Biofilm Structure, Behavior, and Hydrodynamics

L. B. Purevdorj-Gage; P. Stoodley

doi:10.1128/9781555817718.ch9

Chapter 9 : Biofilm Structure, Behavior, and Hydrodynamics

Authors: L. B. Purevdorj-Gage¹, P. Stoodley²

VIEW AFFILIATIONS HIDE AFFILIATIONS

Affiliations: 1: Center for Biofilm Engineering, Montana State University, Bozeman, Montana 59717; 2: Center for Genomic Sciences, Allegheny-Singer Research Center, Pittsburgh, Pennsylvania 15212

Content Type: Monograph

Publication Year: 2004

Category: Environmental Microbiology; Microbial Genetics and Molecular Biology

Book DOI: 10.1128/9781555817718

Chapter DOI: 10.1128/9781555817718.ch9

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:

Biofilm Structure, Behavior, and Hydrodynamics, Page 1 of 2

< Previous page | Next page > /docserver/preview/fulltext/10.1128/9781555817718/9781555818944_Chap09-1.gif /docserver/preview/fulltext/10.1128/9781555817718/9781555818944_Chap09-2.gif

Abstract:

This chapter covers the major discoveries associated with biofilm architecture and to discuss some instances where they in turn may be affected by environmental hydrodynamics. Understanding the significance of hydrodynamics in the biofilm life cycle is crucial if we consider the habitats in which the most abundant biofilms tend to accumulate. In summary there are a myriad of factors that influence biofilm development and structure. However, the interaction between hydrodynamics and each of these parameters is poorly characterized. The chapter discusses the influence of hydrodynamics and shear as the major factors that are involved in biofilm architecture, and it is important to keep in mind that all of the identified and yet-to-be-discovered factors are involved in a dynamic, interrelated manner and there is no single global regulating pathway so far known to control this process. The chapter also discusses the roles of hydrodynamics and shear in biofilm structural maturation as well as how they may affect the major factors that are involved in the process. In vitro studies performed in the laboratory and the observations of biofilms growing in the natural environment demonstrate the importance of hydrodynamics and shear in biofilm structural development.

Citation: Purevdorj-Gage, Stoodley P. 2004. Biofilm Structure, Behavior, and Hydrodynamics, p 160-173. In Ghannoum M, O'Toole G (ed), Microbial Biofilms. ASM Press, Washington, DC. doi: 10.1128/9781555817718.ch9

Highlighted Text: Show | Hide

Full text loading...

Figures

Biofilm Structure, Behavior, and Hydrodynamics

[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555817718.chap9-1,webId=/content/author/10.1128/9781555817718.chap9-1,properties={foaf_givenname= L. B., foaf_name= L. B. Purevdorj-Gage, foaf_surname=Purevdorj-Gage, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555817718.chap9-aff1]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555817718.chap9-2,webId=/content/author/10.1128/9781555817718.chap9-2,properties={foaf_givenname=P., foaf_name=P. Stoodley, foaf_surname=Stoodley, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555817718.chap9-aff2]]}]]

/content/10.1128/9781555817718.chap9.fig9-1

FIGURE 1

Structural phenotypes of both natural and laboratory biofilms are strikingly similar. A microbial biofilm growing in a hot spring in Biscuit geyser basin, Yellowstone National Park, forming ripple structures (A) was similar to the ones formed by mixed-species biofilms in the laboratory (B). A microbial biofilm with streamers in Canary Spring, Yellowstone National Park (C), was similar to streamers formed by a laboratory-grown P. aeruginosa biofilm (D). The direction of fluid flow in all panels was left to right. Bars, ∼20 cm (A and C) and 200 µm (B and D).

10.1128/9781555817718/fig9-1_thmb.gif

10.1128/9781555817718/fig9-1.gif

FIGURE 1

/content/10.1128/9781555817718.chap9.fig9-2

FIGURE 2

Dynamic behavior and associated structural phenotypes of bacterial biofilms in flowing fluids. The various dynamic processes are discussed in the text. Schematic by P. Dirckx, Center for Biofilm Engineering, Montana State University, 2003.

