Foodborne diseases are a major health concern that can have severe impact on society and can add tremendous financial burden to our health care systems. Rapid early detection of food contamination is therefore relevant for the containment of food-borne pathogens. Conventional pathogen detection methods, such as microbiological and biochemical identification are time-consuming and laborious, while immunological or nucleic acid-based techniques require extensive sample preparation and are not amenable to miniaturization for on-site detection. Biosensors have shown tremendous promise to overcome these limitations and are being aggressively studied to provide rapid, reliable and sensitive detection platforms for such applications. Novel biological recognition elements are studied to improve the selectivity and facilitate integration on the transduction platform for sensitive detection. Bacteriophages are one such unique biological entity that show excellent host selectivity and have been actively used as recognition probes for pathogen detection. This review summarizes the extensive literature search on the application of bacteriophages (and recently their receptor binding proteins) as probes for sensitive and selective detection of foodborne pathogens, and critically outlines their advantages and disadvantages over other recognition elements.
References
[1]
Riley, L.W.; Remis, R.S.; Helgerson, S.D.; McGee, H.B.; Wells, J.G.; Davis, B.R.; Hebert, R.J.; Olcott, E.S.; Johnson, L.M.; Hargrett, N.T.; et al. Hemorrhagic colitis associated with a rare Escherichia coli serotype. N. Engl. J. Med. 1983, 308, 681–685.
[2]
Wells, J.G.; Davis, B.R.; Wachsmuth, I.K.; Riley, L.W.; Remis, R.S.; Sokolow, R.; Morris, G.K. Laboratory investigation of hemorrhagic colitis outbreaks associated with a rare Escherichia coli serotype. J. Clin. Microbiol. 1983, 18, 512–520.
[3]
Yu, X.; Susa, M.; Knabbe, C.; Schmid, R.D.; Bachmann, T.T. Development and validation of a diagnostic DNA microarray to detect quinolone-resistant Escherichia coli among clinical isolates. J. Clin. Microbiol. 2004, 42, 4083–4091.
[4]
Taha, M.K. Simultaneous approach for nonculture PCR-based identification and serogroup prediction of Neisseria meningitidis. J. Clin. Microbiol. 2000, 38, 855–857.
[5]
Bonner, G.; Klibanov, A.M. Structural stability of DNA in nonaqueous solvents. Biotechnol. Bioeng. 2000, 68, 339–344.
[6]
Gronowski, A.M.; Copper, S.; Baorto, D.; Murray, P.R. Reproducibility problems with the Abbott laboratories LCx assay for Chlamydia trachomatis and Neisseria gonorrhoeae. J. Clin. Microbiol. 2000, 38, 2416–2418.
[7]
Mothershed, E.A.; Whitney, A.M. Nucleic acid-based methods for the detection of bacterial pathogens: Present and future considerations for the clinical laboratory. Clin. Chim. Acta 2006, 363, 206–220.
[8]
Gu, H.; Xu, K.; Xu, C.; Xu, B. Biofunctional magnetic nanoparticles for protein separation and pathogen detection. Chem. Commun. (Camb). 2006, doi:10.1039/B514130C.
[9]
Perelle, S.; Dilasser, F.; Malorny, B.; Grout, J.; Hoorfar, J.; Fach, P. Comparison of PCR-ELISA and LightCycler real-time PCR assays for detecting Salmonella spp. in milk and meat samples. Mol. Cell. Probes. 2004, 18, 409–420.
[10]
Homola, J. Surface plasmon resonance sensors for detection of chemical and biological species. Chem. Rev. 2008, 108, 462–493.
[11]
Palchetti, I.; Mascini, M. Electroanalytical biosensors and their potential for food pathogen and toxin detection. Anal. Bioanal. Chem. 2008, 391, 455–471.
