Environmental Parameters Associated with the Viable but Nonculturable State

  • Michel J. Gauthier


In 1985, Colwell and coworkers introduced the term “viable but nonculturable (VBNC) bacterial cells” to distinguish particular cells that could not form colonies on solid media but maintained metabolic activity and the ability to elongate after the administration of nutrients. The evolution of bacteria towards a VBNC state in natural environments (or under experimental conditions that mimic environmental ones) is now well established and documented (87, 101, 120). This state is obviously of high interest to our general understanding of microbial ecology. It is also of special concern when considering release in the environment of bacterial pathogens or indicators such as fecal coliforms, which may escape detection via routine bacteriological procedures and/or modify their virulence.


Glycine Betaine Enteric Bacterium Nutrient Starvation Micrococcus Luteus VBNC State 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Adhikari, P. C. 1975. Sensitivity of cholera and El Tor vibrios to cold shock. J. Gen. Microbiol. 87:163–166.PubMedGoogle Scholar
  2. 2.
    Alexander, E., D. Pham, and T. R. Steck. 1999. The viable-but-nonculturable condition is induced by copper in Agrobacterium tumefaciens and Rhizobium leguminosarum. Appl. Environ. Microbiol. 65:3754–3756.PubMedGoogle Scholar
  3. 3.
    Allen-Austin, D., B. Austin, and R. R. Colwell. 1984. Survival of Aeromonas salmonicida in river water. FEMS Microbiol. Lett. 21:143–146.CrossRefGoogle Scholar
  4. 4.
    Amy, P. S., C. Durham, D. Hall, and D. L. Haldeman. 1993. Starvation-survival of deep subsurface isolates. Curr. Microbiol. 26:345–352.CrossRefGoogle Scholar
  5. 5.
    Arana, I., A. Muela, J. Iriberri, L. Egea, and I. Barcina. 1992. Role of hydrogen peroxide in loss of culturability mediated by visible light in Escherichia coli in a freshwater ecosystem. Appl. Environ. Microbiol. 58:3903–3907.PubMedGoogle Scholar
  6. 6.
    Barcina, I., J. M. Gonzalez, J. Iriberri, and L. Egea. 1989. Effect of visible light on progressive dormancy of Escherichia coli cells during the survival process in natural freshwater. Appl. Environ. Microbiol. 55:246–251.PubMedGoogle Scholar
  7. 7.
    Barcina, I., J. M. Gonzalez, J. Iriberri, and L. Egea. 1990. Survival strategy of Escherichia coli and Enterococcus faecalis in illuminated fresh and marine systems. J. Appl. Bacteriol. 68:189–198.PubMedCrossRefGoogle Scholar
  8. 8.
    Bauerfeind, S., G. G. Gerhardt, and G. Rheiheimer. 1981. Investigations on the survival of fecal bacteria in experiments with or without sediments. Zentbl. Bakt. Parasitikd. Infekt. Hyg. 174:364–374.Google Scholar
  9. 9.
    Bej, A. K., M. H. Mahbubani, and R. M. Atlas. 1991. Detection of viable Legionella pneumophila in water by polymerase chain reaction and gene probe methods. Appl. Environ. Microbiol. 57:597–600.PubMedGoogle Scholar
  10. 10.
    Beumer, R. R., J. de Vries, and F. M. Rombouts. 1992. Campylobacter jejuni non-culturable coccoid cells. Int. J. Food Microbiol. 15:153–163.PubMedCrossRefGoogle Scholar
  11. 11.
    S. N., M. R. Adams,A. H. L. Chamberlain. 1993. Viabilityculturability of Campylobacter jejuni. In 62nd Annual Meeting of the Society for Applied Bacteriology, Nottingham, U.K.Google Scholar
  12. 12.
    Bryan, P. J., R. J. Steffan, A. DePaola, J. W. Foster, and A. K. Bej. 1999. Adaptative response to cold temperature in Vibrio vulnificus. Curr. Microbiol. 38:168–175.PubMedCrossRefGoogle Scholar
  13. 13.
    Byrd, J. J., and R. R. Colwell. 1990. Maintenance of plasmids pBR322 and pUC8 in nonculturable Escherichia coli in the marine environment. Appl. Environ. Microbiol. 56:2104–2107.PubMedGoogle Scholar
  14. 14.
    Byrd, J. J., H.-S. Xu, and R. R. Colwell. 1991. Viable but nonculturable bacteria in drinking water. Appl. Environ. Microbiol. 57:875–878.PubMedGoogle Scholar
  15. 15.
    Cappelier, J. M., B. Lazaro, A. Rossero, A. Fernandes-Astorga, and M. Federighi. 1997. Double staining (CTC-DAPI) for detection and enumeration of viable but non-culturable Campylobacter jejuni cells. Vet. Res. 28:547–555.PubMedGoogle Scholar
  16. 16.
