Current Microbiology

, Volume 75, Issue 5, pp 611–619 | Cite as

Bacteriophages as Biological Control Agents of Enteric Bacteria Contaminating Edible Oysters

  • Tuan Son Le
  • Paul C. Southgate
  • Wayne O’Connor
  • Sue Poole
  • D. Ipek Kurtbӧke
Article

Abstract

Bacterial contamination on seafood resulting from unhygienic food-handling practices causes foodborne diseases and significant revenue losses. Moreover, control measures are complicated by a high prevalence of antibiotic-resistant bacteria. Alternative measures such as the phage therapy, therefore, is considered as an environmental and consumer-friendly biological control strategy for controlling such bacterial contamination. In this study, we determined the effectiveness of a bacteriophage cocktail in controlling E. coli strains [JM 109, ATCC 13706 and the, extended spectrum beta-lactamase resistant strain (ATCC BAA 196)] and S. enterica subsp. enterica (ATCC 13311) as single and combined contaminants of the edible oysters. Five different E. coli-specific phages (belonging to the Siphoviridae family) and a Salmonella phage (belonging to the Tectiviridae family) were successfully isolated from sewage water samples taken from a local sewage treatment plan in the Sunshine Coast region of Australia. Phage treatments applied to the pathogens when they were presented on the oysters as either single or combined hosts, resulted in significant decrease of the number of these bacteria on edible oysters. Results obtained indicated that bacteriophages could have beneficial applications in oyster-processing plants in controlling pathogenic bacterial infestations. This study thus contributes towards ongoing international efforts into the effective use of bacteriophages for biological control purposes.

Notes

Acknowledgements

Tuan Son Le gratefully acknowledge MOET-VIED/USC PhD scholarship. Authors thank Mr. Daniel Shelley (University of the Sunshine Coast, Australia) for the technical support provided with the TEM micrographs. Authors thank Dr. Nguyen Hong Nguyen (University of the Sunshine Coast, Australia) for advice on statistical analysis.

Compliance with Ethical Standards

Conflict of interest

The authors declare no conflict of interest.

Supplementary material

284_2017_1424_MOESM1_ESM.docx (22 kb)
Supplementary material 1 (DOCX 22 KB)
284_2017_1424_MOESM2_ESM.docx (23 kb)
Supplementary material 2 (DOCX 23 KB)
284_2017_1424_MOESM3_ESM.docx (14 kb)
Supplementary material 3 (DOCX 13 KB)
284_2017_1424_MOESM4_ESM.docx (15 kb)
Supplementary material 4 (DOCX 15 KB)
284_2017_1424_MOESM5_ESM.docx (15 kb)
Supplementary material 5 (DOCX 14 KB)