[12]
Su, X.L.; Li, Y. A self-assembled monolayer-based piezoelectric immunosensor for rapid detection of Escherichia coli O157:H7. Biosens. Bioelectron. 2004, 19, 563–574.
[13]
Mujika, M.; Arana, S.; Castano, E.; Tijero, M.; Vilares, R.; Ruano-Lopez, J.M.; Cruz, A.; Sainz, L.; Berganza, J. Magnetoresistive immunosensor for the detection of Escherichia coli O157:H7 including a microfluidic network. Biosens. Bioelectron. 2009, 24, 1253–1258.
[14]
Berkenpas, E.; Millard, P.; Pereira da Cunha, M. Detection of Escherichia coli O157:H7 with langasite pure shear horizontal surface acoustic wave sensors. Biosens. Bioelectron. 2006, 21, 2255–2262.
[15]
Campbell, G.A.; Mutharasan, R. A method of measuring Escherichia coli 0157:H7 at 1 cell·mL?1 in 1 liter sample using antibody functionalized piezoelectric-excited millimeter-sized cantilever sensor. Environ. Sci. Technol. 2007, 41, 1668–1674.
Greenberg, A.S.; Avila, D.; Hughes, M.; Hughes, A.; McKinney, E.C.; Flajnik, M.F. A new antigen receptor gene family that undergoes rearrangement and extensive somatic diversification in sharks. Nature 1995, 374, 168–173.
[18]
Goldman, E.R.; Anderson, G.P.; Liu, J.L.; Delehanty, J.B.; Sherwood, L.J.; Osborn, L.E.; Cummins, L.B.; Hayhurst, A. Facile generation of heat-stable antiviral and antitoxin single domain antibodies from a semisynthetic llama library. Anal. Chem. 2006, 78, 8245–8255.
[19]
Trilling, A.K.; de Ronde, H.; Noteboom, L.; van Houwelingen, A.; Roelse, M.; Srivastava, S.K.; Haasnoot, W.; Jongsma, M.A.; Kolk, A.; Zuilhof, H.; Beekwilder, J. A broad set of different llama antibodies specific for a 16 kDa heat shock protein of Mycobacterium tuberculosis. PLoS One 2011, 6, e26754.
[20]
Byrne, B.; Stack, E.; Gilmartin, N.; O'Kennedy, R. Antibody-based sensors: Principles, problems and potential for detection of pathogens and associated toxins. Sensors 2009, 9, 4407–4445.
[21]
Zink, R.; Loessner, M.J. Classification of virulent and temperate bacteriophages of Listeria spp. on the basis of morphology and protein analysis. Appl. Environ. Microbiol. 1992, 58, 296–302.
[22]
Balasubramanian, S.; Sorokulova, I.B.; Vodyanoy, V.J.; Simonian, A.L. Lytic phage as a specific and selective probe for detection of Staphylococcus aureus—A surface plasmon resonance spectroscopic study. Biosens. Bioelectron. 2007, 22, 948–955.
[23]
Lakshmanan, R.S.; Guntupalli, R.; Hu, J.; Kim, D.J.; Petrenko, V.A.; Barbaree, J.M.; Chin, B.A. Phage immobilized magnetoelastic sensor for the detection of Salmonella typhimurium. J. Microbiol. Methods 2007, 71, 55–60.
[24]
Lakshmanan, R.S.; Guntupalli, R.; Hu, J.; Petrenko, V.A.; Barbaree, J.M.; Chin, B.A. Detection of Salmonella typhimurium in fat free milk using a phage immobilized magnetoelastic sensor. Sens. Actuators B Chem. 2007, 126, 544–550.
[25]
Singh, A.; Glass, N.; Tolba, M.; Brovko, L.; Griffiths, M.; Evoy, S. Immobilization of bacteriophages on gold surfaces for the specific capture of pathogens. Biosens. Bioelectron. 2009, 24, 3645–3651.
