한국식품저장유통학회지 (Food Science and Preservation)

  • 제30권1호
  • /
  • Pages.42-51
  • /
  • 2023
  • /
  • 3022-5477(pISSN)
  • /
  • 3022-5485(eISSN)
한국식품저장유통학회 (The Korean Society of Food Preservation)
권호 표지
DOI QR코드

DOI QR Code

Isolation and characterization of a lytic Salmonella Typhimurium-specific phage as a potential biofilm control agent

  • Su-Hyeon Kim (School of Food Science and Biotechnology, Kyungpook National University) ;
  • Mi-Kyung Park (School of Food Science and Biotechnology, Kyungpook National University)
  • 투고 : 2023.01.19
  • 심사 : 2023.02.01
  • 발행 : 2023.02.28
PDF 다운로드
⟨ 이전 논문 다음 논문 ⟩

초록

This study aimed to characterize a lytic Salmonella Typhimurium-specific (ST) phage and its biofilm control capability against S. Typhimurium biofilm on polypropylene surface. ST phage was isolated, propagated, and purified from water used in a slaughterhouse. The morphology of ST phage was observed via transmission electron microscopy. Its bactericidal effect was evaluated by determining bacterial concentrations after the phage treatment at various multiplicities of infection (MOIs) of 0.01, 1.0, and 100. Once the biofilm was formed on the polypropylene tube after incubation at 37℃ for 48 h, the phage was treated and its antibiofilm capability was determined using crystal violet staining and plate count method. The phage was isolated and purified at a final concentration of ~11 log PFU/mL. It was identified as a myophage with an icosahedral head (~104 nm) and contractile tail (~90-115 nm). ST phage could significantly decrease S. Typhimurium population by ~2.8 log CFU/mL at an MOI of 100. After incubation for 48 h, biofilm formation on polypropylene surface was confirmed with a bacterial population of ~6.9 log CFU/cm2. After 1 h treatment with ST phage, the bacterial population in the biofilm was reduced by 2.8 log CFU/cm2. Therefore, these results suggest that lytic ST phage as a promising biofilm control agent for eradicating S. Typhimurium biofilm formed on food contact surfaces.

키워드

과제정보

This research was supported by Kyungpook National University Research Fund, 2021.