References

  1. 1.
    Ackermann H-W, Nguyen T (1983) Sewage coliphages studied by electron microscopy. Appl Environ Microbiol 45(3):1049–1059PubMedPubMedCentralGoogle Scholar
  2. 2.
    Amarillas L, Chaidez C, González-Robles A, Lugo-Melchor Y, León-Félix J (2016) Characterization of novel bacteriophage phiC119 capable of lysing multidrug-resistant Shiga toxin-producing Escherichia coli O157: H7. PeerJ 4:e2423CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Bean NH, Goulding JS, Lao C, Angulo FJ (1996) Surveillance for foodborne-disease outbreaks–United States, 1988–1992. MMWR CDC surveillance summaries: morbidity and mortality weekly report CDC surveillance summaries. 45 (5):1–66Google Scholar
  4. 4.
    Bradley S, Anderson D, Jones L (1961) Phylogeny of actinomycetes as revealed by susceptibility to actinophage. Dev Ind Microbiol 2:223–237Google Scholar
  5. 5.
    Carrasco E, Morales-Rueda A, García-Gimeno RM (2012) Cross-contamination and recontamination by Salmonella in foods: a review. Food Res Int 45(2):545–556CrossRefGoogle Scholar
  6. 6.
    Chan BK, Abedon ST, Loc-Carrillo C (2013) Phage cocktails and the future of phage therapy. Future Microbiol 8(6):769–783CrossRefPubMedGoogle Scholar
  7. 7.
    Croci L, Suffredini E (2002) Microbiological risk associated with seafood consumption. Annali dell’Istituto superiore di sanita 39(1):35–45Google Scholar
  8. 8.
    Defoirdt T, Boon N, Sorgeloos P, Verstraete W, Bossier P (2007) Alternatives to antibiotics to control bacterial infections: luminescent vibriosis in aquaculture as an example. Trends Biotechnol 25(10):472–479CrossRefPubMedGoogle Scholar
  9. 9.
    Duran GM, Marshall DL (2005) Ready-to-eat shrimp as an international vehicle of antibiotic-resistant bacteria. J Food Protect 68(11):2395–2401CrossRefGoogle Scholar
  10. 10.
    Gunathilaka GU (2014) Characterization of bacteriophages from environmental water samples and the potential of bacteriophages tailspike proteins (tsp) in bacteria detection. Wayne State University Theses 300Google Scholar
  11. 11.
    Hatha AM, Maqbool T, Kumar SS (2003) Microbial quality of shrimp products of export trade produced from aquacultured shrimp. Int J Food Microbiol 82(3):213–221CrossRefGoogle Scholar
  12. 12.
    Hudson J (2011) Minimum growth temperatures of foodborne pathogens and recommended chiller temperatures. Client Report FW1104 A report for MAF Food Safety ESRGoogle Scholar
  13. 13.
    Hudson JA, Billington C, Cornelius A, Wilson T, On S, Premaratne A, King N (2013) Use of a bacteriophage to inactivate Escherichia coli O157: H7 on beef. Food Microbiol 36(1):14–21CrossRefPubMedGoogle Scholar
  14. 14.
    Jain S, Chen L, Dechet A, Hertz AT, Brus DL, Hanley K, Wilson B, Frank J, Greene KD, Parsons M (2008) An outbreak of enterotoxigenic Escherichia coli associated with sushi restaurants in Nevada, 2004. Clin Infect Dis 47(1):1–7CrossRefPubMedGoogle Scholar
  15. 15.
    Jan A, Bhat K, Bhat S, Mir M, Bhat M, Imtiyaz A, Rather J (2013) Surface sterilization method for reducing microbial contamination of field grown strawberry explants intended for in vitro culture. Afr J Biotechnol 12:(39)Google Scholar
  16. 16.
    Jun JW, Kim JH, Shin SP, Han JE, Chai JY, Park SC (2013) Protective effects of the Aeromonas phages pAh1-C and pAh6-C against mass mortality of the cyprinid loach (Misgurnus anguillicaudatus) caused by Aeromonas hydrophila. Aquaculture 416:289–295CrossRefGoogle Scholar
  17. 17.
    Kim E-j, Kwak S (2016) Virulence Factors and Stability of Coliphages Specific to Escherichia coli O157: H7 and to Various E. coli Infection. J Microbiol Biotechnol 26(12):2060–2065CrossRefPubMedGoogle Scholar
  18. 18.
    Kulikov EE, Golomidova AK, Letarova MA, Kostryukova ES, Zelenin AS, Prokhorov NS, Letarov AV (2014) Genomic sequencing and biological characteristics of a novel Escherichia coli bacteriophage 9 g, a putative representative of a new Siphoviridae genus. Viruses 6(12):5077–5092CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Kurtböke DI, Palk A, Marker A, Neuman C, Moss L, Streeter K, Katouli M (2016) Isolation and characterization of Enterobacteriaceae species infesting post-harvest strawberries and their biological control using bacteriophages. Appl Microbiol Biotechnol 100(19):8593–8606CrossRefPubMedGoogle Scholar
