Starved and Nonculturable Microorganisms in Biofilms

  • Kevin C. Marshall


Casual observation of most solid surfaces immersed in aqueous environments reveals the presence of a slimy layer developing on the surfaces. These slimes, termed biofilms, form on exposed surfaces as a result of bacterial adhesion to, followed by growth and exopolymer production at, the solid-liquid interface (26, 28, 60, 67). The numbers and types of bacteria per unit volume of biofilm in different environments vary considerably, depending on factors such as the nature of the substratum, the trophic level of the aqueous phase, the flow rate, and the degree of turbulence (22). The complex communities of microorganisms found in biofilms ensure that these systems play a major role in microbially catalyzed reactions in natural environments, particularly in the degradation of organic molecules and in nitrification and other mineral transformation processes. Some of the most intensively studied biofilms, in terms of their structure, biology, and biogeochemistry, are the microbial mats found in shallow submerged or intermittently exposed littoral marine areas (25, 36, 97).


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  1. 1.
    Amann, R., W. Ludwig, and K.-H. Schleifer. 1992. Identification and in situ detection of individual bacterial cells. FEMS Microbiol. Lett. 100:45–50.Google Scholar
  2. 2.
    Amann, R. I., J. Stromley, R. Devereux, R. Key, and D. A. Stahl. 1992. Molecular and microscopic identification of sulfate-reducing bacteria in multispecies biofilms. Appl. Environ. Microbiol. 58:614–623.PubMedGoogle Scholar
  3. 3.
    Amann, R. I., B. Zarda, D. A. Stahl, and K.-H. Schleifer. 1992. Identification of individual prokaryotic cells by using enzyme-labeled, rRNA-targeted oligonucleotide probes. Appl. Environ. Microbiol. 58:3007–3011.PubMedGoogle Scholar
  4. 4.
    Amy, P. S., and R. Y. Morita. 1983. Starvation-survival patterns of sixteen freshly isolated openocean bacteria. Appl. Environ. Microbiol. 45:1109–1115.PubMedGoogle Scholar
  5. 5.
    Anwar, H., and J. W. Costerton. 1992. Effective use of antibiotics in the treatment of biofilmassociated infections. ASM News 58:665–668.Google Scholar
  6. 6.
    Anwar, H., M. K. Dasgupta, and J. W. Costerton. 1990. Testing the susceptibility of bacteria in biofilms to antibacterial agents. Antimicrob. Agents Chemother. 34:2043–2046.PubMedGoogle Scholar
  7. 7.
    Anwar, H., J. L. Strap, and J. W. Costerton. 1992. Establishment of aging biofilms: possible mechanism of bacterial resistance to antibiotic therapy. Antimicrob. Agents Chemother. 36:1347–1351.PubMedGoogle Scholar
  8. 8.
    Baier, R. E. 1980. Substrata influences on adhesion of microorganisms and their resultant new surface properties, p. 59–104. In G. Bitton and K. C. Marshall (ed.), Adsorption of Microorganisms to Surfaces. Wiley-Interscience, New York, N.Y.Google Scholar
  9. 9.
    Barer, M. R., L. T. Gribbon, C. R. Harwood, and C. E. Nwoguh. 1993. The viable but nonculturable hypothesis and medical bacteriology. Rev. Med. Microbiol. 4:183–191.CrossRefGoogle Scholar
  10. 10.
    Bej, A. K., M. H. Mahbubani, and R. M. Atlas. 1991. Detection of viable Legionella pneuophila in water by polymerase chain reaction and gene probe methods. Appl. Environ. Microbiol. 57:597–600.PubMedGoogle Scholar
  11. 11.
    Belas, R., A. Mileham, M. Simon, and M. Silverman. 1984. Transposon mutagenesis of marine Vibrio spp. J. Bacteriol. 158:890–896.PubMedGoogle Scholar
  12. 12.