[26]
Cademartiri, R.; Anany, H.; Gross, I.; Bhayani, R.; Griffiths, M.; Brook, M.A. Immobilization of bacteriophages on modified silica particles. Biomaterials 2010, 31, 1904–1910.
[27]
Nanduri, V.; Sorokulova, I.B.; Samoylov, A.M.; Simonian, A.L.; Petrenko, V.A.; Vodyanoy, V. Phage as a molecular recognition element in biosensors immobilized by physical adsorption. Biosens. Bioelectron. 2007, 22, 986–992.
[28]
Arya, S.K.; Singh, A.; Naidoo, R.; Wu, P.; McDermott, M.T.; Evoy, S. Chemically immobilized T4-bacteriophage for specific Escherichia coli detection using surface plasmon resonance. Analyst 2011, 136, 486–492.
[29]
Handa, H.; Gurczynski, S.; Jackson, M.P.; Auner, G.; Mao, G. Recognition of Salmonella Typhimurium by Immobilized Phage P22 Monolayers. Surf. Sci. 2008, 602, 1392–1400.
[30]
Handa, H.; Gurczynski, S.; Jackson, M.P.; Mao, G. Immobilization and molecular interactions between bacteriophage and lipopolysaccharide bilayers. Langmuir 2010, 26, 12095–12103.
[31]
Shabani, A.; Zourob, M.; Allain, B.; Marquette, C.A.; Lawrence, M.F.; Mandeville, R. Bacteriophage-modified microarrays for the direct impedimetric detection of bacteria. Anal. Chem. 2008, 80, 9475–9482.
[32]
Boratynski, J.; Syper, D.; Weber-Dabrowska, B.; Lusiak-Szelachowska, M.; Pozniak, G.; Gorski, A. Preparation of endotoxin-free bacteriophages. Cell. Mol. Biol. Lett. 2004, 9, 253–259.
[33]
Humphrey, S.B.; Stanton, T.B.; Jensen, N.S.; Zuerner, R.L. Purification and characterization of VSH-1, a generalized transducing bacteriophage of Serpulina hyodysenteriae. J. Bacteriol. 1997, 179, 323–329.
[34]
Brorson, K.; Shen, H.; Lute, S.; Perez, J.S.; Frey, D.D. Characterization and purification of bacteriophages using chromatofocusing. J. Chromatogr. A 2008, 1207, 110–121.
[35]
Naidoo, R.; Singh, A.; Arya, S.K.; Beadle, B.; Glass, N.; Tanha, J.; Szymanski, C.M.; Evoy, S. Surface-immobilization of chromatographically purified bacteriophages for the optimized capture of bacteria. Bacteriophage 2012, 2, 15–24.
[36]
Singh, A.; Arya, S.K.; Glass, N.; Hanifi-Moghaddam, P.; Naidoo, R.; Szymanski, C.M.; Tanha, J.; Evoy, S. Bacteriophage tailspike proteins as molecular probes for sensitive and selective bacterial detection. Biosens. Bioelectron. 2010, 26, 131–138.
[37]
Lindberg, A.A.; Wollin, R.; Gemski, P.; Wohlhieter, J.A. Interaction between bacteriophage Sf6 and Shigella flexner. J. Virol. 1978, 27, 38–44.
[38]
Smith, G.P. Filamentous fusion phage: Novel expression vectors that display cloned antigens on the virion surface. Science 1985, 228, 1315–1317.
[39]
Pande, J.; Szewczyk, M.M.; Grover, A.K. Phage display: Concept, innovations, applications and future. Biotechnol. Adv. 2010, 28, 849–858.
[40]
Petrenko, V. Evolution of phage display: From bioactive peptides to bioselective nanomaterials. Expert Opin. Drug Deliv. 2008, 5, 825–836.
Gervais, L.; Gel, M.; Allain, B.; Tolba, M.; Brovko, L.; Zourob, M.; Mandeville, R.; Griffiths, M.; Evoy, S. Immobilization of biotinylated bacteriophages on biosensor surfaces. Sens. Actuators B Chem. 2007, 125, 615–621.
