The viable but nonculturable state in bacteria

Journal of Microbiology

Volumn 43, Issue , 2005, Pages 93-100

  Oliver, James D ^a  

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

Author keywords

Culturability; Resuscitation; Survival; Viability; Virulence

Indexed keywords

ANTIBIOTIC THERAPY; BACTERIAL CELL; BACTERIAL GROWTH; BACTERIAL VIRULENCE; BACTERIUM; CELL VIABILITY; CULTURE MEDIUM; ENVIRONMENTAL FACTOR; GASTRITIS; HELICOBACTER PYLORI; HUMAN; MICROBIOLOGY; NONHUMAN; PROCEDURES CONCERNING CELLS; SHORT SURVEY;

BACTERIA; COLONY COUNT, MICROBIAL; CULTURE MEDIA; HUMANS; VIRULENCE;

EID: 15944387317     PISSN: 12258873     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Short Survey

References (71)

1. Adams, B.L., T.C. Bates, and J.D. Oliver. 2003. Survival of Helicobacter pylori in a natural freshwater environment. Appl. Environ. Microbiol. 69, 7462-7466.
2. Asaka, M., A.R. Sepulveda, T. Sugiyama, and D.Y. Graham. 2001. Gastric Cancer, p. 481-498. In H. Mobley, G.L. Mendez, and S.T. Hazell (eds.), Helicobacter pylori: physiology and genetics. American Society for Microbiology, Washington, D.C.
3. Banin, E., T. Israely, A. Kushmaro, Y Loga, E. Orr, and E. Rosenber. 2000. Penetration of the coral-bleacing bacterium Vibrio shiloi into Oculina patagonica. Appl. Environ. Microbiol. 66, 3031-3036.
4. Barer, M.R. 1997. Viable but non-culturable and dormant bacteria: time to resolve an oxymoron and a misnomer? J. Med. Microbiol. 46, 629-631.
5. Barer, M.R. and C.R. Harwood. 1999. Bacterial viability and culturability. Adv. Micro. Physiol. 41, 93-137.
6. Barer, M.R., A.S. Kaprelyants, D.H. Weichart, C.R. Harwood, and D.B. Kell. 1998. Microbial stress and culturability: conceptual and operational domains. Microbiology 144, 2009-2010.
7. Barrett, T. 1998. Ph.D. thesis, Univ. Aberdeen.
8. Bates T., B. Adams, and J.D. Oliver. 2003. Survival of VBNC Helicobacter pylori cocci following antibiotic treatment. Intern. Conf. on Helicobacter pylori. Aarhus, Denmark.
9. Begosian, G. and E.V. Bourneuf. 2001. A matter of bacterial life and death. EMBO Reports 2, 770-774.
10. Begosian, G., N.D. Aardema, E.V. Bourneuf, P.J.L. Morris, and J.P. ONeil. 2000. Recovery of hydrogen peroxide-sensitive culturable cells of Vibrio vulnificus gives the appearance of resuscitation from a viable but nonculturable state. J. Bacteriol. 182, 5070-5075.
11. Bej, A.K., N. Vickery, F.E. Brasher, C. Jeffreys, A. Jones, D.D. A. DePaola, and D.W. Cook. 1997. Use of PCR to determine genomic diversity and distribution of siderophore-mediated iron acquisition genes in clinical and environmental isolates of Vibrio vulnificus. Abstr. Q177, p. 485. Abstr. Annu. Meet. Amer. Soc. Microbiol.
12. Beumer, R.R., J. de Vries, and F.M. Rombouts. 1992. Campylobacler jejuni non-culturable coccoid cells. Intern. J. Food Microbiol. 15, 153-163.
13. Bloomfield, S.F., G.S.A.B. Stewart, C.E.R. Dodd, I.R. Booth, and E.G.M. Power. 1998. The viable but nonculturable phenomenon explained? Microbiology 144, 1-3.
14. Breeuwer, P. and T. Abee. 2000. Assessment of viability of microorganisms employing fluorescence techniques. Intern. J. Food Microbiol. 55, 193-200.
15. Bunker, S.T., T.C. Bates, and J.D. Oliver. 2004. Effects of temperature on detection of plasmid and chromosomally encoded gfp-and lux-labeled Pseudomonas fluorescens in soil. Environ. Biosafety Res. 3, 1-8.
16. Catrenich, C.E. and K.M. Makin. 1991. Characterization of the morphologic conversion of Helicobacter pylori from bacillary to coccoid forms. Scand. J. Gastroenterol. 181, 58-64.