    Belas, R., M. Simon, and M. Silverman. 1986. Regulation of lateral flagella gene transcription in Vibrio parahaemolyticus. J. Bacteriol. 167:210–218.PubMedGoogle Scholar
  13. 13.
    Berkeley, R. C. W., J. M. Lynch, J. Melling, P. R. Rutter, and B. Vincent (ed.). 1980. Microbial Adhesion to Surfaces. Ellis Horwood Publ., Chichester, U.K.Google Scholar
  14. 14.
    Blenkinsopp, S. A., A. E. Khoury, and J. W. Costerton. 1992. Electrical enhancement of biocide efficacy against Pseudomonas aeruginosa biofilms. Appl. Environ. Microbiol. 58:3770–3773.PubMedGoogle Scholar
  15. 15.
    Brown, M. R. W., D. G. Allison, and P. Gilbert. 1988. Resistance of bacterial biofilms to antibiotics: a growth-rate related effect? J. Antimicrob. Chemother. 22:777–783.PubMedCrossRefGoogle Scholar
  16. 16.
    Bryers, J. D. 1990. Biofilms in biotechnology, p. 733–773. In W. G. Characklis and K. C. Marshall (ed.), Biofilms. Wiley-Interscience, New York, N.Y.Google Scholar
  17. 17.
    Caldwell, D. E., S. H. Lai, and J. M. Tiedje. 1973. A two-dimensional steady-state diffusion gradient for ecological studies. Bull. Ecol. Res. Comm.-NFR (Statens Naturvetensk, Forskningsrad, Sweden) 17:151–158.Google Scholar
  18. 18.
    Caldwell, D. E., D. R. Korber, and J. R. Lawrence. 1992. Confocal laser microscopy and computer image analysis in microbial ecology. Adv. Microb. Ecol. 12:1–67.CrossRefGoogle Scholar
  19. 19.
    Cargill, K. L., B. H. Pyle, R. L. Sauer, and G. A. McFeters. 1992. Effects of culture conditions and biofilm formation on the iodine susceptibility of Legionella pneumophila. Can. J. Microbiol. 38:423–429.PubMedCrossRefGoogle Scholar
  20. 20.
    Chang, C. C., and K. Merritt. 1992. Microbial adherence on poly(methyl methacrylate) (PMMA) surfaces. J. Biomed. Mater. Res. 26:197–207.PubMedCrossRefGoogle Scholar
  21. 21.
    Characklis, W. G. 1990. Microbial biofouling control, p. 585–633. In W. G. Characklis and K. C. Marshall (ed.), Biofilms. Wiley-Interscience, New York, N.Y.Google Scholar
  22. 22.
    Characklis, W. G., and K. C. Marshall (ed.). 1990. Biofilms. Wiley-Interscience, New York, N.Y.Google Scholar
  23. 23.
    Characklis, W. G., M. H. Turakia, and N. Zelver. 1990. Transport and interfacial transfer phenomena, p. 265–340. In W. G. Characklis and K. C. Marshall (ed.), Biofilms. Wiley-Interscience, New York, N.Y.Google Scholar
  24. 24.
    Characklis, W. G., G. A. McFeters, and K. C. Marshall. 1990. Physiological ecology in biofilm systems, p. 341–394. In W. G. Characklis and K. C. Marshall (ed.), Biofilms. Wiley-Interscience, New York, N.YGoogle Scholar
  25. 25.
    Cohen, Y., and E. Rosenberg (ed.). 1989. Microbial Mats: Physiological Ecology of Benthic Microbial Communities. American Society for Microbiology, Washington, D.C.Google Scholar
  26. 26.
    Costerton, J. W., K.-J. Cheng, G. G. Geesey, T. Ladd, J. C. Nickel, M. Dasgupta, and T. J. Marrie. 1987. Bacterial biofilms in nature and disease. Annu. Rev. Microbiol. 41:435–464.PubMedCrossRefGoogle Scholar
  27. 27.
