title: Yersinia enterocolitica-Specific Infection by Bacteriophages TG1 and ϕR1-RT Is Dependent on Temperature-Regulated Expression of the Phage Host Receptor OmpF.
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 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.
  
  
  
  Only a small number of bacteriophages infecting Y. enterocolitica, the predominant causative agent of yersiniosis, have been previously described. Here, two newly isolated Y. enterocolitica phages were studied in detail, with the aim of elucidating the host cell receptors required for infection. Our research further expands the repertoire of phages available for consideration as potential antimicrobial agents or as diagnostic tools for this important bacterial pathogen.
authors.affiliation: Laboratory Services Division, University of Guelph, Guelph, Ontario, Canada Department of Food Science, University of Guelph, Guelph, Ontario, Canada.
authors.forename: Carlos G
authors.identifier: 0000-0002-3605-521X
authors.initials: CG
authors.lastname: Leon-Velarde
authors.affiliation: Department of Clinical Sciences Lund, Infection Medicine, Lund University, Lund, Sweden Institute of Biotechnology and Department of Biosciences, University of Helsinki, Helsinki, Finland.
authors.forename: Lotta
authors.initials: L
authors.lastname: Happonen
authors.affiliation: Department of Bacteriology and Immunology, Medicum, and Research Programs Unit, Immunobiology, University of Helsinki, Helsinki, Finland.
authors.forename: Maria
authors.initials: M
authors.lastname: Pajunen
authors.affiliation: Department of Bacteriology and Immunology, Medicum, and Research Programs Unit, Immunobiology, University of Helsinki, Helsinki, Finland.
authors.forename: Katarzyna
authors.initials: K
authors.lastname: Leskinen
authors.affiliation: Department of Pathobiology, University of Guelph, Guelph, Ontario, Canada Department of Molecular and Cellular Biology, University of Guelph, Guelph, Ontario, Canada.
authors.forename: Andrew M
authors.initials: AM
authors.lastname: Kropinski
authors.affiliation: Department of Bacteriology and Immunology, Medicum, and Research Programs Unit, Immunobiology, University of Helsinki, Helsinki, Finland.
authors.forename: Laura
authors.initials: L
authors.lastname: Mattinen
authors.affiliation: Department of Bacteriology and Immunology, Medicum, and Research Programs Unit, Immunobiology, University of Helsinki, Helsinki, Finland.
authors.forename: Monika
authors.initials: M
authors.lastname: Rajtor
authors.affiliation: Department of Bacteriology and Immunology, Medicum, and Research Programs Unit, Immunobiology, University of Helsinki, Helsinki, Finland.
authors.forename: Joanna
authors.initials: J
authors.lastname: Zur
authors.affiliation: Applied Sciences, University of Northumbria, Newcastle upon Tyne, United Kingdom.
authors.forename: Darren
authors.initials: D
authors.lastname: Smith
authors.affiliation: Laboratory Services Division, University of Guelph, Guelph, Ontario, Canada.
authors.forename: Shu
authors.initials: S
authors.lastname: Chen
authors.affiliation: Department of Bacteriology and Immunology, Medicum, and Research Programs Unit, Immunobiology, University of Helsinki, Helsinki, Finland.
authors.forename: Ayesha
authors.initials: A
authors.lastname: Nawaz
authors.affiliation: National Microbiology Laboratory at Guelph, Public Health Agency of Canada, Guelph, Ontario, Canada.
authors.forename: Roger P
authors.initials: RP
authors.lastname: Johnson
authors.affiliation: Department of Food Science, University of Guelph, Guelph, Ontario, Canada.
authors.forename: Joseph A
authors.initials: JA
authors.lastname: Odumeru
authors.affiliation: Canadian Research Institute for Food Safety, University of Guelph, Guelph, Ontario, Canada Department of Food Science, University of Guelph, Guelph, Ontario, Canada.
authors.forename: Mansel W
authors.initials: MW
authors.lastname: Griffiths
authors.affiliation: Department of Bacteriology and Immunology, Medicum, and Research Programs Unit, Immunobiology, University of Helsinki, Helsinki, Finland Division of Clinical Microbiology, Helsinki University Hospital, HUSLAB, Helsinki, Finland mikael.skurnik@helsinki.fi.
authors.forename: Mikael
authors.identifier: 0000-0001-8791-9260
authors.initials: M
authors.lastname: Skurnik
mesh_terms: D001426:Bacterial Proteins / Q000235:genetics / Q000378:metabolism*; D001435:Bacteriophages / Q000145:classification / Q000235:genetics / Q000302:isolation & purification / Q000502:physiology*; D016679:Genome, Viral; D058507:Host Specificity; D006801:Humans; D010802:Phylogeny; D018272:Porins / Q000235:genetics / Q000378:metabolism*; D011991:Receptors, Virus / Q000235:genetics / Q000378:metabolism*; D013696:Temperature; D014779:Virus Replication; D015009:Yersinia Infections / Q000382:microbiology; D015008:Yersinia enterocolitica / Q000235:genetics / Q000378:metabolism / Q000821:virology*
chemical_list: D001426:Bacterial Proteins; C109237:OmpF protein; D018272:Porins; D011991:Receptors, Virus