Abstract
Salmonella Enteritidis remains a major threat for food safety. To take efforts to develop phage-based biocontrol for S. Enteritidis contamination in food, in this study, the phages against S. Enteritidis were isolated from sewage samples, characterized by host range assays, DNA restriction enzyme pattern analyses, and transmission electron microscope observations, and tested for antibacterial activity in food; some potent phages were further characterized by bioinformatic analyses. Results showed that based on the plaque quality and host range, seven lytic phages _targeting S. Enteritidis were selected, considered as seven distinct phages through DNA physical maps, and classified as Myoviridae or Siphoviridae family by morphologic observations; the combined use of such seven strain phages as a “food additive” could succeed in controlling the artificial S. Enteritidis contamination in the different physical forms of food at a range of temperatures; by bioinformatic analyses, both selected phage BPS11Q3 and BPS15Q2 seemed to be newfound obligate lytic phage strains with no indications for any potentially harmful genes in their genomes. In conclusion, our results showed a potential of isolated phages as food additives for controlling S. Enteritidis contamination in some salmonellosis outbreak-associated food vehicles, and there could be minimized potential risk associated with using BPS11Q3 and BPS15Q2 in food.
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References
Majowicz SE, Musto J, Scallan E et al (2010) The global burden of nontyphoidal Salmonella gastroenteritis. Clin Infect Dis 50:882–889
European Food Safety Authority (EFSA) (2015) The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2013. EFSA J. doi:10.2903/j.efsa.2015.3991
Food Safety and Inspection Service (FSIS) (2015) Serotypes profile of Salmonella isolates from meat and poultry products January 1998 through December 2013. Official website of Food Safety and Inspection Service. http://www.fsis.usda.gov/wps/wcm/connect/c7b5903c-8e8b-4f85-9b5c-12eaf990d2dd/Salmonella-Serotype-Annual-2013.pdf?MOD=AJPERES/. Accessed 11 March 2016
Jackson BR, Griffin PM, Cole D et al (2013) Outbreak-associated Salmonella enterica serotypes and food commodities, United States, 1998–2008. Emerg Infect Dis 19:1239–1244
OzFoodNet Working Group (OFWG) (2015) Monitoring the incidence and causes of diseases potentially transmitted by food in Australia: annual report of the OzFoodNet network, 2011. Commun Dis Intell Q Rep 39:E236–E264
Yang B, Cui Y, Shi C et al (2014) Counts, serotypes, and antimicrobial resistance of Salmonella isolates on retail raw poultry in the People’s Republic of China. J Food Prot 77:894–902
Zhang J, Jin H, Hu J et al (2014) Serovars and antimicrobial resistance of non-typhoidal Salmonella from human patients in Shanghai, China, 2006–2010. Epidemiol Infect 142:826–832
Wu H, Xia X, Cui Y et al (2013) Prevalence of extended-spectrum b-lactamase-producing Salmonella on retail chicken in six provinces and two national cities in the People’s Republic of China. J Food Prot 76:2040–2044
Yang X, Huang J, Wu Q et al (2016) Prevalence, antimicrobial resistance and genetic diversity of Salmonella, isolated from retail ready-to-eat foods in China. Food Control 60:50–56
Endersen L, O’Mahony J, Hill C et al (2014) Phage therapy in the food industry. Annu Rev Food Sci Technol 5:327–349
Kutter E, De VD, Gvasalia G et al (2010) Phage therapy in clinical practice: treatment of human infections. Curr Pharm Biotechnol 11:69–86
Kelly D, McAuliffe O, Ross RP et al (2014) Overview of therapeutic applications of bacteriophages. In: Borysowski J (ed) Phage therapy: current research and applications. Caister, Norfolk, pp 159–187
