Phages of Listeria offer novel tools for diagnostics and biocontrol

Frontiers in Microbiology

Volumn 5, Issue APR, 2014, Pages

  Hagens, Steven ^a   Loessner, Martin J ^b  

^a Micreos Food Safety   (Netherlands)

^b ETH ZURICH   (Switzerland)

Author keywords

Bacteriophage; Biocontrol; Diagnostics; Endolysins; Tools; Typing

Indexed keywords

PROTEIN P100; PROTEIN P35; PROTEIN P70; VIRULENCE FACTOR;

ABORTION; ANTIMICROBIAL ACTIVITY; ARTICLE; BACTERIOPHAGE; BACTERIOPHAGE TYPING; BIOLOGICAL CONTROL AGENT; BIOLOGICAL PEST CONTROL; CHEESE; DNA INTEGRATION; ELECTROCHEMICAL IMPEDANCE SPECTROSCOPY; FLUORESCENCE MICROSCOPY; FOOD POISONING; FOOD PROCESSING; FOOD SAFETY; GASTROENTERITIS; IMMOBILIZATION; LISTERIA; LISTERIA MONOCYTOGENES; LISTERIOSIS; LYSOGENIC MYCOBACTERIUM; LYSOGENIZATION; MOLECULAR DIAGNOSTICS; NONHUMAN; PYROCOCCUS FURIOSUS;

EID: 84899670615     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2014.00159     Document Type: Article

References (69)

