p12579_1 (47), with which it displayed 99% and 100% identity, respectively, at the protein level. The IncY replicon mobile elements associated with strains producing ESBL genes have been described in several epidemiologic studies (19,48,49) but, unlike RCS47 RepA, the IncY replicon is found on both phages and plasmids (10; T. Billard-Pomares and C. Branger, unpublished data).…”

Section: Resultsmentioning

confidence: 86%

Characterization of a P1-Like Bacteriophage Carrying an SHV-2 Extended-Spectrum β-Lactamase from an Escherichia coli Strain

Billard-Pomarès

Fouteau

Jacquet

et al. 2014

Antimicrob Agents Chemother

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h P1 bacteriophages lysogenize bacteria as independent plasmid-like elements. We describe here a P1-like bacteriophage, RCS47, carrying a bla SHV-2 gene, isolated from a clinical strain of Escherichia coli from phylogroup B1, and we report the prevalence of P1-like prophages in natural E. coli isolates. We found that 70% of the sequence of RCS47, a 115-kb circular molecule, was common to the reference P1 bacteriophage under GenBank accession no. AF234172.1, with the shared sequences being 99% identical. RCS47 had acquired two main foreign DNA fragments: a 9,636-bp fragment mobilized by two IS26 elements containing a bla SHV-2 gene, and an 8,544-bp fragment mobilized by two IS5 elements containing an operon encoding a dimethyl sulfoxide reductase. The reference P1 prophage plasmid replication gene belonged to the IncY incompatibility group, whereas that of RCS47 was from an unknown group. The lytic capacity of RCS47 and bla SHV-2 gene transduction, through the lysogenization of RCS47 in the recipient E. coli strains, were not demonstrated. The prevalence of P1-like prophages in various animal and human E. coli strain collections, as determined by the PCR detection of repL, the lytic replication gene, was 12.6%. No differences in the prevalences of these prophages were found between extended-spectrum ␤-lactamase (ESBL)-producing and non-ESBL-producing strains (P ‫؍‬ 0.69), but this prevalence was lower in phylogroup B2 than in the other phylogroups (P ‫؍‬ 0.008), suggesting epistatic interactions between P1 family phages and the genetic background of E. coli strains. P1-like phages are part of the mobile elements that carry antibiotic resistance. The high prevalence of P1-like prophages suggests their role may be underestimated.

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“…The stepwise evolution of GUD Ϫ SOR Ϫ O157:H7 strains from an O55:H7 ancestor has been described in great detail (6)(7)(8)(9)(10). At least one genome sequence from each proposed evolutionary node (except for 9.1a and 9.2e) is available, permitting for the first time the ordered reconstruction of CRISPR dynamics in E. coli over a several-thousand-year span (10).…”

Section: Resultsmentioning

confidence: 99%

“…One of the most wellknown and studied STEC strains is E. coli O157:H7. This serotype evolved from an O55:H7 ancestor, and a stepwise evolutionary model was proposed and updated in several studies (6)(7)(8)(9)(10). The non-O157 STEC strains, on the other hand, are underreported due to limitations in laboratory isolation and detection methods.…”

mentioning

confidence: 99%

The Evolutionary Divergence of Shiga Toxin-Producing Escherichia coli Is Reflected in Clustered Regularly Interspaced Short Palindromic Repeat (CRISPR) Spacer Composition

Yin

Jensen

Bai

et al. 2013

Appl Environ Microbiol

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eThe Shiga toxin-producing Escherichia coli (STEC) strains, including those of O157:H7 and the "big six" serogroups (i.e., serogroups O26, O45, O103, O111, O121, and O145), are a group of pathogens designated food adulterants in the United States. The relatively conserved nature of clustered regularly interspaced short palindromic repeats (CRISPRs) in phylogenetically related E. coli strains makes them potential subtyping markers for STEC detection, and a quantitative PCR (qPCR)-based assay was previously developed for O26:H11, O45:H2, O103:H2, O111:H8, O121:H19, O145:H28, and O157:H7 isolates. To better evaluate the sensitivity and specificity of this qPCR method, the CRISPR loci of 252 O157 and big-six STEC isolates were sequenced and analyzed along with 563 CRISPR1 and 624 CRISPR2 sequences available in GenBank. General conservation of spacer content and order was observed within each O157 and big-six serogroup, validating the qPCR method. Meanwhile, it was found that spacer deletion, the presence of an insertion sequence, and distinct alleles within a serogroup are sources of false-negative reactions. Conservation of CRISPR arrays among isolates expressing the same flagellar antigen, specifically, H7, H2, and H11, suggested that these isolates share an ancestor and provided an explanation for the false positives previously observed in the qPCR results. An analysis of spacer distribution across E. coli strains provided limited evidence for temporal spacer acquisition. Conversely, comparison of CRISPR sequences between strains along the stepwise evolution of O157:H7 from its O55:H7 ancestor revealed that, over this ϳ7,000-year span, spacer deletion was the primary force generating CRISPR diversity.

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Escherichia coli Serotype O55:H7 Diversity Supports Parallel Acquisition of Bacteriophage at Shiga Toxin Phage Insertion Sites during Evolution of the O157:H7 Lineage

Cited by 59 publications

References 81 publications

Identification and Characterization of Spontaneous Deletions within the Sp11-Sp12 Prophage Region of Escherichia coli O157:H7 Sakai

Identification and Characterization of Spontaneous Deletions within the Sp11-Sp12 Prophage Region of Escherichia coli O157:H7 Sakai

Characterization of a P1-Like Bacteriophage Carrying an SHV-2 Extended-Spectrum β-Lactamase from an Escherichia coli Strain

The Evolutionary Divergence of Shiga Toxin-Producing Escherichia coli Is Reflected in Clustered Regularly Interspaced Short Palindromic Repeat (CRISPR) Spacer Composition

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