    Costerton, J. W., Z. Lewandowski, D. DeBeer, D. Caldwell, D. Korber, and G. James. 1994. Biofilms, the customized microniche. J. Bacteriol. 176:2137–2142.PubMedGoogle Scholar
  28. 28.
    Costerton, J. W., Z. Lewandowski, D. E. Caldwell, D. R. Korber, and H. M. Lappin-Scott. 1995. Microbial biofilms. Annu. Rev. Microbiol. 49:711–745.PubMedCrossRefGoogle Scholar
  29. 29.
    Costerton, J. W., P. S. Stewart, and E. P. Greenberg. 1999. Bacterial biofilms: a common cause of persistent infections. Science 284:1318–1322.PubMedCrossRefGoogle Scholar
  30. 30.
    Dagostino, L., A. E. Goodman, and K. C. Marshall. 1991. Physiological responses induced in bacteria adhering to surfaces. Biofouling 4:113–119.CrossRefGoogle Scholar
  31. 31.
    Dalsgaard, T., and N. P. Revsbech. 1992. Regulating factors of dentrification in trickling filter biofilms as measured with the oxygen/nitrous oxide microsensor. FEMS Microbial Ecol. 101:151–164.Google Scholar
  32. 32.
    Davies, D. G., A. M. Chakrabarty, and G. G. Geesey. 1993. Exopolysaccharide production in biofilms: substratum activation of alginate gene expression by Pseudomonas aeruginosa. Appl. Environ. Microbiol. 59:1181–1186.PubMedGoogle Scholar
  33. 33.
    Davies, D. G., M. R. Parsek, J. P. Pearson, B. H. Iglewski, J. W. Costerton, and E. P. Greenberg. 1998. The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 280: 295–298.PubMedCrossRefGoogle Scholar
  34. 34.
    de Beer, D., J. C. van den Heuvel, and S. P. P. Ottengraf. 1993. Microelectrode measurements of the activity distribution in nitrifying bacterial aggregates. Appl. Environ. Microbiol. 59:573–579.PubMedGoogle Scholar
  35. 35.
    de Beer, D., P. Stoodley, F. Roe, and Z. Lewandowski. 1994. Effects of biofilm structures on oxygen distribution and mass transfer. Biotechnol. Bioeng. 43:1131–1138.PubMedCrossRefGoogle Scholar
  36. 36.
    de Beer, D., P. Stoodley, and Z. Lewandowski. 1997. Measurement of local diffusion coefficients in biofilms by microinjection and confocal microscopy. Biotechnol. Bioeng. 53:151–158.PubMedCrossRefGoogle Scholar
  37. 37.
    de Weger, L. A., P. Dunbar, W. F. Mahafee, B. J. J. Lugtenberg, and G. S. Sayler. 1991. Use of bioluminescence markers to detect Pseudomonas spp. in the rhizosphere. Appl. Environ. Microbiol. 57:3641–3644.PubMedGoogle Scholar
  38. 38.
    Evans, D. J., M. R. W. Brown, D. G. Allison, and P. Gilbert. 1991. Susceptibility of Pseudomonas aeruginosa and Escherichia coli biofilms towards ciprofloxacin: effect of specific growth rate. J. Antimicrob. Chemother. 27:177–184.PubMedCrossRefGoogle Scholar
  39. 39.
    Ford, T., and R. Mitchell. 1990. The ecology of microbial corrosion. Adv. Microb. Ecol. 11:231–262.CrossRefGoogle Scholar
  40. 40.
    Gerchakov, S. M., D. S. Marszalek, F. J. Roth, and L. R. Udey. 1977. Succession of periphytic microorganisms on metal and glass surfaces, p. 203–211. In V. Romanovsky (ed.), Proc. 4th Intern. Congr. Mar Corrosion Fouling. Centre de Recherches et d’Etudes Oceanographiques, Boulogne, France.Google Scholar
  41. 41.