10.1128/9781555817718/fig9-2_thmb.gif

10.1128/9781555817718/fig9-2.gif

FIGURE 2

/content/10.1128/9781555817718.chap9.fig9-3

FIGURE 3

A structurally specialized P. aeruginosa biofilm cluster. The cluster is composed of an outer layer of nonmotile cells that form a “wall” (indicated by the white arrows). In the interior of the cluster cells swim about rapidly before flowing out, leaving the cluster empty. The flow direction is indicated by the black arrow. Bar, 20 µm.

10.1128/9781555817718/fig9-3_thmb.gif

10.1128/9781555817718/fig9-3.gif

FIGURE 3

References

/content/book/10.1128/9781555817718.chap9

1. Aizawa, S. I. 1996. Flagellar assembly in Salmonella typhimurium. Mol. Microbiol. 19: 1– 5.

2. Allison, D. G.,, B. Ruiz,, C. San Jose,, A. Jaspe,, and P. Gilbert. 1998. Extracellular products as mediators of the formation and detachment of Pseudomonas fluorescens biofilms. FEMS Microbiol. Lett. 167: 179– 184.

3. Applegate, D. H.,, and J. D. Bryers. 1991. Effects of carbon and oxygen limitations and calcium concentrations on biofilm removal processes. Biotechnol. Bioeng. 37: 17– 25.

4. Bryers, J. D., 1988. Modeling biofilm accumulation, p. 109– 144. In M. Bazin, and J. I. Prosser (ed.), Physiological Models in Microbiology. CRC Press, Boca Raton, Fla.

5. Caiazza, N. C,, and G. A. O’Toole. 2003. Alphatoxin is required for biofilm formation by Staphylococcus aureus. J. Bacteriol. 185: 3214– 3217.

6. Caldwell, D. E.,, D. R. Korber,, and J. R. Lawrence. 1992. Confocal laser microscopy and digital image analysis in microbial ecology. Adv. Microb. Ecol. 12: 1– 67.

7. Cescutti, P.,, R. Toffanin,, P. Pollesello,, and I. W. Sutherland. 1999. Structural determination of the acidic exopolysaccharide produced by a Pseudomonas sp. strain 1.15. Carbohydr. Res. 315: 159– 168.

8. Characklis, W. G. 1973. Attached microbial growths. II. Frictional resistance due to microbial slimes. Water Res. 7: 1249– 1258.

9. Characklis, W. G.,, and K. C. Marshall. 1990. Biofilms, p. 397– 443. John Wiley & Sons, New York, N.Y.

10. Costerton, J. W.,, and P. S. Stewart. 2001. Battling biofilms. Sci. Am. 285: 75– 81.

11. Costerton, J. W.,, K.-J. Cheng,, G. G. Geesey,, T. I. Ladd,, J. C. Nickel,, M. Dasgupta,, and T. J. Marrie. 1987. Bacterial biofilms in nature and disease. Annu. Rev. Microbiol. 41: 435– 464.

12. Costerton, J. W.,, P. S. Stewart,, and E. P. Greenberg. 1999. Bacterial biofilms: a common cause of persistent infections. Science 284: 1318– 1322.

13. Costerton, J. W.,, Z. Lewandowski,, D. De Beer,, D. Caldwell,, D. Korber,, and G. James. 1994. Biofilms, the customized microniche. J. Bacteriol. 176: 2137– 2142.

14. Cramton, S. E.,, C. Gerke,, N. F. Schnell,, W. W. Nichols,, and F. Cotz. 1999. The intercellular adhesion (ica) locus is present in Staphylococcus aureus and is required for biofilm formation. Infect. Immun. 67: 5427– 5433.

15. Cucarella, C.,, C. Solano,, J. Valle,, B. Amorena, Í. Lasa, and J. R. Penadés. 2001. Bap, a Staphylococcus aureus surface protein involved in biofilm formation. J. Bacteriol. 183: 2888– 2928.

16. 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.

17. De Beer, D.,, P. Stoodley,, F. Roe,, and Z. Lewandowski. 1994. Effects of biofilm structures on oxygen distribution and mass transport. Biotechnol. Bioeng. 43: 1131– 1138.

18. De Kievit, T. R.,, R. Gillis,, S. Marx,, C. Brown,, and B. H. Iglewski. 2001. Quorum-sensing genes in P. aeruginosa biofilms: their role and expression patterns. Appl. Environ. Microbiol. 67: 1865– 1873.