[43]
Tolba, M.; Minikh, O.; Brovko, L.Y.; Evoy, S.; Griffiths, M.W. Oriented immobilization of bacteriophages for biosensor applications. Appl. Environ. Microbiol. 2010, 76, 528–535.
[44]
Serwer, P.; Hayes, S.J. Agarose gel electrophoresis of bacteriophages and related particles. I. Avoidance of binding to the gel and recognizing of particles with packaged DNA. Electrophoresis 1982, 3, 76–80.
[45]
Anany, H.; Chen, W.; Pelton, R.; Griffiths, M.W. Biocontrol of Listeria monocytogenes and Escherichia coli O157:H7 in meat by using phages immobilized on modified cellulose membranes. Appl. Environ. Microbiol. 2011, 77, 6379–6387.
[46]
Waddell, T.E.; Poppe, C. Construction of mini-Tn10luxABcam/Ptac-ATS and its use for developing a bacteriophage that transduces bioluminescence to Escherichia coli O157:H7. FEMS Microbiol. Lett. 2000, 182, 285–289.
[47]
Pearson, R.E.; Jurgensen, S.; Sarkis, G.J.; Hatfull, G.F.; Jacobs, W.R., Jr. Construction of D29 shuttle phasmids and luciferase reporter phages for detection of mycobacteria. Gene 1996, 183, 129–136.
[48]
Sarkis, G.J.; Jacobs, W.R., Jr.; Hatfull, G.F. L5 luciferase reporter mycobacteriophages: A sensitive tool for the detection and assay of live mycobacteria. Mol. Microbiol. 1995, 15, 1055–1067.
[49]
Jacobs, W.R., Jr.; Barletta, R.G.; Udani, R.; Chan, J.; Kalkut, G.; Sosne, G.; Kieser, T.; Sarkis, G.J.; Hatfull, G.F.; Bloom, B.R. Rapid assessment of drug susceptibilities of Mycobacterium tuberculosis by means of luciferase reporter phages. Science 1993, 260, 819–822.
[50]
Kuhn, J.; Suissa, M.; Wyse, J.; Cohen, I.; Weiser, I.; Reznick, S.; Lubinsky-Mink, S.; Stewart, G.; Ulitzur, S. Detection of bacteria using foreign DNA: The development of a bacteriophage reagent for Salmonella. Int. J. Food Microbiol. 2002, 74, 229–238.
[51]
Pagotto, F.; Griffiths, M.; Brovko, L. Phage-Mediated Detection of Staphylococcus Aureus and Escherichia Coli O157: H7 Using Bioluminescence. Proceeding of the International Dairy Federation Symposium on Bacteriological Quality of Raw Milk, Wolfpassing, Austria, 13–15 March 1996.
[52]
Loessner, M.J.; Rees, C.E.; Stewart, G.S.; Scherer, S. Construction of luciferase reporter bacteriophage A511::luxAB for rapid and sensitive detection of viable Listeria cells. Appl. Environ. Microbiol. 1996, 62, 1133–1140.
[53]
Loessner, M.J.; Rudolf, M.; Scherer, S. Evaluation of luciferase reporter bacteriophage A511::luxAB for detection of Listeria monocytogenes in contaminated foods. Appl. Environ. Microbiol. 1997, 63, 2961–2965.
[54]
Harvey, D.; Harrington, C.; Heuzenroeder, M.W.; Murray, C. Lysogenic phage in Salmonella enterica serovar heidelberg (Salmonella Heidelberg): Implications for organism tracing. FEMS Microbiol. Lett. 1993, 108, 291–295.
[55]
Kim, J.W.; Dutta, V.; Elhanafi, D.; Lee, S.; Osborne, J.A.; Kathariou, S. A novel restriction-modification system is responsible for temperature-dependent phage resistance in Listeria monocytogenes ECII. Appl. Environ. Microbiol. 2012, 78, 1995–2004.
