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Title: Genomic Comparison of Escherichia coli O104:H4 Isolates from 2009 and 2011 Reveals Plasmid, and Prophage Heterogeneity, Including Shiga Toxin Encoding Phage stx2

Abstract

In May of 2011, an enteroaggregative Escherichia coli O104:H4 strain that had acquired a Shiga toxin 2-converting phage caused a large outbreak of bloody diarrhea in Europe which was notable for its high prevalence of hemolytic uremic syndrome cases. Several studies have described the genomic inventory and phylogenies of strains associated with the outbreak and a collection of historical E. coli O104:H4 isolates using draft genome assemblies. We present the complete, closed genome sequences of an isolate from the 2011 outbreak (2011C–3493) and two isolates from cases of bloody diarrhea that occurred in the Republic of Georgia in 2009 (2009EL–2050 and 2009EL–2071). Comparative genome analysis indicates that, while the Georgian strains are the nearest neighbors to the 2011 outbreak isolates sequenced to date, structural and nucleotide-level differences are evident in the Stx2 phage genomes, the mer/tet antibiotic resistance island, and in the prophage and plasmid profiles of the strains, including a previously undescribed plasmid with homology to the pMT virulence plasmid of Yersinia pestis. In addition, multiphenotype analysis showed that 2009EL–2071 possessed higher resistance to polymyxin and membrane-disrupting agents. Finally, we show evidence by electron microscopy of the presence of a common phage morphotype among the European and Georgian strainsmore » and a second phage morphotype among the Georgian strains. The presence of at least two stx2 phage genotypes in host genetic backgrounds that may derive from a recent common ancestor of the 2011 outbreak isolates indicates that the emergence of stx2 phage-containing E. coli O104:H4 strains probably occurred more than once, or that the current outbreak isolates may be the result of a recent transfer of a new stx2 phage element into a pre-existing stx2-positive genetic background.« less

Authors:
 [1];  [2];  [3];  [2];  [2];  [4];  [1];  [1];  [5];  [3];  [1];  [1];  [3];  [1];  [6];  [2];  [2];  [1];  [2];  [1] more »;  [7];  [8];  [1];  [9];  [7];  [1];  [2];  [4];  [3];  [1];  [9];  [2];  [1];  [4];  [10];  [1];  [6];  [6];  [1];  [11];  [2];  [3];  [1];  [2];  [2] « less
  1. Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
  2. Naval Medical Research Center and Henry M. Jackson Foundation for Military Medicine, Frederick, MD (United States)
  3. U.S. Army Research Inst. for Infectious Disease, Frederick, MD (United States)
  4. U.S. Army Edgewood Chemical Biological Center, Aberdeen Proving Ground, MD (United States)
  5. National Center for Disease Control and Public Health, Tbilisi (Republic of Georgia). South Caucasus Field Epidemiology. Lab. Training Program
  6. Centers for Disease Control and Prevention (CDC), Atlanta, GA (United States). Enteric Diseases Lab. Branch
  7. U.S. Army Edgewood Chemical Biological Center, Aberdeen Proving Ground, MD (United States); Excet Inc, Springfield, VA (United States)
  8. U.S. Army Edgewood Chemical Biological Center, Aberdeen Proving Ground, MD (United States); Science Applications International Corporation, Abingdon, MD (United States)
  9. BioTeam, Inc., Middleton, MA (United States)
  10. U.S. Army Research Inst. for Infectious Disease, Frederick, MD (United States); Team Ke’aki Tech, Frederick, MD (United States)
  11. Defense Threat Reduction Agency, Alexandria, VA (United States)
Publication Date:
Research Org.:
Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division; Defense Threat Reduction Agency (DTRA)
Contributing Org.:
Threat Characterization Consortium
OSTI Identifier:
1627555
Grant/Contract Number:  
AC52-06NA25396
Resource Type:
Accepted Manuscript
Journal Name:
PLoS ONE
Additional Journal Information:
Journal Volume: 7; Journal Issue: 11; Journal ID: ISSN 1932-6203
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Bacteriophages; genomics; viral genomics; single nucleotide polymorphisms; toxins; sequence alignment; transposable elements; Escherichia coli