19. Donlan, R. M. 2002. Biofilms: microbial life on surfaces. Emerg. Infect. Dis. 8: 881– 890.

20. Edwards, J. K.,, P. L. Bond,, T. M. Gihring,, and J. F. Banfield. 2000. An archaeal iron-oxidizing extreme acidophile important in acid mine drainage. Science 287: 1731– 1732.

21. Fang, H. H. P.,, and X. S. Jia. 1996. Extraction of extracellular polymer from anaerobic sludges. Biotechnol. Tech. 10: 803– 808.

22. Flemming, H. C.,, J. Wingender,, C. Mayer,, V. Korstgens,, and W. Borchard,. 2000. Cohesiveness in biofilm matrix polymers, p. 87– 105. In D. Allison,, P. Gilbert,, H. M. Lappin-Scott,, and M. Wilson, (ed.), Community Structure and Cooperation in Biofilms. SGM Symposium Series 59. Cambridge University Press, Cambridge, United Kingdom.

23. Froeliger, E. H.,, and P. Fives-Taylor. 2001. Streptococcus parasanguis fimbria associated adhesion Fap1 is required for biofilm formation. Infect. Immun. 69: 2512– 2519.

24. Frølund, B.,, R. Palmgren,, K. Keiding,, and P. H. Nielsen. 1996. Extraction of extracellular polymers from activated sludge using a cation exchange resin. Water Res. 30: 1749– 1758.

25. Frølund, B.,, T. Griebe,, and P. H. Nielsen. 1995. Enzymatic activity in the activated-sludge floc matrix. Appl. Microbiol. Biotechnol. 43: 755– 761.

26. Gantzer, C. J.,, B. E. Rittmann,, and E. E. Herricks. 1991. Effects of long-term water velocity changes on streambed biofilm activity. Water Res. 25: 15– 20.

27. Gavín, R.,, A. A. Rabaan,, S. Merino,, J. M. Tomás,, I. Gryllos,, and J. G. Shaw. 2002. Lateral flagella of Aeromonas species are essential for epithelial cell adherence and biofilm formation. Mol. Microbiol. 43: 383– 397.

28. Grotenhuis, J. T. C.,, M. Smit,, C. M. Plugge,, X. Yuansheng,, A. A. M. van Lammeren,, A. J. M. Stams,, and J. B. Zehnder. 1991. Bacteriological composition and structure of granular sludge adapted to different substrates. Appl. Environ. Microbiol. 57: 1942– 1949.

29. Hall-Stoodley, L.,, and P. Stoodley. 2002. Development regulation of microbial biofilms. Curr. Opin. Biotechnol. 13: 228– 233.

30. Hamon, M. A.,, and B. A. Lazazzera. 2001. The sporulation transcription factor Spo0A is required for biofilm development in Bacillus subtilis. Mol. Microbiol. 42: 1199– 1209.

31. Handley, P. S.,, A. H. Rickard,, N. J. High,, and S. A. Leach,. 2001. Coaggregation, is it a universal phenomenon?, p. 1– 10. In P. Gilbert,, D. Allison,, J. Verran,, M. Brading,, and J. Walker (ed.), Biofilm Community Interactions: Chance or Necessity Bioline Press, Cardiff, United Kingdom.

32. Harshey, R. M. 1994. Bees aren’t the only ones: swarming in Gram-negative bacteria. Mol. Microbiol. 13: 389– 394.

33. Hentzer, M.,, G. M. Teitzel,, G. J. Balzer,, A. Heydorn,, S. Molin,, M. Givskov,, and M. R. Parsek. 2001. Alginate overproduction affects Pseudomonas aeruginosa biofilm structure and function. J. Bacteriol. 183: 5395– 5401.

34. Hermanowicz, S. W.,, U. Schindler,, and P. A. Wilderer. 1995. Fractal structure of biofilms: new tools for investigation of morphology. Water Sci. Technol. 32: 99– 105.

35. Heukelekian, H.,, and A. Heller. 1940. Relation between food concentration and surface for bacterial growth. J. Bacteriol. 40: 547– 558.

36. Heydorn, A.,, A. T. Nielsen,, M. Hentzer,, C. Sternberg,, M. Givskov,, B. K. Ersbøll,, and S. Molin. 2000. Quantification of biofilm structures by the novel computer program COMSTAT. Microbiology 146: 2395– 2407.

