Skip to main content
SpringerLink
Log in
Book cover

Nonculturable Microorganisms in the Environment pp 7–18Cite as

Morphological Changes Leading to the Nonculturable State

  • Chapter

Abstract

Specific morphological changes occur when bacterial cells are introduced into nutrient-depleted environments. In addition, bacteria that are indigenous to these conditions tend to be smaller than bacteria found in nutrient-rich environments. Changes in bacterial morphology during starvation-survival have been previously reviewed (45, 61). The conditions under which bacteria alter their morphology are discussed, with reasons for the changes suggested.

This is a preview of subscription content, log in via an institution.

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   84.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Albertson, N. H., G. W. Jones, and S. Kjelleberg. 1987. The detection of starvation-specific antigens of two marine bacteria. J. Gen. Microbiol. 133:2225–2232.

    CAS  Google Scholar 

  2. Aldea, M., T. Garrido, C. Hernandez-Chico, M. Vicente, and S. R. Kushner. 1989. Induction of growth-phase-dependent promoter triggers transcription of bolA, an Escherichia coli morphogene. EMBO J. 8:3923–3931.

    PubMed  CAS  Google Scholar 

  3. Aldea, M., C. Hernandez-Chico, A. G. de la Campa, S. R. Kushner, and M. Vicente. 1988. Identification, cloning, and expression of bolA, an ftsZ-dependent morphogene of Escherichia coli. J. Bacteriol. 170:5169–5176.

    PubMed  CAS  Google Scholar 

  4. Ammerman, J. W., J. A. Fuhrman, A. Hagstrom, and F. Azam. 1984. Bacterioplankton growth in seawater. I. Growth kinetics and cellular characteristics in seawater cultures. Mar. Ecol. Prog. Ser. 18:31–39.

    Article  Google Scholar 

  5. Amy, P. S., C. Durham, D. Hall, and L. Haldeman. 1993. Starvation-survival of deep subsurface isolates. Curr. Microbiol. 26:345–352.

    Article  CAS  Google Scholar 

  6. Amy, P. S., and R. Y. Morita. 1983. Starvation-survival patterns of sixteen freshly isolated openocean bacteria. Appl. Environ. Microbiol. 45:1109–1115.

    PubMed  CAS  Google Scholar 

  7. Amy, P. S., C. Pauling, and R. Y. Morita. 1983. Recovery from nutrient starvation by a marine Vibrio sp. Appl. Environ. Microbiol. 45:1685–1690.

    PubMed  CAS  Google Scholar 

  8. Amy, P. S., C. Pauling, and R. Y. Morita. 1983. Starvation-survival processes of a marine vibrio. Appl. Environ. Microbiol. 45:1041–1048.

    PubMed  CAS  Google Scholar 

  9. Anderson, J. I. W., and W. P. Heffernan. 1965. Isolation and characterization of filterable marine bacteria. J. Bacteriol. 90:1713–1718.

    PubMed  CAS  Google Scholar 

  10. Andersson, A., U. Larsson, and A. Hagstrom. 1986. Size-selective grazing by a microflagellate on pelagic bacteria. Mar. Ecol. Prog. Ser. 33:51–57.

    Article  Google Scholar 

  11. Bae, H. C., E. H. Cota-Robles, and L. E. Casida, Jr. 1972. Microflora of soil as viewed by transmission electron microscopy. Appl. Microbiol. 23:637–648.

    PubMed  CAS  Google Scholar 

  12. Baker, R. M., F. L. Singleton, and M. A. Hood. 1983. Effects of nutrient deprivation of Vibrio cholerae. Appl. Environ. Microbiol. 46:930–940.

    PubMed  CAS  Google Scholar 

  13. Bakhrouf, A., M. Jeddi, A. Bouddabous, and M. J. Gauthier. 1989. Evolution of Pseudomonas aeruginosa cells towards a filterable stage in seawater. FEMS Microbiol. Lett. 59:187–190.

    Article  Google Scholar 

  14. Bakken, L. R., and R. A. Olsen. 1987. The relationship between cell size and viability of soil bacteria. Microb. Ecol. 13:103–114.

