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.
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References
Ackermann H-W, Nguyen T (1983) Sewage coliphages studied by electron microscopy. Appl Environ Microbiol 45(3):1049–1059
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
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
Bradley S, Anderson D, Jones L (1961) Phylogeny of actinomycetes as revealed by susceptibility to actinophage. Dev Ind Microbiol 2:223–237
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
Chan BK, Abedon ST, Loc-Carrillo C (2013) Phage cocktails and the future of phage therapy. Future Microbiol 8(6):769–783
Croci L, Suffredini E (2002) Microbiological risk associated with seafood consumption. Annali dell’Istituto superiore di sanita 39(1):35–45
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
Duran GM, Marshall DL (2005) Ready-to-eat shrimp as an international vehicle of antibiotic-resistant bacteria. J Food Protect 68(11):2395–2401
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
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
Hudson J (2011) Minimum growth temperatures of foodborne pathogens and recommended chiller temperatures. Client Report FW1104 A report for MAF Food Safety ESR
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
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
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)
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
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
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
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
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
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
Lucas JS, Southgate PC (2012) Aquaculture: farming aquatic animals and plants, 2nd Edn. Blackwell Publishing Ltd, Oxford. 541–566.
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
Mazzocco A, Waddell TE, Lingohr E, Johnson RP (2009) Enumeration of bacteriophages by the direct plating plaque assay. Mol Biol 501:77–80
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
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
NSW Food Authority (2009) Microbiological quality guide for ready-to-eat foods: A guide to interpreting microbiological results. NSW/FA/CP028/0906:1-9
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
Savage J, Hobsbawn P (2014) Australian fisheries and aquaculture statistics 2014. Fisheries Research and Development Corporation Project 245
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
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
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
Zhang H, Wang R, Bao H (2013) Phage inactivation of foodborne Shigella on ready-to-eat spiced chicken. Poultry Sci 92(1):211–217
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.
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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
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DOI: https://doi.org/10.1007/s00284-017-1424-6