Applied Microbiology and Biotechnology

, Volume 76, Issue 3, pp 513–519 | Cite as

Application of bacteriophages for detection and control of foodborne pathogens

Mini-Review

Abstract

The incidence of foodborne infectious diseases is stable or has even increased in many countries. Consequently, our awareness regarding hygiene measures in food production has also increased dramatically over the last decades. However, even today’s modern production techniques and intensive food-monitoring programs have not been able to effectively control the problem. At the same time, increased production volumes are distributed to more consumers, and if contaminated, potentially cause mass epidemics. Accordingly, research directed to improve food safety has also been taken forward, also exploring novel methods and technologies. Such an approach is represented by the use of bacteriophage for specific killing of unwanted bacteria. The extreme specificity of phages renders them ideal candidates for applications designed to increase food safety during the production process. Phages are the natural enemies of bacteria, and can be used for biocontrol of bacteria without interfering with the natural microflora or the cultures in fermented products. Moreover, phages or phage-derived proteins can also be used to detect the presence of unwanted pathogens in food or the production environments, which allows quick and specific identification of viable cells. This review intends to briefly summarize and explain the principles and current standing of these approaches.

Keywords

Bacteriophage Pathogens Listeria Salmonella E. coli Mycobacterium 

References

  1. Almeida GN, Gibbs PA, Hogg TA, Teixeira PC (2006) Listeriosis in Portugal: an existing but under reported infection. BMC Infect Dis 6:153CrossRefGoogle Scholar
  2. Atterbury RJ, Dillon E, Swift C, Connerton PL, Frost JA, Dodd CE, Rees CE, Connerton IF (2005) Correlation of Campylobacter bacteriophage with reduced presence of hosts in broiler chicken ceca. Appl Environ Microbiol 71:4885–4887CrossRefGoogle Scholar
  3. Bach SJ, McAllister TA, Veira DM, Gannon VPJ, Holley RA (2003) Effect of bacteriophage DC22 on Escherichia coli O157:H7 in an artificial rumen system (Rusitec) and inoculated sheep. Anim Res 52:89–101CrossRefGoogle Scholar
  4. Banaiee N, Bobadilla-del-Valle M, Riska PF, Bardarov S, Jr., Small PM, Ponce-de-Leon A, Jacobs WR Jr, Hatfull GF, Sifuentes-Osornio J (2003) Rapid identification and susceptibility testing of Mycobacterium tuberculosis from MGIT cultures with luciferase reporter mycobacteriophages. J Med Microbiol 52:557–561CrossRefGoogle Scholar
  5. Blasco R, Murphy MJ, Sanders MF, Squirrell DJ (1998) Specific assays for bacteria using phage mediated release of adenylate kinase. J Appl Microbiol 84:661–666CrossRefGoogle Scholar
  6. Bruttin A, Brussow H (2005) Human volunteers receiving Escherichia coli phage T4 orally: a safety test of phage therapy. Antimicrob Agents Chemother 49:2874–2878CrossRefGoogle Scholar
  7. Carlton RM, Noordman WH, Biswas B, de Meester ED, Loessner MJ (2005) Bacteriophage P100 for control of Listeria monocytogenes in foods: genome sequence, bioinformatic analyses, oral toxicity study, and application. Regul Toxicol Pharmacol 43:301–312CrossRefGoogle Scholar
  8. Eklund MW, Poysky FT, Reed SM, Smith CA (1971) Bacteriophage and the toxigenicity of Clostridium botulinum type C. Science 172:480–482CrossRefGoogle Scholar
  9. Eriksson U, Lindberg AA (1977) Adsorption of phage P22 to Salmonella typhimurium. J Gen Virol 34:207–221Google Scholar
  10. Estrela AI, Pooley HM, de Lencastre H, Karamata D (1991) Genetic and biochemical characterization of Bacillus subtilis 168 mutants specifically blocked in the synthesis of the teichoic acid poly(3-O-beta-D-glucopyranosyl-N-acetylgalactosamine 1-phosphate): gneA, a new locus, is associated with UDP-N-acetylglucosamine 4-epimerase activity. J Gen Microbiol 137:943–950Google Scholar
  11. Farber JM, Peterkin PI (1991) Listeria monocytogenes, a food-borne pathogen. Microbiol Rev 55:476–511Google Scholar