    Article  Google Scholar 

  15. Beumer, R. R., J. de Vries, and F. M. Rombouts. 1992. Campylobacter jejuni nonculturable coccoid cells. Int. J. Food Microbiol. 15:153–163.

    Article  PubMed  CAS  Google Scholar 

  16. Boylen, C. W. 1973. Survival of Arthrobacter crystallopoietes during prolonged periods of extreme dessication. J. Bacteriol. 113:33–37.

    PubMed  CAS  Google Scholar 

  17. Boylen, C. W., and M. H. Mulks. 1978. The survival of coryneform bacteria during periods of prolonged nutrient starvation. J. Gen. Microbiol. 105:323–334.

    CAS  Google Scholar 

  18. Boylen, C. W., and J. L. Pate. 1973. Fine structure of Arthrobacter crystallopoietes during longterm starvation of rod and spherical stage cells. Can. J. Microbiol. 19:1–5.

    Article  PubMed  CAS  Google Scholar 

  19. Buchanan, C. E., and M. O. Sowell. 1982. Synthesis of penicillin-binding protein 6 by stationaryphase Escherichia coli. J. Bacteriol. 151:491–494.

    PubMed  CAS  Google Scholar 

  20. Byrd, J. J., H.-S. Xu, and R. R. Colwell. 1993. Viable but nonculturable bacteria in drinking water. Appl. Environ. Microbiol. 57:875–878.

    Google Scholar 

  21. Byrd, J. J., L. R. Zeph, and L. E. Casida, Jr. 1985. Bacterial control of Agromyces ramosus in soil. Can. J. Microbiol. 31:1157–1163.

    Article  CAS  Google Scholar 

  22. Casida, L. E., Jr. 1965. Abundant microorganisms in soil. Appl. Microbiol. 13:327–334.

    PubMed  Google Scholar 

  23. Casida, L. E., Jr. 1971. Microorganisms in unamended soil as observed by various forms of microscopy and staining. Appl. Microbiol. 21:1040–1045.

    PubMed  Google Scholar 

  24. Casida, L. E., Jr. 1977. Small cells in pure cultures of Agromyces ramosus and in natural soil. Can. J. Microbiol. 23:214–216.

    Article  PubMed  Google Scholar 

  25. Chrzanowski, T. H., and K. Simek. 1990. Prey-size selection by freshwater flagellated protozoa. Limnol. Oceanogr. 35:1429–1436.

    Article  Google Scholar 

  26. Conn, H. J. 1948. The most abundant groups of bacteria in soil. Bacteriol. Rev. 12:257–273.

    Google Scholar 

  27. Cusack, F., S. Singh, C. McCarthy, J. Grieco, M. de Rocco, D. Nguyen, H. Lappin-Scott, and J. W. Costerton. 1992. Enhanced oil recovery—three-dimensional sandpack simulation of ultramicrobacteria resuscitation in reservoir formation. J. Gen. Microbiol. 138:647–655.

    Google Scholar 

  28. Daley, R. J., and J. E. Hobbie. 1975. Direct count of aquatic bacteria by a modified epifluorescent technique. Limnol. Oceanogr. 20:875–881.

    Article  Google Scholar 

  29. Eberl, L., M. Givskov, C. Sternberg, S. Moller, G. Christiansen, and S. Molin. 1996. Physiological responses of Pseudomonas putida KT2442 to phosphate starvation. Microbiology 142:155–163.

    Article  CAS  Google Scholar 

  30. Faquin, W. C., and J. D. Oliver. 1984. Arginine uptake by a psychrophilic marine Vibrio sp. during starvation-induced morphogenesis. J. Gen. Microbiol. 130:1331–1335.

    CAS  Google Scholar 

  31. Fattom, A., and M. Shilo. 1985. Production of emulcyan by Phormidium J-1: its activity and function. FEMS Microbiol. Ecol. 31:3–9.

    Article  CAS  Google Scholar 

  32. Felter, R. A., R. R. Colwell, and G. B. Chapman. 1969. Morphology and round body formation in Vibrio marinus. J. Bacteriol. 99:326–335.

    PubMed  CAS  Google Scholar 

  33. Gonzalez, J. M., E. B. Sheer, and B. F. Sheer. 1990. Size-selective grazing on bacteria by natural assemblages of estuarine flagellates and ciliates. Appl. Environ. Microbiol. 56:583–589.