37. Heydorn, A.,, B. Ersboll,, K. J. Kato,, M. Hentzer,, M. R. Parsek,, A. T. Nielsen,, M. Givskov,, and S. Molin. 2002. Statistical analysis of Pseudomonas aeruginosa biofilm development: impact of mutations in genes involved in twitching motility, cell-to-cell signalling, and stationary-phase sigma factor expression. Appl. Environ. Microbiol. 68: 2008– 2017.

38. Huber, B.,, K. Riedel,, M. Hentzer,, A. Heydorn,, A. Gotschlich,, M. Givskov,, S. Molin,, and L. Eberl. 2001. The cep quorum sensing system of Burkholderia cepacia H11 controls biofilm formation and swarming motility. Microbiology 47: 2517– 2528.

39. Jackson, D. W.,, J. W. Simecka,, and T. Romeo. 2002. Catabolite repression of Escherichia coli biofilm formation. J. Bacteriol. 184: 3406– 3410.

40. Jahnke, L. L.,, W. Eder,, R. Huber,, J. M. Hope,, K. U. Hinrichs,, J. M. Hayes,, D. V. J. Des Marais,, S. L. Cady,, and R. E. Summons. 2001. Signature lipids and stable carbon isotope analyses of octopus spring hyperthermophilic communities compared with those of aquificales representatives. Appl. Environ. Microbiol. 67: 5179– 5189.

41. Jones, H. C.,, I. L. Roth, , and W. M. Saunders III. 1969. Electron microscopic study of a slime layer. J. Bacteriol. 99: 316– 325.

42. Kaplan, J. B.,, F. M. Meyenhofer,, and D. H. Fine. 2003. Biofilm growth and detachment of Actinobacillus actinomycetemcomitans. J. Bacteriol. 185: 1399– 1404.

43. Klapper, I.,, C. J. Rupp,, R. Cargo,, B. Purevdorj,, and P. Stoodley. 2002. A viscoelastic fluid description of bacterial biofilm material properties. Biotechnol. Bioeng. 80: 289– 296.

44. Korber, D. R.,, J. R. Lawrence,, and D. E. Caldwell. 1994. Effect of motility on surface colonization and reproductive success of Pseudomonas fluorescens in dual-dilution continuous culture and batch culture systems. Appl. Environ. Microbiol. 60: 1421– 1429.

45. Körstgens, V.,, H.-C. Flemming,, J. Wingender,, and W. Borchard. 2001. Uniaxial compression measurement device for investigation of the mechanical stability of biofilms. J. Microbiol. Methods 46: 9– 17.

46. 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.

47. Li, Y. H.,, N. Tang,, M. B. Aspiras,, P. C. Y. Lau,, J. H. Lee,, R. P. Ellen,, and D. G. Cvitkovitch. 2002. A quorum sensing signaling system essential for genetic competence in Streptococcus mutans is involved in biofilm formation. J. Bacteriol. 184: 2699– 2708.

48. Liu, H.,, and H. H. P. Fang. 2002. Extraction of extracellular polymeric substances (EPS) of sludges. J. Biotechnol. 95: 249– 256.

49. Liu, Y.,, and J. H. Tay. 2001. Metabolic response of biofilm to shear stress in fixed-film culture. J. Appl. Microbiol. 90: 337– 342.

50. Loo, C. Y.,, D. A. Corliss,, and N. Ganeshkumar. 2000. Streptococcus gordonii biofilm formation: identification of genes that code for biofilm phenotypes. J. Bacteriol. 182: 1374– 1382.

51. Lynch, M. J.,, S. Swift,, D. F. Kirke,, C. W. Keevil,, C. E. Dodds,, and P. Williams. 2002. The regulation of biofilm development by quorum sensing in Aeromonas hydrophila. Environ. Microbiol. 4: 18– 28.

52. Massol-Deya, A. A.,, J. Whallon,, R. F. Hickey,, and J. M. Tiedje. 1995. Channel structures in aerobic biofilms of fixed-film reactors treating contaminated groundwater. Appl. Environ. Microbiol. 61: 769– 777.

