The Public Health Significance of Viable but Nonculturable Bacteria

  • James D. Oliver


A bacterium in the viable but nonculturable (VBNC) state is defined here as a cell which fails to grow on the routine bacteriological media on which it would normally grow and develop into a colony, but which is in fact alive and capable of metabolic activity. The term “nonculturable” seems to be a misnomer as, under the proper conditions, it appears that these cells are able to “resuscitate” to the metabolically active and culturable state (this point, along with a brief discussion on why cells enter this state of dormancy, is presented later in this chapter). In this review, the discussion of cells entering the VBNC state is limited to those cells which respond to a natural environmental stress (e.g., a temperature downshift) in such a manner. Thus, this review does not include a discussion of the detrimental effects of such agents as antibiotics, chlorine, heavy metals, or other chemicals to which cells may be exposed and which may result in cell injury or death (this area is reviewed in chapter 15). Similarly, this review does not describe cells that are most correctly termed “nonculturable,” e.g., those animal symbionts which have never been cultured in the laboratory. Such cells are described in chapter 5. Instead, this chapter is limited to a discussion of human bacterial pathogens which are known to enter the VBNC state. Finally, I have for the most part selected to review only those studies which have employed such methods as the “direct viable count” originally described by Kogure et al. (38), p-iodonitrotetrazolium violet (INT) reduction (86), or 5-cyano-2,3-ditolyl tetrazolium chloride (CTC) hydrolysis (64) to demonstrate viability in cells no longer culturable. These methods have been described in an earlier review on the VBNC state (49), as well as in other chapters of this monograph. Despite these restrictions, bacterial cells from at least 16 different genera, mostly but not exclusively gram negative, comprising over 30 different species, have now been reported to enter the VBNC state (50).


Public Health Significance VBNC State Coccoid Form VBNC Cell Coccoid Cell 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    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 Escherchia coli in a freshwater ecosystem. Appl. Environ. Microbiol. 58:3903–3907.PubMedGoogle Scholar
  2. 2.
    Atlas, R. M., J. F. Williams, and M. K. Huntington. 1995. Legionella contamination of dentalunit waters. Appl. Environ. Microbiol. 61:1208–1213.PubMedGoogle Scholar
  3. 3.
    Baker, R. M., F. L. Singleton, and M. A. Hood. 1983. Effects of nutrient deprivation on Vibrio cholerae. Appl. Environ. Microbiol. 46:930–940.PubMedGoogle Scholar
  4. 4.
    Barcina, I., J. M. González, J. Iriberri, and L. Egea. 1989. Effect of visible light on progressive dormancy of Escherichia coli cells during the survival process in natural fresh water. Appl. Environ. Microbiol. 55:246–251.PubMedGoogle Scholar
  5. 5.
    Barcina, I., J. M. González, 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
  6. 6.
    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
  7. 7.
    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
  8. 8.
    Binnerup, S. J., O. Hojberg, and D. Gerlif. 1995. Resuscitation demonstrated in a mixed batch of culturable and non-culturable Pseudomonas aeruginosa PAO303. Int. Symp. Microb. Ecol. 7:1–5.3, 103.Google Scholar
  9. 9.
    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.PubMedCrossRefGoogle Scholar
  10. 10.
    Brauns, L. A., and J. D. Oliver. 1994. Polymerase chain reaction of whole cell lysates of Vibrio vulnificus. Food Biotechnol. 8:1–6.CrossRefGoogle Scholar
  11. 11.
    Brauns, L. A., M. C. Hudson, and J. D. Oliver. 1991. Use of the polymerase chain reaction in detection of culturable and nonculturable Vibrio vulnificus cells. Appl. Environ. Microbiol. 57:2651–2655.PubMedGoogle Scholar
  12. 12.
    Brayton, P., M. Tamplin, A. Huq, and R. Colwell. 1987. Enumeration of Vibrio cholerae O1 in Bangladesh waters by fluorescent-antibody direct viable count. Appl. Environ. Microbiol. 53:2862–2865.PubMedGoogle Scholar
  13. 13.
    Buck, G. E. 1990. Campylobacter pylori and gastroduodenal disease. Clin. Microbiol. Rev. 3:1–12.PubMedGoogle Scholar
  14. 14.
    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
  15. 15.
    Byrd, J. J., and R. R. Colwell. 1993. Long-term survival and plasmid maintenance of Escherichia coli in marine microcosms. FEMS Microbiol. Lett. 12:9–14.CrossRefGoogle Scholar
  16. 16.
    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
  17. 17.
    Centers for Disease Control. 1993. Summary of Notifiable Diseases, United States, 1992. Massachusetts Medical Society, Waltham, Mass.Google Scholar
  18. 18.
    Chmielewski, R. A. N., 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
  19. 19.
    Coleman, S. S., and J. D. Oliver. 1996. Optimization of conditions for the polymerase chain reaction amplification of DNA from culturable and nonculturable cells of Vibrio vulnificus. FEMS Microbiol. Ecol. 19:127–132.CrossRefGoogle Scholar
  20. 20.
    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. Biotechnology 3:817–820.CrossRefGoogle Scholar
  21. 21.
    Colwell, R. R., P. Brayton, D. Herrington, B. Tall, A. Huq, and M. M. Levine. 1996. Viable but nonculturable Vibrio cholerae O1 revert to a culturable state in the human intestine. World J. Microbiol. Biotechnol. 12:28–31CrossRefGoogle Scholar
  22. 22.
    Cornax, R., M. A. Morinigo, P. Romero, and J. J. Borrego. 1990. Survival of pathogenic microorganisms in seawater. Curr. Microbiol. 20:293–298.CrossRefGoogle Scholar
  23. 23.
    Dawe, L. L., and W. R. Penrose. 1978. “Bactericidal” property of seawater: death or debilitation? Appl. Environ. Microbiol. 35:829–833.PubMedGoogle Scholar
  24. 24.
    Dirksen, J., and P. Flagg. 1988. Pathogenic organisms in dairy products; cause, effects and control. Food Sci. Technol. Today 2:41–43.Google Scholar
  25. 25.
    Ekweozor, C. C., C. E. Nwoguh, and M. R. Barer. 1998. Transient increases in colony counts observed in declining populations of Campylobacter jejuni held at low temperature. FEMS Microbiol. Lett. 158:267–272.PubMedCrossRefGoogle Scholar
  26. 26.
    Fujioka, R. S., H. H. Hashimoto, E. B. Siwak, and R. H. F. Young. 1981. Effect of sunlight on survival of indicator bacteria in seawater. Appl. Environ. Microbiol. 41:690–696.PubMedGoogle Scholar
  27. 27.
    Garcia-Lara, J., P. Menon, P. Servais, and G. Billen. 1991. Mortality of fecal bacteria in seawater. Appl. Environ. Microbiol. 57:885–888.PubMedGoogle Scholar
  28. 28.
    Gauthier, M. J., P. M. Munroe, and S. Mohajer. 1987. Influence of salts and sodium chloride on the recovery of Escherichia coli from seawater. Curr. Microbiol. 15:5–10.CrossRefGoogle Scholar
  29. 29.
    Greenberg, A. E. 1956. Survival of enteric organisms in sea water. Public Health Rep. 71:77–86.PubMedCrossRefGoogle Scholar
  30. 30.
    Gribbon, L. T., and M. R. Barer. 1995. Oxidative metabolism in nonculturable Helicobacter pylori and Vibrio vulnificus cells studied by substrate-enhanced tetrazolium reduction and digital image processing. Appi Environ. Microbiol. 61:3379–3384.Google Scholar
  31. 31.
    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
  32. 31a.
    Huq, A., R. R. Colwell, R. Rahman, A. Ali, M. A. R. Chowdhury, S. Parveen, D. A. Sack, and E. Russek-Cohen. 1990. Occurrence of Vibrio cholerae in the aquatic environment measured by fluorescent antibody and culture method. Appl. Environ. Microbiol. 56:2370–2373.PubMedGoogle Scholar
  33. 32.
    Hussong, D., R. R. Colwell, M. O’Brien, A. D. Weiss, A. D. Pearson, R. M. Weiner, and W. D. Burge. 1987. Viable L. pneumophila not detectable by culture on agar media. Biotechnology 5:947–950.CrossRefGoogle Scholar
  34. 33.
    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
  35. 34.
    Jacob, J., W. Martin, and C. Holler. 1993. Characterization of viable but nonculturable state of Campylobacter coli, characterized with respect to electron-microscopic findings, whole cell protein and lipooligosaccharide (LOS) patterns. Zentbl. Mikrobiol. 148:3–10.Google Scholar
  36. 35.
    Ketchum, B. H., J. C. Ayers, and R. F. Vaccaro. 1952. Processes contributing to the decrease of coliform bacteria in a tidal estuary. Ecology 33:247–258.CrossRefGoogle Scholar
  37. 36.
    Khan, M. U., G. T. Curlin, and M. I. Huq. 1979. Epidemiolgy of Shigella dysenteriae type 1 infections in Dacca [sic] urban area. Trop. Geogr. Med. 31:213–223.PubMedGoogle Scholar
  38. 37.
    Klein, P. D., D. Y. Graham, A. Gaillor, A. R. Opekun, and E. O. Smith. 1991. Water source as risk factor for H. pylori infection in Peruvian children. Lancet 337:1503–1505.PubMedCrossRefGoogle Scholar
  39. 38.
    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
  40. 39.
    Korhonen, L. K., and P. J. Martikainen. 1991. Survival of Escherichia coli and Campylobacter jejuni in untreated and filtered lake water. J. Appl. Bacteriol. 71:379–382.PubMedCrossRefGoogle Scholar
  41. 40.
    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
  42. 40a.
    Linkous, D. A., and J. D. Oliver. 1999. Pathogenesis of Vibrio vulnificus. FEMS Microbiol. Lett. 174:207–214.PubMedCrossRefGoogle Scholar
  43. 41.
    Martinez, J., J. Garacia-Lara, and J. Vibes-Rego. 1989. Estimation of Escherichia coli mortality in seawater by the decrease in 3H-label and electron transport system activity. Microb. Ecol. 17: 219–225.CrossRefGoogle Scholar
  44. 42.
    McGovern, V. P., and J. D. Oliver. 1995. Induction of cold-responsive proteins in Vibrio vulnificus. J. Bacteriol. 177:4131–4133.PubMedGoogle Scholar
  45. 43.
    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
  46. 44.
    Mizunoe, Y., S. N. Wai, A. Takade, and S.-I. Yoshida. 1999. Restoration of culturability of starvation-stressed and low-temperature-stressed Escherichia coli 0157 cells using H2O2-degrading compounds. Arch. Microbiol. 172:63–67.PubMedCrossRefGoogle Scholar
  47. 45.
    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
  48. 46.
    Mukamolova, G. V., A. S. Kaprelyants, and D. B. Kell. 1995. Secretion of an antibacterial factor during resuscitation of dormant cells in Micrococcus luteus cultures held in an extended stationary state. Antonie van Leeuwenhoek 67:289–295.PubMedCrossRefGoogle Scholar
  49. 47.
    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
  50. 48.
    Oliver, J. D. 1989. Vibrio vulnificus, p. 569–600. In M. P. Doyle (ed.), Foodborne Bacterial Pathogens. Marcel Dekker, Inc., New York, N.Y.Google Scholar
  51. 49.
    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
  52. 50.
    Oliver, J. D. 1995. The viable but non-culturable state in the human pathogen, Vibrio vulnificus. FEMS Microbiol. Lett. 133:203–208.PubMedCrossRefGoogle Scholar
  53. 51.
    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.PubMedGoogle Scholar
  54. 52.
    Oliver, J. D., and J. B. Kaper. 1997. Vibrio species. In M. P. Doyle, L. R. Beuchat, and T. J. Montville (ed.), Food Microbiology: Fundamentals and Frontiers. ASM Press, Washington, D.C.Google Scholar
  55. 53.
    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
  56. 54.
    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
  57. 55.
    Oliver, J. D., D. McDougald, T. Barrett, L. A. Glover, and J. I. Prosser. 1995. Effect of temperature and plasmid carriage on nonculturability in organisms targeted for release. FEMS Microbiol. Ecol. 17:229–238.CrossRefGoogle Scholar
  58. 56.
    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
  59. 57.
    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. Microb. Ecol. 22:75–83.CrossRefGoogle Scholar
  60. 58.
    Perkins, S. E., L. L. Yan, Z. Shen, A. Hayward, J. C. Murphy, and J. G. Fox. 1996. Use of PCR and culture to detect Helicobacter pylori in naturally infected cats following triple antimicrobial therapy. Antimicrob. Agents Chemother. 40:1486–1490.PubMedGoogle Scholar
  61. 59.
    Peterson, W. L. 1991. Helicobacter pylori and peptic ulcer disease. N. Engl. J. Med. 324:1043–1048.PubMedCrossRefGoogle Scholar
  62. 60.
    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
  63. 61.
    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.PubMedGoogle Scholar
  64. 62.
    Rhoades, H. E. 1954. The illustration of the morphology of Vibrio fetus by electron microscopy. Am. J. Vet. Res. 15:630–633.PubMedGoogle Scholar
  65. 63.
    Rigsbee, W., L. M. Simpson, and J. D. Oliver. 1997. Detection of the viable but nonculturable state in Escherichia coli O157:H7. J. Food Safety 16:255–262.CrossRefGoogle Scholar
  66. 64.
    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.PubMedGoogle Scholar
  67. 65.
    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
  68. 66.
    Roszak, D. B., and R. R. Colwell. 1987. Survival strategies of bacteria in the natural environment. Microbiol. Rev. 51:365–379.PubMedGoogle Scholar
  69. 67.
    Roszak, D. B., and R. R. Colwell. 1987. Metabolic activity of bacterial cells enumerated by direct viable count. Appl. Environ. Microbiol. 53:2889–2983.PubMedGoogle Scholar
  70. 68.
    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
  71. 69.
    Roth, W. G., M. P. Leckie, and D. N. Dietzler. 1988. Restoration of colony-forming activity in osmotically stressed Escherichia coli by betaine. Appl. Environ. Microbiol. 54:3142–3146.PubMedGoogle Scholar
  72. 70.
    Ryan, K. J. 1990. Enterobacteriaceae, p. 357–383. In J. C. Sherris (ed.), Medical Microbiology: an Introduction to Infectious Diseases, 2nd ed. Appleton & Lange, Publishers, Norwalk, Conn.Google Scholar
  73. 71.
    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
  74. 72.
    Skirrow, M. B. 1989. Campylobacter perspectives. PHLS Microbiol. Digest 6:113–117.Google Scholar
  75. 73.
    Smith, P. R., E. Farrell, and K. Dunican. 1974. Survival of R+ Escherichia coli in sea water. Appl. Microbiol. 27:983–984.PubMedGoogle Scholar
  76. 74.
    Steinert, M., L. Emody, R. Amann, and Jorg Hacker. 1997. Resuscitation of viable but nonculturable Legionella pneumophila Philadelphia JR32 by Acanthamoeba castellanii. Appl. Environ. Microbiol. 63:2047–2053.PubMedGoogle Scholar
  77. 75.
    Taylor, D. N., and M. J. Blaser. 1991. The epidemiology of Helicobacter pylori infection. Epidemiol. Rev. 13:42–59.PubMedGoogle Scholar
  78. 76.
    Tholozan, J. L., J. M. Cappelier, J. P. Tissier, G. Delattre, and M. Federighi. 1999. Physiological characterization of viable-but-nonculturable Campylobacter jejuni cells. Appl. Environ. Microbiol. 65:1110–1116.PubMedGoogle Scholar
  79. 77.
    Wai, S. N., T. Moriya, K. Kondo, M. Hiroyasu, 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
  80. 77a.
    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.PubMedGoogle Scholar
  81. 78.
    Weichart, D., J. D. Oliver, and S. Kjelleberg. 1992. Low temperature induced non-culturability and killing of Vibrio vulnificus. FEMS Microbiol. Lett. 100:205–210.Google Scholar
  82. 79.
    West, A. P., M. R. Millar, and D. S. Tompkins. 1990. Survival of Helicobacter pylori in water and saline. J. Clin. Pathol. 43:609.PubMedCrossRefGoogle Scholar
  83. 80.
    West, A. P., M. R. Millar, and D. S. Tompkins. 1992. Effect of physical environment on survival of H. pylori. J. Clin. Pathol. 45:228–231.PubMedCrossRefGoogle Scholar
  84. 81.
    Whitesides, M. D., and J. D. Oliver. 1997. Resuscitation of Vibrio vulnificus from the viable but nonculturable state. Appl. Environ. Microbiol. 63:1002–1005.PubMedGoogle Scholar
  85. 82.
    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
  86. 83.
    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.CrossRefGoogle Scholar
  87. 84.
    Xu, H.-S., N. C. Roberts, L. B. Adams, P. A. West, R. J. Siebeling, A. Huq, M. I. Huq, R. Rahman, and R. R. Colwell. 1984. An indirect fluorescent antibody staining procedure for detection of Vibrio cholerae serovar O1 cells in aquatic environmental samples. J. Microbiol. Methods 2:221–231.CrossRefGoogle Scholar
  88. 85.
    Yamamoto, H., Y. Hashimoto, and T. Ezaki. 1996. Study of nonculturable Legionella pneumophila cells during multiple-nutrient starvation. FEMS Microbiol. Ecol. 20:149–154.CrossRefGoogle Scholar
  89. 86.
    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.Google Scholar

Copyright information

© ASM Press, Washington, D.C. 2000

Authors and Affiliations

  • James D. Oliver
    • 1
  1. 1.Interdisciplinary Biotechnology Program, Department of BiologyUniversity of North Carolina at CharlotteCharlotteUSA

Personalised recommendations