    PubMed  CAS  Google Scholar 

  34. Grossman, N., and E. Z. Ron. 1989. Apparent minimal size required for cell division in Escherichia coli. J. Bacteriol. 171:80–82.

    PubMed  CAS  Google Scholar 

  35. Grossman, N., E. Z. Ron, and C. L. Woldringh. 1982. Changes in cell dimension during amino acid starvation of Escherichia coli. J. Bacteriol. 152:35–41.

    PubMed  CAS  Google Scholar 

  36. 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.

    PubMed  CAS  Google Scholar 

  37. 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.

    Article  CAS  Google Scholar 

  38. Holmquist, L., and S. Kjelleberg. 1993. The carbon starvation stimulon in the marine Vibrio sp. S14 (CCUG15956) includes three periplasmic space protein responders. J. Gen. Microbiol. 139:209–215.

    CAS  Google Scholar 

  39. Humphrey, B., S. Kjelleberg, and K. C. Marshall. 1983. Responses of marine bacteria under starvation conditions at a solid-water interface. Appl. Environ. Microbiol. 45:43–47.

    PubMed  CAS  Google Scholar 

  40. Humphrey, B. A., and K. C. Marshall. 1984. The triggering effect of surfaces and surfactants on heat output, oxygen consumption and size reduction of a starving marine Vibrio. Arch. Microbiol. 140:166–170.

    Article  PubMed  CAS  Google Scholar 

  41. James, G. A., D. R. Korber, D. E. Caldwell, and J. W. Costerton. 1995. Digital image analysis of growth and starvation responses of a surface-colonizing Acinetobacter sp. J. Bacteriol. 177:907–915.

    PubMed  CAS  Google Scholar 

  42. Jannasch, H. W. 1955. Zur Okologie ser zymogenen planktischen Bacterienflora naturlicher Gewasser. Arch. Mikrobiol. 23:146–180.

    Article  PubMed  CAS  Google Scholar 

  43. Jannasch, H. W. 1958. Studies on planktonic bacteria by means of a direct membrane filter method. J. Gen. Microbiol. 18:609–620.

    PubMed  CAS  Google Scholar 

  44. Kjelleberg, S., and M. Hermansson. 1984. Starvation-induced effects on bacterial surface characteristics. Appl. Environ. Microbiol. 48:497–503.

    PubMed  CAS  Google Scholar 

  45. Kjelleberg, S., M. Hermansson, P. Marden, and G. W. Jones. 1987. The transient phase between growth and nongrowth of heterotrophic bacteria with emphasis on the marine environment. Annu. Rev. Microbiol. 41:25–49.

    Article  PubMed  CAS  Google Scholar 

  46. Kjelleberg, S., B. A. Humphrey, and K. C. Marshall. 1982. Effect of interfaces on small, starved marine bacteria. Appl. Environ. Microbiol. 43:1166–1172.

    PubMed  CAS  Google Scholar 

  47. Kjelleberg, S., B. A. Humphrey, and K. C. Marshall. 1983. Initial phases of starvation and activity of bacteria at surfaces. Appl. Environ. Microbiol. 46:978–984.

    PubMed  CAS  Google Scholar 

  48. Kogure, K., U. Simidu, and N. Taga. 1979. A tentative direct microscopic method for counting living marine bacteria. Can. J. Microbiol. 24:415–420.

    Article  Google Scholar 

  49. Kurath, G., and R. Y. Morita. 1983. Starvation-survival physiological studies of a marine Pseudomonas sp. Appl. Environ. Microbiol. 45:1206–1211.

    PubMed  CAS  Google Scholar 

  50. Kuuppo-Leinikki, P. 1990. Protozoan grazing on planktonic bacteria and its impact on bacterial population. Mar. Ecol. Prog. Ser. 63:227–238.

    Article  Google Scholar 

  51. Lange, R., and R. Hengge-Aronis. 1991. Growth phase-regulated expression of bolA and morphology of stationary-phase Escherichia coli cells are regulated by the novel sigma factor σs. J. Bacteriol. 173:4474–4481.