  12. Favrin SJ, Jassim SA, Griffiths MW (2001) Development and optimization of a novel immunomagnetic separation-bacteriophage assay for detection of Salmonella enterica serovar enteritidis in broth. Appl Environ Microbiol 67:217–224CrossRefGoogle Scholar
  13. Figueroa-Bossi N, Uzzau S, Maloriol D, Bossi L (2001) Variable assortment of prophages provides a transferable repertoire of pathogenic determinants in Salmonella. Mol Microbiol 39:260–271CrossRefGoogle Scholar
  14. Fiorentin L, Vieira ND, Barioni W Jr. (2005) Oral treatment with bacteriophages reduces the concentration of Salmonella enteritidis PT4 in caecal contents of broilers. Avian Pathol 34:258–263CrossRefGoogle Scholar
  15. Gasanov U, Hughes D, Hansbro PM (2005) Methods for the isolation and identification of Listeria spp. and Listeria monocytogenes: a review. FEMS Microbiol Rev 29:851–875CrossRefGoogle Scholar
  16. Goode D, Allen VM, Barrow PA (2003) Reduction of experimental Salmonella and Campylobacter contamination of chicken skin by application of lytic bacteriophages. Appl Environ Microbiol 69:5032–5036CrossRefGoogle Scholar
  17. Goodridge L, Chen J, Griffiths M (1999) 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 47:43–50CrossRefGoogle Scholar
  18. Grif K, Karch H, Schneider C, Daschner FD, Beutin L, Cheasty T, Smith H, Rowe B, Dierich MP, Allerberger F (1998) Comparative study of five different techniques for epidemiological typing of Escherichia coli O157. Diagn Microbiol Infect Dis 32:165–176CrossRefGoogle Scholar
  19. Hopkins KL, Desai M, Frost JA, Stanley J, Logan JM (2004) Fluorescent amplified fragment length polymorphism genotyping of Campylobacter jejuni and Campylobacter coli strains and its relationship with host specificity, serotyping, and phage typing. J Clin Microbiol 42:229–235CrossRefGoogle Scholar
  20. Hung CH, Wu HC, Tseng YH (2002) Mutation in the Xanthomonas campestris xanA gene required for synthesis of xanthan and lipopolysaccharide drastically reduces the efficiency of bacteriophage (phi)L7 adsorption. Biochem Biophys Res Commun 291:338–343CrossRefGoogle Scholar
  21. Joys TM (1965) Correlation between susceptibility to bacteriophage PBS1 and motility in Bacillus subtilis. J Bacteriol 90:1575–1577Google Scholar
  22. Kennedy JE, Bitton G (1987) Bacteriophages in foods. In: Goyal SM, Gerba CP, Bitton G (eds) Phage ecology. Wiley, New York, pp 289–316Google Scholar
  23. Kim KP, Klumpp J, Loessner MJ (2007) Enterobacter sakazakii bacteriophages can prevent bacterial growth in reconstituted infant formula. Int J Food Microbiol 115:195–203CrossRefGoogle Scholar
  24. Kodikara CP, Crew HH, Stewart GS (1991) Near on-line detection of enteric bacteria using lux recombinant bacteriophage. FEMS Microbiol Lett 67:261–265CrossRefGoogle Scholar
  25. Korndoerfer, IP, Danzer J, Schmelcher M, Zimmer M, Skerra A, Loessner MJ (2006) The crystal structure of the bacteriophage PSA endolysin reveals a unique fold responsible for specific recognition of Listeria cell walls. J Mol Biol 364:678–689CrossRefGoogle Scholar
  26. Kretzer JW, Lehmann R, Banz M, Kim KP, Korn C, Loessner MJ (2007) Use of high affinity cell wall-binding domains of bacteriophage endolysins for immobilization and separation of bacterial cells. Appl Environ Microbiol 73:1992–2000CrossRefGoogle Scholar
  27. Kuhn J, Suissa M, Wyse J, Cohen I, Weiser I, Reznick S, Lubinsky-Mink S, Stewart G, Ulitzur S (2002) Detection of bacteria using foreign DNA: the development of a bacteriophage reagent for Salmonella. Int J Food Microbiol 74:229–238CrossRefGoogle Scholar
  28. Leverentz B, Conway WS, Alavidze Z, Janisiewicz WJ, Fuchs Y, Camp MJ, Chighladze E, Sulakvelidze A (2001) Examination of bacteriophage as a biocontrol method for Salmonella on fresh-cut fruit: a model study. J Food Prot 64:1116–1121Google Scholar
  29. Leverentz B, Conway WS, Camp MJ, Janisiewicz WJ, Abuladze T, Yang M, Saftner R, Sulakvelidze A (2003) Biocontrol of Listeria monocytogenes on fresh-cut produce by treatment with lytic bacteriophages and a bacteriocin. Appl Environ Microbiol 69:4519–4526CrossRefGoogle Scholar