  20. 20.
    Leverentz B, Conway WS, Alavidze Z, Janisiewicz WJ, Fuchs Y, Camp MJ, Chighladze E, Sulakvelidze A (2001) Examination of bacteriophage as a biocontrol method for Salmonella on fresh-cut fruit: a model study. J Food Protect 64(8):1116–1121CrossRefGoogle Scholar
  21. 21.
    Li L, Zhang Z (2014) Isolation and characterization of a virulent bacteriophage SPW specific for Staphylococcus aureus isolated from bovine mastitis of lactating dairy cattle. Mol Biol Rep 41(9):5829–5838CrossRefPubMedGoogle Scholar
  22. 22.
    Lucas JS, Southgate PC (2012) Aquaculture: farming aquatic animals and plants, 2nd Edn. Blackwell Publishing Ltd, Oxford. 541–566.CrossRefGoogle Scholar
  23. 23.
    Matyar F, Kaya A, Dinçer S (2008) Antibacterial agents and heavy metal resistance in Gram-negative bacteria isolated from seawater, shrimp and sediment in Iskenderun Bay, Turkey. Sci Total Environ 407(1):279–285CrossRefPubMedGoogle Scholar
  24. 24.
    Mazzocco A, Waddell TE, Lingohr E, Johnson RP (2009) Enumeration of bacteriophages by the direct plating plaque assay. Mol Biol 501:77–80Google Scholar
  25. 25.
    Moineau S, Pandian S, Klaenhammer TR (1994) Evolution of a lytic bacteriophage via DNA acquisition from the Lactococcus lactis chromosome. Appl Environ Microb 60(6):1832–1841Google Scholar
  26. 26.
    Niu YD, McAllister TA, Nash JH, Kropinski AM, Stanford K (2014) Four Escherichia coli O157: H7 phages: a new bacteriophage genus and taxonomic classification of T1-like phages. PLoS ONE 9(6):e100426CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    NSW Food Authority (2009) Microbiological quality guide for ready-to-eat foods: A guide to interpreting microbiological results. NSW/FA/CP028/0906:1-9Google Scholar
  28. 28.
    O’flynn G, Ross R, Fitzgerald G, Coffey A (2004) Evaluation of a cocktail of three bacteriophages for biocontrol of Escherichia coli O157: H7. App Environ Microb 70(6):3417–3424CrossRefGoogle Scholar
  29. 29.
    Savage J, Hobsbawn P (2014) Australian fisheries and aquaculture statistics 2014. Fisheries Research and Development Corporation Project 245Google Scholar
  30. 30.
    Sharma M, Patel JR, Conway WS, Ferguson S, Sulakvelidze A (2009) Effectiveness of bacteriophages in reducing Escherichia coli O157: H7 on fresh-cut cantaloupes and lettuce. J Food Protect 72(7):1481–1485CrossRefGoogle Scholar
  31. 31.
    Viazis S, Akhtar M, Feirtag J, Diez-Gonzalez F (2011) Reduction of Escherichia coli O157: H7 viability on hard surfaces by treatment with a bacteriophage mixture. Int J Food Microbiol 145(1):37–42CrossRefPubMedGoogle Scholar
  32. 32.
    Viazis S, Akhtar M, Feirtag J, Diez-Gonzalez F (2011) Reduction of Escherichia coli O157: H7 viability on leafy green vegetables by treatment with a bacteriophage mixture and trans-cinnamaldehyde. Food Microbiol 28(1):149–157CrossRefPubMedGoogle Scholar
  33. 33.
    Zhang H, Wang R, Bao H (2013) Phage inactivation of foodborne Shigella on ready-to-eat spiced chicken. Poultry Sci 92(1):211–217CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2017

Authors and Affiliations

  • Tuan Son Le
    • 1
    • 2
  • Paul C. Southgate
    • 3
  • Wayne O’Connor
    • 4
  • Sue Poole
    • 5
  • D. Ipek Kurtbӧke
    • 1
  1. 1.GeneCology Research Centre and the Faculty of Science, Health, Education and EngineeringUniversity of the Sunshine CoastMaroochydore DCAustralia
  2. 2.Research Institute for Marine FisheriesHai PhongVietnam
  3. 3.Australian Centre for Pacific Islands Research and the Faculty of Science, Health, Education and EngineeringUniversity of the Sunshine CoastMaroochydoreAustralia
  4. 4.NSW FisheriesPort Stephens Fisheries InstituteTaylors BeachAustralia
  5. 5.Innovative Food TechnologiesDepartment of Agriculture & FisheriesBrisbaneAustralia

Personalised recommendations