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Food Microbiology

Bacteriophages Isolated from Chicken Meat and the Horizontal Transfer of Antimicrobial Resistance Genes

Amira Shousha, Nattakarn Awaiwanont, Dmitrij Sofka, Frans J. M. Smulders, Peter Paulsen, Michael P. Szostak, Tom Humphrey, Friederike Hilbert
J. Björkroth, Editor
Amira Shousha
aInstitute of Meat Hygiene, Meat Technology and Food Science, University of Veterinary Medicine, Vienna, Austria
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Nattakarn Awaiwanont
aInstitute of Meat Hygiene, Meat Technology and Food Science, University of Veterinary Medicine, Vienna, Austria
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Dmitrij Sofka
aInstitute of Meat Hygiene, Meat Technology and Food Science, University of Veterinary Medicine, Vienna, Austria
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Frans J. M. Smulders
aInstitute of Meat Hygiene, Meat Technology and Food Science, University of Veterinary Medicine, Vienna, Austria
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Peter Paulsen
aInstitute of Meat Hygiene, Meat Technology and Food Science, University of Veterinary Medicine, Vienna, Austria
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Michael P. Szostak
bInstitute of Microbiology, University of Veterinary Medicine, Vienna, Austria
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Tom Humphrey
cMedical Microbiology and Infectious Diseases Group, College of Medicine, Swansea University, Swansea, Wales, United Kingdom
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Friederike Hilbert
aInstitute of Meat Hygiene, Meat Technology and Food Science, University of Veterinary Medicine, Vienna, Austria
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J. Björkroth
Roles: Editor
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DOI: 10.1128/AEM.00872-15
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    FIG 1

    Proportion of resistance-transducing phages among all isolated phages. Kanamycin resistance-transducing phages were detected the most often (n = 43 of 243 phages detected), followed by chloramphenicol (n = 8) and tetracycline (n = 4) resistance-transducing phages. Three phages were found to transduce kanamycin plus ampicillin resistance, and two phages transduced kanamycin plus chloramphenicol resistance. ϕCmr, ϕKmr, ϕTetr, ϕKmr Ampr, and ϕKmr Cmr, chloramphenicol, kanamycin, tetracycline, kanamycin and ampicillin, and kanamycin and chloramphenicol resistance-transducing phages, respectively.

Tables

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  • TABLE 1

    Primers and conditions for PCR of resistance genes

    Target genePrimer nameSequenceAnnealing temp (°C)PCR amplification product size (bp)Reference
    tet(A)tet(A)-f5′-GCTACATCCTGCTTGCCTTC-3′5721044
    tet(A)-r5′-CATAGATCGCCGTGAAGAGG-3′
    tet(B)tet(B)-f5′-TTGGTTAGGGGCAAGTTTTG-3′5765944
    tet(B)-r5′-GTAATGGGCCAATAACACCG-3′
    tet(C)tet(C)-f5′-CTTGAGAGCCTTCAACCCAG-3′5541844
    tet(C)-r5′-ATGGTCGTCATCTACCTGCC-3′
    aphA1aphA-1a-f5′-AACGTCTTGCTCGAGGCCGCG-3′6567045
    aphA-1a-r5′-GGCAAGATCCTGGTATCGGTCTGC-3′
    blaCMYblaCMY-f5′-TGGCCGTTGCCGTTATCTAC-3′5587046
    blaCMY-r5′-CCCGTTTTATGCACCCATGA-3′
    blaIMPblaIMP-f5′-GAATAGAGTGGATTAATTCTC-3′5523247
    blaIMP-r5′-GGTTTAAYAAAACAACCACC-3′
    blaOXAblaOXA-2-f5′-CAAGCCAAAGGCACGATAGTTG-3′5656147
    blaOXA-2-r5′-CTCAACCCATCCTACCCACC-3′
    blaPSEblaPSE-f5′-TGCTTCGCAACTATGACTAC-3′5543846
    blaPSE-r5′-AGCCTGTGTTTGAGCTAGAT-3′
    blaTEM-1blaTEM-1-f5′-CAGCGGTAAGATCCTTGAGA-3′5564346
    blaTEM-1-r5′-ACTCCCCGTCGTGTAGATAA-3′
    catIcatI-f5′-AGTTGCTCAATGTACCTATAACC-3′5054748
    catI-r5′-TTGTAATTCATTAAGCATTCTGCC-3′
    floRfloR-f5′-CGCCGTCATTCCTCACCTTC-3′5021548
    floR-r5′-GATCACGGGCCACGCTGTGTC-3′
  • TABLE 2

