1887

Abstract

Pseudomonads are able to form a variety of biofilms that colonize the air–liquid (A–L) interface of static liquid microcosms, and differ in matrix composition, strength, resilience and degrees of attachment to the microcosm walls. From SBW25, mutants have evolved during prolonged adaptation–evolution experiments which produce robust biofilms of the physically cohesive class at the A–L interface, and which have been well characterized. In this study we describe a novel A–L interface biofilm produced by SBW25 that is categorized as a viscous mass (VM)-class biofilm. Several metals were found to induce this biofilm in static King's B microcosms, including copper, iron, lead and manganese, and we have used iron to allow further examination of this structure. Iron was demonstrated to induce SBW25 to express cellulose, which provided the matrix of the biofilm, a weak structure that was readily destroyed by physical disturbance. This was confirmed by a low (0.023–0.047 g) maximum deformation mass and relatively poor attachment as measured by crystal violet staining. Biofilm strength increased with increasing iron concentration, in contrast to attachment levels, which decreased with increasing iron. Furthermore, iron added to mature biofilms significantly increased strength, suggesting that iron also promotes interactions between cellulose fibres that increase matrix interconnectivity. Whilst weak attachment is important in maintaining the biofilm at the A–L interface, surface-interaction effects involving cellulose, which reduced surface tension by ∼3.8 mN m, may also contribute towards this localization. The fragility and viscoelastic nature of the biofilm were confirmed by controlled-stress amplitude sweep tests to characterize critical rheological parameters, which included a shear modulus of 0.75 Pa, a zero shear viscosity of 0.24 Pa s and a flow point of 0.028 Pa. Growth and morphological data thus far support a non-specific metal-associated physiological, rather than mutational, origin for production of the SBW25 VM biofilm, which is an example of the versatility of bacteria to inhabit optimal niches within their environment.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.025064-0
2009-05-01
2019-09-17
Loading full text...

Full text loading...

/deliver/fulltext/micro/155/5/1397.html?itemId=/content/journal/micro/10.1099/mic.0.025064-0&mimeType=html&fmt=ahah