    Gest, H. 1993. Bacterial growth and reproduction in nature and in the laboratory. ASM News. 59: 542–543.Google Scholar
  42. 42.
    Gilbert, P., F. Collier, and M. R. W. Brown. 1990. Influence of growth rate on susceptibility to antimicrobial agents: biofilms, cell cycle, dormancy, and stringent response. Antimicrob. Agents Chemother. 34:1865–1868.PubMedGoogle Scholar
  43. 43.
    Goodman, A. E., and K. C. Marshall. 1995. Genetic responses of bacteria at surfaces, p. 80–98. In H. M. Lappin-Scott and J. W. Costerton (ed.), Microbial Biofilms. Cambridge University Press, Cambridge, U.K.CrossRefGoogle Scholar
  44. 44.
    Griffith, P. C., and M. Fletcher. 1991. Hydrolysis of protein and model dipeptide substrates by attached and unattached marine Pseudomonas sp. strain NCMB 2021. Appl. Environ. Microbiol. 57: 2186–2191.PubMedGoogle Scholar
  45. 45.
    Gristina, A. G., J. J. Dobbins, M. S. Giammara, J. C. Lewis, and W. C. DeVries. 1988. Biomaterial-centered sepsis and the total artificial heart. JAMA 259:870–874.PubMedCrossRefGoogle Scholar
  46. 46.
    Hermansson, M., and K. C. Marshall. 1985. Utilization of surface localized substrate by nonadhesive marine bacteria. Microbiol. Ecol. 11:91–105.CrossRefGoogle Scholar
  47. 47.
    Herrick, J. B., E. L. Madsen, C. A. Batt, and W. C. Ghiorse. 1993. Polymerase chain reaction amplification of naphthalenecatabolic and 16S rRNA gene sequences from indigenous sediment bacteria. Appl. Environ. Microbiol. 59:687–694.PubMedGoogle Scholar
  48. 48.
    Holben, W. E., B. M. Schroter, V. G. Calabrese, R. H. Olsen, J. K. Kukor, V. O. Biederbeck, A. E. Smith, and J. M. Tiedje. 1992. Gene probe analysis of soil microbial populations selected by amendment with 2,4-dichlorophen-oxyacetic acid. Appl. Environ. Microbiol. 58:3941–3948.PubMedGoogle Scholar
  49. 49.
    Hoyle, B. D., L. J. Williams, and J. W. Costerton. 1993. Production of mucoid exopolysaccharide during development of Pseudomonas aeruginosa biofilms. Infect. Immun. 61:777–780.PubMedGoogle Scholar
  50. 50.
    Kane, M. D., L. K. Poulsen, and D. A. Stahl. 1993. Monitoring the enrichment and isolation of sulfate-reducing bacteria by using oligonucleotide hybridization probes designed from environmentally derived 16S rRNA sequences. Appl. Environ. Microbiol. 59:682–686.PubMedGoogle Scholar
  51. 51.
    Kefford, B., S. Kjelleberg, and K. C. Marshall. 1982. Bacterial scavenging: Utilization of fatty acids localized at a solid-liquid interface. Arch. Microbiol. 133:257–260.CrossRefGoogle Scholar
  52. 52.
    King, J. M. H., P. M. Digrazia, B. Applegate, R. Burlage, J. Sanseverino, P. Dunbar, F. Larimer, and G. S. Sayler. 1990. Rapid, sensitive bioluminescent reporter technology for naphthalene exposure and biodegradation. Science 249:778–781.PubMedCrossRefGoogle Scholar
  53. 53.
    Kinniment, S. L., and J. W. T. Wimpenny. 1992. Measurements of the distribution of adenylate concentrations and adenylate energy charge across Pseudomonas aeruginosa biofilms. Appl. Environ. Microbiol. 58:1629–1635.PubMedGoogle Scholar
  54. 54.
    Kjelleberg, S. 1993. Starvation in Bacteria. Plenum Press, New York, N.Y.Google Scholar
  55. 55.