1. Anany, H., Chen, W., Pelton, R., and Griffiths, M. W. (2011). Biocontrol of Listeria monocytogenes and Escherichia coli O157:H7 in meat by using phages immobilized on modified cellulose membranes. Appl. Environ. Microbiol. 77, 6379-6387. doi: 10.1128/AEM.05493-11
2. Arachchi, G. J., Cruz, C. D., Dias-Wanigasekera, B. M., Mcintyre, L., Billington, C., Hudson, A., et al. (2013). Host range and in vitro lysis of Listeria monocytogenes seafood isolates by bacteriophages. Food Sci. Technol. Int. doi: 10.1177/1082013213497211 [Epub ahead of print].
3. Audurier, A., Chatelain, R., Chalons, F., and Piechaud, M. (1979). Bacteriophage typing of 823 "Listeria monocytogenes" strains isolated in France from 1958 to 1978 (author's transl). Ann. Microbiol. (Paris) 130B, 179-189.
4. Audurier, A., Taylor, A. G., Carbonnelle, B., and Mclauchlin, J. (1984). A phage typing system for Listeria monocytogenes and its use in epidemiological studies. Clin. Invest. Med. 7, 229-232.
5. Bakulov, I. A., Kotliarov, V. M., and Kol'pikova, T. I. (1984). Sensitivity of the phage titer increase test in detecting Listeria. Zh. Mikrobiol. Epidemiol. Immunobiol. 40-43.
6. Bertsch, D., Rau, J., Eugster, M. R., Haug, M. C., Lawson, P. A., Lacroix, C., et al. (2013). Listeria fleischmannii sp. nov., isolated from cheese. Int. J. Syst. Evol. Microbiol. 63, 526-532. doi: 10.1099/ijs.0.036947-0
7. Bron, P. A., Monk, I. R., Corr, S. C., Hill, C., and Gahan, C. G. (2006). Novel luciferase reporter system for in vitro and organ-specific monitoring of differential gene expression in Listeria monocytogenes. Appl. Environ. Microbiol. 72, 2876-2884. doi: 10.1128/AEM.72.4.2876-2884.2006
8. Bigot, B., Lee, W. J., Mcintyre, L., Wilson, T., Hudson, J. A., Billington, C., et al. (2011). Control of Listeria monocytogenes growth in a ready-to-eat poultry product using a bacteriophage. Food Microbiol. 28, 1448-1452. doi: 10.1016/j.fm.2011.07.001
9. Carlton, R. M., Noordman, W. H., Biswas, B., De Meester, E. D., and Loessner, M. J. (2005). Bacteriophage P100 for control of Listeria monocytogenes in foods: genome sequence, bioinformatic analyses, oral toxicity study, and application. Regul. Toxicol. Pharmacol. 43, 301-312. doi: 10.1016/j.yrtph.2005.08.005
10. Chibeu, A., Agius, L., Gao, A., Sabour, P. M., Kropinski, A. M., and Balamurugan, S. (2013). Efficacy of bacteriophage LISTEXP100 combined with chemical antimicrobials in reducing Listeria monocytogenes in cooked turkey and roast beef. Int. J. Food Microbiol. 167, 208-214. doi: 10.1016/j.ijfoodmicro.2013.08.018
11. Dell'Era, S., Buchrieser, C., Couve, E., Schnell, B., Briers, Y., Schuppler, M., et al. (2009). Listeria monocytogenes L-forms respond to cell wall deficiency by modifying gene expression and the mode of division. Mol. Microbiol. 73, 306-322. doi: 10.1111/j.1365-2958.2009.06774.x
12. Dorscht, J., Klumpp, J., Bielmann, R., Schmelcher, M., Born, Y., Zimmer, M., et al. (2009). Comparative genome analysis of Listeria bacteriophages reveals extensive mosaicism, programmed translational frameshifting, and a novel prophage insertion site. J. Bacteriol. 191, 7206-7215. doi: 10.1128/JB.01041-09
13. Estela, L. A., and Sofos, J. N. (1993). Comparison of conventional and reversed phage typing procedures for identification of Listeria spp. Appl. Environ. Microbiol. 59, 617-619.
14. Fischetti, V. A. (2010). Bacteriophage endolysins: a novel anti-infective to control Gram-positive pathogens. Int. J. Med. Microbiol. 300, 357-362. doi: 10.1016/j.ijmm.2010.04.002
15. Fleming, D. W., Cochi, S. L., MacDonald, K. L., Brondrum, J., Hayes, P. S., Plikaytis, B. D., et al. (1985). Pasteurized milk as a vehicle of infection in an outbreak of listeriosis. N. Engl. J. Med. 14, 404-407. doi: 10.1056/NEJM198502143120704
16. Freeman, V. J. (1951). Studies on the virulence of bacteriophage-infected strains of Corynebacterium diphtheriae. J. Bacteriol. 61, 675-688.
17. Freitag, N. (2000). "Genetic tools for use with Listeria monocytogenes," in Gram-Positive Pathogens, ed. V. A. Fischetti (Washington, DC: ASM Press), 488-498.
