The defective prophage pool of Escherichia coli O157: Prophage-prophage interactions potentiate horizontal transfer of virulence determinants

Md Asadulghani, Yoshitoshi Ogura, Tadasuke Ooka, Takehiko Itoh, Akira Sawaguchi, Atsushi Iguchi, Keisuke Nakayama, Tetsuya Hayashi

Research output: Contribution to journalArticle

118 Citations (Scopus)

Abstract

Bacteriophages are major genetic factors promoting horizontal gene transfer (HGT) between bacteria. Their roles in dynamic bacterial genome evolution have been increasingly highlighted by the fact that many sequenced bacterial genomes contain multiple prophages carrying a wide range of genes. Enterohemorrhagic Escherichia coli O157 is the most striking case. A sequenced strain (O157 Sakai) possesses 18 prophages (Sp1-Sp18) that encode numerous genes related to O157 virulence, including those for two potent cytotoxins, Shiga toxins (Stx) 1 and 2. However, most of these prophages appeared to contain multiple genetic defects. To understand whether these defective prophages have the potential to act as mobile genetic elements to spread virulence determinants, we looked closely at the Sp1-Sp18 sequences, defined the genetic defects of each Sp, and then systematically analyzed all Sps for their biological activities. We show that many of the defective prophages, including the Stx1 phage, are inducible and released from O157 cells as particulate DNA. In fact, some prophages can even be transferred to other E. coli strains. We also show that new Stx1 phages are generated by recombination between the Stx1 and Stx2 phage genomes. The results indicate that these defective prophages are not simply genetic remnants generated in the course of O157 evolution, but rather genetic elements with a high potential for disseminating virulence-related genes and other genetic traits to other bacteria. We speculate that recombination and various other types of inter-prophage interactions in the O157 prophage pool potentiate such activities. Our data provide new insights into the potential activities of the defective prophages embedded in bacterial genomes and lead to the formulation of a novel concept of inter-prophage interactions in defective prophage communities.

Original languageEnglish
Article numbere1000408
JournalPLoS pathogens
Volume5
Issue number5
DOIs
Publication statusPublished - May 1 2009
Externally publishedYes

Fingerprint

Prophages
Escherichia coli O157
Virulence
Bacterial Genomes
Bacteriophages
Genetic Recombination
Shiga Toxin 1
Shiga Toxin 2
Interspersed Repetitive Sequences
Genes
Enterohemorrhagic Escherichia coli
Bacteria
Horizontal Gene Transfer
Molecular Evolution
Cytotoxins

All Science Journal Classification (ASJC) codes

  • Parasitology
  • Microbiology
  • Immunology
  • Molecular Biology
  • Genetics
  • Virology

Cite this

The defective prophage pool of Escherichia coli O157 : Prophage-prophage interactions potentiate horizontal transfer of virulence determinants. / Asadulghani, Md; Ogura, Yoshitoshi; Ooka, Tadasuke; Itoh, Takehiko; Sawaguchi, Akira; Iguchi, Atsushi; Nakayama, Keisuke; Hayashi, Tetsuya.

In: PLoS pathogens, Vol. 5, No. 5, e1000408, 01.05.2009.

Research output: Contribution to journalArticle

Asadulghani, Md ; Ogura, Yoshitoshi ; Ooka, Tadasuke ; Itoh, Takehiko ; Sawaguchi, Akira ; Iguchi, Atsushi ; Nakayama, Keisuke ; Hayashi, Tetsuya. / The defective prophage pool of Escherichia coli O157 : Prophage-prophage interactions potentiate horizontal transfer of virulence determinants. In: PLoS pathogens. 2009 ; Vol. 5, No. 5.
@article{4e98a357c3434d72956d59ae400c4dcb,
title = "The defective prophage pool of Escherichia coli O157: Prophage-prophage interactions potentiate horizontal transfer of virulence determinants",
abstract = "Bacteriophages are major genetic factors promoting horizontal gene transfer (HGT) between bacteria. Their roles in dynamic bacterial genome evolution have been increasingly highlighted by the fact that many sequenced bacterial genomes contain multiple prophages carrying a wide range of genes. Enterohemorrhagic Escherichia coli O157 is the most striking case. A sequenced strain (O157 Sakai) possesses 18 prophages (Sp1-Sp18) that encode numerous genes related to O157 virulence, including those for two potent cytotoxins, Shiga toxins (Stx) 1 and 2. However, most of these prophages appeared to contain multiple genetic defects. To understand whether these defective prophages have the potential to act as mobile genetic elements to spread virulence determinants, we looked closely at the Sp1-Sp18 sequences, defined the genetic defects of each Sp, and then systematically analyzed all Sps for their biological activities. We show that many of the defective prophages, including the Stx1 phage, are inducible and released from O157 cells as particulate DNA. In fact, some prophages can even be transferred to other E. coli strains. We also show that new Stx1 phages are generated by recombination between the Stx1 and Stx2 phage genomes. The results indicate that these defective prophages are not simply genetic remnants generated in the course of O157 evolution, but rather genetic elements with a high potential for disseminating virulence-related genes and other genetic traits to other bacteria. We speculate that recombination and various other types of inter-prophage interactions in the O157 prophage pool potentiate such activities. Our data provide new insights into the potential activities of the defective prophages embedded in bacterial genomes and lead to the formulation of a novel concept of inter-prophage interactions in defective prophage communities.",
author = "Md Asadulghani and Yoshitoshi Ogura and Tadasuke Ooka and Takehiko Itoh and Akira Sawaguchi and Atsushi Iguchi and Keisuke Nakayama and Tetsuya Hayashi",
year = "2009",
month = "5",
day = "1",
doi = "10.1371/journal.ppat.1000408",
language = "English",
volume = "5",
journal = "PLoS Pathogens",
issn = "1553-7366",
publisher = "Public Library of Science",
number = "5",

}

TY - JOUR

T1 - The defective prophage pool of Escherichia coli O157

T2 - Prophage-prophage interactions potentiate horizontal transfer of virulence determinants

AU - Asadulghani, Md

AU - Ogura, Yoshitoshi

AU - Ooka, Tadasuke

AU - Itoh, Takehiko

AU - Sawaguchi, Akira

AU - Iguchi, Atsushi

AU - Nakayama, Keisuke

AU - Hayashi, Tetsuya

PY - 2009/5/1

Y1 - 2009/5/1

N2 - Bacteriophages are major genetic factors promoting horizontal gene transfer (HGT) between bacteria. Their roles in dynamic bacterial genome evolution have been increasingly highlighted by the fact that many sequenced bacterial genomes contain multiple prophages carrying a wide range of genes. Enterohemorrhagic Escherichia coli O157 is the most striking case. A sequenced strain (O157 Sakai) possesses 18 prophages (Sp1-Sp18) that encode numerous genes related to O157 virulence, including those for two potent cytotoxins, Shiga toxins (Stx) 1 and 2. However, most of these prophages appeared to contain multiple genetic defects. To understand whether these defective prophages have the potential to act as mobile genetic elements to spread virulence determinants, we looked closely at the Sp1-Sp18 sequences, defined the genetic defects of each Sp, and then systematically analyzed all Sps for their biological activities. We show that many of the defective prophages, including the Stx1 phage, are inducible and released from O157 cells as particulate DNA. In fact, some prophages can even be transferred to other E. coli strains. We also show that new Stx1 phages are generated by recombination between the Stx1 and Stx2 phage genomes. The results indicate that these defective prophages are not simply genetic remnants generated in the course of O157 evolution, but rather genetic elements with a high potential for disseminating virulence-related genes and other genetic traits to other bacteria. We speculate that recombination and various other types of inter-prophage interactions in the O157 prophage pool potentiate such activities. Our data provide new insights into the potential activities of the defective prophages embedded in bacterial genomes and lead to the formulation of a novel concept of inter-prophage interactions in defective prophage communities.

AB - Bacteriophages are major genetic factors promoting horizontal gene transfer (HGT) between bacteria. Their roles in dynamic bacterial genome evolution have been increasingly highlighted by the fact that many sequenced bacterial genomes contain multiple prophages carrying a wide range of genes. Enterohemorrhagic Escherichia coli O157 is the most striking case. A sequenced strain (O157 Sakai) possesses 18 prophages (Sp1-Sp18) that encode numerous genes related to O157 virulence, including those for two potent cytotoxins, Shiga toxins (Stx) 1 and 2. However, most of these prophages appeared to contain multiple genetic defects. To understand whether these defective prophages have the potential to act as mobile genetic elements to spread virulence determinants, we looked closely at the Sp1-Sp18 sequences, defined the genetic defects of each Sp, and then systematically analyzed all Sps for their biological activities. We show that many of the defective prophages, including the Stx1 phage, are inducible and released from O157 cells as particulate DNA. In fact, some prophages can even be transferred to other E. coli strains. We also show that new Stx1 phages are generated by recombination between the Stx1 and Stx2 phage genomes. The results indicate that these defective prophages are not simply genetic remnants generated in the course of O157 evolution, but rather genetic elements with a high potential for disseminating virulence-related genes and other genetic traits to other bacteria. We speculate that recombination and various other types of inter-prophage interactions in the O157 prophage pool potentiate such activities. Our data provide new insights into the potential activities of the defective prophages embedded in bacterial genomes and lead to the formulation of a novel concept of inter-prophage interactions in defective prophage communities.

UR - http://www.scopus.com/inward/record.url?scp=67249140993&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=67249140993&partnerID=8YFLogxK

U2 - 10.1371/journal.ppat.1000408

DO - 10.1371/journal.ppat.1000408

M3 - Article

C2 - 19412337

AN - SCOPUS:67249140993

VL - 5

JO - PLoS Pathogens

JF - PLoS Pathogens

SN - 1553-7366

IS - 5

M1 - e1000408

ER -