Application of bacteriophages for detection of foodborne pathogens

Bacterial contamination of food products presents a challenge for the food industry and poses a high risk for the consumer. Despite increasing awareness and improved hygiene measures, foodborne pathogens remain a threat for public health, and novel methods for detection of these organisms are needed. Bacteriophages represent ideal tools for diagnostic assays because of their high target cell specificity, inherent signal-amplifying properties, easy and inexpensive production, and robustness. Every stage of the phage lytic multiplication cycle, from the initial recognition of the host cell to the final lysis event, may be harnessed in several ways for the purpose of bacterial detection. Besides intact phage particles, phage-derived affinity molecules such as cell wall binding domains and receptor binding proteins can serve for this purpose. This review provides an overview of existing phage-based technologies for detection of foodborne pathogens, and highlights the most recent developments in this field, with particular emphasis on phage-based biosensors.

[1]  Alexander Sulakvelidze,et al.  Bacteriophages: Biology and Applications , 2007 .

[2]  Shu-I Tu,et al.  SPR biosensor for the detection of L. monocytogenes using phage-displayed antibody. , 2007, Biosensors & bioelectronics.

[3]  S. Na,et al.  Escherichia coli detection by GFP-labeled lysozyme-inactivated T4 bacteriophage. , 2004, Journal of biotechnology.

[4]  R Blasco,et al.  Specific assays for bacteria using phage mediated release of adenylate kinase , 1998, Journal of applied microbiology.

[5]  Steven Ripp,et al.  Bacteriophage-amplified bioluminescent sensing of Escherichia coli O157:H7 , 2008, Analytical and bioanalytical chemistry.

[6]  Shankar Balasubramanian,et al.  Lytic phage as a specific and selective probe for detection of Staphylococcus aureus--A surface plasmon resonance spectroscopic study. , 2007, Biosensors & bioelectronics.

[7]  Shin Horikawa,et al.  Direct detection of Salmonella typhimurium on fresh produce using phage-based magnetoelastic biosensors. , 2010, Biosensors & bioelectronics.

[8]  Minhaz Uddin Ahmed,et al.  A bacteriophage endolysin-based electrochemical impedance biosensor for the rapid detection of Listeria cells. , 2012, The Analyst.

[9]  M. Griffiths,et al.  Development and Characterization of a Fluorescent-Bacteriophage Assay for Detection of Escherichia coli O157:H7 , 1999, Applied and Environmental Microbiology.

[10]  Stephane Evoy,et al.  Bacteriophage based probes for pathogen detection. , 2012, The Analyst.

[11]  Wojtek J. Bock,et al.  Detection of bacteria using bacteriophages as recognition elements immobilized on long-period fiber gratings. , 2011, Optics express.

[12]  V. Fischetti,et al.  Bacteriophage lytic enzymes: novel anti-infectives. , 2005, Trends in microbiology.

[13]  P. Wolber.  Bacterial ice nucleation. , 1993, Advances in microbial physiology.

[14]  R. Mole,et al.  Phage as a diagnostic : the use of phage in TB diagnosis , 2001 .

[15]  I-Hsuan Chen,et al.  Affinity-selected filamentous bacteriophage as a probe for acoustic wave biodetectors of Salmonella typhimurium. , 2006, Biosensors & bioelectronics.

[16]  I. Pavlik,et al.  Rapid detection methods for viable Mycobacterium avium subspecies paratuberculosis in milk and cheese. , 2010, International journal of food microbiology.

[17]  M. Griffiths,et al.  Evaluation of a rapid microbial detection method via phage lytic amplification assay coupled with Live/Dead fluorochromic stains , 2007, Letters in applied microbiology.

[18]  M. Griffiths,et al.  Bacteriophage-based biosorbents coupled with bioluminescent ATP assay for rapid concentration and detection of Escherichia coli. , 2010, Journal of microbiological methods.

[19]  J Rishpon,et al.  Combined phage typing and amperometric detection of released enzymatic activity for the specific identification and quantification of bacteria. , 2003, Analytical chemistry.

[20]  Jamshid Tanha,et al.  Silica encapsulated SERS nanoprobe conjugated to the bacteriophage tailspike protein for targeted detection of Salmonella. , 2012, Chemical communications.

[21]  Stephane Evoy,et al.  Specific detection of Campylobacter jejuni using the bacteriophage NCTC 12673 receptor binding protein as a probe. , 2011, The Analyst.

