The viable but non-culturable state and its relevance in food safety

Current Opinion in Food Science

Volumn 8, Issue , 2016, Pages 127-133

  Ayrapetyan, Mesrop ^a,b   Oliver, James D ^a  

^a UNIVERSITY OF NORTH CAROLINA AT CHARLOTTE   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84966376456     PISSN: 22147993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cofs.2016.04.010     Document Type: Review

References (74)

1. Amann J. Die direkte Zählung der Wasserbakterien mittels des Ultramikroskops. Centralbl Bakteriol 1911, 29:381-384.
2. Staley J.T., Konopka A. Measurement of in situ activities of nonphotosynthetic microorganisms in aquatic and terrestrial habitats. Annu Rev Microbiol 1985, 39:321-346.
3. Ayrapetyan M., Williams T.C., Oliver J.D. Interspecific quorum sensing mediates the resuscitation of viable but nonculturable vibrios. Appl Environ Microbiol 2014.
4. Bari S.M., Roky M.K., Mohiuddin M., Kamruzzaman M., Mekalanos J.J., Faruque S.M. Quorum-sensing autoinducers resuscitate dormant Vibrio cholerae in environmental water samples. Proc Natl Acad Sci U S A 2013, 110:9926-9931.
5. Ling L.L., Schneider T., Peoples A.J., Spoering A.L., Engels I., Conlon B.P., Mueller A., Schaberle T.F., Hughes D.E., Epstein S., et al. A new antibiotic kills pathogens without detectable resistance. Nature 2015, 517:455-459.
6. Nichols D., Cahoon N., Trakhtenberg E.M., Pham L., Mehta A., Belanger A., Kanigan T., Lewis K., Epstein S.S. Use of ichip for high-throughput in situ cultivation of "uncultivable" microbial species. Appl Environ Microbiol 2010, 76:2445-2450.
7. Nichols D., Lewis K., Orjala J., Mo S., Ortenberg R., O'Connor P., Zhao C., Vouros P., Kaeberlein T., Epstein S.S. Short peptide induces an "uncultivable" microorganism to grow in vitro. Appl Environ Microbiol 2008, 74:4889-4897.
8. Xu H.S., Roberts N., Singleton F.L., Attwell R.W., Grimes D.J., Colwell R.R. Survival and viability of nonculturable Escherichia coli and Vibrio cholerae in the estuarine and marine environment. Microb Ecol 1982, 8:313-323.
9. Bogosian G., Bourneuf E.V. A matter of bacterial life and death. EMBO Rep 2001, 2:770-774.
10. Oliver J.D. Recent findings on the viable but nonculturable state in pathogenic bacteria. FEMS Microbiol Rev 2010, 34:415-425.
11. Colwell R.R. Survival strategies of bacteria in the natural environment. J Infect Chemother 2000, 6:121-125.
12. Li L., Mendis N., Trigui H., Oliver J.D., Faucher S.P. The importance of the viable but non-culturable state in human bacterial pathogens. Front Microbiol 2014, 5.
13. Salma M., Rousseaux S., Sequeira-Le Grand A., Divol B., Alexandre H. Characterization of the viable but nonculturable (VBNC) state in Saccharomyces cerevisiae. PLOS ONE 2013, 8:e77600.
14. Serpaggi V., Remize F., Recorbet G., Gaudot-Dumas E., Sequeira-Le Grand A., Alexandre H. Characterization of the "viable but nonculturable" (VBNC) state in the wine spoilage yeast Brettanomyces. Food Microbiol 2012, 30:438-447.
15. Nelson E.J., Chowdhury A., Flynn J., Schild S., Bourassa L., Shao Y., LaRocque R.C., Calderwood S.B., Qadri F., Camilli A. Transmission of Vibrio cholerae is antagonized by lytic phage and entry into the aquatic environment. PLoS Pathog 2008, 4:e1000187.
16. Manina G., McKinney J.D. A single-cell perspective on non-growing but metabolically active (NGMA) bacteria. Curr Top Microbiol Immunol 2013.
17. Kamruzzaman M., Udden S.M., Cameron D.E., Calderwood S.B., Nair G.B., Mekalanos J.J., Faruque S.M. Quorum-regulated biofilms enhance the development of conditionally viable, environmental Vibrio cholerae. Proc Natl Acad Sci U S A 2010, 107:1588-1593.
18. Potgieter M., Bester J., Kell D.B., Pretorius E. The dormant blood microbiome in chronic, inflammatory diseases. FEMS Microbiol Rev 2015, 39:567-591.
19. Ayrapetyan M., Williams T.C., Oliver J.D. Bridging the gap between viable but non-culturable and antibiotic persistent bacteria. Trends Microbiol 2015, 23:7-13.
20. Besnard V., Federighi M., Cappelier J.M. Development of a direct viable count procedure for the investigation of VBNC state in Listeria monocytogenes. Lett Appl Microbiol 2000, 31:77-81.
21. Chaveerach P., ter Huurne A.A., Lipman L.J., van Knapen F. Survival and resuscitation of ten strains of Campylobacter jejuni and Campylobacter coli under acid conditions. Appl Environ Microbiol 2003, 69:711-714.
22. Day A.P., Oliver J.D. Changes in membrane fatty acid composition during entry of Vibrio vulnificus into the viable but nonculturable state. J Microbiol 2004, 42:69-73.
23. Xiao X.L., Tian C., Yu Y.G., Wu H. Detection of viable but nonculturable Escherichia coli O157:H7 using propidium monoazide treatments and qPCR. Can J Microbiol 2013, 59:157-163.
24. Anvarian A.H., Smith M.P., Overton T.W. The effects of orange juice clarification on the physiology of Escherichia coli; growth-based and flow cytometric analysis. Int J Food Microbiol 2016, 219:38-43.
25. Kramer B., Muranyi P. Effect of pulsed light on structural and physiological properties of Listeria innocua and Escherichia coli. J Appl Microbiol 2014, 116:596-611.
26. 2 and mild heat processing on natural microorganisms in apple juice. Int J Food Microbiol 2010, 137:81-87.
27. 2 and its characteristics. PLOS ONE 2013, 8:e62388.
28. Asakura H., Kawamoto K., Haishima Y., Igimi S., Yamamoto S., Makino S. Differential expression of the outer membrane protein W (OmpW) stress response in enterohemorrhagic Escherichia coli O157:H7 corresponds to the viable but non-culturable state. Res Microbiol 2008, 159:709-717.
29. Zhang S., Ye C., Lin H., Lv L., Yu X. UV disinfection induces a VBNC state in Escherichia coli and Pseudomonas aeruginosa. Environ Sci Technol 2015, 49:1721-1728.
30. Khamisse E., Firmesse O., Christieans S., Chassaing D., Carpentier B. Impact of cleaning and disinfection on the non-culturable and culturable bacterial loads of food-contact surfaces at a beef processing plant. Int J Food Microbiol 2012, 158:163-168.
31. Masuku S.M. Sanitation assessment of food contact surfaces and lethality of moist heat and a disinfectant against Listeria strains inoculated on deli slicer components 2012, University of Arkansas.
32. Goncalves F.D., de Carvalho C.C. Phenotypic modifications in Staphylococcus aureus cells exposed to high concentrations of vancomycin and teicoplanin. Front Microbiol 2016, 7:13.
33. Helaine S., Cheverton A.M., Watson K.G., Faure L.M., Matthews S.A., Holden D.W. Internalization of Salmonella by macrophages induces formation of nonreplicating persisters. Science 2014, 343:204-208.
34. Nowakowska J., Oliver J.D. Resistance to environmental stresses by Vibrio vulnificus in the viable but nonculturable state. FEMS Microbiol Ecol 2013, 84:213-222.
35. Wong H.C., Wang P. Induction of viable but nonculturable state in Vibrio parahaemolyticus and its susceptibility to environmental stresses. J Appl Microbiol 2004, 96:359-366.
36. Ayrapetyan M., Williams T.C., Baxter R., Oliver J.D. Viable but nonculturable and persister cells coexist stochastically and are induced by human serum. Infect Immun 2015, 83:4194-4203.
37. Orman M.A., Henry T.C., DeCoste C.J., Brynildsen M.P. Analyzing persister physiology with fluorescence-activated cell sorting. Methods Mol Biol 2016, 1333:83-100.
38. Maisonneuve E., Gerdes K. Molecular mechanisms underlying bacterial persisters. Cell 2014, 157:539-548.
39. Demidenok O.I., Kaprelyants A.S., Goncharenko A.V. Toxin-antitoxin vapBC locus participates in formation of the dormant state in Mycobacterium smegmatis. FEMS Microbiol Lett 2014, 352:69-77.
40. Kong I.S., Bates T.C., Hulsmann A., Hassan H., Smith B.E., Oliver J.D. Role of catalase and oxyR in the viable but nonculturable state of Vibrio vulnificus. FEMS Microbiol Ecol 2004, 50:133-142.
41. Morishige Y., Fujimori K., Amano F. Differential resuscitative effect of pyruvate and its analogues on VBNC (viable but non-culturable) Salmonella. Microbes Environ 2013, 28:180-186.
42. Tanaka T., Kawasaki K., Daimon S., Kitagawa W., Yamamoto K., Tamaki H., Tanaka M., Nakatsu C.H., Kamagata Y. A hidden pitfall in the preparation of agar media undermines microorganism cultivability. Appl Environ Microbiol 2014, 80:7659-7666.
43. Senoh M., Hamabata T., Takeda Y. A factor converting viable but nonculturable Vibrio cholerae to a culturable state in eukaryotic cells is a human catalase. Microbiologyopen 2015, 4:589-596.
44. Fakruddin M., Mannan K.S., Andrews S. Viable but nonculturable bacteria: food safety and public health perspective. ISRN Microbiol 2013, 2013:703813.
45. Besnard V., Federighi M., Declerq E., Jugiau F., Cappelier J.M. Environmental and physico-chemical factors induce VBNC state in Listeria monocytogenes. Vet Res 2002, 33:359-370.
46. Quiros C., Herrero M., Garcia L.A., Diaz M. Quantitative approach to determining the contribution of viable-but-nonculturable subpopulations to malolactic fermentation processes. Appl Environ Microbiol 2009, 75:2977-2981.
47. Gunasekera T.S., Sorensen A., Attfield P.V., Sorensen S.J., Veal D.A. Inducible gene expression by nonculturable bacteria in milk after pasteurization. Appl Environ Microbiol 2002, 68:1988-1993.
48. Baffone W., Casaroli A., Citterio B., Pierfelici L., Campana R., Vittoria E., Guaglianone E., Donelli G. Campylobacter jejuni loss of culturability in aqueous microcosms and ability to resuscitate in a mouse model. Int J Food Microbiol 2006, 107:83-91.
49. Oliver J.D., Bockian R. In vivo resuscitation, and virulence towards mice, of viable but nonculturable cells of Vibrio vulnificus. Appl Environ Microbiol 1995, 61:2620-2623.
50. Rivers B., Steck T.R. Viable but nonculturable uropathogenic bacteria are present in the mouse urinary tract following urinary tract infection and antibiotic therapy. Urol Res 2001, 29:60-66.
51. Colwell R.R., Brayton P.R., Herrington D., Tall B.D., Huq A., Levine M.M. Viable but nonculturable Vibrio cholerae O1 revert to a culturable state in human intestine. World J Microb Biotechnol 1996, 12:28-31.
52. Alleron L., Khemiri A., Koubar M., Lacombe C., Coquet L., Cosette P., Jouenne T., Frere J. VBNC Legionella pneumophila cells are still able to produce virulence proteins. Water Res 2013, 47:6606-6617.
53. Liu Y., Wang C., Tyrrell G., Li X.F. Production of Shiga-like toxins in viable but nonculturable Escherichia coli O157:H7. Water Res 2010, 44:711-718.
54. Dinu L.D., Bach S. Induction of viable but nonculturable Escherichia coli O157:H7 in the phyllosphere of lettuce: a food safety risk factor. Appl Environ Microbiol 2011, 77:8295-8302.
55. Giao M.S., Keevil C.W. Listeria monocytogenes can form biofilms in tap water and enter into the viable but non-cultivable state. Microb Ecol 2014, 67:603-611.
56. Aurass P., Prager R., Flieger A. EHEC/EAEC O104:H4 strain linked with the 2011 German outbreak of haemolytic uremic syndrome enters into the viable but non-culturable state in response to various stresses and resuscitates upon stress relief. Environ Microbiol 2011, 13:3139-3148.