Citation Formats

Ahmed, Sanaa A., Awosika, Joy, Baldwin, Carson, Bishop-Lilly, Kimberly A., Biswas, Biswajit, Broomall, Stacey, Chain, Patrick S. G., Chertkov, Olga, Chokoshvili, Otar, Coyne, Susan, Davenport, Karen, Detter, J. Chris, Dorman, William, Erkkila, Tracy H., Folster, Jason P., Frey, Kenneth G., George, Matroner, Gleasner, Cheryl, Henry, Matthew, Hill, Karen K., Hubbard, Kyle, Insalaco, Joseph, Johnson, Shannon, Kitzmiller, Aaron, Krepps, Michael, Lo, Chien-Chi, Luu, Truong, McNew, Lauren A., Minogue, Timothy, Munk, Christine A., Osborne, Brian, Patel, Mohit, Reitenga, Krista G., Rosenzweig, C. Nicole, Shea, April, Shen, Xiaohong, Strockbine, Nancy, Tarr, Cheryl, Teshima, Hazuki, van Gieson, Eric, Verratti, Kathleen, Wolcott, Mark, Xie, Gary, Sozhamannan, Shanmuga, and Gibbons, Henry S. Genomic Comparison of Escherichia coli O104:H4 Isolates from 2009 and 2011 Reveals Plasmid, and Prophage Heterogeneity, Including Shiga Toxin Encoding Phage stx2. United States: N. p., 2012. Web. doi:10.1371/journal.pone.0048228.
Ahmed, Sanaa A., Awosika, Joy, Baldwin, Carson, Bishop-Lilly, Kimberly A., Biswas, Biswajit, Broomall, Stacey, Chain, Patrick S. G., Chertkov, Olga, Chokoshvili, Otar, Coyne, Susan, Davenport, Karen, Detter, J. Chris, Dorman, William, Erkkila, Tracy H., Folster, Jason P., Frey, Kenneth G., George, Matroner, Gleasner, Cheryl, Henry, Matthew, Hill, Karen K., Hubbard, Kyle, Insalaco, Joseph, Johnson, Shannon, Kitzmiller, Aaron, Krepps, Michael, Lo, Chien-Chi, Luu, Truong, McNew, Lauren A., Minogue, Timothy, Munk, Christine A., Osborne, Brian, Patel, Mohit, Reitenga, Krista G., Rosenzweig, C. Nicole, Shea, April, Shen, Xiaohong, Strockbine, Nancy, Tarr, Cheryl, Teshima, Hazuki, van Gieson, Eric, Verratti, Kathleen, Wolcott, Mark, Xie, Gary, Sozhamannan, Shanmuga, & Gibbons, Henry S. Genomic Comparison of Escherichia coli O104:H4 Isolates from 2009 and 2011 Reveals Plasmid, and Prophage Heterogeneity, Including Shiga Toxin Encoding Phage stx2. United States. https://doi.org/10.1371/journal.pone.0048228
Ahmed, Sanaa A., Awosika, Joy, Baldwin, Carson, Bishop-Lilly, Kimberly A., Biswas, Biswajit, Broomall, Stacey, Chain, Patrick S. G., Chertkov, Olga, Chokoshvili, Otar, Coyne, Susan, Davenport, Karen, Detter, J. Chris, Dorman, William, Erkkila, Tracy H., Folster, Jason P., Frey, Kenneth G., George, Matroner, Gleasner, Cheryl, Henry, Matthew, Hill, Karen K., Hubbard, Kyle, Insalaco, Joseph, Johnson, Shannon, Kitzmiller, Aaron, Krepps, Michael, Lo, Chien-Chi, Luu, Truong, McNew, Lauren A., Minogue, Timothy, Munk, Christine A., Osborne, Brian, Patel, Mohit, Reitenga, Krista G., Rosenzweig, C. Nicole, Shea, April, Shen, Xiaohong, Strockbine, Nancy, Tarr, Cheryl, Teshima, Hazuki, van Gieson, Eric, Verratti, Kathleen, Wolcott, Mark, Xie, Gary, Sozhamannan, Shanmuga, and Gibbons, Henry S. Thu . "Genomic Comparison of Escherichia coli O104:H4 Isolates from 2009 and 2011 Reveals Plasmid, and Prophage Heterogeneity, Including Shiga Toxin Encoding Phage stx2". United States. https://doi.org/10.1371/journal.pone.0048228. https://www.osti.gov/servlets/purl/1627555.
@article{osti_1627555,