  30. Leverentz B, Conway WS, Janisiewicz W, Camp MJ (2004) Optimizing concentration and timing of a phage spray application to reduce Listeria monocytogenes on honeydew melon tissue. J Food Prot 67:1682–1686Google Scholar
  31. Loc Carrillo C, Atterbury RJ, el-Shibiny A, Connerton PL, Dillon E, Scott A, Connerton IF (2005) Bacteriophage therapy to reduce Campylobacter jejuni colonization of broiler chickens. Appl Environ Microbiol 71:6554–6563CrossRefGoogle Scholar
  32. Loessner MJ (1991) Improved procedure for bacteriophage typing of Listeria strains and evaluation of new phages. Appl Environ Microbiol 57:882–884Google Scholar
  33. Loessner MJ, Rees CE, Stewart GS, Scherer S (1996) Construction of luciferase reporter bacteriophage A511::luxAB for rapid and sensitive detection of viable Listeria cells. Appl Environ Microbiol 62:1133–1140Google Scholar
  34. Loessner MJ, Rudolf M, Scherer S (1997) Evaluation of luciferase reporter bacteriophage A511::luxAB for detection of Listeria monocytogenes in contaminated foods. Appl Environ Microbiol 63:2961–2965Google Scholar
  35. Loessner MJ, Kramer K, Ebel F, Scherer S (2002) C-terminal domains of Listeria bacteriophage peptidoglycan hydrolases determine specific recognition and high affinity binding to bacterial cell wall carbohydrates. Mol Microbiol 44:335–349CrossRefGoogle Scholar
  36. Majtanova L, Majtan V (2006) Phage types and virulence markers of clinical isolates of Salmonella enteritidis. Epidemiol Mikrobiol Imunol 55:87–91Google Scholar
  37. Modi R, Hirvi Y, Hill A, Griffiths MW (2001) Effect of phage on survival of Salmonella enteritidis during manufacture and storage of cheddar cheese made from raw and pasteurized milk. J Food Prot 64:927–933Google Scholar
  38. Moore JE, Corcoran D, Dooley JS, Fanning S, Lucey B, Matsuda M, McDowell DA, Megraud F, Millar BC, O’Mahony R, O’Riordan L, O’Rourke M, Rao JR, Rooney PJ, Sails A, Whyte P (2005) Campylobacter. Vet Res 36:351–382CrossRefGoogle Scholar
  39. Nicolle P, Le Minor L, Buttiaux R, Ducrest P (1952) Phage typing of Escherichia coli isolated from cases of infantile gastroenteritis. I. Tables of the types currently classified. Bull Acad Natl Med 136:480–483Google Scholar
  40. O’Brien AD, Newland JW, Miller SF, Holmes RK, Smith HW, Formal SB (1984) Shiga-like toxin-converting phages from Escherichia coli strains that cause hemorrhagic colitis or infantile diarrhea. Science 226:694–696CrossRefGoogle Scholar
  41. O’Brien AD, Melton AR, Schmitt CK, McKee ML, Batts ML, Griffin DE (1993) Profile of Escherichia coli O157:H7 pathogen responsible for hamburger-borne outbreak of hemorrhagic colitis and hemolytic uremic syndrome in Washington. J Clin Microbiol 31:2799–2801Google Scholar
  42. Oda M, Morita M, Unno H, Tanji Y (2004) Rapid detection of Escherichia coli O157:H7 by using green fluorescent protein-labeled PP01 bacteriophage. Appl Environ Microbiol 70:527–534CrossRefGoogle Scholar
  43. O’Flynn G, Ross RP, Fitzgerald GF, Coffey A (2004) Evaluation of a cocktail of three bacteriophages for biocontrol of Escherichia coli O157:H7. Appl Environ Microbiol 70:3417–3424CrossRefGoogle Scholar
  44. Raya RR, Varey P, Oot RA, Dyen MR, Callaway TR, Edrington TS, Kutter EM, Brabban AD (2006) Isolation and characterization of a new T-even bacteriophage, CEV1, and determination of its potential to reduce Escherichia coli O157:H7 levels in sheep. Appl Environ Microbiol 72:6405–6410CrossRefGoogle Scholar
  45. Rees CED, Loessner MJ (2005) Phage for the detection of pathogenic bacteria. In: Kutter E, Sulakvelidze A (eds) Bacteriophages: biology and applications. CRC Press, Boca Raton, FL, USA, pp 276–284Google Scholar
  46. Riley LW, Remis RS, Helgerson SD, McGee HB, Wells JG, Davis BR, Hebert RJ, Olcott ES, Johnson LM, Hargrett NT, Blake PA, Cohen ML (1983) Hemorrhagic colitis associated with a rare Escherichia coli serotype. N Engl J Med 308:681–685CrossRefGoogle Scholar
  47. Riska PF, Su Y, Bardarov S, Freundlich L, Sarkis G, Hatfull G, Carriere C, Kumar V, Chan J, Jacobs WR Jr (1999) Rapid film-based determination of antibiotic susceptibilities of Mycobacterium tuberculosis strains by using a luciferase reporter phage and the Bronx Box. J Clin Microbiol 37:1144–1149Google Scholar