57. Kwan B.W., Chowdhury N., Wood T.K. Combatting bacterial infections by killing persister cells with mitomycin C. Environ Microbiol 2015.
58. Saroj S., Shashidhar R., Bandekar J. Gamma radiation used as hygienization technique for foods does not induce viable but non-culturable state (VBNC) in Salmonella enterica subsp. enterica serovar Typhimurium. Curr Microbiol 2009, 59:420-424.
59. Ramamurthy T., Ghosh A., Pazhani G.P., Shinoda S. Current perspectives on viable but non-culturable (VBNC) pathogenic bacteria. Front Public Health 2014, 2:103.
60. Liang X., Soupir M.L., Rigby S., Jarboe L.R., Zhang W. Flow cytometry is a promising and rapid method for differentiating between freely suspended Escherichia coli and E. coli attached to clay particles. J Appl Microbiol 2014, 117:1730-1739.
61. Pasquaroli S., Zandri G., Vignaroli C., Vuotto C., Donelli G., Biavasco F. Antibiotic pressure can induce the viable but non-culturable state in Staphylococcus aureus growing in biofilms. J Antimicrob Chemother 2013, 68:1812-1817.
62. Tamburini S., Foladori P., Ferrentino G., Spilimbergo S., Jousson O. Accurate flow cytometric monitoring of Escherichia coli subpopulations on solid food treated with high pressure carbon dioxide. J Appl Microbiol 2014, 117:440-450.
63. Lin Y.W., Li D., Gu A.Z., Zeng S.Y., He M. Bacterial regrowth in water reclamation and distribution systems revealed by viable bacterial detection assays. Chemosphere 2016, 144:2165-2174.
64. Fu B., Jiang Q., Liu H.B., Liu H. Quantification of viable but nonculturable Salmonella spp. and Shigella spp. during sludge anaerobic digestion and their reactivation during cake storage. J Appl Microbiol 2015, 119:1138-1147.
65. Jiang Q., Fu B., Chen Y., Wang Y., Liu H. Quantification of viable but nonculturable bacterial pathogens in anaerobic digested sludge. Appl Microbiol Biotechnol 2013, 97:6043-6050.
66. Magajna B., Schraft H. Evaluation of propidium monoazide and quantitative PCR to quantify viable Campylobacter jejuni biofilm and planktonic cells in log phase and in a viable but nonculturable state. J Food Prot 2015, 78:1303-1311.
67. Santiago P., Moreno Y., Ferrus M.A. Identification of viable Helicobacter pylori in drinking water supplies by cultural and molecular techniques. Helicobacter 2015, 20:252-259.
68. Sharma H., Mutharasan R. Review of biosensors for foodborne pathogens and toxins. Sens Actuators B Chem 2013, 183:535-549.
69. Togo C.A., Wutor V.C., Limson J.L., Pletschke B.I. Novel detection of Escherichia coli beta-d-glucuronidase activity using a microbially-modified glassy carbon electrode and its potential for faecal pollution monitoring. Biotechnol Lett 2007, 29:531-537.
70. Cheng M.S., Lau S.H., Chow V.T., Toh C.S. Membrane-based electrochemical nanobiosensor for Escherichia coli detection and analysis of cells viability. Environ Sci Technol 2011, 45:6453-6459.
71. Labib M., Zamay A.S., Kolovskaya O.S., Reshetneva I.T., Zamay G.S., Kibbee R.J., Sattar S.A., Zamay T.N., Berezovski M.V. Aptamer-based viability impedimetric sensor for bacteria. Anal Chem 2012, 84:8966-8969.
72. Fernandes E., Martins V.C., Nobrega C., Carvalho C.M., Cardoso F.A., Cardoso S., Dias J., Deng D., Kluskens L.D., Freitas P.P., et al. A bacteriophage detection tool for viability assessment of Salmonella cells. Biosens Bioelectron 2014, 52:239-246.
73. Packard M.M.S.M., Alocilja E.C. On-Chip Dielectrophoretic Separation and Concentration of Viable, Non-Viable and Viable but not Culturable (VBNC) Escherichia coli 2012, Lawrence Livermore National Laboratory.
74. Diler E., Obst U., Schmitz K., Schwartz T. A lysozyme and magnetic bead based method of separating intact bacteria. Anal Bioanal Chem 2011, 401:253-265.