53. McClaine, J. W.,, and R. M. Ford. 2002. Characterizing the adhesion of motile and nonmotile Escherichia coli to a glass surface using a parallel-plate flow chamber. Biotechnol. Bioeng. 78: 179– 189.

54. McLean, R. J. C.,, M. Whitely,, D. J. Stickler,, and W. C. Fuqua. 1997. Evidence of autoinducer activity in naturally occurring biofilms. FEMS Microbiol. Lett. 154: 259– 263.

55. Moller, S.,, D. Korber,, G. Woolfaardt,, S. Molin,, and D. Caldwell. 1997. Impact of nutrient composition on a degradative biofilm community. Appl. Environ. Microbiol. 63: 2433– 2438.

56. Mueller, R. F. 1996. Bacterial transport and colonization in low nutrient environments. Water Res. 30: 2681– 2690.

57. Murga, R. T.,, S. Foster,, E. Brown,, J. M. Pruickler,, B. S. Fields,, and R. M. Donlan. 2001. Role of biofilms in the survival of Legionella pneumophila in a model potable-water system. Microbiology 147: 3121– 3126.

58. Nickel, J. C.,, J. W. Costerton,, R. J. C. McLean,, and M. Olson. 1994. Bacterial biofilms: influence on the pathogenesis, diagnosis and treatment of urinary-tract infections. J. Antimicrob. Chemother. 33: 31– 41.

59. Nivens, D. E, D. E. Ohman, J. Williams, and M. J. Franklin. 2001. Role of alginate and its O acetylation in formation of Pseudomonas aeruginosa microcolonies and biofilms. J. Bacteriol. 183: 1047– 1057.

60. O’Toole, G. A.,, and R. Kolter. 1998. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol. Microbiol. 30: 295– 304.

61. O’Toole, G.,, H. B. Kaplan,, and R. Kolter. 2000. Biofilm formation as microbial development. Annu. Rev. Microbiol. 54: 49– 79.

62. Peyton, B. M. 1996. Effects of shear stress and substrate loading rate on Pseudomonas aeruginosa biofilm thickness and density. Water Res. 30: 29– 36.

63. Picioreanu, C.,, M. C. van Loosdrecht,, and J. J. Heijnen. 2001. Two-dimensional model of biofilm etachment caused by internal stress from liquid flow. Biotechnol. Bioeng. 72: 205– 218.

64. Piriou, P.,, S. Dukan,, Y. Levi,, and P. A. Jarrige. 1997. Prevention of bacterial growth in drinking water distribution systems. Water Sci. Technol. 35: 283– 287.

65. Pratt, L. A.,, and R. Kolter. 1998. Genetic analysis of Escherichia coli biofilm formation: roles of flagella, motility, chemotaxis, and type I pili. Mol. Microbiol. 30: 285– 293.

66. Prouty, A. M.,, W. H. Schwesinger,, and J. S. Gunn. 2002. Biofilm formation and interaction with the surfaces of gallstones by Salmonella spp. Infect. Immun. 70: 2640– 2649.

67. Purevdorj, B.,, J. W. Costerton,, and P. Stoodley. 2002. Influence of hydrodynamics and cell signaling on the structure and behavior of Pseudomonas aeruginosa biofilms. Appl. Environ. Microbiol. 68: 4457– 4464.

68. Rasmussen, B. 2000. Filamentous microfossils in a 3,235-million-year-old volcanogenic massive sulphide deposit. Nature 405: 676– 679.

69. Reysenbach, A. L.,, and S. L. Cady. 2001. Microbiology of ancient and modern hydrothermal systems. Trends Microbiol. 9: 79– 86.

70. Reysenbach, A. L.,, M. Ehringer,, and K. Hershberger. 2000. Microbial diversity at 83 degrees C in Calcite Springs, Yellowstone National Park: another environment where the Aquificales and “Korarchaeota” coexist. Extremophiles 4: 61– 67.

71. Rickard, A. H.,, A. J. McBain,, R. G. Ledder, Handley, and P. S. Gilbert. 2003. Coaggregation between freshwater bacteria within biofilm and planktonic communities. FEMS Microbiol. Lett. 220: 133– 140.

72. Rickard, A. H.,, C. M. Buswell,, S. A. Leach,, N. J. High,, and P. S. Handley. 2002. Phylogenetic relationships and coaggregation ability of freshwater biofilm bacteria. Appl. Environ. Microbiol. 68: 3644– 3650.