    Kjelleberg, S., B. A. Humphrey, B. A. Marshall, and K. C. Marshall. 1982. The effect of interfaces on small starved marine bacteria. Appl. Environ. Microbiol. 43:1166–1172.PubMedGoogle Scholar
  56. 56.
    Kjelleberg, S., M. Hermansson, P. Mardén, and G. W. Jones. 1987. The transient phase between growth and non-growth of heterotrophic bacteria, with emphasis on the marine environment. Annu. Rev. Microbiol. 41:25–49.PubMedCrossRefGoogle Scholar
  57. 57.
    Koch, A. L. 1990. Diffusion: The crucial process in many aspects of the biology of bacteria. Adv. Microb. Ecol. 11:37–70.CrossRefGoogle Scholar
  58. 58.
    Kolenbrander, P. E., and J. London. 1992. Ecological significance of coaggregation among oral bacteria. Adv. Microb. Ecol. 12:183–217.CrossRefGoogle Scholar
  59. 59.
    Korber, D. R., J. R. Lawrence, H. M. Lappin-Scott, and J. W. Costerton. 1995. Growth of microorganisms on surfaces, p. 15–45. In H. M. Lappin-Scott and J. W. Costerton (ed.), Microbial Biofilms. Cambridge University Press, Cambridge, U.K.CrossRefGoogle Scholar
  60. 60.
    Lappin-Scott, H. M., and J. W. Costerton (ed.). 1995. Microbial Biofilms. Cambridge University Press, Cambridge, U.K.Google Scholar
  61. 61.
    Lawrence, J. R., D. R. Korber, B. D. Hoyle, J. W. Costerton, and D. E. Caldwell. 1991. Optical sectioning of microbial biofilms. J. Bacteriol. 173:6558–6567.PubMedGoogle Scholar
  62. 62.
    Lee, A. 1985. Neglected niches: the microbial ecology of the gastrointestinal tract. Adv. Microb. Ecol., 8:115–162.CrossRefGoogle Scholar
  63. 63.
    Leung, J. W., G. T. Lau, J. J. Sung, and J. W. Costerton. 1992. Decreased bacterial adherence to silver-coated stent material: an in vitro study. Gastrointest. Endosc. 38:338–340.PubMedCrossRefGoogle Scholar
  64. 64.
    Little, B., P. Wagner, R. Ray, R. Pope, and R. Scheetz. 1991. Biofilms: an ESEM evaluation of artifacts introduced during SEM preparation. J. Indust. Microbiol. 8:213–222.CrossRefGoogle Scholar
  65. 65.
    Maki, J. S., D. Rittschof, D. Mitchell, and R. Mitchell. 1992. Inhibition of larval barnacle attachment to bacterial films: an investigation of physical properties. Microb. Ecol. 23:97–106.CrossRefGoogle Scholar
  66. 66.
    Manz, W., U. Szewzyk, P. Ericsson, R. Amann, K.-H. Schleifer, and T.-A. Stenstrom. 1993. In situ identification of bacteria in drinking water and adjoining biofilms by hybridization with 16S and 23S rRNA-directed fluorescent oligonucleode probes. Appl. Environ. Microbiol. 59:2293–2298.PubMedGoogle Scholar
  67. 67.
    Marshall, K. C. 1976. Interfaces in Microbial Ecology, Harvard University Press, Cambridge, Mass.Google Scholar
  68. 68.
    Marshall, K. C. 1984. Microbial Adhesion and Aggregation. Springer-Verlag, Berlin, Germany.CrossRefGoogle Scholar
  69. 69.
    Marshall, K. C. 1992. Planktonic versus sessile life of prokaryotes, p. 262–275. In A. Balows, H. G. Trüper, M. Dworkin, W. Harder, and K. H. Schliefer (ed.), The Prokaryotes, a Handbook on the Biology of Bacteria, Ecophxsiology, Isolation, Identification, Applications, 2nd ed. Springer-Verlag, New York, N.Y.Google Scholar
  70. 70.