    PubMed  CAS  Google Scholar 

  52. Lange, R., and R. Hengge-Aronis. 1991. Identification of a central regulator of stationary-phase gene expression of Escherichia coli. Mol. Microbiol. 5:49–59.

    Article  PubMed  CAS  Google Scholar 

  53. Lappin-Scott, H. M., F. M. Cusack, F. A. Macleod, and J. W. Costerton. 1988. Nutrient resuscitation and growth of starved cells in sandstone cores—a novel approach to enhance oil recovery. Appl. Environ. Microbiol. 54:1373–1382.

    PubMed  CAS  Google Scholar 

  54. Lappin-Scott, H. M., F. M. Cusack, F. A. Macleod, and J. W. Costerton. 1988. Starvation and nutrient resuscitation of Klebsiella pneumoniae isolated from oil well waters. J. Appl. Bacteriol. 64: 541–550.

    Article  PubMed  CAS  Google Scholar 

  55. Larsson, U., and A. Hagstrom. 1982. Fractionated phytoplankton primary production, exudate release, and bacterial production in a Baltic eutrophication gradient. Mar. Biol. 67:57–70.

    Article  Google Scholar 

  56. Lin, C. L., C. S. Lin, and S. T. Tan. 1995. Mutations showing specificity for normal growth or Mn(II)-dependent post-exponential-phase cell division in Deinococcus radiodurans. Microbiology 141:1707–1714.

    Article  CAS  Google Scholar 

  57. MacDonell, M. T., and M. A. Hood. 1982. Isolation and characterization of ultramicrobacteria from a Gulf Coast estuary. Appl. Environ. Microbiol. 43:556–571.

    Google Scholar 

  58. MacDonell, M. T., and M. A. Hood. 1984. Ultramicrovibrios in Gulf Coast estuarine water: isolation, characterization and incidence, p. 551–562. In R. R. Colwell (ed.), Vibrios in the Environment. John Wiley and Sons, Inc., New York, N.Y.

    Google Scholar 

  59. Marden, P., A. Tunlid, K. Malmcrona-Friberg, G. Odham, and S. Kjelleberg. 1985. Physiological and morphological changes during short term starvation of marine bacterial isolates. Arch. Microbiol. 142:326–332.

    Article  Google Scholar 

  60. Martin, A., Jr. 1963. A filterable Vibrio from fresh water. Proc. Pa. Acad. Sci. 36:174–178.

    Google Scholar 

  61. Morita, R. Y. 1985. Starvation and miniaturisation of heterotrophs, with special emphasis on maintenance of the starved viable state, p. 111–130. In M. M. Fletcher and G. D. Floodgate (ed.), Bacteria in Their Natural Environments. Academic Press, London, United Kingdom.

    Google Scholar 

  62. Moyer, G. L., and R. Y. Morita. 1989. Effect of growth rate and starvation-survival on cellular DNA, RNA, and protein of a psychrophilic marine bacterium. Appl. Environ. Microbiol. 55:2710–2716.

    PubMed  CAS  Google Scholar 

  63. Moyer, G. L., and R. Y. Morita. 1989. Effect of growth rate and starvation-survival on the viability and stability of a psychrophilic marine bacterium. Appl. Environ. Microbiol. 55:1122–1127.

    CAS  Google Scholar 

  64. Nelson, D. R., Y. Sadlowski, M. Eguchi, and S. Kjelleberg. 1997. The starvation-stress response of Vibrio (Listonella) anguillarum. Microbiology 143:2305–2312.

    Article  CAS  Google Scholar 

  65. Nissen, H. 1987. Longterm starvation of a marine bacterium, Alteromonas denitrificans, isolated from a Norwegian fjord. FEMS Microbiol. Ecol. 45:173–183.

    Article  CAS  Google Scholar 

  66. Novitsky, J. A. and R. Y. Morita. 1976. Morphological characterization of small cells resulting from nutrient starvation of a psychrophilic marine vibrio. Appl. Environ. Microbiol. 32:617–622.

    PubMed  CAS  Google Scholar 

  67. Novitsky, J. A., and R. Y. Morita. 1977. Survival of a psychrophilic marine vibrio under long-term nutrient starvation. Appl. Environ. Microbiol. 33:635–641.