[22]  H. Ding,et al.  A conductance method for the identification of Escherichia coli O157:H7 using bacteriophage AR1. , 2002, Journal of food protection.

[23]  F. Fernández,et al.  Viable Staphylococcus aureus Quantitation using 15N Metabolically Labeled Bacteriophage Amplification Coupled with a Multiple Reaction Monitoring Proteomic Workflow* , 2011, Molecular & Cellular Proteomics.

[24]  P. Patel,et al.  Bacteriophage-based rapid and sensitive detection of Escherichia coli O157:H7 isolates from ground beef. , 2010, Foodborne pathogens and disease.

[25]  Rosemonde Mandeville,et al.  Bacteriophage-modified microarrays for the direct impedimetric detection of bacteria. , 2008, Analytical chemistry.

[26]  K. Voorhees,et al.  Simultaneous detection of two bacterial pathogens using bacteriophage amplification coupled with matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. , 2005, Rapid communications in mass spectrometry : RCM.

[27]  J. Schölmerich,et al.  Bioluminescence and chemiluminescence - new perspectives , 1987 .

[28]  I. Molineux,et al.  Diagnostic Bioluminescent Phage for Detection of Yersinia pestis , 2009, Journal of Clinical Microbiology.

[29]  Yibin Ying,et al.  New Trends in Impedimetric Biosensors for the Detection of Foodborne Pathogenic Bacteria , 2012, Sensors.

[30]  M. Zimmer,et al.  Green fluorescent protein (GFP): applications, structure, and related photophysical behavior. , 2002, Chemical reviews.

[31]  M. Loessner,et al.  Evaluation of luciferase reporter bacteriophage A511::luxAB for detection of Listeria monocytogenes in contaminated foods , 1997, Applied and environmental microbiology.

[32]  I. Molineux,et al.  'Bioluminescent' reporter phage for the detection of Category A bacterial pathogens. , 2011, Journal of visualized experiments : JoVE.

[33]  L. Debarbieux,et al.  Tools from viruses: bacteriophage successes and beyond. , 2012, Virology.

[34]  M. Griffiths,et al.  Optimization and validation of a simple method using P22::luxAB bacteriophage for rapid detection of Salmonella enterica serotypes A, B, and D in poultry samples. , 2008, Journal of food protection.

[35]  S. Ulitzur,et al.  Construction of lux bacteriophages and the determination of specific bacteria and their antibiotic sensitivities. , 2000, Methods in enzymology.

[36]  Martin Wagner,et al.  Evaluation of paramagnetic beads coated with recombinant Listeria phage endolysin-derived cell-wall-binding domain proteins for separation of Listeria monocytogenes from raw milk in combination with culture-based and real-time polymerase chain reaction-based quantification. , 2010, Foodborne pathogens and disease.

[37]  M. Griffiths,et al.  Development and Optimization of a Novel Immunomagnetic Separation- Bacteriophage Assay for Detection ofSalmonella enterica Serovar Enteritidis in Broth , 2001, Applied and Environmental Microbiology.

[38]  M. Griffiths,et al.  Influence of phage population on the phage‐mediated bioluminescent adenylate kinase (AK) assay for detection of bacteria , 2001, Letters in applied microbiology.

[39]  H. Unno,et al.  Rapid Detection of Escherichia coli O157:H7 by Using Green Fluorescent Protein-Labeled PP01 Bacteriophage , 2004, Applied and Environmental Microbiology.

[40]  P E Stanley,et al.  A review of bioluminescent ATP techniques in rapid microbiology. , 1989, Journal of bioluminescence and chemiluminescence.

[41]  Peng Wu,et al.  Chemically immobilized T4-bacteriophage for specific Escherichia coli detection using surface plasmon resonance. , 2011, The Analyst.

[42]  F. Bolton.  An investigation of indirect conductimetry for detection of some food-borne bacteria. , 1990, The Journal of applied bacteriology.

[43]  M. Griffiths.  The role of ATP bioluminescence in the food industry: new light on old problems , 1996 .

[44]  L. Goodridge,et al.  Luminescence based enzyme-labeled phage (Phazyme) assays for rapid detection of Shiga toxin producing Escherichia coli serogroups , 2011, Bacteriophage.

[45]  T. Parish,et al.  Inactivation of mycobacteriophage D29 using ferrous ammonium sulphate as a tool for the detection of viable Mycobacterium smegmatis and M. tuberculosis. , 1998, Research in microbiology.