    Carlucci, A. F., and D. Pramer. 1960. An evaluation of factors affecting the survival of Escherichia coli in seawater. II. Salinity, pH and nutrients. Appl. Microbiol. 8:243–247.PubMedGoogle Scholar
  17. 17.
    Carrillo, M., E. Estrada, and T. C. Hazen. 1985. Survival and enumeration of the fecal indicators Bifidobacterium adolescentis and Escherichia coli in a tropical rain forest watershed. Appl. Environ. Microbiol. 50:468–476.PubMedGoogle Scholar
  18. 18.
    Cellini, L., I. Robuffo, E. Di Campli, S. Di Bartolomeo, T. Taraborelli, and B. Dainelli. 1998. Recovery of Helicobacter pylori ATCC43504 from a viable but not culturable state: regrowth or resuscitation? APMIS 106:571–579.PubMedCrossRefGoogle Scholar
  19. 19.
    Chamberlin, C. E., and R. Mitchell. 1978. A decay model for enteric bacteria in natural waters, p. 325–348. In R. Mitchell (ed.), Water Pollution Microbiology, vol. 2. Wiley, New York, N.Y.Google Scholar
  20. 20.
    Chambers, S. T., and C. M. Kunin. 1985. The osmoprotective properties of urine for bacteria: the protective effect of betaine and human urine against low pH and high concentrations of electrolytes, sugars and urea. J. Infect. Dis. 152:1308–1315.PubMedCrossRefGoogle Scholar
  21. 21.
    Chambers, S. T., and C. M. Kunin. 1987. Isolation of glycine betaine and proline betaine form human urine. Assessment of their role as osmoprotective agents for bacteria and the kidney. J. Clin. Invest. 79:731–737.PubMedCrossRefGoogle Scholar
  22. 22.
    Chambers, S. T., and C. M. Kunin. 1987. Osmoprotective activity for Escherichia coli in mammalian renal inner medulla and urine: correlation of glycine and proline betaines and sorbitol with response to osmotic stress. J. Clin. Invest. 80:1255–1260.PubMedCrossRefGoogle Scholar
  23. 23.
    Chmielewski, R. A., and J. F. Frank. 1995. Formation of viable but nonculturable Salmonella during starvation in chemically defined solutions. Lett. Appl. Microbiol. 20:380–384.PubMedCrossRefGoogle Scholar
  24. 24.
    Cho, J. C., and S. J. Kim. 1999. Green fluorescent protein-based direct viable count to verify a viable but non-culturable state of Salmonella typhi in environmental samples. J. Microbiol. Methods. 36:227–235.PubMedCrossRefGoogle Scholar
  25. 25.
    Cho, J. C., and S. J. Kim. 1999. Viable, but non-culturable state of a green fluorescence proteintagged environmental isolate of Salmonella typhi in ground water and pond water. FEMS Microbiol. Lett. 170:257–264.PubMedCrossRefGoogle Scholar
  26. 26.
    Chowdhury, M. A., A. Huq, B. Xu, F. J. Madeira, and R. R. Colwell. 1997. Effect of alum on free-living and copepod-associated Vibio cholerae O1 and 0139. Appl. Environ. Microbiol. 63:3323–3326.PubMedGoogle Scholar
  27. 27.
    Colwell, R. R. 1987. Vibrios in the Environment. John Wiley and Sons, New York, N.Y.Google Scholar
  28. 28.
    Colwell, R. R., P. R. Brayton, D. J. Grimes, D. B. Roszak, S. A. Huq, and L. M. Palmer. 1985. Viable but non-culturable Vibrio cholerae and related pathogens in the environment: implications for the release of genetically engineered microorganisms. Bio/Technology 3:817–820.CrossRefGoogle Scholar
  29. 29.
    Colwell, R. R., M. L. Tamplin, P. R. Brayton, A. L. Gauzens, B. D. Tall, D. Herrington, M. M. Levine, S. Hall, A. Huq, and D. A. Sack. 1990. Environmental aspects of Vibrio cholerae in transmission of cholera, p. 327–343. In R.B. Sack and Y. Zinnaka (ed.), Advances on Cholera and Related Diarrheas, KTK Scientific, Tokyo, Japan.Google Scholar
  30. 30.
    Combarro, M.-P., M. J. Gauthier, G. N. Flatau, and R. L. Clément. 1992. Effect of a transient incubation in wastewater on the sensitivity to seawater of Escherichia coli cells grown under intestinal-like conditions. Biomed. Lett. 47:185–190.Google Scholar
  31. 31.
    Csonka, L. N. 1989. Physiological and genetic responses of bacteria to osmotic stress. Microbiol. Rev. 53:212–247.Google Scholar
  32. 32.