    Numbers of chicken meat samples by type of resistant E. coli isolate

    TABLE 2
    • a Ampr, Cmr, Kmr, and Tetr, ampicillin, chloramphenicol, kanamycin, and tetracycline resistant, respectively.

  • TABLE 3

    Lysotypes of antimicrobial resistance-transducing phages

    LTa patternLysis of the indicated E. coli strainsPhage(s) transducing resistance to the indicated antimicrobialb
    ATCC 13706JM109W3110MC1061DH5αKanamycinChloramphenicolAmpicillinTetracycline
    LT1++++++++++++−ϕE2b, ϕE5a, ϕE5b, ϕE5c, ϕE5d, ϕE5eϕE6b, ϕE16e, ϕE30eϕE5c, ϕE9bϕE10c, ϕE10d
    ϕE7a, ϕE7b, ϕE7c, ϕE7d, ϕE7e, ϕE9bϕE49dϕE13dϕE15d, ϕE40e
    ϕE9d, ϕE12b, ϕE12e, ϕE13a, ϕE13b
    ϕE13c, ϕE13d, ϕE13e, ϕE16a, ϕE16d
    ϕE19b, ϕE19c, ϕE22c, ϕE23b, ϕE23c
    ϕE28a, ϕE28b, ϕE28c, ϕE28d, ϕE30a, ϕE49a
    LT2+++++++++−ϕE2cϕE43e
    LT3+++++++++−ϕE2d
    LT4++++++++−ϕE2e
    LT5+++++++++−ϕE6a, ϕE19a
    LT6++++++++++−ϕE6d, ϕE9c, ϕE27c
    LT7+++++++−ϕE9a, ϕE15c
    LT8++++++++++−ϕE12c, ϕE12d, ϕE34eϕE12c
    LT9+++++++−ϕE19e
    LT10++++++++++−ϕE34aϕE34a
    LT11++++++++−ϕE35d
    LT12+++++++++++−ϕE35e
    LT13+++−−−−ϕE39d
    • ↵a LT, lysotype.

    • ↵b The phage designations indicate the chicken meat sample (E) number (indicated by Arabic numerals) and the phage isolate number (indicated by lowercase letters); for example, ϕE5a represents the first phage isolate from chicken meat sample number 5.

  • TABLE 4

    Association between isolation of antimicrobial-resistant E. coli and resistance-transducing phages from the same chicken meat sample

    Antimicrobial resistanceaNo. of samples positive for:P
    E. coliTransducing phageBoth
    Ampr44331.0000
    Cmr18910.1304
    Kmr2217120.0148b
    Tetr40320.4959
    • ↵a Ampr, Cmr, Kmr, and Tetr, ampicillin, chloramphenicol, kanamycin, and tetracycline resistant, respectively.

    • ↵b Statistically significant relation between isolation of antimicrobial-resistant E. coli and resistance-transducing phages.

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Bacteriophages Isolated from Chicken Meat and the Horizontal Transfer of Antimicrobial Resistance Genes
Amira Shousha, Nattakarn Awaiwanont, Dmitrij Sofka, Frans J. M. Smulders, Peter Paulsen, Michael P. Szostak, Tom Humphrey, Friederike Hilbert
Applied and Environmental Microbiology Jun 2015, 81 (14) 4600-4606; DOI: 10.1128/AEM.00872-15

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Bacteriophages Isolated from Chicken Meat and the Horizontal Transfer of Antimicrobial Resistance Genes
Amira Shousha, Nattakarn Awaiwanont, Dmitrij Sofka, Frans J. M. Smulders, Peter Paulsen, Michael P. Szostak, Tom Humphrey, Friederike Hilbert
Applied and Environmental Microbiology Jun 2015, 81 (14) 4600-4606; DOI: 10.1128/AEM.00872-15
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