18. Gandhi, M., and Chikindas, M. L. (2007). Listeria: a foodborne pathogen that knows how to survive. Int. J. Food Microbiol. 113, 1-15. doi: 10.1016/j.ijfoodmicro.2006.07.008
19. Gerner-Smidt, P., Rosdahl, V. T., and Frederiksen, W. (1993). A new Danish Listeria monocytogenes phage typing system. APMIS 101, 160-167. doi: 10.1111/j.1699-0463.1993.tb00096.x
20. Glaser, P., Frangeul, L., Buchrieser, C., Rusniok, C., Amend, A., Baquero, F., et al. (2001). Comparative genomics of Listeria species. Science 294, 849-852. doi: 10.1126/science.1063447
21. Graves, L. M., Helsel, L. O., Steigerwalt, A. G., Morey, R. E., Daneshvar, M. I., Roof, S. E., et al. (2010). Listeria marthii sp. nov., isolated from the natural environment, Finger Lakes National Forest. Int. J. Syst. Evol. Microbiol. 60, 1280-1288. doi: 10.1099/ijs.0.014118-0ijs.0.014118-0
22. Grundling, A., Burrack, L. S., Bouwer, H. G., and Higgins, D. E. (2004). Listeria monocytogenes regulates flagellar motility gene expression through MogR, a transcriptional repressor required for virulence. Proc. Natl. Acad. Sci. U.S.A. 101, 12318-12323. doi: 10.1073/pnas.0404924101
23. Guenther, S., Huwyler, D., Richard, S., and Loessner, M. J. (2009). Virulent bacteriophage for efficient biocontrol of Listeria monocytogenes in ready-to-eat foods. Appl. Environ. Microbiol. 75, 93-100. doi: 10.1128/AEM.01711-08
24. Guenther, S., and Loessner, M. J. (2011). Bacteriophage biocontrol of Listeria monocytogenes on soft ripened white mold and red-smear cheeses. Bacteriophage 1, 94-100. doi: 10.4161/bact.1.2.15662
25. Habann, M., Leiman, P. G., Vandersteegen, K., Van den Bossche, A., Lavigne, R., Shneider, M. M., et al. (2014). Listeria phage A511, a model for the contractile tail machineries of SPO1-related bacteriophages. Mol. Microbiol. 92, 84-99. doi: 10.1111/mmi.12539
26. Hagens, S., De Wouters, T., Vollenweider, P., and Loessner, M. J. (2011). Reporter bacteriophage A511::celB transduces a hyperthermostable glycosidase from Pyrococcus furiosus for rapid and simple detection of viable Listeria cells. Bacteriophage 1, 143-151. doi: 10.4161/bact.1.3.16710
27. Hagens, S., and Loessner, M. J. (2010). Bacteriophage for biocontrol of foodborne pathogens: calculations and considerations. Curr. Pharm. Biotechnol. 11, 58-68. doi: 10.2174/138920110790725429
28. Hodgson, D. A. (2000). Generalized transduction of serotype 1/2 and serotype 4b strains of Listeria monocytogenes. Mol. Microbiol. 35, 312-323. doi: 10.1046/j.1365-2958.2000.01643.x
29. Junillon, T., Vimont, A., Mosticone, D., Mallen, B., Baril, F., Rozand, C., et al. (2012). Simplified detection of food-borne pathogens: an in situ high affinity capture and staining concept. J. Microbiol. Methods 91, 501-505. doi: 10.1016/j.mimet.2012.09.015
30. Kim, J. W., Siletzky, R. M., and Kathariou, S. (2008). Host ranges of Listeria-specific bacteriophages from the turkey processing plant environment in the United States. Appl. Environ. Microbiol. 74, 6623-6630. doi: 10.1128/AEM.01282-08
31. Klumpp, J., Dorscht, J., Lurz, R., Bielmann, R., Wieland, M., Zimmer, M., et al. (2008). The terminally redundant, non-permuted genome of Listeria bacteriophage A511: a model for the SPO1-like myoviruses of gram-positive bacteria. J. Bacteriol. 190, 5753-5765. doi: 10.1128/JB.00461-08
32. Kretzer, J. W., Lehmann, R., Schmelcher, M., Banz, M., Kim, K. P., Korn, C., et al. (2007). Use of high-affinity cell wall-binding domains of bacteriophage endolysins for immobilization and separation of bacterial cells. Appl. Environ. Microbiol. 73, 1992-2000. doi: 10.1128/AEM.02402-06
33. Lauer, P., Chow, M. Y., Loessner, M. J., Portnoy, D. A., and Calendar, R. (2002). Construction, characterization, and use of two Listeria monocytogenes site-specific phage integration vectors. J. Bacteriol. 184, 4177-4186. doi: 10.1128/JB.184.15.4177-4186.2002
34. Leclercq, A., Clermont, D., Bizet, C., Grimont, P. A., Le Fleche-Mateos, A., Roche, S. M., et al. (2010). Listeria rocourtiae sp. nov. Int. J. Syst. Evol. Microbiol. 60, 2210-2214. doi: 10.1099/ijs.0.017376-0ijs.0.017376-0
