Skip to main content
Log in

Bacteriophages as Biological Control Agents of Enteric Bacteria Contaminating Edible Oysters

  • Published:
Current Microbiology Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Ackermann H-W, Nguyen T (1983) Sewage coliphages studied by electron microscopy. Appl Environ Microbiol 45(3):1049–1059

    CAS  PubMed  PubMed Central  Google Scholar 

  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:e2423

    Article  PubMed  PubMed Central  Google Scholar 

  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):1–66

  4. Bradley S, Anderson D, Jones L (1961) Phylogeny of actinomycetes as revealed by susceptibility to actinophage. Dev Ind Microbiol 2:223–237

    Google Scholar 

  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):545–556

    Article  Google Scholar 

  6. Chan BK, Abedon ST, Loc-Carrillo C (2013) Phage cocktails and the future of phage therapy. Future Microbiol 8(6):769–783

    Article  CAS  PubMed  Google Scholar 

  7. Croci L, Suffredini E (2002) Microbiological risk associated with seafood consumption. Annali dell’Istituto superiore di sanita 39(1):35–45

    Google Scholar 

  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):472–479

    Article  CAS  PubMed  Google Scholar 

  9. Duran GM, Marshall DL (2005) Ready-to-eat shrimp as an international vehicle of antibiotic-resistant bacteria. J Food Protect 68(11):2395–2401

    Article  Google Scholar 

  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 300

  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):213–221

    Article  Google Scholar 

  12. Hudson J (2011) Minimum growth temperatures of foodborne pathogens and recommended chiller temperatures. Client Report FW1104 A report for MAF Food Safety ESR

  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):14–21

    Article  CAS  PubMed  Google Scholar 

  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):1–7

    Article  PubMed  Google Scholar 

  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. 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 416:289–295

    Article  Google Scholar 

  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):2060–2065

    Article  PubMed  Google Scholar 

  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):5077–5092

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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):8593–8606

    Article  PubMed  Google Scholar 

  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):1116–1121

    Article  CAS  Google Scholar 

  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):5829–5838

    Article  CAS  PubMed  Google Scholar 

  22. Lucas JS, Southgate PC (2012) Aquaculture: farming aquatic animals and plants, 2nd Edn. Blackwell Publishing Ltd, Oxford. 541–566.

    Book  Google Scholar 

  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):279–285

    Article  CAS  PubMed  Google Scholar 

  24. Mazzocco A, Waddell TE, Lingohr E, Johnson RP (2009) Enumeration of bacteriophages by the direct plating plaque assay. Mol Biol 501:77–80

    CAS  Google Scholar 

  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):1832–1841

    CAS  Google Scholar 

  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):e100426

    Article  PubMed  PubMed Central  Google Scholar 

  27. NSW Food Authority (2009) Microbiological quality guide for ready-to-eat foods: A guide to interpreting microbiological results. NSW/FA/CP028/0906:1-9

  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):3417–3424

    Article  Google Scholar 

  29. Savage J, Hobsbawn P (2014) Australian fisheries and aquaculture statistics 2014. Fisheries Research and Development Corporation Project 245

  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):1481–1485

    Article  Google Scholar 

  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):37–42

    Article  PubMed  Google Scholar 

  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):149–157

    Article  PubMed  Google Scholar 

  33. Zhang H, Wang R, Bao H (2013) Phage inactivation of foodborne Shigella on ready-to-eat spiced chicken. Poultry Sci 92(1):211–217

    Article  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to D. Ipek Kurtbӧke.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Le, T.S., Southgate, P.C., O’Connor, W. et al. Bacteriophages as Biological Control Agents of Enteric Bacteria Contaminating Edible Oysters. Curr Microbiol 75, 611–619 (2018). https://doi.org/10.1007/s00284-017-1424-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00284-017-1424-6

Navigation