Ran W, Han H, Hui Z, Hongduo B et al (2012) Isolation and characterization of a lytic bacteriophage of enterotoxigenic Escherichia coli K88. Acta Agric Boreal-Sin 27:163–167
Akhtar M, Viazis S, Diez-Gonzalez F (2014) Isolation, identification and characterization of lytic, wide host range bacteriophages from waste effluents against Salmonella enterica serovars. Food Control 38:67–74
Kutter E (2009) Phage host range and efficiency of plating. In: Clokie MRJ (ed) Bacteriophages: methods and protocols. Humana, New York, pp 141–149
Viazis S, Akhtar M, Feirtag J et al (2011) Isolation and characterization of lytic bacteriophages against Enterohaemorrhagic Escherichia coli. J Appl Microbiol 110:1323–1331
Raya RR, Hebert EM (2009) Isolation of phage via induction of lysogens. In: Clokie MRJ (ed) Bacteriophages: methods and protocols. Humana, New York, pp 23–32
Ma YL, Lu CP (2008) Isolation and identification of a bacteriophage capable of infecting Streptococcus suis, type 2 strains. Vet Microbiol 132:340–347
Sambrook JF, Russell DW (2001) Chapter 2 bacteriophage λ and its vectors. In: Sambrook JF (ed) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory, New York, pp 147–243
Jan P, Lavigne R (2010) Introduction to bacteriophage biology and diversity. In: Sabour PM (ed) Bacteriophages in the control of food- and waterborne pathogens. The American Society for Microbiology, Washington DC, pp 11–29
Lobocka M, Hejnowicz MS, Gagata U et al (2014) The first step to bacteriophage therapy: how to choose the correct phage. In: Borysowski J (ed) Phage therapy: current research and applications. Caister, Norfolk, pp 23–67
Augustine J, Bhat SG (2015) Biocontrol of Salmonella Enteritidis in spiked chicken cuts by lytic bacteriophages Φsp-1 and Φsp-3. J Basic Microbiol 55:500–503
Guenther S, Herzig O, Fieseler L et al (2012) Biocontrol of Salmonella Typhimurium in RET foods with the virulent bacteriophage FO1-E2. Int J Food Microbiol 154:66–72
Hui Z, Ran W, Hongduo B (2013) Phage inactivation of foodborne Shigella on ready-to-eat spiced chicken. Poult Sci 92:211–217
Kang HW, Kim JW, Jung TS et al (2013) Wksl3, a new biocontrol agent for Salmonella enterica serovars Enteritidis and typhimurium in foods: characterization, application, sequence analysis, and oral acute toxicity study. Appl Environ Microbiol 79:1956–1968
Mahony J, Mauliffe O (2010) Bacteriophages as biocontrol agents of food pathogens. Curr Opin Biotechnol. doi:10.1016/j.copbio.2010.10.008
Tiwari BR, Kim S, Kim J (2012) Complete genomic sequence of Salmonella enterica serovar Enteritidis phage SE2. J Virol 86:7712
Wang J, Niu YD, Chen J et al (2015) Complete genome sequence of Escherichia coli O145: nM bacteriophage vB_EcoM_AYO145A, a new member of O1-like phages. Gen Announc. doi:10.1128/genomeA.00539-15
Switt AIM, Orsi RH, Bakker HCD et al (2013) Genomic characterization provides new insight into Salmonella phage diversity. BMC Genom. doi:10.1186/1471-2164-14-481
Acknowledgements
We are grateful to Dr. Hongduo Bao (Institute of Food Safety of JAAS), Dr. Baowei Yang (College of Food Science and Engineering of NAFU), and Dr. Zhongwei Liu (Guizhou University) for their cooperations. This work was supported by the National Natural Science Foundation of China (Grant Number 31302009) and Natural Science Foundation of Guizhou Education University (Grant Number 14YB010).
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Han, H., Wei, X., Wei, Y. et al. Isolation, Characterization, and Bioinformatic Analyses of Lytic Salmonella Enteritidis Phages and Tests of Their Antibacterial Activity in Food. Curr Microbiol 74, 175–183 (2017). https://doi.org/10.1007/s00284-016-1169-7
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DOI: https://doi.org/10.1007/s00284-016-1169-7