17. Colwell, R.R., P.R. Brayton, D.J. Grimes, D.R. Roszak, S.A. Huq, and L.M. Palmer. 1985. Viable, but non-culturable Vibrio cholerae and related pathogens in the environment: implication for release of genetically engineered microorganisms. Bio/Technology 3, 817-820.
18. Colwell, R.R., P.R. Brayton, D. Herrington, B.D. Tall, A. Huq, and M.M. Levine. 1996. Viable but nonculturable Vibrio cholerae O1 revert to a culturable state in human intestine. World J. Microb. Biotechnol. 12, 28-31.
19. Créach, V., A.-C. Baudoux, G. Bertru, and B. Le Rouzic. 2003. Direct estimate of active bacteria: CTC use and limitations. J. Microbiol. Meth. 52, 19-28.
20. Day, A.P and J.D. Oliver. 2004. Changes in membrane fatty acid composition during entry of Vibrio vulnificus into the viable but nonculturable state. J. Microbiol. 42, 69-73.
21. Federighi, M., J.L. Tholozan, J.M. Cappelier, J.P Tissier, and J.L. Jouve. 1998. Evidence of non-coccoid viable but non-culturable Campylobacter jejuni cells in microcosm water by direct viable count, CTC-DAPI double staining, and scanning electron microscopy. Food Microbiol. 15, 539-550.
22. Gunasekera, T.S., A. Sørensen, P.V. Attfield, S.J. Sørensen, and D.A. Veal. 2002. Inducible gene expression by nonculturable bacteria in milk after pasteurization. Appl. Environ. Microbiol. 68, 1988-1993.
23. Hegarty, J.P., M.T. Dowd, and K.H. Baker. 1999. Occurrence of Helicobacter pylori in surface water in the United States. J. Appl. Microbiol. 87, 697-701.
24. Heim, S., M.D.M. Lleo, B. Bonato, C.A. Guzman, and P. Canepari. 2002. The viable but nonculturable state and starvation are different stress responses of Enterococcus faecalis, as determined by proteome analysis. J. Bacteriol. 184, 6739-6745.
25. Hülsmann, A., T.M. Rosche, I.-S. Kong, H.M. Hassan, D.M Beam, and J.D. Oliver. 2003. RpoS-dependent stress response and exoenzyme production in Vibrio vulnificus. Appl. Environ. Microbiol. 69, 6114-6120.
26. Hulfen, K., S.W. Han, H. Enroth, P.D. Klein, A.R. Opekun, R.H. Gilman, D.G. Evans, L. Engstrand, D.Y. Graham, and F.A. El-Zaatari. 1996. Helicobacter pylori in the drinking water in Peru. Gastroenterology 110, 1031-1035.
27. Jones, D.M., E.M. Sutcliffe, and A. Curry. 1991. Recovery of viable but non-culturable Campylobacter jejuni. J. Gen. Microbiol. 137, 2477-2482.
28. Kell, D.B., A.S. Kapreylants, D.H. Weichart, C.L. Harwood, and M.R. Barer. 1998. Viability and activity in readily culturable bacteria: a review and discussion of the practical issues. Ant. van Leeuvenhoek 73, 169-187.
29. Kogure, K., U. Simidu, and N. Taga. 1979. A tentative direct microscopic method for counting living marine bacteria. Can. J. Microbiol. 25, 415-420.
30. Kong, I.-S., A. Huelsmann, T.C. Bates, H. Hassan, and J.D. Oliver. 2004. The role of reactive oxygen species in the viable but non-culturable state in Vibrio vulnificus. FEMS Microbiol. Ecol. 50, 133-142.
31. Lambert, J.R., S.K. Lin, and J. Aranda-Michel. 1995. Helicobacter pylon. Scand. J. Gastroenterol. 30(Suppl. 208), 33-46.
32. Lleò, M.M., S. Pierobon, M.C. Tafi, C. Signoreto, and P. Canepari, 2000. mRNA detection by reverse transcription-PCR for monitoring viability over time in an Enterococcus faecalis viable but nonculturable population maintained in a laboratory microcosm. Appl. Environ. Microbiol. 66, 4564-4567.
33. Lleò, M.M., B. Bonato, M.C. Tafi, C. Signoretto, M. Boaretti, and P. Canepari. 2001. Resuscitation rate in different enterococcal species in the viable but non-culturable state. J. Appl. Microbiol. 91, 1095-1102.