35. Lenz, L. L., Mohammadi, S., Geissler, A., and Portnoy, D. A. (2003). SecA2-dependent secretion of autolytic enzymes promotes Listeria monocytogenes pathogenesis. Proc. Natl. Acad. Sci. U.S.A. 100, 12432-12437. doi: 10.1073/pnas.2133653100
36. Lenz, L. L., and Portnoy, D. A. (2002). Identification of a second Listeria secA gene associated with protein secretion and the rough phenotype. Mol. Microbiol. 45, 1043-1056. doi: 10.1046/j.1365-2958.2002.03072.x
37. Leverentz, B., Conway, W. S., Camp, M. J., Janisiewicz, W. J., Abuladze, T., Yang, M., et al. (2003). Biocontrol of Listeria monocytogenes on fresh-cut produce by treatment with lytic bacteriophages and a bacteriocin. Appl. Environ. Microbiol. 69, 4519-4526. doi: 10.1128/AEM.69.8.4519-4526.2003
38. Leverentz, B., Conway, W. S., Janisiewicz, W., and Camp, M. J. (2004). Optimizing concentration and timing of a phage spray application to reduce Listeria monocytogenes on honeydew melon tissue. J. Food Prot. 67, 1682-1686.
39. Loessner, M. J. (1991). Improved procedure for bacteriophage typing of Listeria strains and evaluation of new phages. Appl. Environ. Microbiol. 57, 882-884.
40. Loessner, M. J., and Busse, M. (1990). Bacteriophage typing of Listeria species. Appl. Environ. Microbiol. 56, 1912-1918.
41. Loessner, M. J., Inman, R. B., Lauer, P., and Calendar, R. (2000). Complete nucleotide sequence, molecular analysis and genome structure of bacteriophage A118 of Listeria monocytogenes: implications for phage evolution. Mol. Microbiol. 35, 324-340. doi: 10.1046/j.1365-2958.2000.01720.x
42. Loessner, M. J., Rees, C. E., Stewart, G. S., and Scherer, S. (1996). Construction of luciferase reporter bacteriophage A511::luxAB for rapid and sensitive detection of viable Listeria cells. Appl. Environ. Microbiol. 62, 1133-1140.
43. Loessner, M. J., Rudolf, M., and Scherer, S. (1997). Evaluation of luciferase reporter bacteriophage A511::luxAB for detection of Listeria monocytogenes in contaminated foods. Appl. Environ. Microbiol. 63, 2961-2965.
44. Loessner, M. J., Wendlinger, G., and Scherer, S. (1995). Heterogeneous endolysins in Listeria monocytogenes bacteriophages: a new class of enzymes and evidence for conserved holin genes within the siphoviral lysis cassettes. Mol. Microbiol. 16, 1231-1241. doi: 10.1111/j.1365-2958.1995.tb02345.x
45. McLauchlin, J., Audurier, A., and Taylor, A. G. (1986). The evaluation of a phage-typing system for Listeria monocytogenes for use in epidemiological studies. J. Med. Microbiol. 22, 357-365. doi: 10.1099/00222615-22-4-357
46. Oliveira, M., Vinas, I., Colas, P., Anguera, M., Usall, J., and Abadias, M. (2014). Effectiveness of a bacteriophage in reducing Listeria monocytogenes on fresh-cut fruits and fruit juices. Food Microbiol. 38, 137-142. doi: 10.1016/j.fm.2013.08.018
47. Pedulla, M. L., Ford, M. E., Houtz, J. M., Karthikeyan, T., Wadsworth, C., Lewis, J. A., et al. (2003). Origins of highly mosaic mycobacteriophage genomes. Cell 113, 171-182. doi: 10.1016/S0092-8674(03)00233-2
48. Rabinovich, L., Sigal, N., Borovok, I., Nir-Paz, R., and Herskovits, A. A. (2012). Prophage excision activates Listeria competence genes that promote phagosomal escape and virulence. Cell 150, 792-802. doi: 10.1016/j.cell.2012.06.036
49. Rocourt, J., Audurier, A., Courtieu, A. L., Durst, J., Ortel, S., Schrettenbrunner, A., et al. (1985). A multi-centre study on the phage typing of Listeria monocytogenes. Zentralbl. Bakteriol. Mikrobiol. Hyg. A 259, 489-497.
50. Schmelcher, M., Donovan, D. M., and Loessner, M. J. (2012). Bacteriophage endolysins as novel antimicrobials. Future Microbiol. 7, 1147-1171. doi: 10.2217/fmb.12.97
51. Schmelcher, M., Shabarova, T., Eugster, M. R., Eichenseher, F., Tchang, V. S., Banz, M., et al. (2010). Rapid multiplex detection and differentiation of Listeria cells by use of fluorescent phage endolysin cell wall binding domains. Appl. Environ. Microbiol. 76, 5745-5756. doi: 10.1128/AEM.00801-10
52. Schmuki, M. M., Erne, D., Loessner, M. J., and Klumpp, J. (2012). Bacteriophage P70: unique morphology and unrelatedness to other Listeria bacteriophages. J. Virol. 86, 13099-13102. doi: 10.1128/JVI.02350-12JVI.02350-12
