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Yersinia enterocolitica-specific infection by bacteriophages TG1 and φR1-RT is dependent on temperature-regulated expression of the phage host receptor OmpF

Leon-Velarde, Carlos G.; Happonen, Lotta LU ; Pajunen, Maria; Leskinen, Katarzyna; Kropinski, Andrew M.; Mattinen, Laura; Rajtor, Monika; Zur, Joanna; Smith, Darren and Chen, Shu, et al. (2016) In Applied and Environmental Microbiology 82(17). p.5340-5353
Abstract

Bacteriophages present huge potential both as a resource for developing novel tools for bacterial diagnostics and for use in phage therapy. This potential is also valid for bacteriophages specific for Yersinia enterocolitica. To increase our knowledge of Y. enterocolitica- specific phages, we characterized two novel yersiniophages. The genomes of the bacteriophages vB_YenM_TG1 (TG1) and vB_YenM_φR1-RT (φR1-RT), isolated from pig manure in Canada and from sewage in Finland, consist of linear double-stranded DNA of 162,101 and 168,809 bp, respectively. Their genomes comprise 262 putative coding sequences and 4 tRNA genes and share 91% overall nucleotide identity. Based on phylogenetic analyses of their whole-genome sequences and large... (More)

Bacteriophages present huge potential both as a resource for developing novel tools for bacterial diagnostics and for use in phage therapy. This potential is also valid for bacteriophages specific for Yersinia enterocolitica. To increase our knowledge of Y. enterocolitica- specific phages, we characterized two novel yersiniophages. The genomes of the bacteriophages vB_YenM_TG1 (TG1) and vB_YenM_φR1-RT (φR1-RT), isolated from pig manure in Canada and from sewage in Finland, consist of linear double-stranded DNA of 162,101 and 168,809 bp, respectively. Their genomes comprise 262 putative coding sequences and 4 tRNA genes and share 91% overall nucleotide identity. Based on phylogenetic analyses of their whole-genome sequences and large terminase subunit protein sequences, a genus named Tg1virus within the family Myoviridae is proposed, with TG1 and φR1-RT (R1RT in the ICTV database) as member species. These bacteriophages exhibit a host range restricted to Y. enterocolitica and display lytic activity against the epidemiologically significant serotypes O:3, O:5,27, and O:9 at and below 25°C. Adsorption analyses of lipopolysaccharide (LPS) and OmpF mutants demonstrate that these phages use both the LPS inner core heptosyl residues and the outer membrane protein OmpF as phage receptors. Based on RNA sequencing and quantitative proteomics, we also demonstrate that temperature-dependent infection is due to strong repression of OmpF at 37°C. In addition, φR1-RT was shown to be able to enter into a pseudolysogenic state. Together, this work provides further insight into phage-host cell interactions by highlighting the importance of understanding underlying factors which may affect the abundance of phage host receptors on the cell surface.

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Applied and Environmental Microbiology
volume
82
issue
17
pages
14 pages
publisher
American Society for Microbiology
external identifiers
  • scopus:84987876550
  • wos:000381500700028
ISSN
0099-2240
DOI
10.1128/AEM.01594-16
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English
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yes
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53773fd4-1274-4e73-8415-df7efec4436b
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2017-02-07 11:45:31
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2017-10-01 05:30:00
@article{53773fd4-1274-4e73-8415-df7efec4436b,
  abstract     = {<p>Bacteriophages present huge potential both as a resource for developing novel tools for bacterial diagnostics and for use in phage therapy. This potential is also valid for bacteriophages specific for Yersinia enterocolitica. To increase our knowledge of Y. enterocolitica- specific phages, we characterized two novel yersiniophages. The genomes of the bacteriophages vB_YenM_TG1 (TG1) and vB_YenM_φR1-RT (φR1-RT), isolated from pig manure in Canada and from sewage in Finland, consist of linear double-stranded DNA of 162,101 and 168,809 bp, respectively. Their genomes comprise 262 putative coding sequences and 4 tRNA genes and share 91% overall nucleotide identity. Based on phylogenetic analyses of their whole-genome sequences and large terminase subunit protein sequences, a genus named Tg1virus within the family Myoviridae is proposed, with TG1 and φR1-RT (R1RT in the ICTV database) as member species. These bacteriophages exhibit a host range restricted to Y. enterocolitica and display lytic activity against the epidemiologically significant serotypes O:3, O:5,27, and O:9 at and below 25°C. Adsorption analyses of lipopolysaccharide (LPS) and OmpF mutants demonstrate that these phages use both the LPS inner core heptosyl residues and the outer membrane protein OmpF as phage receptors. Based on RNA sequencing and quantitative proteomics, we also demonstrate that temperature-dependent infection is due to strong repression of OmpF at 37°C. In addition, φR1-RT was shown to be able to enter into a pseudolysogenic state. Together, this work provides further insight into phage-host cell interactions by highlighting the importance of understanding underlying factors which may affect the abundance of phage host receptors on the cell surface.</p>},
  author       = {Leon-Velarde, Carlos G. and Happonen, Lotta and Pajunen, Maria and Leskinen, Katarzyna and Kropinski, Andrew M. and Mattinen, Laura and Rajtor, Monika and Zur, Joanna and Smith, Darren and Chen, Shu and Nawaz, Ayesha and Johnson, Roger P. and Odumeru, Joseph A. and Griffiths, Mansel W. and Skurnik, Mikael},
  issn         = {0099-2240},
  language     = {eng},
  number       = {17},
  pages        = {5340--5353},
  publisher    = {American Society for Microbiology},
  series       = {Applied and Environmental Microbiology},
  title        = {Yersinia enterocolitica-specific infection by bacteriophages TG1 and φR1-RT is dependent on temperature-regulated expression of the phage host receptor OmpF},
  url          = {http://dx.doi.org/10.1128/AEM.01594-16},
  volume       = {82},
  year         = {2016},
}