    Marshall, K. C. 1992. Biofilms: an overview of bacterial adhesion, activity, and control at surfaces. ASM News 58:202–207.Google Scholar
  71. 71.
    Marshall, K. C. 1993. Microbial ecology: whither goest thou?, p. 5–8. In R. Guerrero and C. Pedrós-Alió (ed.), Trends in Microbial Ecology. Spanish Society for Microbiology, Barcelona, Spain.Google Scholar
  72. 72.
    Marszalek, D. S., S. M. Gerchakov, and L. R. Udey. 1979. Influence of substrate composition on marine microfouling. Appl. Environ. Microbiol. 38:987–995.PubMedGoogle Scholar
  73. 73.
    McFeters, G. A. 1990. Enumeration, occurrence, and significance of injured indicator bacteria in drinking water, p. 478–492. In G. A. McFeters (ed.), Drinking Water Microbiology, Progress and Recent Development. Springer-Verlag, New York, N.Y.CrossRefGoogle Scholar
  74. 74.
    Mitchell, J. G., R. Weller, M. Beconi, J. Sell, J. Sell and J. Holland. 1993. A practical optical trap for manipulating and isolating bacteria from complex microbial communities. Microb. Ecol. 25:113–119.CrossRefGoogle Scholar
  75. 75.
    Morita, R. Y. 1982. Starvation-survival of heterotrophs in the marine environment. Adv. Microb. Ecol. 6:171–198.CrossRefGoogle Scholar
  76. 76.
    Muyzer, G., E. C. de Waal, and A. G. Uitterlinden. 1993. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl. Environ. Microbiol. 59:695–700.PubMedGoogle Scholar
  77. 77.
    Nealson, K. H., B. Wimpee, and C. Wimpee. 1993. Identification of Vibrio splendidus as a member of the planktonic luminous bacteria from the Persian Gulf and Kuwait region with luxA probes. Appl. Environ. Microbiol. 59:2684–2689.PubMedGoogle Scholar
  78. 78.
    Neihof, R., and G. Loeb. 1974. Dissolved organic matter in seawater and the electric charge of immersed surfaces. J. Mar. Res. 32:5–12.Google Scholar
  79. 79.
    Nichols, W. W., M. J. Evans, M. P. E. Slack, and H. L. Walmsley. 1989. The penetration of antibiotics into aggregates of mucoid and nonmucoid Pseudomonas aeruginosa. J. Gen. Microbiol. 135:1291–1303.PubMedGoogle Scholar
  80. 80.
    Nickel, J. C., I. Ruseska, J. B. Wright, and J. W. Costerton. 1985. Tobramycin resistance of Pseudomonas aeruginosa cells growing as a biofilm on urinary catheter material. Antimicrob. Agents Chemother. 27:619–624.PubMedGoogle Scholar
  81. 81.
    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
  82. 82.
    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
  83. 83.
    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
  84. 84.
    Pace, N. R., D. A. Stahl, D. J. Lane, and G. J. Olsen. 1986. The analysis of natural microbial populations by ribosomal RNA sequences. Adv. Microb. Ecol. 9:1–55.Google Scholar
  85. 85.
    Poulsen, L. K., G. Ballard, and D. A. Stahl. 1993. Use of rRNA fluorescence in situ hybridization for measuring the activity of single cells in young and established biofilms. Appl. Environ. Microbiol. 59:1354–1360.PubMedGoogle Scholar
  86. 86.
    Power, K., and K. C. Marshall. 1988. Cellular growth and reproduction of marine bacteria on surface bound substrate. Biofouling 1:163–174.CrossRefGoogle Scholar
  87. 87.
    Revsbech, N. P. and B. B. Jorgensen. 1986. Microelectrodes: their use in microbial ecology. Adv. Microb. Ecol. 9:293–352.Google Scholar
  88. 88.
