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Journal of Bacteriology, October 2007, p. 7223-7233, Vol. 189, No. 20
0021-9193/07/$08.00+0     doi:10.1128/JB.00824-07
Copyright © 2007, American Society for Microbiology. All Rights Reserved.

Short-Tailed Stx Phages Exploit the Conserved YaeT Protein To Disseminate Shiga Toxin Genes among Enterobacteria{triangledown}

Darren L. Smith, Chloë E. James,{dagger} Martin J. Sergeant,{ddagger} Yan Yaxian,§ Jon R. Saunders, Alan J. McCarthy, and Heather E. Allison*

Microbiology Research Group, BioSciences Building, School of Biological Sciences, University of Liverpool, Crown Street, Liverpool, Merseyside, L69 7ZB United Kingdom

Received 25 May 2007/ Accepted 17 July 2007

Infection of Escherichia coli by Shiga toxin-encoding bacteriophages (Stx phages) was the pivotal event in the evolution of the deadly Shiga toxin-encoding E. coli (STEC), of which serotype O157:H7 is the most notorious. The number of different bacterial species and strains reported to produce Shiga toxin is now more than 500, since the first reported STEC infection outbreak in 1982. Clearly, Stx phages are spreading rapidly, but the underlying mechanism for this dissemination has not been explained. Here we show that an essential and highly conserved gene product, YaeT, which has an essential role in the insertion of proteins in the gram-negative bacterial outer membrane, is the surface molecule recognized by the majority (ca. 70%) of Stx phages via conserved tail spike proteins associated with a short-tailed morphology. The yaeT gene was initially identified through complementation, and its role was confirmed in phage binding assays with and without anti-YaeT antiserum. Heterologous cloning of E. coli yaeT to enable Stx phage adsorption to Erwinia carotovora and the phage adsorption patterns of bacterial species possessing natural yaeT variants further supported this conclusion. The use of an essential and highly conserved protein by the majority of Stx phages is a strategy that has enabled and promoted the rapid spread of shigatoxigenic potential throughout multiple E. coli serogroups and related bacterial species. Infection of commensal bacteria in the mammalian gut has been shown to amplify Shiga toxin production in vivo, and the data from this study provide a platform for the development of a therapeutic strategy to limit this YaeT-mediated infection of the commensal flora.

* Corresponding author. Mailing address: Microbiology Research Group, BioSciences Building, School of Biological Sciences, University of Liverpool, Crown Street, Liverpool, Merseyside, L69 7ZB United Kingdom. Phone: 44 (0)151 7954571. Fax: 44 (0)151 7954410. E-mail: hallison{at}liverpool.ac.uk

{triangledown} Published ahead of print on 10 August 2007.

{dagger} Present address: Enveloppe Bacterienne, Permeabilite et Antibiotiques, Faculte de Medecine, 27 Bd Jean Moulin, 13385 Marseille Cedex 05, France.

{ddagger} Present address: Warwick HRI Wellesbourne, Warwick, Warwickshire, CV35 9EF United Kingdom.

§ Present address: School of Agriculture, Shanghai Jiao Tong University, Shanghai, 201101, Peoples Republic of China.

Journal of Bacteriology, October 2007, p. 7223-7233, Vol. 189, No. 20
0021-9193/07/$08.00+0     doi:10.1128/JB.00824-07
Copyright © 2007, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Garcia-Aljaro, C., Muniesa, M., Jofre, J., Blanch, A. R. (2009). Genotypic and Phenotypic Diversity among Induced, stx2-Carrying Bacteriophages from Environmental Escherichia coli Strains. Appl. Environ. Microbiol. 75: 329-336 [Abstract] [Full Text]  
  • Smith, D. L., Wareing, B. M., Fogg, P. C. M., Riley, L. M., Spencer, M., Cox, M. J., Saunders, J. R., McCarthy, A. J., Allison, H. E. (2007). Multilocus Characterization Scheme for Shiga Toxin-Encoding Bacteriophages. Appl. Environ. Microbiol. 73: 8032-8040 [Abstract] [Full Text]  


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