53. Smith, H. W., Green, P., and Parsell, Z. (1983). Vero cell toxins in Escherichia coli and related bacteria: transfer by phage and conjugation and toxic action in laboratory animals, chickens and pigs. J. Gen. Microbiol. 129, 3121-3137.
54. Soni, K. A., Desai, M., Oladunjoye, A., Skrobot, F., and Nannapaneni, R. (2012). Reduction of Listeria monocytogenes in queso fresco cheese by a combination of listericidal and listeriostatic GRAS antimicrobials. Int. J. Food Microbiol. 155, 82-88. doi: 10.1016/j.ijfoodmicro.2012.01.010
55. Soni, K. A., and Nannapaneni, R. (2010a). Bacteriophage significantly reduces Listeria monocytogenes on raw salmon fillet tissue. J. Food Prot. 73, 32-38.
56. Soni, K. A., and Nannapaneni, R. (2010b). Removal of Listeria monocytogenes biofilms with bacteriophage P100. J. Food Prot. 73, 1519-1524.
57. Soni, K. A., Nannapaneni, R., and Hagens, S. (2010). Reduction of Listeria monocytogenes on the surface of fresh channel catfish fillets by bacteriophage Listex P100. Foodborne Pathog. Dis. 7, 427-434. doi: 10.1089/fpd.2009.0432
58. Tolba, M., Ahmed, M. U., Tlili, C., Eichenseher, F., Loessner, M. J., and Zourob, M. (2012). A bacteriophage endolysin-based electrochemical impedance biosensor for the rapid detection of Listeria cells. Analyst 137, 5749-5756. doi: 10.1039/c2an35988j
59. van der Mee-Marquet, N., Loessner, M., and Audurier, A. (1997). Evaluation of seven experimental phages for inclusion in the international phage set for the epidemiological typing of Listeria monocytogenes. Appl. Environ. Microbiol. 63, 3374-3377.
60. Vázquez-Boland, J. A., Kuhn, M., Berche, P., Chakraborty, T., Dominguez-Bernal, G., Goebel, W., et al. (2001). Listeria pathogenesis and molecular virulence determinants. Clin. Microbiol. Rev. 14, 584-640. doi: 10.1128/CMR.14.3.584-640.2001
61. Verghese, B., Lok, M., Wen, J., Alessandria, V., Chen, Y., Kathariou, S., et al. (2011). ComK prophage junction fragments as markers for Listeria monocytogenes genotypes unique to individual meat and poultry processing plants and a model for rapid niche-specific adaptation, biofilm formation, and persistence. Appl. Environ. Microbiol. 77, 3279-3292. doi: 10.1128/AEM.00546-11
62. Walcher, G., Stessl, B., Wagner, M., Eichenseher, F., Loessner, M. J., and Hein, I. (2010). 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. Foodborne Pathog. Dis. 7, 1019-1024. doi: 10.1089/fpd.2009.0475
63. Waldor, M. K., and Mekalanos, J. J. (1996). Lysogenic conversion by a filamentous phage encoding cholera toxin. Science 272, 1910-1914. doi: 10.1126/science.272.5270.1910
64. Wendlinger, G., Loessner, M. J., and Scherer, S. (1996). Bacteriophage receptors on Listeria monocytogenes cells are the N-acetylglucosamine and rhamnose substituents of teichoic acids or the peptidoglycan itself. Microbiology 142(Pt 4), 985-992. doi: 10.1099/00221287-142-4-985
65. Wommack, K. E., and Colwell, R. R. (2000). Virioplankton: viruses in aquatic ecosystems. Microbiol. Mol. Biol. Rev. 64, 69-114. doi: 10.1128/MMBR.64.1.69-114.2000
66. Zimmer, M., Sattelberger, E., Inman, R., Scherer, S., Calendar, R., and Loessner, M. J. (2003). Genome and proteome of Listeria monocytogenes bacteriophage PSA: an unusual case for programmed +1 translational frameshifting in structural protein synthesis. Mol. Microbiol. 50, 303-317. doi: 10.1046/j.1365-2958.2003.03684.x
67. Zink, R., and Loessner, M. J. (1992). Classification of virulent and temperate bacteriophages of Listeria spp. on the basis of morphology and protein analysis. Appl. Environ. Microbiol. 58, 296-302.
68. Zink, R., Loessner, M. J., Glas, I., and Scherer, S. (1994). Supplementary Listeria-typing with defective Listeria phage particles (monocins). Lett. Appl. Microbiol. 19, 99-101. doi: 10.1111/j.1472-765X.1994.tb00915.x
69. Zink, R., Loessner, M. J., and Scherer, S. (1995). Characterization of cryptic prophages (monocins) in Listeria and sequence analysis of a holin/endolysin gene. Microbiology 141(Pt 10), 2577-2584. doi: 10.1099/13500872-141-10-257