73. Rickard, A. H.,, S. A. Leach,, C. M. Buswell,, N. J. High,, and P. S. Handley. 2000. Coaggregation between aquatic bacteria is mediated by specific-growth-phase-dependent lectin-saccharide interactions. Appl. Environ. Microbiol. 66: 431– 434.

74. Sauer, K, , A. K. Camper, , G. D. Ehrlich, , J. W. Costerton, , and D. G. Davies. 2002. Pseudomonas aeruginosa displays multiple phenotypes during development as a biofilm. J. Bacteriol. 184: 1140– 1154.

75. Schmidt, J. E.,, and B. K. Ahring. 1999. Immobilization patterns and dynamics of acetate-utilizing methanogens immobilized in sterile granular sludge in upflow anaerobic sludge blanket reactors. Appl. Environ. Microbiol. 65: 1050– 1054.

76. Singh, P. K.,, A. L. Schaefer,, M. R. Parsek,, T. O. Moninger,, M. J. Welsh,, and E. P. Greenberg. 2000. Quorum-sensing signals indicate that cystic fibrosis lungs are infected with bacterial biofilms. Nature 407: 762– 764.

77. Stewart, P. S. 1993. A model of biofilm detachment. Biotechnol. Bioeng. 41: 111– 117.

78. Stewart, P. S.,, G. A. McFeters,, and C. T. Huang,. 2000. Biofilm formation and persistence, p. 373– 405. In J. D. Bryers (ed.), Biofilms II: Process Analysis and Application. Wiley-Liss, New York, N.Y.

79. Stickler, D. J,, N. S. Morris, , R. J. McLean, , and C. Fuqua. 1998. Biofilms on indwelling urethral catheters produce quorum-sensing signal molecules in situ and in vitro. Appl. Environ. Microbiol. 64: 3486– 3490.

80. Stoodley, P.,, A. Jacobsen,, B. C. Dunsmore,, B. Purevdorj,, S. Wilson,, H. M. Lappin-Scott,, and J. W. Costerton. 2001. The influence of fluid shear and AlCl3 on the material properties of Pseudomonas aeruginosa PAO1 and Desulfovibrio sp. EX265 biofilms. Water Sci. Technol. 43: 113– 120.

81. Stoodley, P.,, D. De Beer,, and Z. Lewandowski. 1994. Liquid flow in biofilm systems. Appl. Environ. Microbiol. 60: 2711– 2716.

82. Stoodley, P.,, D. De Beer,, J. D. Boyle,, and H. M. Lappin-Scott. 1999a. Evolving perspectives of biofilm structure. Biofouling 14: 75– 94.

83. Stoodley, P.,, F. Jørgensen,, P. Williams,, and H. M. Lappin-Scott,. 1999b. The role of hydrodynamics and AHL signalling molecules as determinants of the structure of Pseudomonas aeruginosa biofilms, p. 323– 330. In R. Bayston, , M. Brading, , P. Gilbert, , J. Walker, , and J. W. T. Wimpenn (ed.) , Biofilms: The Good, the Bad, and the Ugly, Bioline Press, Cardiff, United Kingdom.

84. Stoodley, P.,, K. Sauer,, D. G. Davies,, and J. W. Costerton. 2002a. Biofilms as complex differentiated communities. Annu. Rev. Microbiol. 56: 187– 209.

85. Stoodley, P.,, R. Cargo,, C. J. Rupp,, S. Wilson,, and I. Klapper. 2002b. Biofilm mechanics and shear induced deformation and detachment. J. Ind. Microbiol. Biotechnol. 29: 361– 368.

86. Stoodley, P.,, Z. Lewandowski,, J. Boyle,, and H. M. Lappin-Scott. 1998. Oscillation characteristics of biofilm streamers in flowing water as related to drag and pressure drop. Biotechnol. Bioeng. 57: 536– 544.

87. Stoodley, P.,, Z. Lewandowski,, J. D. Boyle,, and H. M. Lappin-Scott. 1999c. The formation of migratory ripples in a mixed species bacterial biofilm growing in turbulent flow. Environ. Microbiol. 1: 447– 457.

