title: Heterogeneity in Induction Level, Infection Ability, and Morphology of Shiga Toxin-Encoding Phages (Stx Phages) from Dairy and Human Shiga Toxin-Producing Escherichia coli O26:H11 Isolates.
abstract: Shiga toxin (Stx)-producing Escherichia coli (STEC) bacteria are foodborne pathogens responsible for diarrhea and hemolytic-uremic syndrome (HUS). Shiga toxin, the main STEC virulence factor, is encoded by the stx gene located in the genome of a bacteriophage inserted into the bacterial chromosome. The O26:H11 serotype is considered to be the second-most-significant HUS-causing serotype worldwide after O157:H7. STEC O26:H11 bacteria and their stx-negative counterparts have been detected in dairy products. They may convert from the one form to the other by loss or acquisition of Stx phages, potentially confounding food microbiological diagnostic methods based on stx gene detection. Here we investigated the diversity and mobility of Stx phages from human and dairy STEC O26:H11 strains. Evaluation of their rate of in vitro induction, occurring either spontaneously or in the presence of mitomycin C, showed that the Stx2 phages were more inducible overall than Stx1 phages. However, no correlation was found between the Stx phage levels produced and the origin of the strains tested or the phage insertion sites. Morphological analysis by electron microscopy showed that Stx phages from STEC O26:H11 displayed various shapes that were unrelated to Stx1 or Stx2 types. Finally, the levels of sensitivity of stx-negative E. coli O26:H11 to six Stx phages differed among the 17 strains tested and our attempts to convert them into STEC were unsuccessful, indicating that their lysogenization was a rare event.
authors.affiliation: Université Paris-Est, Anses, Laboratory for Food Safety, Maisons-Alfort, France.|Actalia Produits Laitiers, Laboratoire de Microbiologie d'Intérêt Laitier, La Roche sur Foron, France.
authors.forename: Ludivine
authors.initials: L
authors.lastname: Bonanno
authors.affiliation: INRA, UMR1319, Micalis, Jouy en Josas, France.
authors.forename: Marie-Agnès
authors.initials: MA
authors.lastname: Petit
authors.affiliation: Université de Lyon, VetAgro Sup, Laboratoire d'Études des Microorganismes Alimentaires Pathogènes/Laboratoire National de Référence pour les Escherichia coli y Compris les E. coli Producteurs de Shiga-Toxines, Marcy l'Etoile, France.|Université de Lyon, UMR 5557 Ecologie Microbienne, Université Lyon 1, CNRS, VetAgro Sup, Equipe Bactéries Pathogènes et Opportunistes, Villeurbanne, France.
authors.forename: Estelle
authors.initials: E
authors.lastname: Loukiadis
authors.affiliation: Actalia Produits Laitiers, Laboratoire de Microbiologie d'Intérêt Laitier, La Roche sur Foron, France.
authors.forename: Valérie
authors.initials: V
authors.lastname: Michel
authors.affiliation: Université Paris-Est, Anses, Laboratory for Food Safety, Maisons-Alfort, France frederic.auvray@anses.fr.
authors.forename: Frédéric
authors.initials: F
authors.lastname: Auvray
mesh_terms: D001435:Bacteriophages / Q000235:genetics / Q000254:growth & development / Q000302:isolation & purification* / Q000378:metabolism; D003611:Dairy Products / Q000382:microbiology*; D004927:Escherichia coli Infections / Q000382:microbiology*; D006801:Humans; D008242:Lysogeny; D010802:Phylogeny; D022621:Shiga Toxin / Q000378:metabolism; D054323:Shiga-Toxigenic Escherichia coli / Q000235:genetics / Q000302:isolation & purification / Q000472:pathogenicity* / Q000821:virology*; D014774:Virulence
chemical_list: D022621:Shiga Toxin
references.citation: Infect Immun. 1992 Aug;60(8):3464-7
references.pmid: 1639518
references.citation: J Clin Microbiol. 2015 Feb;53(2):486-92
references.pmid: 25428148
references.citation: Appl Environ Microbiol. 2015 Jun;81(11):3712-21
references.pmid: 25819955
references.citation: Environ Microbiol. 2004 Jul;6(7):716-25
references.pmid: 15186350
references.citation: Lancet. 2005 Mar 19-25;365(9464):1073-86
