Recent advances in bacteriophage based biosensors for food-borne pathogen detection

Sensors (Switzerland)

Volumn 13, Issue 2, 2013, Pages 1763-1786

  Singh, Amit ^a   Poshtiban, Somayyeh ^a   Evoy, Stephane ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Bacteriophage; Biological probes; Biosensors; Food borne pathogens; Pathogens; Signal transduction

Indexed keywords

BIOLOGICAL ENTITIES; BIOLOGICAL PROBES; BIOLOGICAL RECOGNITION; FOOD-BORNE PATHOGENS; RECEPTOR-BINDING PROTEINS; RECOGNITION ELEMENT; SELECTIVE DETECTION; SENSITIVE DETECTION;

BACTERIOPHAGES; HEALTH CARE; NUCLEIC ACIDS; PATHOGENS; PROBES; SIGNAL TRANSDUCTION;

BIOSENSORS;

NUCLEIC ACID; PROTEIN;

BACTERIOPHAGE; FOOD POISONING; GENETIC PROCEDURES; HUMAN; METABOLISM; METHODOLOGY; MICROBIOLOGY; MOLECULAR PROBE; REVIEW; VIROLOGY;

BACTERIOPHAGES; BIOSENSING TECHNIQUES; FOODBORNE DISEASES; HUMANS; MOLECULAR PROBES; NUCLEIC ACIDS; PROTEINS;

EID: 84875153748     PISSN: 14248220     EISSN: None     Source Type: Journal    
DOI: 10.3390/s130201763     Document Type: Review

References (83)

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. -1 in 1 liter sample using antibody functionalized piezoelectric-excited millimeter-sized cantilever sensor. Environ. Sci. Technol. 2007, 41, 1668-1674.
16. Hamers-Casterman, C.; Atarhouch, T.; Muyldermans, S.; Robinson, G.; Hamers, C.; Songa, E.B.; Bendahman, N.; Hamers, R. Naturally occurring antibodies devoid of light chains. Nature 1993, 363, 446-448.
17. 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.
41. Smith, G.P.; Petrenko, V.A. Phage Display. Chem. Rev. 1997, 97, 391-410.
42. 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. In 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.
58. Leiman, P.G.; Shneider, M.M. Contractile tail machines of bacteriophages. Adv. Exp. Med. Biol. 2012, 726, 93-114.
59. 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.
72. Goldman, E.R.; Pazirandeh, M.P.; Mauro, J.M.; King, K.D.; Frey, J.C.; Anderson, G.P. Phage-displayed peptides as biosensor reagents. J. Mol. Recognit. 2000, 13, 382-387.
73. 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.