    PubMed  CAS  Google Scholar 

  68. Novitsky, J. A., and R. Y. Morita. 1978. Possible strategy for the survival of marine bacteria under starvation conditions. Marine Biol. 48:289–295.

    Article  Google Scholar 

  69. Nystrom, T., and S. Kjelleberg. 1989. Role of protein synthesis in the cell division and starvation induced resistance to autolysis of a marine Vibrio during the initial phase of starvation. J. Gen. Microbiol. 135:1599–1606.

    Google Scholar 

  70. Nystrom, T., C. Larsson, and L. Gustafsson. 1996. Bacterial defense against aging: role of the Escherichia coli ArcA regulator in gene expression, readjusted energy flux and survival during stasis. EMBO J. 15:3219–3228.

    PubMed  CAS  Google Scholar 

  71. 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.

    PubMed  CAS  Google Scholar 

  72. Oppenheimer, C. H. 1952. The membrane filter in marine microbiology. J. Bacteriol. 64:783–786.

    PubMed  CAS  Google Scholar 

  73. Postma, J., and H. J. Altemuller. 1990. Bacteria in thin soil sections stained with fluorescent brightner Calcofluor White M2R. Soil Biol. Biochem. 22:89–96.

    Article  CAS  Google Scholar 

  74. Postma, J., J. D. van Elsas, J. M. Govaert, and J. van Veen. 1988. The dynamics of Rhizobium leguminosarum biovar trifolii introduced into soil as determined by immunofluorescence and selective plating techniques. FEMS Microbiol. Ecol. 53:251–260.

    Google Scholar 

  75. Reeve, C. A., P. S. Amy, and A. Martin. 1984. Role of protein synthesis in the survival of carbonstarved Escherichia coli K-12. J. Bacteriol. 160:1041–1046.

    PubMed  CAS  Google Scholar 

  76. Rhodes, H. E. 1954. The illustration of the morphology of Vibrio fetus by electron microscopy. Am. J. Vet. Res. 15:630–633.

    Google Scholar 

  77. Rice, S. A., and J. D. Oliver. 1992. Starvation response of the marine barophile CNPT-3. Appl. Environ. Microbiol. 58:2432–2437.

    PubMed  CAS  Google Scholar 

  78. Rockabrand, D., T. Aurgher, G. Korinek, K. Livers, and P. Blum. 1995. An essential role for the Escherichia coli DnaK protein in starvation-induced thermotolerance, H2O2 resistance, and reductive division. J. Bacteriol. 177:3695–3703.

    PubMed  CAS  Google Scholar 

  79. Rockabrand, D., K. Livers, T. Austin, R. Kaiser, D. Jensen, R. Burgess, and P. Blum. 1998. Roles of DnaK and RpoS in starvation-induced thermotolerance of Escherichia coli. J. Bacteriol. 180:846–854.

    PubMed  CAS  Google Scholar 

  80. 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.

    PubMed  CAS  Google Scholar 

  81. Ron, E. Z., N. Grossman, and C. E. Helmstetter. 1977. Control of cell division in Escherichia coli effect of amino acid starvation. J. Bacteriol. 129:569–573.

    PubMed  CAS  Google Scholar 

  82. Rosenberg, E., N. Kaplan, O. Pines, M. Rosenberg, and D. Gutnick. 1983. Capsular polysaccharides interfere with adherence of Acinetobacter calcoaceticus to hydrocarbon. FEMS Microbiol. Lett. 17:157–160.

    Article  CAS  Google Scholar 

  83. Simek, K., and T. H. Chrzanowski. 1992. Direct and indirect evidence of size-selective grazing on pelagic bacteria by freshwater nanoflagellates. Appl. Environ. Microbiol. 58:3715–3720.

    PubMed  CAS  Google Scholar 

  84. Smibert, R. M. 1978. The genus Campylobacter. Annu. Rev. Microbiol. 32:673–709.

    Article  PubMed  CAS  Google Scholar 

  85. Smigielski, A. J., B. J. Wallace, and K. C. Marshall. 1989. Changes in membrane functions during short-term starvation of Vibrio fluvialis strain NCTC 11328. Arch. Microbiol. 151:336–347.

