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Infection and Immunity, September 1998, p. 4496-4498, Vol. 66, No. 9
0019-9567/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.

In Vivo Transduction with Shiga Toxin 1-Encoding Phage

David W. K. Acheson,1 Joachim Reidl,2 Xiaoping Zhang,1 Gerald T. Keusch,1 John J. Mekalanos,3 and Matthew K. Waldor1,*

Division of Geographic Medicine and Infectious Diseases and Tupper Research Institute, Tufts University School of Medicine,1 and Department of Microbiology and Molecular Genetics and the Shipley Institute of Medicine, Harvard Medical School,3 Boston, Massachusetts, and Research Center for Infectious Disease, University of Wuerzburg, Wuerzburg, Germany2

Received 3 April 1998/Returned for modification 15 May 1998/Accepted 2 June 1998

    ABSTRACT
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Abstract
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To facilitate the study of intestinal transmission of the Shiga toxin 1 (Stx1)-converting phage H-19B, Tn10d-bla mutagenesis of an Escherichia coli H-19B lysogen was undertaken. Two mutants containing insertions in the gene encoding the A subunit of Stx1 were isolated. The resultant ampicillin-resistant E. coli strains lysogenic for these phages produced infectious H-19B particles but not active toxin. These lysogens were capable of transducing an E. coli recipient strain in the murine gastrointestinal tract, thereby demonstrating that lysogens of Shiga toxin-converting phages give rise to infectious virions within the host gastrointestinal tract.

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Bacteriophages have played a critical role in the evolution of many bacterial pathogens (reviewed in references 3 and 6). Integrating (temperate) phages often alter the properties of the host bacterial cell upon establishment of lysogeny, a process known as phage conversion. The toxins of a number of both gram-negative and gram-positive pathogens have been found to be encoded in the genomes of temperate bacteriophages. The presence of genes encoding virulence factors in phage genomes provides a means for the dissemination of these genes; however, the sites and conditions which favor bacteriophage conversion have not been studied.

The bacteriophage-encoded Shiga toxins (Stxs) are believed to play an important role in the pathogenesis of hemorrhagic colitis, hemolytic-uremic syndrome, and thrombotic thrombocytopenic purpura that may result from human infection with lysogenic Escherichia coli (8). Stxs are A-B-type toxins which bind to the host glycolipid Gb3 (11). The enzymatically active A subunit of Stx acts as an rRNA N-glycosidase on the eukaryotic 60S ribosomal subunit and thereby inhibits protein synthesis (7). Stx1 and Stx2 are the two principal Stxs found in E. coli. Williams Smith and Linggood originally reported in 1971 that lysates of H19B, an E. coli O26:H11 strain isolated from an outbreak of infantile diarrhea, could transfer enterotoxinogenicity to E. coli K-12 in vitro (21). This phage, known as H-19B, was subsequently shown to encode Stx1 and to have DNA sequence homology to phage lambda  (10). Another lambdoid phage, designated 933W (isolated from an E. coli O157:H7 strain from a patient with hemorrhagic colitis), encodes Stx2 (15, 16). Although O157:H7 is the most commonly isolated E. coli serotype associated with Stx production and its related diseases in the United States, more than 30 other E. coli serotypes have been found to produce Stx and to be associated with disease (2). Transient Stx production has also been observed in other (non-E. coli) bacterial species, including Enterobacter cloacae (18) and Citrobacter freundii (20) isolated from patients with hemolytic-uremic syndrome. Dissemination of the lambdoid phages which encode Stx1 and Stx2 is the likely mechanism accounting for the spread of these toxins among diverse E. coli serotypes and into other bacterial species. In the present study, we sought to determine whether the Stx1-encoding phage H-19B can be transmitted to another E. coli strain within the murine intestine. An H-19B phage that was marked with an antibiotic resistance marker was constructed to allow detection of intraintestinal H-19B transmission by transduction.

Construction of H-19B derivatives which encode ampicillin resistance. An antibiotic resistance marker was introduced into the genome of the Stx1-encoding phage H-19B to facilitate the study of the intestinal transmissibility of this lambdoid phage. Tn10d-bla, an 861-bp minitransposon which was constructed to allow identification of phage-encoded exported proteins (19), was used for this purpose. This small element generates translational fusions between the mature portion of beta -lactamase and the amino-terminal portion of the target gene product (19). Plasmid pJR207 (19), which harbors Tn10d-bla, was introduced into E. coli C600 H-19B in seven independent transformations, and ampicillin-resistant (Apr) colonies were selected as described previously (19). Approximately 10,000 Apr colonies were then pooled, washed, and UV induced to produce seven independent H-19B phage pool lysates. The streptomycin-resistant (Smr) E. coli strain MC4100 (5) was then used as a recipient strain for transduction with these lysates. Ampicillin-resistant colonies were purified and tested for lysogeny by cross-streaking. Lysogens were then used to produce new phage stocks which were subsequently used to lysogenize MC4100. All lysogens were resistant to ampicillin, thereby confirming the linkage of the Apr gene to the H-19B phage genome.