    Rodriquez, 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.Google Scholar
  89. 89.
    Rogers, J., and C. W. Keevil. 1992. Immunogold and fluorescein immunolabelling of Legionella pneumophila within an aquatic biofilm visualized by using episcopic differential contrast microscopy. Appl. Environ. Microbiol. 58:2326–2330.PubMedGoogle Scholar
  90. 90.
    Roslev, P., and G. M. King. 1993. Application of a tetrazolium salt with a water-soluble formazan as an indicator of viability in respiring bacteria. Appl. Environ. Microbiol. 59:2891–2896.PubMedGoogle Scholar
  91. 91.
    Roszak, D. B., and R. R. Colwell. 1987. Survival strategies of bacteria in the natural environment. Microbiol. Rev. 51:365–379.PubMedGoogle Scholar
  92. 92.
    Samuelsson, M.-O., and D. L. Kirchman. 1991. Degradation of adsorbed protein by attached bacteria in relation to surface hydrophobicity. Appl. Environ. Microbiol. 56:3643–3648.Google Scholar
  93. 93.
    Savage, D. C., and M. Fletcher. 1985. Bacteria Adhesion: Mechanisms and Physiological Significance. Plenum Press, New York, N.Y.Google Scholar
  94. 94.
    Schaule, G., H.-C. Flemming, and H. F. Ridgway. 1993. Use of 5-cyano-2, 3-ditoyl tetrazolium chloride for quantifying planktonic and sessile respiring bacteria in drinking water. Appl. Environ. Microbiol. 59:3850–3857.PubMedGoogle Scholar
  95. 95.
    Schneider, R. P., and K. C. Marshall. 1994. Retention of the Gram-negative marine bacterium SW8 on surfaces—effects of microbial physiology, substratum nature and conditioning films. Colloids & Surfaces, B: Biointerfaces 2:387–396.CrossRefGoogle Scholar
  96. 96.
    Silcock, D. J., R. N. Waterhouse, L. A. Glover, J. I. Prosser, and K. Killham. 1992. Detection of a single genetically modified bacterial cell in soil by using charge coupled device-enhanced microscopy. Appl. Environ. Microbiol. 58:2444–2448.PubMedGoogle Scholar
  97. 97.
    Skyring, G. W., and J. Bauld. 1990. Microbial mats in Australian coastal environments. Adv. Microb. Ecol. 11:461–498.CrossRefGoogle Scholar
  98. 98.
    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.CrossRefGoogle Scholar
  99. 99.
    Stewart, P. S., B. M. Peyton, W. J. Drury, and R. Murga. 1993. Quantitative observations of heterogeneities in Pseudomonas aeruginosa biofilms. Appl. Environ. Microbiol. 59:327–329.PubMedGoogle Scholar
  100. 100.
    Stewart, P. S., T. Griebe, R. Srinivasan, C.-I. Chen, F. P. Yu, D. deBeer, and G. A. McFeters. 1994. Comparison of respiratory activity and culturability during monochloramine disinfection of binary population biofilms. Appl. Environ. Microbiol. 60:1690–1692.PubMedGoogle Scholar
  101. 101.
    Stewart, P. S. 1996. Theoretical aspects of antibiotic diffusion into microbial biofilms. Antimicrob. Agents Chemother. 40:2517–2522.PubMedGoogle Scholar
  102. 102.
    Stoodley, P., Z. Lewandowski, J. D. Boyle, and H. M. Lappin-Scott. 1998. Oscillation characteristics of biofilm streamers in turbulent flowing water as related to drag and pressure drop. Biotechnol. Bioeng. 57:536–544.PubMedCrossRefGoogle Scholar
  103. 103.
    Stoodley, P., I. Dodds, Z. Lewandowski, A. B. Cunningham, J. D. Boyle, and H. M. Lappin-Scott. 1999. Influence of hydrodynamics and nutrients on biofilm structure. J. Appl. Microbiol. 85: 19S–28S.CrossRefGoogle Scholar
  104. 104.
