Bacteriophages for Biocontrol of Biofilms in Food System
Keywords:
bacteriophage, biofilms, food safetyAbstract
Biofilms are a very common form of adaptation that allows bacteria to survive in unfavorable environments. Biofilms produced by pathogenic bacteria in food systems are a problem to food safety. Biofilms are a problem in the use of antibiotics and biocides due to the presence of a natural extracellular matrix and the presence of bacterial cells that are metabolically inactive but survive in the biofilm (persister cells). Some chemicals that are very effective when used to attack free cells but not in the form of biofilm (planktonic cells) become ineffective when applied to biofilms. On the other hand, bacteriophages have the ability to attack bacterial growth in the form of biofilms. The presence of a large number of bacterial cells surviving in the biofilm supports the action of bacteriophages in the biofilm. Bacterial cells are hosts for bacteriophages, so if the host is present in large numbers, it causes bacteriophages to infect more quickly and efficiently because bacteriophage multiplication is faster if more hosts are available. Bacteriophages also have a number of properties that make biofilms susceptible to attack. Bacteriophages are known to produce (or be able to induce) enzymes that degrade the extracellular matrix. Bacteriophages can also infect persister cells and enter a dormant phase in inactive cells in the biofilm but become active again if the bacterial cells are also metabolically active again. Some biofilms are even able to support bacteriophage replication better than free cells. Bacteriophages can be applied to destroy biofilms of pathogenic bacteria in food systems so as to improve food safety.
Downloads
References
Flemming, H.C. Biofilms. In The Encyclopedia of Life Sciences; John Wiley and Sons: Chichester, UK, 2008.
Abedon, S.T. Lysis from without. Bacteriophage 2011, 1, 46–49.
Abedon, S.T.; Thomas-Abedon, C. Phage therapy pharmacology. Curr. Pharm. Biotechnol. 2010, 11, 28–47.
Bartell, P.F.; Orr, T.E. Origin of polysaccharide depolymerase associated with bacteriophage infection. J. Virol. 1969, 3, 290–296.
Broudy, T.A.; Pancholi, V.; Fischetti, V.A. The in vitro Interaction of Streptococcus pyogenes with human pharyngeal cells induces a phage-encoded extracellular DNase. Infect. Immun. 2002, 70, 2805–2811.
Ceri, H.; Olson, M.E.; Stremick, C.; Read, R.R.; Buret, A. The Calgary biofilm device: New technology for rapid determination of antibiotic susceptibilities of bacterial biofilms. J. Clin. Microbiol. 1999, 37, 1771–1776.
Cornelissen, A.; Ceyssens, P.J.; T’Syen, J.; van Praet, H.; Noben, J.P.; Shaburova, O.V.; Krylov, V.N.; Volckaert, G.; Lavigne, R. The T7-related Pseudomonas putida phage f15 displays virion-associated biofilm degradation properties. PLoS One 2011, 6, e18597.
Criado, M.T., Suarez, B., Ferreiros, C.M.. The importance of bacterial adhesion in the dairy industry. Food Technol. 1994, 48, 123–126.
Endersen, L., Buttimer, C., Nevin, E., Coffey, A., Neve, H., Oliveira, H., Lavigne, R., O’Mahony, J. Investigating the Biocontrol and Anti-Biofilm Potential of a Three Phage Cocktail Against Cronobacter sakazakii in Different Brands of Infant Formula. Int. J. Food Microbiol. 2017, 253: 1–11.
Genigeorgis, C. Biofilm: Their signifince to cleaning in the meat sector. In: BURT,S.A.AND BAUER, F. (Eds), New Challenges in Meat Hygiene: Specific problems in cleaning and disinfection, Ecceamst, European Consortium for Continuing Education in Advanced Meat Science and Technology,.1995. pp. 29-47
Glonti, T.; Chanishvili, N.; Taylor, P.W. Bacteriophage-derived enzyme that depolymerizes the alginic acid capsule associated with cystic fibrosis isolates of Pseudomonas aeruginosa. J. Appl. Microbiol. 2010, 108, 695–702.
Gutiérrez, D.; Martínez, B.; Rodríguez, A.; García, P. Genomic characterization of two Staphylococcus epidermidis bacteriophages with anti-biofilm potential. BMC Genomics 2012, 13, e228.
Harper, D.R.; Parracho,H.M.R.T.; Walker, J.; Sharp, R.; Hughes, G.; Werthén.; M, Lehman, M., and Morales, S. Bacteriophages and Biofilms. Antibiotics 2014, 3, 270-284
Leiman, P.G.; Chipman, P.R.; Kostyuchenko, V.A.; Mesyanzhinov, V.V.; Rossman, M.G. Three-dimensional rearrangement of proteins in the tail of bacteriophage T4 on infection of its host. Cell 2004, 118, 419–429.