    Csonka, L. N., and A. D. Hanson. 1991. Prokaryotic osmoregulation: genetics and physiology. Annu. Rev. Microbiol. 45:569–606.PubMedCrossRefGoogle Scholar
  33. 33.
    Davies, C. M., and L. M. Evison. 1991. Sunlight and the survival of enteric bacteria in natural waters. J. Appl. Bacteriol. 70:265–274.PubMedCrossRefGoogle Scholar
  34. 34.
    Davies, C. M., J. A. Long, M. Donald, and N. J. Ashbolt. 1995. Survival of fecal microorganisms in marine and freshwater sediments. Appl. Environ. Microbiol. 61:1888–1896.PubMedGoogle Scholar
  35. 35.
    Desmonts, C., J. Minet, R. R. Colwell, and M. Cormier. 1990. Fluorescent-antibody method useful for detecting viable but nonculturable Salmonella spp. in chlorinated wastewater. Appl. Environ. Microbiol. 56:1448–1452.PubMedGoogle Scholar
  36. 36.
    Dukan, S., Y. Levi, and D. Touati. 1997. Recovery of culturability of an HOCl-stressed population of Escherichia coli after incubation in phosphate buffer: resuscitation or regrowth? Appl. Environ. Microbiol. 63:4204–4209.PubMedGoogle Scholar
  37. 37.
    Duncan, S., L. A. Glover, K. Killham, and J. I. Prosser. 1994. Luminescence-based detection of activity of starved and viable but nonculturable bacteria. Appl. Environ. Microbiol. 60:1308–1316.PubMedGoogle Scholar
  38. 38.
    Eisenstark, A., C. Miller, J. Jones, and S. Leven. 1992. Escherichia coli genes involved in cell survival during dormancy: role of oxidative stress. Biochem. Biophys. Res. Commun. 188:1054–1059.PubMedCrossRefGoogle Scholar
  39. 39.
    Ensign, J. C. 1970. Long-term starvation survival of rod and spherical cells of Arthrobacter crystallopoietes. J. Bacteriol. 103:569–577.PubMedGoogle Scholar
  40. 40.
    Faust, M. A., A. E. Aotaky, and M. T. Hargadon. 1975. Effect of physical parameters on the in situ survival of Escherichia coli MC-6 in an estuarine environment. Appl. Microbiol. 30:800–806.PubMedGoogle Scholar
  41. 41.
    Flint, K. P. 1987. Long term survival of Escherichia coli in river water. J. Appl. Bacteriol. 63:261–270.PubMedCrossRefGoogle Scholar
  42. 42.
    Fry, J. C., and T. Zia. 1982. A method for estimating viability of aquatic bacteria by slide culture. J. Appl. Bacteriol. 53:189–198.CrossRefGoogle Scholar
  43. 43.
    Gauthier, M. J., P. M. Munro, and S. Mohadjer. 1987. Influence of salt and sodium chloride on the recovery of Escherichia coli from seawater. Curr. Microbiol. 15:5–10.CrossRefGoogle Scholar
  44. 44.
    Gauthier, M. J., and D. LeRudulier. 1990. Survival in seawater of Escherichia coli cells grown in marine sediments containing glycine betaine. Appl. Environ. Microbiol. 56:2915–2918.PubMedGoogle Scholar
  45. 45.
    Gauthier, M. J., G. N. Flatau, D. LeRudulier, R. L. Clément, and M. P. Combarro-Combarro. 1991. Intracellular accumulation of potassium and glutamate specifically enhances survival of Escherichia coli in seawater. Appl. Environ. Microbiol. 57:272–276.PubMedGoogle Scholar
  46. 46.
    Gauthier, M. J., S. A. Benson, G. N. Flatau, R. L. Clément, V. A. Breittmayer, and P. M. Munro. 1992. OmpC and OmpF porins influence viability and culturability of Escherichia coli cells incubated in seawater. Microb. Releases. 1:47–50.PubMedGoogle Scholar
  47. 47.
    Gauthier, M. J., G. N. Flatau, P. M. Munro, and R. L. Clément. 1993. Glutamate uptake and synthesis by Escherichia coli cells in seawater: effects on culturability loss and glycine betaine transport. Microb. Releases 2:53–59.PubMedGoogle Scholar
  48. 48.
    Gerba, C. P., and J. S. McLeod. 1976. Effect of sediments on the survival of Escherichia coli in marine waters. Appl. Environ. Microbiol. 32:114–120.PubMedGoogle Scholar
  49. 49.
    Ghoul, M., T. Bernard, and M. Cormier. 1990. Evidence that Escherichia coli accumulates glycine betaine from marine sediments. Appl. Environ. Microbiol. 56:551–554.PubMedGoogle Scholar
  50. 50.
    Gonzalez, J. M., J. Iriberri, L. Egea, and I. Barcina. 1992. Characterization of culturability, protistan grazing and death of enteric bacteria in aquatic ecosystems. Appl. Environ. Microbiol. 58: 998–1004.PubMedGoogle Scholar
  51. 51.
