A precise reconstruction of the emergence and constrained radiations of Escherichia coli O157 portrayed by backbone concatenomic analysis

Shana R. Leopold, Vincent Magrini, Nicholas J. Holt, Nurmohammad Shaikh, Elaine R. Mardis, Joseph Cagno, Yoshitoshi Ogura, Atsushi Iguchi, Tetsuya Hayashi, Alexander Mellmanng, Helge Karch, Thomas E. Besser, Stanley A. Sawyer, Thomas S. Whittam, Phillip I. Tarr

Research output: Contribution to journalArticle

83 Citations (Scopus)

Abstract

Single nucleotide polymorphisms (SNPs) in stable genome regions provide durable measurements of species evolution. We systematically identified each SNP in concatenations of all backbone ORFs in 7 newly or previously sequenced evolutionarily instructive pathogenic Escherichia coli O157:H7, O157:H -, and O55:H7. The 1,113 synonymous SNPs demonstrate emergence of the largest cluster of this pathogen only in the last millennium. Unexpectedly, shared SNPs within circumscribed clusters of organisms suggest severely restricted survival and limited effective population sizes of pathogenic O157:H7, tenuous survival of these organisms in nature, source-sink evolutionary dynamics, or, possibly, a limited number of mutations that confer selective advantage. A single large segment spanning the rfb-gnd gene cluster is the only backbone region convincingly acquired by recombination as O157 emerged from O55. This concatenomic analysis also supports using SNPs to differentiate closely related pathogens for infection control and forensic purposes. However, constrained radiations raise the possibility of making false associations between isolates.

Original languageEnglish
Pages (from-to)8713-8718
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume106
Issue number21
DOIs
Publication statusPublished - May 26 2009
Externally publishedYes

Fingerprint

Escherichia coli O157
Single Nucleotide Polymorphism
Radiation
Multigene Family
Infection Control
Population Density
Genetic Recombination
Open Reading Frames
Genome
Mutation

All Science Journal Classification (ASJC) codes

  • General

Cite this

A precise reconstruction of the emergence and constrained radiations of Escherichia coli O157 portrayed by backbone concatenomic analysis. / Leopold, Shana R.; Magrini, Vincent; Holt, Nicholas J.; Shaikh, Nurmohammad; Mardis, Elaine R.; Cagno, Joseph; Ogura, Yoshitoshi; Iguchi, Atsushi; Hayashi, Tetsuya; Mellmanng, Alexander; Karch, Helge; Besser, Thomas E.; Sawyer, Stanley A.; Whittam, Thomas S.; Tarr, Phillip I.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 106, No. 21, 26.05.2009, p. 8713-8718.

Research output: Contribution to journalArticle

Leopold, SR, Magrini, V, Holt, NJ, Shaikh, N, Mardis, ER, Cagno, J, Ogura, Y, Iguchi, A, Hayashi, T, Mellmanng, A, Karch, H, Besser, TE, Sawyer, SA, Whittam, TS & Tarr, PI 2009, 'A precise reconstruction of the emergence and constrained radiations of Escherichia coli O157 portrayed by backbone concatenomic analysis', Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 21, pp. 8713-8718. https://doi.org/10.1073/pnas.0812949106
Leopold, Shana R. ; Magrini, Vincent ; Holt, Nicholas J. ; Shaikh, Nurmohammad ; Mardis, Elaine R. ; Cagno, Joseph ; Ogura, Yoshitoshi ; Iguchi, Atsushi ; Hayashi, Tetsuya ; Mellmanng, Alexander ; Karch, Helge ; Besser, Thomas E. ; Sawyer, Stanley A. ; Whittam, Thomas S. ; Tarr, Phillip I. / A precise reconstruction of the emergence and constrained radiations of Escherichia coli O157 portrayed by backbone concatenomic analysis. In: Proceedings of the National Academy of Sciences of the United States of America. 2009 ; Vol. 106, No. 21. pp. 8713-8718.
@article{85ca3acd59624889b3d12c3921eb91a2,
title = "A precise reconstruction of the emergence and constrained radiations of Escherichia coli O157 portrayed by backbone concatenomic analysis",
abstract = "Single nucleotide polymorphisms (SNPs) in stable genome regions provide durable measurements of species evolution. We systematically identified each SNP in concatenations of all backbone ORFs in 7 newly or previously sequenced evolutionarily instructive pathogenic Escherichia coli O157:H7, O157:H -, and O55:H7. The 1,113 synonymous SNPs demonstrate emergence of the largest cluster of this pathogen only in the last millennium. Unexpectedly, shared SNPs within circumscribed clusters of organisms suggest severely restricted survival and limited effective population sizes of pathogenic O157:H7, tenuous survival of these organisms in nature, source-sink evolutionary dynamics, or, possibly, a limited number of mutations that confer selective advantage. A single large segment spanning the rfb-gnd gene cluster is the only backbone region convincingly acquired by recombination as O157 emerged from O55. This concatenomic analysis also supports using SNPs to differentiate closely related pathogens for infection control and forensic purposes. However, constrained radiations raise the possibility of making false associations between isolates.",
author = "Leopold, {Shana R.} and Vincent Magrini and Holt, {Nicholas J.} and Nurmohammad Shaikh and Mardis, {Elaine R.} and Joseph Cagno and Yoshitoshi Ogura and Atsushi Iguchi and Tetsuya Hayashi and Alexander Mellmanng and Helge Karch and Besser, {Thomas E.} and Sawyer, {Stanley A.} and Whittam, {Thomas S.} and Tarr, {Phillip I.}",
year = "2009",
month = "5",
day = "26",
doi = "10.1073/pnas.0812949106",
language = "English",
volume = "106",
pages = "8713--8718",
journal = "Proceedings of the National Academy of Sciences of the United States of America",
issn = "0027-8424",
number = "21",