Monk, A.; Parracho, H.; Cass, J.; McConville, M.; Harper, D.; Werthén, M.; Erikson, K. Bacteriophages and biofilms: A waiting game? In Proceedings of the 18th Biennial Evergreen International Phage Biology Meeting, Olympia, WA, USA, 9–14 August 2009.
O’Toole, G.A. and Kotler, R. Initiation of biofilm formation in Pseudomonas flourescences WCS 365 proceeds via multiple, convergent signaling pathways: a genetic analysis. Molecular Microbiology. 1998. 28(3), 449-461.
O’Toole G, Kaplan HB, Kolter R. Biofilm formation as microbial development. Annual Review on Microbiology 2000, 54, 49-79.
Yan, J.; Mao, J.; Xie, J. Bacteriophage polysaccharide depolymerases and biomedical applications. BioDrugs 2013, 28, 265–274.
Pearl, S.; Gabay, C.; Kishony, R.; Oppenheim, A.; Balaban, N.Q. Nongenetic Individuality in the host-phage interaction. PLoS Biol. 2008, 5, e120.
Sharp, R.; Hughes, G.; Hart, A.; Walker, J.T. Bacteriophage for the treatment of bacterial biofilms. U.S. Patent 7758856 B2, 2006.
Sillankorva, S.; Neubauer, P.; Azaredo, J. Use of Bacteriophages to Control Biofilms; LAP Lambert Academic Publishing: Saarbrücken, Germany, 2011.
Son, J.S.; Lee, S.J.; Jun, S.Y.; Yoon, S.J.; Kang, S.H.; Paik, H.R.; Kang, J.O.; Choi, Y.J.Antibacterial and biofilm removal activity of a podoviridae Staphylococcus aureus bacteriophage SAP-2 and a derived recombinant cell-wall-degrading enzyme. Appl. Microbiol. Biotechnol.2010, 86, 1439–1449.
Sharp, R.; Walker, J.T.; Riley, P.; Budge, C.; West, K.; Hughes, G. Bacteriophage therapy to control biofilms of Pseudomonas aeruginosa in the lungs of patient with cystic fibrosis. In Biofilm Communities—Order from Chaos; McBain, A., Allison, D., Brading, M., Rickard, A. Verran, J., Walker, J., Eds.; Bioline: Cardiff, UK, 2003; pp. 237–245.
Hanlon, G.W.; Denyer, S.P.; Olliff, C.J.; Ibrahim, L.J. Reduction in exopolysaccharide viscosity as an aid to bacteriophage penetration through Pseudomonas aeruginosa biofilms. Appl. Environ. Microbiol. 2001, 67, 2746–2753.
Doolittle, M.M.; Cooney, J.J.; Caldwell, D.E. Tracing the interaction of bacteriophage with bacterial biofilms using fluorescent and chromogenic probes. J. Ind. Microbiol. 1996, 16, 331–341.
Tait, K.; Skillman, L.C.; Sutherland, I.W. The efficacy of bacteriophage as a method of biofilm eradication. Biofouling 2002, 18, 305–311.
Kay, M.K.; Erwin, T.C.; McLean, R.J.; Aron, G.M. Bacteriophage ecology in Escherichia coli and Pseudomonas aeruginosa mixed-biofilm communities. Appl. Environ. Microbiol. 2011, 77,821–829.
Sadekuzzaman, M., S. Yang, M. F. R. Mizan, et al. 2017. “Reduction of Escherichia coli O157:H7 in Biofilms Using Bacteriophage BPECO 19. J. Food Sci. 82(6)
Soothill, J.S.; Hawkins, C.; Harper, D.R. Bacteriophage-containing therapeutic agents. U.S. Patent 8105579 B2, 2011.
Sulakvelidze, A.; Pasternack, G.R. Pseudomonas aeruginosa bacteriophage and uses thereof. U.S. Patent 7622293 B2, 2008.
Lu, T.K.; Collins, J.J. Dispersing biofilms with engineered enzymatic bacteriophage. Proc. Natl. Acad. Sci. 2007, 27, 11197–11202.
Yilmaz, C.; Colak, M.; Yilmaz, B.C.; Ersoz, G.; Kutateladze, M.; Gozlugol, M. Bacteriophage therapy in implant-related infections: An experimental study. J. Bone Jt. Surg. Am. 2013, 95,117–125.
Ganegama Arachchi, G.J.; Cridge, A.G.; Dias-Wanigasekera, B.M.; Cruz, C.D.; McIntyre, L.; Liu, R.; Flint S.H.; Mutukumira, A.N. Effectiveness of phages in the decontamination of Listeria monocytogenes adhered to clean stainless steel, stainless steel coated with fish protein, and as a biofilm. J. Ind. Microbiol. Biotechnol. 2013, 40, 1105–1116.
Zhang, Y.; Hu, Z. Combined treatment of Pseudomonas aeruginosa biofilms with bacteriophages and chlorine. Biotechnol. Bioeng. 2013, 110, 286–295.