    Gottschal, J. C. 1992. Substrate capturing and growth in various ecosystems. J. Appl. Bacteriol. 73:39s–48s.CrossRefGoogle Scholar
  52. 52.
    Gourmelon, M., J. Cillard, and M. Pommepuy. 1994. Visible light damage to Escherichia coli in seawater: oxidative stress hypothesis. J. Appl. Bacteriol. 77:105–112.PubMedCrossRefGoogle Scholar
  53. 53.
    Grimes, D. J., and R. R. Colwell. 1986. Viability and virulence of Escherichia coli suspended by membrane chamber in semitropical ocean water. FEMS Microbiol. Lett. 34:161–165.CrossRefGoogle Scholar
  54. 54.
    Harvey, P., and S. Leach. 1998. Analysis of coccal cell formation by Campylobacter jejuni using continuous culture techniques, and the importance of oxidative stress. J. Appl. Microbiol. 85:398–404.PubMedCrossRefGoogle Scholar
  55. 55.
    Hazen, T. C., F. A. Fuentes, and J. W. Santo Domingo. 1986. In situ survival and activity of pathogens and their indicators, p. 406–411. In F. Megusar and M. Gantar (ed.), Perspectives in Microbial Ecology. Slovene Society for Microbiology, Ljubljana, Slovenia.Google Scholar
  56. 56.
    Heidelberg, J. F., M. Shahamat, M. Levin, I. Rahman, G. Stelma, C. Grim, and R. R. Colwell 1997. Effects of aerosolization on culturability and viability of gram-negative bacteria. Appl. Environ. Microbiol. 63:3585–3588.PubMedGoogle Scholar
  57. 57.
    Hengge-Aronis, R., R. Lange, N. Henneberg, and D. Fischer. 1993. Osmotic regulation of rpoS-dependent genes in Escherichia coli. J. Bacteriol. 175:259–265.PubMedGoogle Scholar
  58. 58.
    Hengge-Aronis, R. 1993. Survival of hunger and stress: the role of rpoS in early stationary phase gene regulation in Escherichia coli. Cell 72:165–168.PubMedCrossRefGoogle Scholar
  59. 59.
    Hoff, K. A. 1989. Survival of Vibrio anguillarum and Vibrio salmonicida at different salinities. Appl. Environ. Microbiol. 55:1775–1786.PubMedGoogle Scholar
  60. 60.
    Holmquist, L., and S. Kjelleberg. 1993. Changes in viability, respiratory activity and morphology of the marine Vibrio sp. strain S14 during starvation of individual nutrients and subsequent recovery. FEMS Microbiol. Ecol. 12:215–224.CrossRefGoogle Scholar
  61. 61.
    Hood, M. A., and G. E. Ness. 1982. Survival of Vibrio cholerae and Escherichia coli in estuarine waters and sediments. Appl. Environ. Microbiol. 43:478–584.Google Scholar
  62. 62.
    Hussong, D., R. R. Colwell, M. O’Brien, E. Weiss, A. D. Pearson, R. M. Weiner, and W. D. Burge. 1987. Viable Legionella pneumophila not detectable by culture on agar media. Bio/Technology 5:947–950.CrossRefGoogle Scholar
  63. 63.
    Islam, M. S., M. K. Hasan, M. A. Miah, G. C. Sur, A. Felsenstein, M. Venkatesan, R. B. Sack, and M. J. Albert. 1993. Use of the polymerase chain reaction and fluorescent-antibody methods for detecting viable but nonculturable Shigella dysenteriae type 1 in laboratory microcosms. Appl. Environ. Microbiol. 59:536–540.PubMedGoogle Scholar
  64. 64.
    Jacob, J., W. Martin, and C. Höller. 1993. Characterization of viable but nonculturable stage of Campylobacter coli, characterized with respect to electron microscopic findings, whole cell protein and lipooligosaccharide LOS. patterns. Zentralbl. Mikrobiol. 148:3–10.PubMedGoogle Scholar
  65. 65.
    Jenkins, D. E., S. A. Chaisson, and A. Matin. 1990. Starvation-induced cross protection against osmotic challenge in Escherichia coli. J. Bacteriol. 172:2779–2781.PubMedGoogle Scholar
  66. 66.
    Jiang, X., and T. J. Chai. 1996. Survival of Vibrio parahaemolyticus at low temperature under starvation conditions and subsequent resuscitation of viable, nonculturable cells. Appl. Environ. Microbiol. 62:1300–1305.PubMedGoogle Scholar
  67. 67.
    Jones, D. M., E. M. Sutcliffe, and A. Curry. 1991. Recovery of viable but non-culturable Campylobacter jejuni. J. Gen. Microbiol. 137:2477–2482.PubMedGoogle Scholar
  68. 68.