참고문헌

  1. Azeredo J, Azevedo NF, Briandet R, Cerca N, Coenye T, Costa AR, Desvaux M, Di Bonaventura G, Hebraud M, Jaglic Z. Critical review on biofilm methods. Crit Rev Microbiol, 43, 313-351 (2017) https://doi.org/10.1080/1040841X.2016.1208146
  2. Azeredo J, Garcia P, Drulis-Kawa Z. Targeting biofilms using phages and their enzymes. Curr Opin Biotechnol, 68, 251-261 (2021)
  3. CDC. Centers for disease control and prevention, national center for emerging and zoonotic infectious diseases, division of foodborne, waterborne, and environmental diseases. Available from: https://www.cdc.gov/salmonella/index.html. Accessed Dec. 12, 2022.
  4. Chang C, Yu X, Guo W, Guo C, Guo X, Li Q, Zhu Y. Bacteriophage-mediated control of biofilm: A promising new dawn for the future. Front Microbiol, 13, 825828 (2022)
  5. Choi IY, Lee JH, Kim HJ, Park MK. Isolation and characterization of a novel broad-host-range bacteriophage infecting Salmonella enterica subsp. enterica for biocontrol and rapid detection. J Microbiol Biotechnol, 27, 2151-2155 (2017) https://doi.org/10.4014/jmb.1711.11017
  6. Corcoran M, Morris D, De Lappe N, Oconnor J, Lalor P, Dockery P, Cormican M. Commonly used disinfectants fail to eradicate Salmonella enterica biofilms from food contact surface materials. Appl Environ Microbiol, 80, 1507- 1514 (2014) https://doi.org/10.1128/AEM.03109-13
  7. Duc HM, Son HM, Yi HPS, Sato J, Ngan PH, Masuda Y, Honjoh KI, Miyamoto T. Isolation, characterization and application of a polyvalent phage capable of controlling Salmonella and Escherichia coli O157: H7 in different food matrices. Food Res Int, 131, 108977 (2020)
  8. Endersen L, Omahony J, Hill C, Ross RP, Mcauliffe O, Coffey A. Phage therapy in the food industry. Annu Rev Food Sci Technol, 5, 327-349 (2014) https://doi.org/10.1146/annurev-food-030713-092415
  9. Fu W, Forster T, Mayer O, Curtin JJ, Lehman SM, Donlan RM. Bacteriophage cocktail for the prevention of biofilm formation by Pseudomonas aeruginosa on catheters in an in vitro model system. Antimicrob Agents Chemother, 54, 397-404 (2010) https://doi.org/10.1128/AAC.00669-09
  10. Garcia KCDOD, De Oliveira Correa IM, Pereira LQ, Silva TM, Mioni MDSR, De Moraes Izidoro AC, Bastos IHV, Goncalves GaM, Okamoto AS, Andreatti Filho RL. Bacteriophage use to control Salmonella biofilm on surfaces present in chicken slaughterhouses. Poult Sci, 96, 3392-3398 (2017) https://doi.org/10.3382/ps/pex124
  11. Gwak KM, Choi IY, Lee J, Oh JH, Park MK. Isolation and characterization of a lytic and highly specific phage against Yersinia enterocolitica as a novel biocontrol agent. J Microbiol Biotechnol, 28, 1946-1954 (2018) https://doi.org/10.4014/jmb.1808.08001
  12. Iibuchi R, Hara-Kudo Y, Hasegawa A, Kumagai S. Survival of Salmonella on a polypropylene surface under dry conditions in relation to biofilm-formation capability. J Food Prot, 73, 1506-1510 (2010) https://doi.org/10.4315/0362-028X-73.8.1506
  13. Islam MS, Zhou Y, Liang L, Nime I, Liu K, Yan T, Wang X, Li J. Application of a phage cocktail for control of Salmonella in foods and reducing biofilms. Viruses, 11, 841 (2019)
  14. Islam MS, Zhou Y, Liang L, Nime I, Yan T, Willias SP, Mia MZ, Bei W, Connerton IF, Fischetti VA. Application of a broad range lytic phage LPST94 for biological control of Salmonella in foods. Microorganisms, 8, 247 (2020)
  15. Kalatzis PG, Bastias R, Kokkari C, Katharios P. Isolation and characterization of two lytic bacteriophages, φst2 and φgrn1; phage therapy application for biological control of Vibrio alginolyticus in aquaculture live feeds. PloS One, 11, e0151101 (2016)
  16. Kim SH, Adeyemi DE, Park MK. Characterization of a new and efficient polyvalent phage infecting E. coli O157: H7, Salmonella spp., and Shigella sonnei. Microorganisms, 9, 2105 (2021)
  17. Kim SH, Park YR, Jung H, Park MK. Characterization of a lytic phage kfs-ec3 infecting multiple foodborne pathogens. Korean J Food Preserv, 29, 1022-1034 (2022) https://doi.org/10.11002/kjfp.2022.29.7.1022
  18. Kuzminska-Bajor M, Korzeniowski P, Sliwka P, Kuczkowski M, Misic D, Milcarz A. Bacteriophage cocktail can effectively control Salmonella biofilm in poultry housing. Front Microbiol, 13, 901770 (2022)
  19. Kwon J, Kim SG, Kim HJ, Giri SS, Kim SW, Lee SB, Park SC. Isolation and characterization of Salmonella jumbo-phage pSal-SNUABM-04. Viruses, 13, 27 (2021)
  20. Lang LH. FDA approves use of bacteriophages to be added to meat and poultry products. Gastroenterology, 131, 1370 (2006)
  21. Lee C, Choi IY, Park DH, Park MK. Isolation and characterization of a novel Escherichia coli O157: H7-specific phage as a biocontrol agent. J Environ Health Sci Engineer, 18, 189-199 (2020) https://doi.org/10.1007/s40201-020-00452-5
  22. Liu A, Liu Y, Peng L, Cai X, Shen L, Duan M, Ning Y, Liu S, Li C, Liu Y. Characterization of the narrow-spectrum bacteriophage LSE7621 towards Salmonella Enteritidis and its biocontrol potential on lettuce and tofu. LWT, 118, 108791 (2020)
  23. Meng X, Shi Y, Ji W, Meng X, Zhang J, Wang H, Lu C, Sun J, Yan Y. Application of a bacteriophage lysin to disrupt biofilms formed by the animal pathogen Streptococcus suis. Appl Environ Microbiol, 77, 8272-8279 (2011)
  24. Milho C, Silva MD, Melo L, Santos S, Azeredo J, Sillankorva S. Control of Salmonella Enteritidis on food contact surfaces with bacteriophage PVP-SE2. Biofouling, 34, 753-768 (2018) https://doi.org/10.1080/08927014.2018.1501475
  25. Mohamed A, Taha O, El-Sherif HM, Connerton PL, Hooton SP, Bassim ND, Connerton IF, El-Shibiny A. Bacteriophage ZCSE2 is a potent antimicrobial against Salmonella enterica serovars: Ultrastructure, genomics and efficacy. Viruses, 12, 424 (2020)
  26. Oh JH, Park MK. Recent trends in Salmonella outbreaks and emerging technology for biocontrol of Salmonella using phages in foods: A review. J Microbiol Biotechnol, 27, 2075-2088 (2017) https://doi.org/10.4014/jmb.1710.10049
  27. Oliveira J, Castilho F, Cunha A, Pereira M. Bacteriophage therapy as a bacterial control strategy in aquaculture. Aquaculture Int, 20, 879-910 (2012) https://doi.org/10.1007/s10499-012-9515-7
  28. Park M, Lee JH, Shin H, Kim M, Choi J, Kang DH, Heu S, Ryu S. Characterization and comparative genomic analysis of a novel bacteriophage, sfp10, simultaneously inhibiting both Salmonella enterica and Escherichia coli O157: H7. Appl Environ Microbiol, 78, 58-69 (2012) https://doi.org/10.1128/AEM.06231-11
  29. Park MK, Park JW, Wikle Iii HC, Chin BA. Evaluation of phage-based magnetoelastic biosensors for direct detection of Salmonella Typhimurium on spinach leaves. Sens Actuators B Chem, 176, 1134-1140 (2013) https://doi.org/10.1016/j.snb.2012.10.084
  30. Reij M, Den Aantrekker E, Force IERaIMT. Recontamination as a source of pathogens in processed foods. Int J Food Microbiol, 91, 1-11 (2004) https://doi.org/10.1016/S0168-1605(03)00295-2
  31. Rodrigues D, Teixeira P, Oliveira R, Azeredo J. Salmonella enterica Enteritidis biofilm formation and viability on regular and triclosan-impregnated bench cover materials. J Food Prot, 74, 32-37 (2011) https://doi.org/10.4315/0362-028X.JFP-10-167
  32. Sadekuzzaman M, Mizan MFR, Yang S, Kim HS, Ha SD. Application of bacteriophages for the inactivation of Salmonella spp. in biofilms. Food Sci Technol Int, 24, 424-433 (2018) https://doi.org/10.1177/1082013218763424
  33. Sarhan WA, Azzazy HM. Phage approved in food, why not as a therapeutic? Expert Rev Anti Infect Ther, 13, 91-101 (2015) https://doi.org/10.1586/14787210.2015.990383
  34. Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson MA, Roy SL, Jones JL, Griffin PM. Foodborne illness acquired in the United States ‒ Major pathogens. Emerg Infect Dis, 17, 7 (2011)
  35. Singh A, Gupta R, Pandey R. Rice seed priming with picomolar rutin enhances rhizospheric Bacillus subtilis CIM colonization and plant growth. PloS One, 11, e0146013 (2016)
  36. Suslow T, Zunega M, Wu J, Harris L, Parnell T. Potential for Transference of Inoculated and Indigenous Bacteria from the Non-Wounded Rind of Melons to the Interior Edible Flesh. 2000 Annual Meeting, International Association of Food Protection, Atlanta, GA.
  37. Tiwari BR, Kim S, Kim J. A virulent Salmonella enterica serovar Enteritidis phage SE2 with a strong bacteriolytic activity of planktonic and biofilmed cells. J Bacteriol Virol, 43, 186-194 (2013) https://doi.org/10.4167/jbv.2013.43.3.186
  38. Vert M, Doi Y, Hellwich KH, Hess M, Hodge P, Kubisa P, Rinaudo M, Schue F. Terminology for biorelated polymers and applications (iupac recommendations 2012). Pure Appl Chem, 84, 377-410 (2012) https://doi.org/10.1351/PAC-REC-10-12-04
  39. Wang C, Chen Q, Zhang C, Yang J, Lu Z, Lu F, Bie X. Characterization of a broad host-spectrum virulent Salmonella bacteriophage fmb-p1 and its application on duck meat. Virus Res, 236, 14-23 (2017) https://doi.org/10.1016/j.virusres.2017.05.001
  40. Wu X, Liu P, Shi H, Wang H, Huang H, Shi Y, Gao S. Photo aging and fragmentation of polypropylene food packaging materials in artificial seawater. Water Research, 188, 116456 (2021)
  41. Zhao X, Zhao F, Wang J, Zhong N. Biofilm formation and control strategies of foodborne pathogens: Food safety perspectives. RSC Adv, 7, 36670-36683 (2017) https://doi.org/10.1039/C7RA02497E
  42. Zinke M, Schroder GF, Lange A. Major tail proteins of bacteriophages of the order Caudovirales. J Biol Chem, 298, 101472 (2022)