34. Makino, S.-I., T. Kii, H. Asakura, T. Shirahata, T. Ikeda, K. Takeshi, and K. Itoh. 2000. Does enterohaemorrhagic Escherichia coli O157 enter the VNC state in salmon roe? Appl. Environ. Microbiol 66, 5536-5539.
35. McDougald, D., J.I. Prosser, L.A. Glover, and J.D. Oliver. 1995. Effect of temperature and plasmid carriage on nonculturability in organisms targeted for release. FEMS Microbiol. Ecol. 17, 229-238.
36. McFeters, G.A., F.P. Yu, B.H. Pyle, and P.S. Stewart. 1995. Physiological assessment of bacteria using fluorochromes. J. Microbiol. Meth. 21, 1-13.
37. McGovern, V.P. and J.D. Oliver. 1995. Induction of cold responsive proteins in Vibrio vulnificus. J. Bacteriol. 177, 4131-4133.
38. 2-degrading compounds. Arch. Microbiol. 172, 63-67.
39. Mizunoe, Y., S.N. Wai, T. Ishikawa, A. Takade, and S.-i. Yoshida. 2000. Resuscitation of viable but nonculturable cells of Vibrio parahaemolyticus induced at low temperature under starvation. FEMS Microbiol. Lett. 186, 115-120.
40. Moreno, Y., M.A. Ferrus, J.L. Alonso, A. Jimenez, and J. Hernandez. 2003. Use of fluorescent in situ hybridization to evidence the presence of Helicobacter pylori in water. Water Res. 37, 2251-2256.
41. Morton, D. and J.D. Oliver. 1994. Induction of carbon starvation proteins in Vibrio vulnificus. Appl. Environ. Microbiol. 60, 3653-3659.
42. Mukamolova, G.V., N.D. Yanopolskaya, D.B. Kell, and A.S. Kaprelyants. 1998a. On resuscitation from the dormant state of Micrococcus luteus. Ant. Van Leeuwen. 73, 237-243.
43. Mukamolova, G.V, A.S. Kaprelyants, D.I. Young, M. Young, and D.B. Kell. 1998b. A bacterial cytokine. Proc. Natl. Acad. Sci. USA 95, 8916-8921.
44. Mukamolova, G.V., S.S. Kormer, D.B. Kell, and A.S. Kaprelyants. 1999. Stimulation of the multiplication of Micrococcus luteus by an autocrine growth factor. Arch Microbiol. 172, 9-14.
45. Oliver, J.D. 1993. Formation of viable but nonculturable cells, p. 239-272. In S. Kjelleberg (ed.), Starvation in Bacteria. Plenum Press, NY.
46. Oliver, J.D. 2000a. Problems in detecting dormant (VBNC) cells and the role of DNA elements in this response, p. 1-15. In J.K. Jansson, J.D. van Elsas, and M.J. Bailey (eds.), Tracking Genetically-Engineered Microorganisms. Landes Biosciences, Georgetown, TX.
47. Oliver, J.D. 2000b. The public health significance of viable but non-culturable bacteria, p. 277-299. In R.R. Colwell and D.J. Grimes (eds.), Nonculturable Microorganisms in the Environment. American Society for Microbiology Press, Washington, D.C.
48. Oliver, J.D. 2000c. The viable but nonculturable state and cellular resuscitation, p. 723-730. In C.R. Bell, M. Brylinsky, and P. Johnson-Green (eds.), Microbial Biosystems: New Frontiers. Atlantic Canada Soc. Microb. Ecol., Halifax, Canada.
49. Oliver, J.D. 2005. Viable but nonculturable bacteria in food environments. In P.M. Fratamico and A.K. Bhunia (eds.), Food Borne Pathogens: Microbiology and Molecular Biology. Horizon Scientific Press, Norfolk, U.K. (in press).
50. Oliver, J.D. and R. Bockian. 1995. In vivo resuscitation, and virulence towards mice, of viable but nonculturable cells of Vibrio vulnificus. Appl. Environ. Microbiol. 61, 2620-2623.
51. Oliver, J.D., L. Nilsson, and S. Kjelleberg. 1991. The formation of nonculturable cells of Vibrio vulnificus and its relationship to the starvation state. Appl. Environ. Microbiol. 57, 2640-2644.
52. Oliver, J.D., M. Dagher, and K. Linden. 2005. Induction of Escherichia coli and Salmonella typhimurium into the viable but non-culturable state following chlorination of wastewater. J. Water and Health (in press).