}

TY - JOUR

T1 - A precise reconstruction of the emergence and constrained radiations of Escherichia coli O157 portrayed by backbone concatenomic analysis

AU - Leopold, Shana R.

AU - Magrini, Vincent

AU - Holt, Nicholas J.

AU - Shaikh, Nurmohammad

AU - Mardis, Elaine R.

AU - Cagno, Joseph

AU - Ogura, Yoshitoshi

AU - Iguchi, Atsushi

AU - Hayashi, Tetsuya

AU - Mellmanng, Alexander

AU - Karch, Helge

AU - Besser, Thomas E.

AU - Sawyer, Stanley A.

AU - Whittam, Thomas S.

AU - Tarr, Phillip I.

PY - 2009/5/26

Y1 - 2009/5/26

N2 - Single nucleotide polymorphisms (SNPs) in stable genome regions provide durable measurements of species evolution. We systematically identified each SNP in concatenations of all backbone ORFs in 7 newly or previously sequenced evolutionarily instructive pathogenic Escherichia coli O157:H7, O157:H -, and O55:H7. The 1,113 synonymous SNPs demonstrate emergence of the largest cluster of this pathogen only in the last millennium. Unexpectedly, shared SNPs within circumscribed clusters of organisms suggest severely restricted survival and limited effective population sizes of pathogenic O157:H7, tenuous survival of these organisms in nature, source-sink evolutionary dynamics, or, possibly, a limited number of mutations that confer selective advantage. A single large segment spanning the rfb-gnd gene cluster is the only backbone region convincingly acquired by recombination as O157 emerged from O55. This concatenomic analysis also supports using SNPs to differentiate closely related pathogens for infection control and forensic purposes. However, constrained radiations raise the possibility of making false associations between isolates.

AB - Single nucleotide polymorphisms (SNPs) in stable genome regions provide durable measurements of species evolution. We systematically identified each SNP in concatenations of all backbone ORFs in 7 newly or previously sequenced evolutionarily instructive pathogenic Escherichia coli O157:H7, O157:H -, and O55:H7. The 1,113 synonymous SNPs demonstrate emergence of the largest cluster of this pathogen only in the last millennium. Unexpectedly, shared SNPs within circumscribed clusters of organisms suggest severely restricted survival and limited effective population sizes of pathogenic O157:H7, tenuous survival of these organisms in nature, source-sink evolutionary dynamics, or, possibly, a limited number of mutations that confer selective advantage. A single large segment spanning the rfb-gnd gene cluster is the only backbone region convincingly acquired by recombination as O157 emerged from O55. This concatenomic analysis also supports using SNPs to differentiate closely related pathogens for infection control and forensic purposes. However, constrained radiations raise the possibility of making false associations between isolates.

UR - http://www.scopus.com/inward/record.url?scp=66649094404&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=66649094404&partnerID=8YFLogxK

U2 - 10.1073/pnas.0812949106

DO - 10.1073/pnas.0812949106

M3 - Article

C2 - 19439656

AN - SCOPUS:66649094404

VL - 106

SP - 8713

EP - 8718

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

SN - 0027-8424

IS - 21

ER -