[46]  J. Valentine,et al.  Culture of Mycobacterium avium subspecies paratuberculosis from the blood of patients with Crohn's disease , 2004, The Lancet.

[47]  Mansel W. Griffiths,et al.  Immobilization of biotinylated bacteriophages on biosensor surfaces , 2007 .

[48]  T. Bull,et al.  Detection and Verification of Mycobacterium avium subsp. paratuberculosis in Fresh Ileocolonic Mucosal Biopsy Specimens from Individuals with and without Crohn's Disease , 2003, Journal of Clinical Microbiology.

[49]  M. Loessner,et al.  Heterogeneous endolysins in Listeria monocytogenes bacteriophages: a new class of enzymes and evidence for conserved holin genes within the siphoviral lysis cassettes , 1995, Molecular microbiology.

[50]  Yating Chai,et al.  Rapid and sensitive detection of Salmonella Typhimurium on eggshells by using wireless biosensors. , 2012, Journal of food protection.

[51]  Jeeseong Hwang,et al.  High-sensitivity bacterial detection using biotin-tagged phage and quantum-dot nanocomplexes. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[52]  G. Stewart,et al.  Near on-line detection of enteric bacteria using lux recombinant bacteriophage. , 1991, FEMS microbiology letters.

[53]  Steven Ripp,et al.  Pathogen detection using engineered bacteriophages , 2012, Analytical and Bioanalytical Chemistry.

[54]  M. Nikolich,et al.  Rapid and Sensitive Detection of Yersinia pestis Using Amplification of Plague Diagnostic Bacteriophages Monitored by Real-Time PCR , 2010, PloS one.

[55]  M. Loessner,et al.  Application of bacteriophages for detection and control of foodborne pathogens , 2007, Applied Microbiology and Biotechnology.

[56]  M. Loessner,et al.  Bacteriophage: Powerful Tools for the Detection of Bacterial Pathogens , 2008 .

[57]  T. Funatsu,et al.  Rapid and Sensitive Detection Method of a Bacterium by Using a GFP Reporter Phage , 2002, Microbiology and immunology.

[58]  C. Poppe,et al.  Construction of mini-Tn10luxABcam/Ptac-ATS and its use for developing a bacteriophage that transduces bioluminescence to Escherichia coli O157:H7. , 2000, FEMS microbiology letters.

[59]  S. Wells,et al.  Herd-level economic losses associated with Johne's disease on US dairy operations. , 1999, Preventive veterinary medicine.

[60]  Jassim,et al.  The specific and sensitive detection of bacterial pathogens within 4 h using bacteriophage amplification , 1998, Journal of applied microbiology.

[61]  M. Griffiths,et al.  Application of a novel immunomagnetic separation-bacteriophage assay for the detection of Salmonella enteritidis and Escherichia coli O157:H7 in food. , 2003, International journal of food microbiology.

[62]  S. Forsythe,et al.  Adenylate kinase amplification of ATP bioluminescence for hygiene monitoring in the food and beverage industry , 2000, Letters in applied microbiology.

[63]  G. Sayler,et al.  Characterization and validation of a bioluminescent bioreporter for the direct detection of Escherichia coli. , 2008, Journal of microbiological methods.

[64]  Joseph Wyse,et al.  Detection of bacteria using foreign DNA: the development of a bacteriophage reagent for Salmonella. , 2002, International journal of food microbiology.

[65]  P. Wolber,et al.  Detection of bacteria by transduction of ice nucleation genes. , 1990, Trends in biotechnology.

[66]  E. Boller,et al.  An economic and rapid diagnostic procedure for the detection of salmonella/shigella using the polyvalent salmonella phage O-1. , 1978, Zentralblatt fur Bakteriologie, Parasitenkunde, Infektionskrankheiten und Hygiene. Erste Abteilung Originale. Reihe A: Medizinische Mikrobiologie und Parasitologie.

[67]  M. Loessner,et al.  Use of High-Affinity Cell Wall-Binding Domains of Bacteriophage Endolysins for Immobilization and Separation of Bacterial Cells , 2007, Applied and Environmental Microbiology.

[68]  S. Evoy,et al.  Oriented Immobilization of Bacteriophages for Biosensor Applications , 2009, Applied and Environmental Microbiology.