53. Oliver, J.D., F. Hite, D. McDougald, N.L. Andon, and L.M. Simpson. 1995. Entry into, and resuscitation from, the viable but nonculturable state by Vibrio vulnificus in an estuarine environment. Appl. Environ. Microbiol. 61, 2624-2630.
54. Peterson, W. I. 1991. Helicobacter pylori and peptic ulcer disease. N. Engl. J. Med. 324, 1043-1048.
55. Porter, J., C. Edwards, and R.W. Pickup. 1995. Rapid assessment of physiological status in Escherichia coli using fluorescent probes. J. Appl. Bacteriol. 4, 399-408.
56. Pruzzo, C., R. Tarsi, M.M. Lleò, C. Signoretto, M. Zampini, R.R. Colwell, and P. Canepari. 2002. Rapid assessment of physiological status in Escherichia coli using fluorescent probes. Curr. Microbiol. 45, 105-110.
57. Rahman, I., M. Shahamat, P.A. Kirchman, E. Russek-Cohen, and R.R. Colwell. 1994. Methionine uptake and cytopathogenicity of viable but nonculturable Shigella dysentenae Type 1. Appl. Environ. Microbiol. 60, 3573-3578.
58. Rahman, I., M. Shahamat, M.A.R. Chowdhury, and R.R. Colwell. 1996. Potential virulence of viable but nonculturable Shigella dysenteriae Type 1. Appl. Environ. Microbiol. 62, 115-120.
59. Rodriguez, G.G., D. Phipps, K. Ishiguro, and H.F. Ridgway. 1992. Use of a fluorescent redox probe for direct visualization of actively respiring bacteria. Appl. Environ. Microbiol. 58, 1801-1808.
60. Rosenberg, E. and Y. Ben-Haim. 2002. Microbial diseases of corals and global warming. Environ. Microbiol. 4, 318-326.
61. Saux, M.F.-L., D. Hervio-Heath, S. Loaec, R.R. Colwell, and M. Pommepuy. 2002. Detection of cytotoxin-hemolysin mRNA in nonculturable populations of environmental and clinical Vibrio vulnificus strains in artificial seawater. Appl. Environ. Microbiol. 68, 5641-5646.
62. Signoretto, C., M.M. Lleò, and P. Canepari. 2002. Modification of the peptidoglycan of Escherichia coli in the viable but nonculturable state. Curr. Microbiol. 44, 125-131.
63. Signoretto, C., M.M. Lleò, M.C. Tafi, and P. Canepari. 2000. Cell wall chemical composition of Enterococcus faecalis in the viable but nonculturable state. Appl. Environ. Microbiol. 66, 1953-1959.
64. Steinert, M., L. R. Emody, Amann et al. 1997. Resuscitation of viable but nonculturable Legionella pneumophila Philadelphia JR32 by Acanthamoeba castellanii. Appl. Environ. Microbiol. 63, 2047-2053.
65. Tholozan, J.L., J.M. Cappelier, J.P. Tissier, G. Delattre, and M. Federighi. 1999. Physiological characterization of viable-but-non-culturable Camplyobacter jejuni cells. Appl. Environ. Microbiol. 65, 1110-1116.
66. Warner, J.M. and J.D. Oliver. 1998. Randomly amplified polymorphic DNA analysis of starved and viable but nonculturable Vibrio vulnificus cells. Appl. Environ. Microbiol. 64, 3025-3028.
67. Whitesides, M.D. and J.D. Oliver. 1997. Resuscitation of Vibrio vulnificus from the viable but nonculturable state. Appl. Environ. Microbiol. 64, 3025-3028.
68. Wolf, P. and J.D. Oliver. 1992. Temperature effects on the viable but nonculturable state of Vibrio vulnificus. FEMS Microbiol. Ecol. 101, 33-39.
69. Xu, H.-S., N. Roberts, F.L. Singleton, R.W. Attwell, D.J. Grimes, and R.R. Colwell. 1982. Survival and viability of nonculturable Escherichia coli and Vibrio cholerae in the estuarine and marine environment. Microb. Ecol. 8, 313-323.
70. Yaron, S. and K. Matthews. 2002. A reverse transcriptase-polymerase chain reaction assay for detection of viable Escherichia coli O157:H7: investigation of specific target genes. J. Appl. Microbiol. 92, 633-640.
71. Zimmerman, R., R. Iturriaga, and J. Becker-Birck. 1978. Simultaneous determination of the total number of aquatic bacteria and the number thereof involved in respiration. Appl. Environ. Microbiol. 36, 926-935.