title = {Genomic Comparison of Escherichia coli O104:H4 Isolates from 2009 and 2011 Reveals Plasmid, and Prophage Heterogeneity, Including Shiga Toxin Encoding Phage stx2},
author = {Ahmed, Sanaa A. and Awosika, Joy and Baldwin, Carson and Bishop-Lilly, Kimberly A. and Biswas, Biswajit and Broomall, Stacey and Chain, Patrick S. G. and Chertkov, Olga and Chokoshvili, Otar and Coyne, Susan and Davenport, Karen and Detter, J. Chris and Dorman, William and Erkkila, Tracy H. and Folster, Jason P. and Frey, Kenneth G. and George, Matroner and Gleasner, Cheryl and Henry, Matthew and Hill, Karen K. and Hubbard, Kyle and Insalaco, Joseph and Johnson, Shannon and Kitzmiller, Aaron and Krepps, Michael and Lo, Chien-Chi and Luu, Truong and McNew, Lauren A. and Minogue, Timothy and Munk, Christine A. and Osborne, Brian and Patel, Mohit and Reitenga, Krista G. and Rosenzweig, C. Nicole and Shea, April and Shen, Xiaohong and Strockbine, Nancy and Tarr, Cheryl and Teshima, Hazuki and van Gieson, Eric and Verratti, Kathleen and Wolcott, Mark and Xie, Gary and Sozhamannan, Shanmuga and Gibbons, Henry S.},
abstractNote = {In May of 2011, an enteroaggregative Escherichia coli O104:H4 strain that had acquired a Shiga toxin 2-converting phage caused a large outbreak of bloody diarrhea in Europe which was notable for its high prevalence of hemolytic uremic syndrome cases. Several studies have described the genomic inventory and phylogenies of strains associated with the outbreak and a collection of historical E. coli O104:H4 isolates using draft genome assemblies. We present the complete, closed genome sequences of an isolate from the 2011 outbreak (2011C–3493) and two isolates from cases of bloody diarrhea that occurred in the Republic of Georgia in 2009 (2009EL–2050 and 2009EL–2071). Comparative genome analysis indicates that, while the Georgian strains are the nearest neighbors to the 2011 outbreak isolates sequenced to date, structural and nucleotide-level differences are evident in the Stx2 phage genomes, the mer/tet antibiotic resistance island, and in the prophage and plasmid profiles of the strains, including a previously undescribed plasmid with homology to the pMT virulence plasmid of Yersinia pestis. In addition, multiphenotype analysis showed that 2009EL–2071 possessed higher resistance to polymyxin and membrane-disrupting agents. Finally, we show evidence by electron microscopy of the presence of a common phage morphotype among the European and Georgian strains and a second phage morphotype among the Georgian strains. The presence of at least two stx2 phage genotypes in host genetic backgrounds that may derive from a recent common ancestor of the 2011 outbreak isolates indicates that the emergence of stx2 phage-containing E. coli O104:H4 strains probably occurred more than once, or that the current outbreak isolates may be the result of a recent transfer of a new stx2 phage element into a pre-existing stx2-positive genetic background.},
doi = {10.1371/journal.pone.0048228},
journal = {PLoS ONE},
number = 11,
volume = 7,
place = {United States},
year = {Thu Nov 01 00:00:00 EDT 2012},
month = {Thu Nov 01 00:00:00 EDT 2012}
}

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