Subsequently one representative H-19B Tn10d-bla insertion from each of the seven independent phage pool lysates was characterized by restriction enzyme and Southern blot analysis. All Tn10d-bla insertions were located within the same 8.1-kb EcoRI fragment known to contain the stxAB operon (9) (Fig. 1). Two of the Tn10d-bla fusions were further characterized by subcloning the fusions from the corresponding phage DNA and determining the precise location of the 5' fusion junctions by using an oligonucleotide corresponding to the 5' end of the bla gene as a sequencing primer. We found that the Tn10d-bla insertion in H-19B-Ap1 was fused to the coding sequence corresponding to amino acid 70 of the A subunit of Stx1, while the Tn10d-bla insertion in H-19B-Ap2 was fused to the sequence corresponding to amino acid 167 of the A subunit of Stx1 (Fig. 1). As anticipated, both of these Tn10d-bla insertions were fused to the correct reading frame of stxA. These results reconfirm the utility of Tn10d-bla insertion mutagenesis for the identification of phage-encoded exported proteins.


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  		FIG. 1.   Tn10d-bla insertions in the H-19B genome. The 3' end of the stxAB operon is encoded on a 2.8-kb HindIII (H)-EcoRI (E) fragment (10). The orientation of the stxAB operon along with the locations of the Tn10d-bla insertions in H-19B-Ap1 and H-19B-Ap2 is shown.

The properties of MC4100 H-19B, MC4100 H-19B-Ap1, and MC4100 H-19B-Ap2 were compared. All three lysogens spontaneously produced approximately the same number of virions as measured by PFU per cell (Table 1). Also, virion production from all three lysogens was induced more than 4 orders of magnitude with mitomycin C (Table 1). The Tn10d-bla insertion in MC4100 H-19B-Ap1 and MC4100 H-19B-Ap2 resulted in the complete abrogation of detectable Vero cell cytotoxicity in cell-free supernatants of mitomycin C-induced cultures (data not shown). However, these insertions did not prevent production of the B subunit of Stx1 from MC4100 H-19B-Ap1 or MC4100 H-19B-Ap2 as detected by an enzyme-linked immunosorbent assay (1). Thus, MC4100 H-19B-Ap1 and MC4100 H-19B-Ap2 are Smr E. coli strains harboring Apr gene-marked detoxified H-19B prophages which, in vitro, produce numbers of infectious H-19B particles similar to those produced by MC4100 H-19B. We used these two Apr gene-marked H-19B lysogens to study the intraintestinal transmission of H-19B.

                              
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  		TABLE 1.   Virion production by Apr gene-marked H-19B lysogens

Intraintestinal transduction of phage H-19B. Oral administration of streptomycin to adult mice has been shown to facilitate the colonization of the murine large intestine with laboratory strains of E. coli (4). We used this model of intestinal colonization in streptomycin-treated mice to investigate whether MC4100 H-19B-Ap1 and MC4100 H-19B-Ap2 produce infectious virions within the intestine. Recovery of intestinally derived transductants of a recipient strain was used as a means to detect intraintestinal virion production.

Streptomycin (0.6 mg/ml) was added to water given to CD-1 mice for 48 h prior to the intragastric administration of MC4100 H-19B-Ap1 (Smr Apr LacZ-), the phage donor strain. Stools collected from mice immediately prior to administration of the phage donor strain were found to have no detectable Smr LacZ- CFU. Forty-five minutes after the administration of the phage donor strain, the mice were intragastrically inoculated with a differentially marked potential phage recipient strain, AK16 (MC4100 srl::Tn5), which is identifiable as Smr kanamycin-resistant (Knr) LacZ- CFU. Approximately 1 × 109 cells of the MC4100 H-19B-Ap1 lysogen and 2 × 109 cells of AK16 were inoculated per mouse. Individual stool samples (pellets) were collected on each of the four days following inoculation, homogenized in 1 ml of Luria broth, and then plated on L agar containing antibiotics to allow the determination of the number of donor CFU (Smr Apr LacZ-), recipient CFU (Smr Knr LacZ-), and transductant CFU (Smr Knr Apr LacZ-) in each pellet. Transductants (Apr colonies of MC4100 srl::Tn5) were recovered in stool samples on each of the four days following inoculation. Twenty-four hours postinoculation, there was approximately one transductant per 104 donor cells recovered in stool (Table 2). Each of 10 randomly picked Apr recipient colonies tested was found to produce StxB by an enzyme-linked immunosorbent assay (1). In addition, filtered supernatants from mitomycin C-induced cultures from each of these AK16 Apr transductant colonies was capable of transducing Apr to a new recipient strain. These results indicate that H-19B-Ap1 phage transduction accounted for the intestinal transmission of the Apr marker. There was a decrease in the frequency of transductants per recipients during the 4-day period when stools were tested (data not shown). At the end of this period the animals were sacrificed, and the frequency of transductants in cecal homogenates was found to be similar to the frequency of transductants in the stool homogenates.