references.pmid: 15781103
references.citation: Foodborne Pathog Dis. 2005 Winter;2(4):357-60
references.pmid: 16366859
references.citation: Emerg Infect Dis. 2000 Sep-Oct;6(5):458-65
references.pmid: 10998375
references.citation: Int J Food Microbiol. 2011 Nov 15;151(1):44-51
references.pmid: 21878400
references.citation: Lett Appl Microbiol. 2011 May;52(5):538-45
references.pmid: 21362002
references.citation: Lancet. 1983 Mar 19;1(8325):619-20
references.pmid: 6131302
references.citation: Appl Environ Microbiol. 2008 Aug;74(16):5113-20
references.pmid: 18586961
references.citation: Math Biosci. 1999 Mar 15;157(1-2):269-86
references.pmid: 10194933
references.citation: Appl Environ Microbiol. 2003 Feb;69(2):1059-66
references.pmid: 12571029
references.citation: Int J Food Microbiol. 2013 Mar 15;162(2):190-212
references.pmid: 22939912
references.citation: J Gen Microbiol. 1983 Oct;129(10):3121-37
references.pmid: 6418852
references.citation: Appl Environ Microbiol. 2011 May;77(10):3536-40
references.pmid: 21441341
references.citation: Appl Environ Microbiol. 2012 Jun;78(12):4065-73
references.pmid: 22504816
references.citation: J Dairy Sci. 2005 Feb;88(2):450-65
references.pmid: 15653509
references.citation: Mol Microbiol. 1998 Jun;28(6):1255-67
references.pmid: 9680214
references.citation: Appl Environ Microbiol. 2007 May;73(10):3144-50
references.pmid: 17400784
references.citation: Methods Mol Biol. 2009;501:69-76
references.pmid: 19066811
references.citation: J Infect Dis. 2005 Oct 15;192(8):1422-9
references.pmid: 16170761
references.citation: J Clin Microbiol. 2000 Jun;38(6):2134-40
references.pmid: 10834966
references.citation: Appl Environ Microbiol. 2005 Mar;71(3):1155-62
references.pmid: 15746313
references.citation: Res Microbiol. 2014 Dec;165(10):803-12
references.pmid: 25463385
references.citation: Appl Environ Microbiol. 1999 Sep;65(9):3855-61
references.pmid: 10473386
references.citation: J Appl Microbiol. 2010 Nov;109(5):1696-705
references.pmid: 20618885
references.citation: Microbiology (Reading). 2000 May;146 ( Pt 5):1085-1090
references.pmid: 10832635
references.citation: Science. 1984 Nov 9;226(4675):694-6
references.pmid: 6387911
references.citation: J Clin Microbiol. 2012 Sep;50(9):2951-63
references.pmid: 22760050
references.citation: Appl Environ Microbiol. 2009 Jan;75(2):329-36
references.pmid: 19011056
references.citation: Int J Food Microbiol. 2014 Aug 1;184:45-9
references.pmid: 24495690
references.citation: Infect Immun. 1998 Sep;66(9):4496-8
references.pmid: 9712806
references.citation: Euro Surveill. 2007 May 31;12(5):E070531.4
references.pmid: 17868586
references.citation: Res Microbiol. 2001 Oct;152(8):687-95
references.pmid: 11686382
references.citation: J Clin Microbiol. 1999 Mar;37(3):497-503
references.pmid: 9986802
references.citation: J Appl Microbiol. 2010 Mar;108(3):1105-1114
references.pmid: 20070447
references.citation: Mol Microbiol. 2002 May;44(4):957-70
references.pmid: 12010491
references.citation: Plasmid. 2012 May;67(3):227-35
references.pmid: 22186359
references.citation: Lancet Infect Dis. 2011 Sep;11(9):671-6
references.pmid: 21703928
references.citation: EFSA J. 2018 Dec 12;16(12):e05500
references.pmid: 32625785
references.citation: Microb Pathog. 2009 Dec;47(6):289-98
references.pmid: 19761828
references.citation: Microbiology (Reading). 2004 Sep;150(Pt 9):2959-2971
references.pmid: 15347754
references.citation: Appl Environ Microbiol. 2009 Mar;75(6):1764-8
references.pmid: 19168651
references.citation: Int J Med Microbiol. 2004 Sep;294(2-3):115-21
references.pmid: 15493821
references.citation: Infect Immun. 2003 Aug;71(8):4554-62
references.pmid: 12874335
references.citation: Front Cell Infect Microbiol. 2014 Jun 20;4:80
references.pmid: 24999453
references.citation: Semin Thromb Hemost. 2010 Sep;36(6):586-93
references.pmid: 20865635
references.citation: Cell. 1982 May;29(1):11-22
references.pmid: 7049397