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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.

SUBMITTER: Asadulghani M

PROVIDER: S-EPMC2669165 | biostudies-literature | 2009 May

REPOSITORIES: biostudies-literature

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

Asadulghani Md M Ogura Yoshitoshi Y Ooka Tadasuke T Itoh Takehiko T Sawaguchi Akira A Iguchi Atsushi A Nakayama Keisuke K Hayashi Tetsuya T

PLoS pathogens 20090501 5

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 ...[more]

PMID: 19412337

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Project description:Type II toxin-antitoxin (TA) systems are classically composed of two genes that encode a toxic protein and a cognate antitoxin protein. Both genes are organized in an operon whose expression is autoregulated at the level of transcription by the antitoxin-toxin complex, which binds operator DNA through the antitoxin's DNA-binding domain. Here, we investigated the transcriptional regulation of a particular TA system located in the immunity region of a cryptic lambdoid prophage in the Escherichia coli O157:H7 EDL933 strain. This noncanonical paaA2-parE2 TA operon contains a third gene, paaR2, that encodes a transcriptional regulator that was previously shown to control expression of the TA. We provide direct evidence that the PaaR2 is a transcriptional regulator which shares functional similarities to the lambda CI repressor. Expression of the paaA2-parE2 TA operon is regulated by two other transcriptional regulators, YdaS and YdaT, encoded within the same region. We argue that YdaS and YdaT are analogous to lambda Cro and CII and that they do not constitute a TA system, as previously debated. We show that PaaR2 primarily represses the expression of YdaS and YdaT, which in turn controls the expression of paaR2-paaA2-parE2 operon. Overall, our results show that the paaA2-parE2 TA is embedded in an intricate lambdoid prophage-like regulation network. Using single-cell analysis, we observed that the entire locus exhibits bistability, which generates diversity of expression in the population. Moreover, we confirmed that paaA2-parE2 is addictive and propose that it could limit genomic rearrangements within the immunity region of the CP-933P cryptic prophage. IMPORTANCE Transcriptional regulation of bacterial toxin-antitoxin (TA) systems allows compensation of toxin and antitoxin proteins to maintain a neutral state and avoid cell intoxication unless TA genes are lost. Such models have been primarily studied in plasmids, but TAs are equally present in other mobile genetic elements, such as transposons and prophages. Here, we demonstrate that the expression of a TA system located in a lambdoid cryptic prophage is transcriptionally coupled to the prophage immunity region and relies on phage transcription factors. Moreover, competition between transcription factors results in bistable expression, which generates cell-to-cell heterogeneity in the population, but without, however, leading to any detectable phenotype, even in cells expressing the TA system. We show that despite the lack of protein sequence similarity, this locus retains major lambda prophage regulation features.

Dataset Information

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

Publications

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

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