    Szewzyk, U., W. Manz, R. Amann, K.-H. Schleifer, and T.-A. Stenstrom. 1994. Growth and in situ detection of a pathogenic Escherichia coli in biofilms of a heterotrophic water bacterium by use of 16S-and 23S-rRNA-directed fluorescent oligonucleotide probes. FEMS Microbiol. Ecol. 13: 169–176.CrossRefGoogle Scholar
  105. 105.
    Tabor, P. S., and R. A. Neihof. 1982. Improved method for determination of respiring individual microorganisms in natural waters. Appl. Environ. Microbiol. 43:1249–1255.PubMedGoogle Scholar
  106. 106.
    ten Bosch, J. J. 1991. Physico-chemical aspects of biological adhesion. Biofouling 4(1–3): 1–247.CrossRefGoogle Scholar
  107. 107.
    Terzieva, S., J. Donnelly, V. Ulevicius, S. A. Grinshpun, K. Willeke, G. N. Selma, and K. P. Brenner. 1996. Comparison of methods for detection and enumeration of airborne microorganisms collected by liquid impingement. Appl. Environ. Microbiol. 62:2264–2272.PubMedGoogle Scholar
  108. 108.
    Tyler, P. A., and K. C. Marshall. 1967. Microbial oxidation of manganese in hydro-electric pipelines. Antonie van Leeuwenhoek 33:171–183.PubMedCrossRefGoogle Scholar
  109. 109.
    Wagner, M., R. Amann, H. Lemmer, and K.-H. Schleifer. 1993. Probing activated sludge with oligonucleotides specific for proteobacteria: inadequacy of culture-dependent methods for describing microbial community structure. Appl. Environ. Microbiol. 59:1520–1525.PubMedGoogle Scholar
  110. 110.
    Ward, D. M., R. Weller, and M. M. Bateson. 1990. 16S rRNA sequences reveal numerous uncultured microorganisms in a natural community. Nature 345:63–65.PubMedCrossRefGoogle Scholar
  111. 111.
    Ward, D. M., R. Weller, and M. M. Bateson. 1990. 16S rRNA sequences reveal uncultured inhabitants of a well-studied thermal community. FEMS Microbiol. Rev. 75:105–116.CrossRefGoogle Scholar
  112. 112.
    Ward, D. M., M. M. Bateson, R. Weller, and A. L. Ruff-Roberts. 1992. Ribosomal RNA analysis of microorganisms as they occur in nature. Adv. Microb. Ecol. 12:219–286.CrossRefGoogle Scholar
  113. 113.
    Weichart, D., J. D. Oliver, and S. Kjelleberg. 1992. Low temperature induced nonculturability and killing of Vibrio vulnificus. FEMS Microbiol. Lett. 100:205–210.Google Scholar
  114. 114.
    Weller, R., M. M. Bateson, B. K. Heimbuch, E. D. Kopczynski, and D. M. Ward. 1992. Uncultivated cyanobacteria, Chloroflexus-like inhabitants, and spirochete-like inhabitants of a hot spring microbial mat. Appl. Environ. Microbiol. 58:3964–3969.PubMedGoogle Scholar
  115. 115.
    Wolfaardt, G. M., J. R. Lawrence, M. J. Hendry, R. D. Robarts, and D. E. Caldwell. 1993. Development of steady-state diffusion gradients for the cultivation of degradative microbial consortia. Appl. Environ. Microbiol. 59:2388–2396.PubMedGoogle Scholar
  116. 116.
    Yu, F. P. and G. A. McFeters. 1994. Rapid in situ assessment of physiological activities in biofilms using fluorescent probes. J. Microbiol. Methods 20:1–10.PubMedCrossRefGoogle Scholar
  117. 117.
    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

  • Kevin C. Marshall
    • 1
  1. 1.School of Microbiology and ImmunologyThe University of New South WalesSydneyAustralia

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