    Article  CAS  Google Scholar 

  86. Tabor, P. S., K. Ohwada, and R. R. Colwell. 1981. Filterable marine bacteria found in the deep sea: distribution, taxonomy and response to starvation. Microb. Ecol. 7:67–83.

    Article  Google Scholar 

  87. Thorne, S. H., and H. D. Williams. 1997. Adaptation to nutrient starvation in Rhizobium leguminosarum bv. Phaseoli: Analysis of survival, stress resistance, and changes in macromolecular synthesis during entry to and exit from stationary phase. J. Bacteriol. 179:6894–6901.

    PubMed  CAS  Google Scholar 

  88. Thorsen, B. K., O. Enger, S. Norland, and K. A. Hoff. 1992. Long-term starvation survival of Yersinia ruckeri at different salinities studied by microscopical and flow cytometric methods. Appl. Environ. Microbiol. 58:1624–1628.

    PubMed  CAS  Google Scholar 

  89. Torella, F., and R. Y. Morita. 1981. Microcultural study of bacterial size changes and microcolony formation by heterotrophic bacteria in seawater. Appl. Environ. Microbiol. 41:518–527.

    Google Scholar 

  90. Ward, J. E., Jr., and J. Lutkenhaus. 1985. Overproduction of Fts Z induces minicell formation in E. coli. Cell 42:941–949.

    Article  PubMed  CAS  Google Scholar 

  91. Watson, S. W., T. J. Novitsky, H. L. Quinby, and F. W. Valois. 1977. Determination of bacterial number and biomass in the marine environment. Appl. Environ. Microbiol. 33:940–946.

    PubMed  CAS  Google Scholar 

  92. Wikner, J., A. Andersson, S. Normark, and A. Hagstrom. 1986. Use of genetically marked minicells as a probe in measurement of predation on bacteria in aquatic environments. Appl. Environ. Microbiol. 52:4–8.

    PubMed  CAS  Google Scholar 

  93. Wrangstadh, M., P. L. Conway, and S. Kjelleberg. 1988. The role of an extracellular polysaccharide produced by the marine Pseudomonas sp. S9 in cellular detachment during starvation. Can. J. Microbiol. 35:309–312.

    Article  Google Scholar 

  94. Zambrano, M. M., D. A. Siegele, M. Almiron, A. Torino, and R. Kolter. 1993. Microbial competition Escherichia coli mutants that take over stationary phase cultures. Science 259:1757–1760.

    Article  PubMed  CAS  Google Scholar 

  95. Zimmerman, R. 1977. Estimation of bacterial numbers and biomass by epifluorescence microscopy and scanning electron microscopy, p. 103–120. In G. Rheinheimer (ed.), Microbial Ecology of a Brackish Water Environment. Springer-Verlag, New York, N.Y.

    Chapter  Google Scholar 

  96. Zimmerman, R., and L.-A. Meyer-Reil. 1974. A new method for fluorescence staining of bacterial populations on membrane filter. Kiel. Meeresforsch. 30:24–27.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biology, St. Mary’s College of Maryland, St. Mary’s City, MD, 20686, USA

    Jeffrey J. Byrd

Authors
  1. Jeffrey J. Byrd
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Center of Marine Biotechnology, Columbus Center, University of Maryland Biotechnology Institute, Baltimore, Maryland, 21202, USA

    Rita R. Colwell

  2. Institute of Marine Sciences, University of Southern Mississippi, Ocean Springs, Mississippi, 39566-7000, USA

    D. Jay Grimes

Rights and permissions

Reprints and permissions

Copyright information

© 2000 ASM Press, Washington, D.C.

About this chapter

Cite this chapter

Byrd, J.J. (2000). Morphological Changes Leading to the Nonculturable State. In: Colwell, R.R., Grimes, D.J. (eds) Nonculturable Microorganisms in the Environment. Springer, Boston, MA. https://doi.org/10.1007/978-1-4757-0271-2_2

Download citation

  • DOI: https://doi.org/10.1007/978-1-4757-0271-2_2

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4757-0273-6

  • Online ISBN: 978-1-4757-0271-2

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation