Skip to main content
Article thumbnail
Location of Repository

The Defective Prophage Pool of Escherichia coli O157: Prophage–Prophage Interactions Potentiate Horizontal Transfer of Virulence Determinants

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

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

Topics: Research Article
Publisher: Public Library of Science
OAI identifier: oai:pubmedcentral.nih.gov:2669165
Provided by: PubMed Central
Download PDF:
Sorry, we are unable to provide the full text but you may find it at the following location(s):
  • http://www.pubmedcentral.nih.g... (external link)
  • Suggested articles

    Citations

    1. (2006). An extensive repertoire of type III secretion effectors in Escherichia coli O157 and the role of lambdoid phages in their dissemination.
    2. (2006). Assembly of bacteriophage P2 and P4 procapsids with internal scaffolding protein.
    3. (2002). Bacteriophage control of bacterial virulence.
    4. (2005). Bacteriophage l and its Genetic Neighborhood. In: Calendar R, ed (2005) The Bacteriophages Oxford
    5. (2005). Bacteriophage Mu. In: Calendar R, ed (2005) The Bacteriophages Oxford
    6. (2004). Bacteriophage P4 Vis protein is needed for prophage excision.
    7. (2003). BLAST++: BLASTing queries in batches.
    8. (2004). Bru ¨ssow H
    9. (2006). Building a virus from scratch: assembly of an infectious virus using purified components in a rigorously defined biochemical assay system.
    10. Camerini-Otero RD (2002) Over 1000 genes are involved in the DNA damage response of Escherichia coli.
    11. (1995). Circuit simulation of genetic networks.
    12. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.
    13. (2001). Comparative gene expression profiles following UV exposure in wild-type and SOS-deficient Escherichia coli.
    14. (2001). Complete genome sequence of enterohemorrhagic Escherichia coli O157: H7 and genomic comparison with a laboratory strain K-12.
    15. (2001). Diversification of Escherichia coli genomes: are bacteriophagesthe major contributors?TrendsMicrobiol 9:481–485.
    16. (2004). Diversity of stx2 converting bacteriophages induced from Shiga-toxin-producing Escherichia coli strains isolated from cattle.
    17. (1977). DNA Replication—Bacteriophage lambda.
    18. (2001). Ecological fitness, genomic islands and bacterial pathogenicity. A Darwinian view of the evolution of microbes.
    19. (2006). Genome Rearrangements, Deletions and Amplifications in the Natural Population of Bartonella henselae.
    20. (2002). Genomic diversity of enterohemorrhagic Escherichia coli O157 revealed by whole genome PCR scanning.
    21. (2007). Genomic View on the Evolution of Enterohemorrhagic Escherichia coli. In:
    22. (2005). Host gene expression changes and DNA amplification during temperate phage induction.
    23. (1990). Host virus interactions in the initiation of bacteriophage lambda DNA replication. Recruitment of Escherichia coli DnaB helicase by lambda P replication protein.
    24. (2006). Isolation and characterization of the smallest bacteriophage P4 derivatives packaged into P4-size head in bacteriophage P2-P4 system.
    25. (2005). Lambda integrase: armed for recombination.
    26. (2006). Lex marks the spot: the virulent side of SOS and a closer look at the LexA regulon.
    27. (1993). Mechanisms of genome propagation and helper exploitation by satellite phage P4.
    28. (2004). MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment.
    29. (1975). Molecular biology of bacteriophage Mu.
    30. (2006). O Side Chain Deficiency Enhances Sensitivity of Escherichia coli to Shiga Toxin 2-Converting Bacteriophages.
    31. (2005). On the role of Cro in lambda prophage induction.
    32. (2000). One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products.
    33. (1996). Outbreaks of enterohaemorrhagic Escherichia coli O157:H7 infection by two different genotype strains in Japan,
    34. (1998). Pathogenesis and diagnosis of Shiga toxinproducing Escherichia coli infections.
    35. (2005). Phage regulatory circuits and virulence gene expression.
    36. (2004). Phages and the Evolution of Bacterial Pathogens: from Genomic Rearrangements to Lysogenic Conversion.
    37. (2003). Prophages and bacterial genomics: What have we learned so far?
    38. (2005). Quantitative kinetic analysis of the bacteriophage lambda genetic network.
    39. (1978). Regional replication of the bacterial chromosome induced by derepression of prophage lambda. IV. Escape synthesis of gal operon in phage 82.
    40. (2002). Regulation of directionality in bacteriophage lambda site-specific recombination: structure of the Xis protein.
    41. (2001). Shiga-toxin-converting bacteriophages.
    42. (2003). Strategies for helicase recruitment and loading in bacteria.
    43. (1951). Studies on the virulence of bacteriophage-infected strains of Corynebacterium diphtheriae.
    44. (1998). The E protein of satellite phage P4 acts as an antirepressor by binding to the C protein of helper phage P2.
    45. (2003). The role played by viruses in the evolution of their hosts: A view based on informational protein phylogenies.
    46. (2000). The terminase enzyme from bacteriophage lambda: a DNA-packaging machine.
    47. (2005). Threshold effects in gene regulation: when some is not enough.
    48. (2003). TM4: a free, open-source system for microarray data management and analysis.

    To submit an update or takedown request for this paper, please submit an Update/Correction/Removal Request.