88. Stoodley, P.,, Z. Lewandowski,, J. D. Boyle,, and H. M. Lappin-Scott. 1999d. Structural deformation of bacterial biofilms caused by short term fluctuations in flow velocity: an in-situ demonstration of biofilm viscoelasticity. Biotechnol. Bioeng. 65: 83– 92.

89. Sutherland, I. W.,, and L. Kennedy. 1996. Polysaccharide lyases from gellan-producing Sphingomonas spp. Microbiology 142: 867– 72.

90. Tolker-Nielsen, T.,, U. C. Brinch,, P. C. Ragas,, J. B. Andersen,, C. S. Jacobsen,, and S. Molin. 2000. Development and dynamics of Pseudomonas sp. Biofilms. J. Bacteriol. 182: 6482– 6489.

91. Towler, B. W.,, C. J. Rupp,, A. B. Cunningham,, and P. Stoodley. 2003. Viscoelastic properties of a mixed culture biofilm from rheometer creep analysis. Biofouling 19: 279– 285.

92. Tsuneda, S.,, S. Park,, H. Hayashi,, J. Jung,, and A. Hirate. 2001. Enhancement of nitrifying biofilm formation using selected EPS produced by heterotrophic bacteria. Water Sci. Technol. 43: 197– 204.

93. Van Loosdrecht, M. C. M, , C. Picioreanu, , and J. J. Heijnen. 1997. A more unifying hypothesis for the structure of microbial biofilms. FEMS Microbiol. Ecol. 24: 181– 183.

94. Van Loosdrecht, M. C. M.,, D. Eikelboom,, A. Gjaltema,, A. Mulder,, L. Tijhuis,, and J. J. Heijnen. 1995. Biofilm structures. Water Sci. Technol. 32: 35– 43.

95. Veiga, M. C.,, K. J. Mahendra,, W. M. Wu,, R. I. Hollingsworth,, and J. G. Zeikus. 1997. Composition and role of extracellular polymers in methanogenic granules. Appl. Environ. Microbiol. 63: 403– 407.

96. Walker, J. T.,, C. W. Mackerness,, D. Mallon,, T. Makin,, T. Williets,, and C. W. Keevil. 1995. Control of legionella-pneumophila in a hospital water-system by chlorine dioxide. J. Ind. Microbiol. 15: 384– 390.

97. Watnick, P. I.,, and R. Kolter. 1999. Steps in the development of Vibrio cholerae El Tor biofilm. Mol. Microbiol. 34: 586– 595.

98. Westall, F.,, M. J. de Wit,, J. Dann,, S. van der Gaast,, C. E. J. de Ronde,, and D. Gerneke. 2001. Early Archean fossil bacteria and biofilms in hydrothermally-influenced sediments from the Barberton greenstone belt, South Africa. Precambrian Res. 106: 93– 116.

99. Whitchurch, C. B.,, T. Tolker-Nielsen,, P. C. Ragas,, and J. S. Mattick. 2002. Extracellular DNA required for bacterial biofilm formation. Science 295: 1487.

100. Wolfaardt, G. M.,, J. R. Lawrence,, R. D. Robarts,, S. J. Caldwell,, and D. E. Caldwell. 1994. Multicellular organization in a degradative biofilm community. Appl. Environ. Microbiol. 60: 434– 446.

101. Yang, X.,, H. Beyenal,, G. Harkin,, and Z. Lewandowski. 2000. Quantifying biofilm structure using image analysis. J. Microbiol. Methods 39: 109– 119.

102. Yang, X.,, H. Beyenal,, G. Harkin,, and Z. Lewandowski. 2001. Evaluation of biofilm image thresholding methods. Water Res. 35: 1149– 1158.

103. Zhang, T. C.,, and P. L. Bishop. 1994. Density, porosity, and pore structure of biofilm. Water Res. 28: 2267– 2277.

104. Zhang, X. Q.,, P. L. Bishop,, and B. K. Kinkle. 1999. Comparison of extraction methods for quantifying extracellular polymers in biofilms. Water Sci. Technol. 39: 211– 218.

105. Zobell, C. E. 1943. The effect of solid surfaces on bacterial activity. J. Bacteriol. 46: 39– 56.

106. Zottola, E. A.,, and K. C. Sasahara. 1994. Microbial biofilms in the food industry: should they be a concern? Int. J. Food Microbiol. 23: 125– 148.