    Jouper-Jaan, A., A. E. Goodman, and S. Kjelleberg. 1992. Bacteria starved for prolonged periods develop increased protection against lethal temperatures. FEMS Microbiol. Ecol. 101:229–236.Google Scholar
  69. 69.
    Kaasen, I., P. Falkenberg, O. B. Styrvold, and A. R. Strom. 1992. Molecular cloning and physical mapping of the otsA genes, which encode the osmoregulatory trehalose pathway of Escherichia coli: evidence that transcription is activated by KatF (AppR). J. Bacteriol. 174:889–898.PubMedGoogle Scholar
  70. 70.
    Kaprelyants, A. S., and D. B. Kell. 1992. Rapid assessment of bacterial viability and vitality by rhodamine 123 and flow cytometry. J. Appl. Bacteriol. 72:410–422.CrossRefGoogle Scholar
  71. 71.
    Kaprelyants, A. S., and D. B. Kell. 1993. Dormancy in stationary-phase cultures of Micrococcus luteus: flow cytometric analysis of starvation and resuscitation. Appl. Environ. Microbiol. 59:3187–3196.PubMedGoogle Scholar
  72. 72.
    Kaprelyants, A. S., J. C. Gottschal, and D. B. Kell. 1994. Dormancy in non-sporulating bacteria. FEMS Microbiol. Rev. 104:271–286.Google Scholar
  73. 73.
    Karmali, M. A., and P. C. Fleming. 1979. Campylobacter enteritis. Can. J. Microbiol. 120:1525–1532.Google Scholar
  74. 74.
    Kjelleberg, S. (ed.). 1993. Starvation in Bacteria. Plenum Press, New York, N.Y.Google Scholar
  75. 75.
    Kogure, K., U. Simidu, and N. Taga. 1979. A tentative direct microscopic method for counting living marine bacteria. Can. J. Microbiol. 25:415–420.PubMedCrossRefGoogle Scholar
  76. 76.
    Konishi, H., and Z. Yoshii. 1986. Determination of the spiral conformation of Aquaspirillum spp. by scanning electron microscopy of elongated cells induced by cephalexin treatment. J. Gen. Microbiol. 132:877–881.PubMedGoogle Scholar
  77. 77.
    Kunin, C. M., T. H. Hua, L. Van Arsdale, and M. Villarejo. 1992. Growth of Escherichia coli in human urine: role of salt tolerance and accumulation of glycine betaine. J. Infect. Dis. 166:1311–1315.PubMedCrossRefGoogle Scholar
  78. 78.
    Lederc, H., D. A. A. Mossel. 1989. Le tube digestif, p. 141-162. In H. Leclerc and D. A. A. Mossel (ed.), Microbiologie: le Tube Digestif, l’Eau et les Aliments. Doin, Paris, France.Google Scholar
  79. 79.
    Linder, K., and J. D. Oliver. 1989. Membrane fatty acid and virulence changes in the viable but nonculturable state of Vibrio vulnificus. Appl. Environ. Microbiol. 55:2837–2842.PubMedGoogle Scholar
  80. 80.
    Lleo, M. D. M., M. C. Tafi, and P. Canepari. 1998. Nonculturable Enterobacter faecalis cells are metabolically active and capable of resuming active growth. Syst. Appl. Microbiol. 21:333–339.PubMedCrossRefGoogle Scholar
  81. 81.
    Lopez-Torres, A. J., L. Prieto, and T. C. Hazen. 1988. Comparison of the in situ survival and activity of Klebsiella pneumoniae and Escherichia coli in tropical marine evironments. Microb. Ecol. 15:41–57.CrossRefGoogle Scholar
  82. 82.
    Magarinos, B., J. L. Romalde, J. L. Barja, and A. E. Toranzo. 1994. Evidence of a dormant but infective state of the fish pathogen Pasteurella piscicida in seawater and sediment. Appl. Environ. Microbiol. 60:180–186.PubMedGoogle Scholar
  83. 83.
    Mai, U. E. H., M. Shahamat, and R. R. Colwell. 1990. Survival of Helicobacter pylori in the environment in a dormant but viable stage. Rev. Esp. Enferm. Dig. 78(Suppl. 1):17.Google Scholar
  84. 84.
    Mason, D. J., E. G. Power, H. Talsania, I. Phillips, and V. A. Gant. 1995. Antibacterial action of ciprofloxacin. Antimicrob. Agents Chemother. 39:2752–2758.PubMedGoogle Scholar
  85. 85.
    Matin, A. 1991. The molecular basis of carbon-starvation-induced general resistance in Escherichia coli. Mol. Microbiol. 5:3–10.PubMedCrossRefGoogle Scholar
  86. 86.
    McCann, M. P., J. P. Kidwell, and A. Matin. 1991. The putative σ factor KatF has a central role in development of starvation-mediated general resistance in Escherichia coli. J. Bacteriol. 173:4188–4194.PubMedGoogle Scholar
  87. 87.
    McKay, A. M. 1992. Viable but non-culturable forms of potentially pathogenic bacteria in water. Lett. Appl. Microbiol. 14:129–135.CrossRefGoogle Scholar
  88. 88.
    Medema, G. J., F. M. Schets, A. W. van de Giessen, and A. H. Havelaar. 1992. Lack of colonization of 1 day old chicks by viable, non-culturable Campylobacter jejuni. J. Appl. Bacteriol. 72: 512–516.PubMedCrossRefGoogle Scholar
  89. 89.
    Moran, A. P., and M. E. Upton. 1986. A comparative study of the rod and coccoid forms of Campylobacter jejuni ATCC 29428. J. Appl. Bacteriol. 60:103–110.PubMedCrossRefGoogle Scholar
  90. 90.
    Morgan, J. A. W., P. A. Cranwell, and R. W. Pickup. 1991. Survival of Aeromonas salmonicida in lake water. Appl. Environ. Microbiol. 57:1777–1782.PubMedGoogle Scholar
  91. 91.
    Morgan, J. A. W., K. J. Clarke, G. Rhodes, and R. W. Pickup. 1992. Non-culturable Aeromonas salmonicida in lake water. Microb. Releases 1:71–78.PubMedGoogle Scholar
  92. 92.
    Morgan, J. A. W., G. Rhodes, and R. W. Pickup. 1993. Survival of nonculturable Aeromonas salmonicida in lake water. Appl. Environ. Microbiol. 59:874–880.PubMedGoogle Scholar
  93. 93.
    Moriarty, D. J. W., and R. T. Bell. 1993. Bacterial growth and starvation in aquatic environments, p. 25–53. In S. Kjelleberg (ed.), Starvation in Bacteria. Plenum Press, New York, N.Y.Google Scholar
  94. 94.
    Morita, R. Y. 1993. Bioavailability of energy and the starvation state, p. 1–23. In S. Kjelleberg (ed.), Starvation in Bacteria. Plenum Press, New York, N.Y.Google Scholar
  95. 95.
    Munro, P. M., F. Laumond, and M. J. Gauthier. 1987. A previous growth of enteric bacteria on salted medium increases their survival in seawater. Lett. Appl. Microbiol. 4:121–124.CrossRefGoogle Scholar
  96. 96.
    Munro, P. M., M. J. Gauthier, V. A. Breittmayer, and J. Bongiovanni. 1989. Influence of osmoregulation processes on starvation survival of Escherichia coli in seawater. Appl. Environ. Microbiol. 55:2017–2024.PubMedGoogle Scholar
  97. 97.
    Munro, P. M., and M. J. Gauthier. 1993. Uptake of glutamate by Vibrio cholerae in media of low and high osmolarity and in seawater. Lett. Appl. Microbiol. 18:197–199.CrossRefGoogle Scholar
  98. 98.
    Munro, P. M., R. L. Clément, M. J. Gauthier, and G. N. Flatau. 1993. Effect of thermal, oxidative, acidic, osmotic or nutritional stresses on subsequent culturability of Escherichia coli in seawater. Microb. Ecol. 27:57–63.Google Scholar
  99. 99.
    Nikaido, H., and M. Vaara. 1987. Outer Membrane, p. 7–22. In F. C. Neidhardt, J. L. Ingraham, K. Brooks, B. Magasanik, M. Schaechter, and E. Umbarger (ed.), Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology. American Society for Microbiology, Washington, D.C.Google Scholar
  100. 100.
    Nilsson, L., J. D. Oliver, and S. Kjelleberg. 1991. Resuscitation of Vibrio vulnificus from the viable but nonculturable state. J. Bacteriol. 173:5054–5059.PubMedGoogle Scholar
  101. 101.
    Oliver, J. D. 1993. Formation of viable but nonculturable cells, p. 239–272. In S. Kjelleberg (ed.), Starvation in Bacteria. Plenum Press, New York, N.Y.Google Scholar
  102. 102.
    Oliver, J. D., and D. Wanucha. 1989. Survival of Vibrio vulnificus at reduced temperatures and elevated nutrient. J. Food Safety 10:79–86.CrossRefGoogle Scholar
  103. 103.
    Oliver, J. D., L. Nilsson, and S. Kjelleberg. 1991. Formation of nonculturable Vibrio vulnificus cells and its relationship to the starvation state. Appl. Environ. Microbiol. 57:2640–2644.PubMedGoogle Scholar
  104. 104.
    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.PubMedGoogle Scholar
  105. 105.
    Orlob, G. T. 1956. Viability of sewage bacteria in seawater. Sewage Ind. Wastes 28:1147–1167.Google Scholar
  106. 106.
    Palmer, L. M., A. M. Baya, D. J. Grimes, and R. R. Colwell. 1984. Molecular genetic and phenotypic alteration of Escherichia coli in natural water microcosms containing toxic chemicals. FEMS Microbiol. Lett. 21:169–173.CrossRefGoogle Scholar
  107. 107.
    Paszko-Kolva, C., M. Shahamat, H. Yamamoto, T. Sawyer, J. Vives-Rego, and R. R. Colwell. 1991. Survival of Legionella pneumophila in the aquatic environment. Microbiol. Ecol. 22:75–83.Google Scholar
  108. 108.
    Paszko-Kolva, C., M. Shahamat, and R. R. Colwell. 1993. Effect of temperature on survival of Legionella pneumophila in the aquatic environment. Microb. Releases 2:73–79.PubMedGoogle Scholar
  109. 109.
    Pedersen, J. C., and T. D. Leser. 1992. Survival of Enterobacter cloacae on leaves. Microb. Releases 1:95–102.Google Scholar
  110. 110.
    Pedersen, J. C., and C. S. Jacobsen. 1993. Fate of Enterobacter cloacae JP120 and Alcaligenes eutrophus AEO106 pRO101. in soil during water stress: effects on culturability and viability. Appl. Environ. Microbiol. 59:1560–1564.PubMedGoogle Scholar
  111. 111.
    Pitonzo, B. J., P. S. Amy, and M. Rudin. 1999a. Effect of gamma radiation on native endolithic microorganisms from a radioactive waste deposit site. Radiat. Res. 152:64–70.PubMedCrossRefGoogle Scholar
  112. 112.
    Pitonzo, B. J., P. S. Amy, and M. Rudin. 1999b. Resuscitation of microorganisms after gamma irradiation. Radiat. Res. 152:71–75.PubMedCrossRefGoogle Scholar
  113. 113.
    Pommepuy, M., M. Butin, A. Derrien, M. Gourmelon, R. R. Colwell, and M. Cormier. 1996. Retention of enteropathogenicity by viable but nonculturable Escherichia coli exposed to seawater and sunlight, Appl. Environ. Microbiol. 62:4621–4626.PubMedGoogle Scholar
  114. 114.
    Postgate, J. R., and J. R. Hunter. 1963. Acceleration of bacterial death by growth substrates. Nature 198:273.PubMedCrossRefGoogle Scholar
  115. 115.
    Preyer, J. M., and J. D. Oliver. 1993. Starvation-induced thermal tolerance as a survival mechanism in a psychrophilic marine bacterium. Appl. Environ. Microbiol. 59:2653–2656.PubMedGoogle Scholar
  116. 116.
    Rahman, I., M. Shahamat, P. A. Kirchman, E. Russek-Cohen, and R. R. Colwell. 1994. Methionine uptake and cytopathogenicity of viable but nonculturable Shigella dysenteriae type 1. Appl. Environ. Microbiol. 60:3573–3578.PubMedGoogle Scholar
  117. 117.
    Rollins, D. M., D. Roszak, and R. R. Colwell. 1985. Dormancy of Campylobacter jejuni in natural aquatic systems, p. 283–285. In A. D. Pearson and M. B. Skirrow (ed.), Campylobacter III, Proceedings of the Third International Symposium on Campylobacter Infections. Public Health Laboratory Service, London, United Kingdom.Google Scholar
  118. 118.
    Rollins, D. M., and R. R. Colwell. 1986. Viable but nonculturable stage of Campylobacter jejuni and its role in survival in the natural aquatic environment. Appl. Environ. Microbiol. 52:531–538.PubMedGoogle Scholar
  119. 119.
    Roszak, D. B., D. J. Grimes, and R. R. Colwell. 1984. Viable but nonrecoverable stage of Salmonella enterindis in aquatic systems. Can. J. Microbiol. 30:334–338.PubMedCrossRefGoogle Scholar
  120. 120.
    Roszak, D. B., and R. R. Colwell. 1987. Survival strategies of bacteria in the natural environment. Microbiol. Rev. 51:365–379.PubMedGoogle Scholar
  121. 121.
    Roth, W. G., M. P. Leckie, and D. N. Dietzler. 1985. Osmotic stress drastically inhibits active transport of carbohydrates by Escherichia coli. Biochem. Biophys. Res. Commun. 126:434–441.PubMedCrossRefGoogle Scholar
  122. 122.
    Roth, W. G., M. P. Leckie, and D. N. Dietzler. 1988. Restoration of colony-forming activity in osmotically stressed Escherichia coli. Appl. Environ. Microbiol. 54:3142–3146.PubMedGoogle Scholar
  123. 123.
    Shahamat, M., U. Mai, C. Paszko-Kolva, M. Kessel, and R. R. Colwell. 1993. Use of autoradiography to assess viability of Helicobacter pylori in water. Appl. Environ. Microbiol. 59:1231–1235.PubMedGoogle Scholar
  124. 124.
    Siegele, D. A., and R. Kolter. 1992. Life after log. J. Bacteriol. 174:345–348.PubMedGoogle Scholar
  125. 125.
    Singh, A., R. Yeager, and G. A. McFeters. 1986. Assessment of in vivo revival, growth, and pathogenicity of Escherichia coli strains after copper-and chlorine-induced injury. Appl. Environ. Microbiol. 52:832–837.PubMedGoogle Scholar
  126. 126.
    Smibert, R. M. 1984. Genus Campylobacter, p. 111–118. In N. R. Krieg and J. G. Holt (ed.), Bergey’s Manual of Systematic Bacteriology, vol. 1. Williams & Wilkins, Baltimore, Md.Google Scholar
  127. 127.
    Smith, J. J., J. P. Howington, and G. A. McFeters. 1994. Survival, physiological response and recovery of enteric bacteria exposed to polar marine environment. Appl. Environ. Microbiol. 60: 2977–2984.PubMedGoogle Scholar
  128. 128.
    Solic, M., and N. Krstulovic. 1992. Separate and combined effects of solar radiation, temperature, salinity, and pH on the survival of faecal coliforms in seawater. Mar. Pollut. Bul. 24:411–416.CrossRefGoogle Scholar
  129. 129.
    Stackebrandt, E. 1992. Unifying phylogeny and phenotypic diversity, p. 19–47. In A. Balows, H. G. Trüper, M. Dworkin, W. Harder, and K.-H. Schleifer (ed.), The Prokaryotes. A Handbook on the Biology of Bacteria: Ecophysiology, Isolation, Identification, Applications, 2nd ed. Springer-Verlag, New York, N.Y.Google Scholar
  130. 130.
    Steinert, M., L. Emody, R. Amann, and J. Hacker. 1997. Resuscitation of viable but nonculturable Legionella pneumophila Philadelphia JR32 by Acanthamoeba castellanii. Appl. Environ. Microbiol. 63:2047–2053.PubMedGoogle Scholar
  131. 131.
    Thomas, T. D., and R. D. Batt. 1968. Survival of Streptococcus lactis in starvation conditions. J. Gen. Microbiol. 50:367–382.PubMedGoogle Scholar
  132. 132.
    Trainor, V. C., R. K. Udy, P. J. Bremer, and G. M. Cook. 1999. Survival of Streptococcus pyogenes under stress and starvation. FEMS Microbiol. Lett. 176:421–428.PubMedCrossRefGoogle Scholar
  133. 133.
    Turpin, P. E., K. A. Maycroft, C. L. Rowlands, E. M. H. Wellington. 1993. Viable but nonculturable salmonellas in soil. J. Appl. Microbiol. 74:421–427.CrossRefGoogle Scholar
  134. 134.
    Wadolkowski, E. A., D. C. Laux, and P. S. Cohen. 1988. Colonization of the streptomycin-treated mouse large intestine by a human fecal Escherichia coli strain: role of growth in mucus. Infect. Immun. 56:1030–1035.PubMedGoogle Scholar
  135. 135.
    Wai, S. N., T. Morita, K. Kondo, H. Misumi, and K. Amako. 1996. Resuscitation of Vibrio cholerae O1 strain TSI-4 from a viable but nonculturable state by heat shock. FEMS Microbiol. Lett. 136:187–191.PubMedCrossRefGoogle Scholar
  136. 136.
    Wang, G., and M. P. Doyle. 1998. Survival of enterohemorrhagic Escherichia coli O157-H7 in water. J. Food Prot. 61:662–667.PubMedGoogle Scholar
  137. 137.
    Weichart, D., and S. Kjelleberg. 1996. Stress resistance and recovery potential of culturable and viable but nonculturable cells of Vibrio vulnificus. Microbiology 142:845–853.PubMedCrossRefGoogle Scholar
  138. 138.
    Wolf, P. W., and J. D. Oliver. 1992. Temperature effects on the viable but nonculturable state of Vibrio vulnificus. FEMS Microbiol. Ecol. 101:33–39.Google Scholar
  139. 139.
    Xu, H.-S., N. Roberts, F. L. Singleton, R. W. Atwell, 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.CrossRefGoogle Scholar
  140. 140.
    Xu, H.-S., and R. R. Colwell. 1989. Overwintering of Vibrio cholerae—viable but non-culturable state and its determination. J. Ocean. Univ. Qingdao 19:77–83. (In Chinese.)Google Scholar
  141. 141.
    Zimmerman, R., E. 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.Google Scholar

Copyright information

© ASM Press, Washington, D.C. 2000

Authors and Affiliations

  • Michel J. Gauthier
    • 1
  1. 1.Faculté de MédecineINSERM Unité 452Nice Cedex 2France

Personalised recommendations