[56]
Chopin, M.C.; Chopin, A.; Bidnenko, E. Phage abortive infection in lactococci: Variations on a theme. Curr. Opin. Microbiol. 2005, 8, 473–479.
[57]
Barrangou, R.; Horvath, P. CRISPR: New horizons in phage resistance and strain identification. Annu. Rev. Food Sci. Technol. 2012, 3, 143–162.
Casjens, S.R.; Molineux, I.J. Short noncontractile tail machines: Adsorption and DNA delivery by podoviruses. Adv. Exp. Med. Biol. 2012, 726, 143–179.
[60]
Golshahi, L.; Lynch, K.H.; Dennis, J.J.; Finlay, W.H. In vitro lung delivery of bacteriophages KS4-M and PhiKZ using dry powder inhalers for treatment of Burkholderia cepacia complex and Pseudomonas aeruginosa infections in cystic fibrosis. J. Appl. Microbiol. 2011, 110, 106–117.
[61]
Waseh, S.; Hanifi-Moghaddam, P.; Coleman, R.; Masotti, M.; Ryan, S.; Foss, M.; MacKenzie, R.; Henry, M.; Szymanski, C.M.; Tanha, J. Orally administered P22 phage tailspike protein reduces Salmonella colonization in chickens: Prospects of a novel therapy against bacterial infections. PLoS One 2010, 5, e13904.
[62]
Singh, A.; Arutyunov, D.; Szymanski, C.M.; Evoy, S. Bacteriophage based probes for pathogen detection. Analyst 2012, 137, 3405–3421.
[63]
Kropinski, A.M.; Arutyunov, D.; Foss, M.; Cunningham, A.; Ding, W.; Singh, A.; Pavlov, A.R.; Henry, M.; Evoy, S.; Kelly, J.; Szymanski, C.M. Genome and proteome of Campylobacter jejuni bacteriophage NCTC 12673. Appl. Environ. Microbiol. 2011, 77, 8265–8271.
[64]
Singh, A.; Arutyunov, D.; McDermott, M.T.; Szymanski, C.M.; Evoy, S. Specific detection of Campylobacter jejuni using the bacteriophage NCTC 12673 receptor binding protein as a probe. Analyst 2011, 136, 4780–4786.
[65]
Goodridge, L.; Chen, J.; Griffiths, M. The use of a fluorescent bacteriophage assay for detection of Escherichia coli O157:H7 in inoculated ground beef and raw milk. Int. J. Food Microbiol. 1999, 47, 43–50.
[66]
Goodridge, L.; Chen, J.; Griffiths, M. Development and characterization of a fluorescent-bacteriophage assay for detection of Escherichia coli O157:H7. Appl. Environ. Microbiol. 1999, 65, 1397–1404.
[67]
Li, S.; Li, Y.; Chen, H.; Horikawa, S.; Shen, W.; Simonian, A.; Chin, B.A. Direct detection of Salmonella typhimurium on fresh produce using phage-based magnetoelastic biosensors. Biosens. Bioelectron. 2010, 26, 1313–1319.
[68]
Edgar, R.; McKinstry, M.; Hwang, J.; Oppenheim, A.B.; Fekete, R.A.; Giulian, G.; Merril, C.; Nagashima, K.; Adhya, S. High-sensitivity bacterial detection using biotin-tagged phage and quantum-dot nanocomplexes. Proc. Natl. Acad. Sci. USA 2006, 103, 4841–4845.
[69]
Tawil, N.; Sacher, E.; Mandeville, R.; Meunier, M. Surface plasmon resonance detection of E. coli and methicillin-resistant S. aureus using bacteriophages. Biosens. Bioelectron. 2012, 37, 24–29.