[69]  Mansel W. Griffiths,et al.  Salmonella Detection in Eggs Using LuX+ Bacteriophages. , 1996, Journal of food protection.

[70]  C. Elliott,et al.  Maximizing Capture Efficiency and Specificity of Magnetic Separation for Mycobacterium avium subsp. paratuberculosis Cells , 2010, Applied and Environmental Microbiology.

[71]  Anthony Turner,et al.  Principles of Bacterial Detection: Biosensors, Recognition Receptors and Microsystems. , 2008 .

[72]  S. Evoy,et al.  Immobilization of bacteriophages on gold surfaces for the specific capture of pathogens. , 2009, Biosensors & bioelectronics.

[73]  A. Shabani,et al.  Magnetically-assisted impedimetric detection of bacteria using phage-modified carbon microarrays. , 2013, Talanta.

[74]  C. Rees,et al.  Evaluation of the natural virucidal activity of teas for use in the phage amplification assay. , 2006, International journal of food microbiology.

[75]  Timothy K Lu,et al.  Advancing bacteriophage-based microbial diagnostics with synthetic biology. , 2013, Trends in biotechnology.

[76]  Craig A. Grimes,et al.  Theory, Instrumentation and Applications of Magnetoelastic Resonance Sensors: A Review , 2011, Sensors.

[77]  Dong-Joo Kim,et al.  Phage immobilized magnetoelastic sensor for the detection of Salmonella typhimurium. , 2007, Journal of microbiological methods.

[78]  M. Griffiths,et al.  The use of a fluorescent bacteriophage assay for detection of Escherichia coli O157:H7 in inoculated ground beef and raw milk. , 1999, International journal of food microbiology.

[79]  M. Griffiths,et al.  Diagnostic and Therapeutic Applications of Lytic Phages , 2003 .

[80]  F. Drobniewski,et al.  Use of a Phage-Based Assay for Phenotypic Detection of Mycobacteria Directly from Sputum , 2003, Journal of Clinical Microbiology.

[81]  V A Petrenko,et al.  Sequential detection of Salmonella typhimurium and Bacillus anthracis spores using magnetoelastic biosensors. , 2009, Biosensors & bioelectronics.

[82]  Stephane Evoy,et al.  Bacteriophage tailspike proteins as molecular probes for sensitive and selective bacterial detection. , 2010, Biosensors & bioelectronics.

[83]  Karl Kramer,et al.  C‐terminal domains of Listeria monocytogenes bacteriophage murein hydrolases determine specific recognition and high‐affinity binding to bacterial cell wall carbohydrates , 2002, Molecular microbiology.

[84]  D. Squirrell,et al.  Rapid and specific detection of bacteria using bioluminescence , 2002 .

[85]  P Silley,et al.  Impedance microbiology--a rapid change for microbiologists. , 1996, The Journal of applied bacteriology.

[86]  A. Gehring,et al.  Minimum detectable level of Salmonellae using a binomial-based bacterial ice nucleation detection assay (BIND). , 2000, Journal of AOAC International.

[87]  M. Loessner,et al.  Phage for the Detection of Pathogenic Bacteria , 2004 .

[88]  J. Guan,et al.  Detection of multiple antibiotic-resistant Salmonella enterica serovar Typhimurium DT104 by phage replication-competitive enzyme-linked immunosorbent assay. , 2006, Journal of food protection.

[89]  F. Fernández,et al.  Detection of Staphylococcus aureus using 15N-labeled bacteriophage amplification coupled with matrix-assisted laser desorption/ionization-time-of-flight mass spectrometry. , 2011, Analytical chemistry.

[90]  C. Rees,et al.  Phage for rapid detection and control of bacterial pathogens in food. , 2006, Advances in applied microbiology.

[91]  Courtney M. Johnson,et al.  Bacteriophage-based bioluminescent bioreporter for the detection of Escherichia coli 0157:H7. , 2007, Journal of food protection.

[92]  D. Schofield,et al.  Phage‐mediated bioluminescent detection of Bacillus anthracis , 2009, Journal of applied microbiology.

[93]  M. Breitbart,et al.  Use of Fluorescently Labeled Phage in the Detection and Identification of Bacterial Species , 2003, Applied spectroscopy.

[94]  A. Kremser,et al.  Subtilisin removes the surface layer of the phage fd coat. , 1992, European journal of biochemistry.