                              
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  		TABLE 2.   Detection of intestinally derived transductants at 24 h

A similarly designed experiment was carried out with MC4100 H-19B-Ap2 as a donor strain in two mice. In this experiment, only 4 × 106 donor cells (more than 2 log units fewer donor cells than used in the previous experiment) were inoculated per mouse. Twenty-four hours later stool samples from both mice contained transductants at approximately the same frequency per donor cell as was observed when MC4100 H-19B-Ap1 was used as a donor (Table 2). Again all tested intestinally derived transductants produced StxB. The detection of H-19B-Apr transductants in stool samples and cecal homogenates demonstrates that infectious virions are produced within the host intestine and furthermore that these virions are capable of transducing other E. coli strains within the gastrointestinal tract.

Host environments may be the common site where new pathogenic strains evolve. Our demonstration that an E. coli H-19B lysogen produces infectious phage within the murine gastrointestinal tract suggests that the site of the emergence of the many Stx-producing E. coli serotypes and the Stx-producing non-E. coli genera may have been within the mammalian gastrointestinal tract. Similarly, a recent report by members of our group that Vibrio cholerae CTXphi lysogens produce infectious virions within the gastrointestinal tract (12) may suggest that new toxinogenic V. cholerae serotypes, such as V. cholerae O139, may arise through phage-mediated transduction of nontoxinogenic strains within the host gastrointestinal tract. Similar phage conversion events may occur on other mucosal surfaces as well. Pappenheimer and Murphy reported a case of corynephage conversion of a nontoxinogenic Corynebacterium diphtheriae strain to toxinogenicity that probably occurred within a woman's upper respiratory tract (17). It has been proposed that phage conversion within a nonimmune host provides an efficient mechanism for the rapid dissemination of phage-encoded virulence genes (3). It is possible that specific mammalian host signals induce bacterial gene transfer events, as has been described for the plant pathogen Agrobacterium tumefaciens (13).

In the present study, the antibiotic resistance gene-marked H-19B facilitated our ability to monitor intraintestinal phage production by lysogens. The bla-marked H-19B phage will also facilitate the study of the bacterial host range for this virus and the study of intestinal factors, such as diet, and therapeutic interventions, such as antibiotics, that may influence the rate of intestinal H-19B transduction. Our previous work indicates that SOS induction of Stx-converting bacteriophages exerts a regulatory effect on Stx production both by increasing the number of toxin gene copies and by the increased expression of a phage-encoded regulatory molecule (14). Future studies will address the question of whether intraintestinal Stx production and Stx-related disease require the in vivo induction of Stx-converting bacteriophages from lysogens.

    ACKNOWLEDGMENTS

We are grateful to the late H. Williams Smith for C600 H19B and to Carol Kumamoto for strain AK16. We thank Joe Newman for advice regarding the intestinal-colonization studies, Anne Kane and the NEMC GRASP Digestive Disease Center for preparing the microbiologic media for our studies, and A. Camilli for critical reading of the manuscript.

This work was supported by grants AI-42347 to M.K.W., AI-39067 to D.W.K.A., AI-16242 and HL-95007 to G.T.K., and P30DK-34928 for the NEMC GRASP Digestive Disease Center.

    FOOTNOTES

* Corresponding author. Mailing address: Division of Geographic Medicine and Infectious Diseases, NEMC 041, 750 Washington St., Boston, MA 02111. Phone: (617) 636-7618. Fax: (617) 636-5292. E-mail: matthew.waldor{at}es.nemc.org.

Editor:   J. T. Barbieri

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Infection and Immunity, September 1998, p. 4496-4498, Vol. 66, No. 9
0019-9567/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.


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