[70]
Blasco, R.; Murphy, M.J.; Sanders, M.F.; Squirrell, D.J. Specific assays for bacteria using phage mediated release of adenylate kinase. J. Appl. Microbiol. 1998, 84, 661–666.
[71]
Wu, Y.; Brovko, L.; Griffiths, M.W. Influence of phage population on the phage-mediated bioluminescent adenylate kinase (AK) assay for detection of bacteria. Lett. Appl. Microbiol. 2001, 33, 311–315.
Yim, P.B.; Clarke, M.L.; McKinstry, M.; De Paoli, L.S.H.; Pease, L.F., III; Dobrovolskaia, M.A.; Kang, H.; Read, T.D.; Sozhamannan, S.; Hwang, J. Quantitative characterization of quantum dot-labeled lambda phage for Escherichia coli detection. Biotechnol. Bioeng. 2009, 104, 1059–1067.
[74]
Olsen, E.V.; Sorokulova, I.B.; Petrenko, V.A.; Chen, I.; Barbaree, J.M.; Vodyanoy, V.J. Affinity-selected filamentous bacteriophage as a probe for acoustic wave biodetectors of Salmonella typhimurium. Biosens. Bioelectron. 2006, 21, 1434–1442.
[75]
Shen, W.; Lakshmanan, R.S.; Mathison, L.C.; Petrenko, V.A.; Chin, B.A. Phage coated magnetoelastic micro-biosensors for real-time detection of Bacillus anthracis spores. Sens. Actuators B Chem. 2009, 137, 501–506.
[76]
Kretzer, J.W.; Lehmann, R.; Schmelcher, M.; Banz, M.; Kim, K.P.; Korn, C.; Loessner, M.J. Use of high-affinity cell wall-binding domains of bacteriophage endolysins for immobilization and separation of bacterial cells. Appl. Environ. Microbiol. 2007, 73, 1992–2000.
[77]
Neufeld, T.; Schwartz-Mittelmann, A.; Biran, D.; Ron, E.Z.; Rishpon, J. Combined phage typing and amperometric detection of released enzymatic activity for the specific identification and quantification of bacteria. Anal. Chem. 2003, 75, 580–585.
[78]
Lee, S.; Onuki, M.; Satoh, H.; Mino, T. Isolation, characterization of bacteriophages specific to Microlunatus phosphovorus and their application for rapid host detection. Lett. Appl. Microbiol. 2006, 42, 259–264.
[79]
Hennes, K.P.; Suttle, C.A. Direct counts of viruses in natural waters and laboratory cultures by epifluorescence microscopy. Limnology Oceanogr. 1995, 40, 1050–1055.
[80]
Hennes, K.P.; Suttle, C.A.; Chan, A.M. Fluorescently labeled virus probes show that natural virus populations can control the structure of marine microbial communities. Appl. Environ. Microbiol. 1995, 61, 3623–3627.
[81]
Rowe, C.A.; Tender, L.M.; Feldstein, M.J.; Golden, J.P.; Scruggs, S.B.; MacCraith, B.D.; Cras, J.J.; Ligler, F.S. Array biosensor for simultaneous identification of bacterial, viral, and protein analytes. Anal. Chem. 1999, 71, 3846–3852.
[82]
Mejri, M.; Baccar, H.; Baldrich, E.; Del Campo, F.J.; Helali, S.; Ktari, T.; Simonian, A.; Aouni, M.; Abdelghani, A. Impedance biosensing using phages for bacteria detection: Generation of dual signals as the clue for in-chip assay confirmation. Biosens. Bioelectron. 2010, 26, 1261–1267.
[83]
Guthy, C.; Belov, M.; Janzen, A.; Quitoriano, N.; Singh, A.; Wright, V.; Finley, E.; Kamins, T.; Evoy, S. Large-scale arrays of nanomechanical sensors for biomolecular fingerprinting. Sens. Actuators B Chem. 2012. in press.