[95]  A. Madonna,et al.  Detection of Escherichia coli using immunomagnetic separation and bacteriophage amplification coupled with matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. , 2003, Rapid communications in mass spectrometry : RCM.

[96]  M. Loessner,et al.  Construction of luciferase reporter bacteriophage A511::luxAB for rapid and sensitive detection of viable Listeria cells , 1996, Applied and environmental microbiology.

[97]  I. Nicholls,et al.  Phage viability in organic media: insights into phage stability , 1998, Journal of molecular recognition : JMR.

[98]  Peter C. Fineran,et al.  Biotechnological exploitation of bacteriophage research. , 2007, Trends in biotechnology.

[99]  R. Hendrix,et al.  Evolutionary relationships among diverse bacteriophages and prophages: all the world's a phage. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[100]  F. Drobniewski,et al.  Evaluation of a new rapid bacteriophage-based method for the drug susceptibility testing of Mycobacterium tuberculosis , 1997, Nature Medicine.

[101]  M. Loessner,et al.  Bacteriophage endolysins as novel antimicrobials. , 2012, Future microbiology.

[102]  R. Young,et al.  Bacteriophage lysis: mechanism and regulation , 1992, Microbiological reviews.

[103]  Simon F. Park,et al.  Detection and enumeration of Campylobacter jejuni and Campylobacter coli by indirect impedimetry with an oxygen scavenging system. , 2003, Journal of food protection.

[104]  S. Ripp,et al.  Linking bacteriophage infection to quorum sensing signalling and bioluminescent bioreporter monitoring for direct detection of bacterial agents , 2006, Journal of applied microbiology.

[105]  M. Loessner,et al.  Reporter bacteriophage A511::celB transduces a hyperthermostable glycosidase from Pyrococcus furiosus for rapid and simple detection of viable Listeria cells , 2011, Bacteriophage.

[106]  Miri Yemini,et al.  Specific electrochemical phage sensing for Bacillus cereus and Mycobacterium smegmatis. , 2007, Bioelectrochemistry.

[107]  A. Stolle,et al.  Impedance microbiology: applications in food hygiene. , 1999, Journal of food protection.

[108]  Rebecca J. Smith,et al.  Development of a New, Combined Rapid Method Using Phage and PCR for Detection and Identification of Viable Mycobacterium paratuberculosis Bacteria within 48 Hours , 2007, Applied and Environmental Microbiology.

[109]  Xiaomei Yan,et al.  Sensitive and selective bacterial detection using tetracysteine-tagged phages in conjunction with biarsenical dye. , 2011, Angewandte Chemie.

[110]  K. Boor,et al.  Detection of viable Mycobacterium avium subsp. paratuberculosis using luciferase reporter systems. , 2004, Foodborne pathogens and disease.

[111]  H. Anany,et al.  Bacteriophages for detection and control of bacterial pathogens in food and food-processing environment. , 2012, Advances in food and nutrition research.

[112]  W. Han,et al.  LysGH15B, the SH3b Domain of Staphylococcal Phage Endolysin LysGH15, Retains High Affinity to Staphylococci , 2011, Current Microbiology.

[113]  M. Loessner,et al.  Domain shuffling and module engineering of Listeria phage endolysins for enhanced lytic activity and binding affinity , 2011, Microbial biotechnology.

[114]  M. Hicks,et al.  Detection of pathogenic bacteria using a homogeneous immunoassay based on shear alignment of virus particles and linear dichroism. , 2012, Analytical chemistry.

[115]  R. Weissleder,et al.  Codon-optimized Gaussia luciferase cDNA for mammalian gene expression in culture and in vivo. , 2005, Molecular therapy : the journal of the American Society of Gene Therapy.

[116]  Christopher T. Elliott,et al.  Development of a novel phage‐mediated immunoassay for the rapid detection of viable Mycobacterium avium subsp. paratuberculosis , 2013, Journal of applied microbiology.

[117]  M. Griffiths,et al.  Reporter bacteriophage assays as a means to detect foodborne pathogenic bacteria , 2002 .

[118]  M. Loessner,et al.  Rapid Multiplex Detection and Differentiation of Listeria Cells by Use of Fluorescent Phage Endolysin Cell Wall Binding Domains , 2010, Applied and Environmental Microbiology.

[119]  Knut Rudi,et al.  Ethidium monoazide for DNA-based differentiation of viable and dead bacteria by 5'-nuclease PCR. , 2003, BioTechniques.