  48. Sarkis GJ, Jacobs WR Jr., Hatfull GF (1995) L5 luciferase reporter mycobacteriophages: a sensitive tool for the detection and assay of live mycobacteria. Mol Microbiol 15:1055–1067CrossRefGoogle Scholar
  49. Scholtens RT (1962) A sub-division of Salmonella typhimurium into phage types based on the method of Craigie and Yen: phages adaptable to species of the B and D group of Salmonella; phage adsorption as diagnostic aid. Antonie Van Leeuwenhoek 28:373–381CrossRefGoogle Scholar
  50. Schwartz M (1983) Phage lambda receptor (lamB protein) in Escherichia coli. Methods Enzymol 97:100–112Google Scholar
  51. Sheng H, Knecht HJ, Kudva IT, Hovde CJ (2006) Application of bacteriophages to control intestinal Escherichia coli O157:H7 levels in ruminants. Appl Environ Microbiol 72:5359–5366CrossRefGoogle Scholar
  52. Stewart GSAB, Smith T, Denyer S (1989) Genetic engineering for bioluminescent bacteria. Food Sci Technol Today 3:19–22Google Scholar
  53. Sturino JM, Klaenhammer TR (2004) Bacteriophage defense systems and strategies for lactic acid bacteria. Adv Appl Microbiol 56:331–378Google Scholar
  54. Sun TP, Webster RE (1987) Nucleotide sequence of a gene cluster involved in entry of E colicins and single-stranded DNA of infecting filamentous bacteriophages into Escherichia coli. J Bacteriol 169:2667–2674Google Scholar
  55. Tanji Y, Furukawa C, Na SH, Hijikata T, Miyanaga K, Unno H (2004) Escherichia coli detection by GFP-labeled lysozyme-inactivated T4 bacteriophage. J Biotechnol 114:11–20CrossRefGoogle Scholar
  56. Tarahovsky YS, Ivanitsky GR, Khusainov AA (1994) Lysis of Escherichia coli cells induced by bacteriophage T4. FEMS Microbiol Lett 122:195–199CrossRefGoogle Scholar
  57. Turpin PE, Maycroft KA, Bedford J, Rowlands CL, Wellington EMH (1993) A rapid luminescent-phage based MPN method for the enumeration of Salmonella typhimurium in environmental samples. Lett Appl Microbiol 16:24–27Google Scholar
  58. Ulitzur S, Kuhn J (1987) Introduction of lux genes into bacteria, a new approach for specific determination of bacteria and their antibiotic susceptibility. In: Schlomerich J, Andreesen R, Kapp A, Ernst M, Woods WG (eds) Bioluminescence and chemiluminescence new perspectives. Wiley, New York, pp 463–472Google Scholar
  59. Ulitzur S, Kuhn J (2000) Construction of lux bacteriophages and the determination of specific bacteria and their antibiotic sensitivities. Methods Enzymol 305:543–557CrossRefGoogle Scholar
  60. Waddell TE, Poppe C (2000) Construction of mini-Tn10luxABcam/Ptac-ATS and its use for developing a bacteriophage that transduces bioluminescence to Escherichia coli O157:H7. FEMS Microbiol Lett 182:285–289CrossRefGoogle Scholar
  61. Wagenaar JA, Van Bergen MA, Mueller MA, Wassenaar TM, Carlton RM (2005) Phage therapy reduces Campylobacter jejuni colonization in broilers. Vet Microbiol 109:275–283CrossRefGoogle Scholar
  62. Whichard JM, Sriranganathan N, Pierson FW (2003) Suppression of Salmonella growth by wild-type and large-plaque variants of bacteriophage Felix O1 in liquid culture and on chicken frankfurters. J Food Prot 66:220–225Google Scholar
  63. Wolber PK (1993) Bacterial ice nucleation. Adv Microb Physiol 34:203–237Google Scholar
  64. Wolber PK, Green RL (1990) Detection of bacteria by transduction of ice nucleation genes. Trends Biotechnol 8:276–279CrossRefGoogle Scholar
  65. Wu Y, Brovko L, Griffiths MW (2001) Influence of phage population on the phage-mediated bioluminescent adenylate kinase (AK) assay for detection of bacteria. Lett Appl Microbiol 33:311–315CrossRefGoogle Scholar
  66. Zink R, Loessner MJ (1992) Classification of virulent and temperate bacteriophages of Listeria spp. on the basis of morphology and protein analysis. Appl Environ Microbiol 58:296–302Google Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  1. 1.Institute of Food Science and NutritionETH ZurichZurichSwitzerland
  2. 2.EBI Food SafetyWageningenThe Netherlands

Personalised recommendations