References

  1. Bantinaki, E., Kassen, R., Knight, C. G., Robinson, Z., Spiers, A. J. & Rainey, P. B. ( 2007; ). Adaptive divergence in experimental populations of Pseudomonas fluorescens. III. Mutational origins of Wrinkly Spreader diversity. Genetics 176, 441–453.[CrossRef]
    [Google Scholar]
  2. Battin, T. J., Sloan, W. T., Kjelleberg, S., Daims, H., Head, I. M., Curtis, T. P. & Eberl, L. ( 2007; ). Microbial landscapes: new paths to biofilm research. Nat Rev Microbiol 5, 76–81.[CrossRef]
    [Google Scholar]
  3. Branda, S. S., Vik, Å., Friedman, L. & Kolter, R. ( 2005; ). Biofilms: the matrix revisited. Trends Microbiol 13, 20–26.[CrossRef]
    [Google Scholar]
  4. Danhorn, T. & Fuqua, C. ( 2007; ). Biofilm formation by plant-associated bacteria. Annu Rev Microbiol 61, 401–422.[CrossRef]
    [Google Scholar]
  5. de Bruijn, I., de Kock, M. J., Yang, M., de Waard, P., van Beek, T. A. & Raaijmakers, J. M. ( 2007; ). Genome-based discovery, structure prediction and functional analysis of cyclic lipopeptide antibiotics in Pseudomonas species. Mol Microbiol 63, 417–428.[CrossRef]
    [Google Scholar]
  6. Fidalgo, M., Barrales, R. R., Ibeas, J. I. & Jimenez, J. ( 2006; ). Adaptive evolution by mutations in the FLO11 gene. Proc Natl Acad Sci U S A 103, 11228–11233.[CrossRef]
    [Google Scholar]
  7. Flemming, H.-C., Neu, T. R. & Wozniak, D. J. ( 2007; ). The EPS matrix: the “house of biofilm cells”. J Bacteriol 189, 7945–7947.[CrossRef]
    [Google Scholar]
  8. Gehrig, S. M. ( 2005; ). Adaptation of Pseudomonas fluorescens SBW25 to the air–liquid interface: a study in evolutionary genetics. DPhil thesis, University of Oxford.
  9. Hall-Stoodley, L., Costerton, J. W. & Stoodley, P. ( 2004; ). Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2, 95–108.[CrossRef]
    [Google Scholar]
  10. Janmey, P. A. & Schliwa, M. ( 2008; ). Rheology. Curr Biol 18, R639–R641.[CrossRef]
    [Google Scholar]
  11. Janmey, P. A., Georges, P. C. & Hvidt, S. ( 2007; ). Basic rheology for biologists. Methods Cell Biol 83, 3–27.
    [Google Scholar]
  12. King, E. O., Ward, M. K. & Raney, D. C. ( 1954; ). Two simple media for the demonstration of pyocyanin and fluorescin. J Lab Clin Med 44, 301–307.
    [Google Scholar]
  13. Klapper, I. & Dockery, J. ( 2006; ). Role of cohesion in the material description of biofilms. Phys Rev E Stat Nonlin Soft Matter Phys 74, 031902 [CrossRef]
    [Google Scholar]
  14. Körstgens, V., Flemming, H.-C., Wingender, J. & Borchard, W. ( 2001; ). Uniaxial compression measurement device for investigation of the mechanical stability of biofilms. J Microbiol Methods 46, 9–17.[CrossRef]
    [Google Scholar]
  15. Mezger, T. G. ( 2006; ). The Rheology Handbook: for Users of Rotational and Oscillatory Rheometers, 2nd edn. Hannover, Germany: Vincentz Network.
  16. Moon, C. D., Zhang, X.-X., Matthijs, S., Schäfer, M., Budzikiewicz, H. & Rainey, P. B. ( 2008; ). Genomic, genetic and structural analysis of pyoverdine-mediated iron acquisition in the plant growth-promoting bacterium Pseudomonas fluorescens SBW25. BMC Microbiol 8, 7 [CrossRef]
    [Google Scholar]
  17. Persson, B., Nilsson, S. & Bergman, R. ( 1999; ). Dynamic surface tension of dilute aqueous solutions of nonionic cellulose derivatives in relation to other macromolecular characterization parameters. J Colloid Interface Sci 218, 433–441.[CrossRef]
    [Google Scholar]
  18. Rainey, P. B. & Bailey, M. J. ( 1996; ). Physical map of the Pseudomonas fluorescens SBW25 chromosome. Mol Microbiol 19, 521–533.[CrossRef]
    [Google Scholar]
  19. Ramey, B. E., Koutsoudis, M., von Bodman, S. B. & Fuqua, C. ( 2004; ). Biofilm formation in plant–microbe associations. Curr Opin Microbiol 7, 602–609.[CrossRef]
    [Google Scholar]
  20. Römling, U. ( 2005; ). Characterization of the rdar morphotype, a multicellular behaviour in Enterobacteriaceae. Cell Mol Life Sci 62, 1234–1246.[CrossRef]
    [Google Scholar]
  21. Rupp, C. J., Fux, C. A. & Stoodley, P. ( 2005; ). Viscoelasticity of Staphylococcus aureus biofilms in response to fluid shear allows resistance to detachment and facilitates rolling migration. Appl Environ Microbiol 71, 2175–2178.[CrossRef]
    [Google Scholar]
  22. Singh, P. K., Parsek, M. R., Greenberg, E. P. & Welsh, M. J. ( 2002; ). A component of innate immunity prevents bacterial biofilm development. Nature 417, 552–555.[CrossRef]
    [Google Scholar]
  23. Spiers, A. J. ( 2007; ). Wrinkly-Spreader fitness in the two-dimensional agar plate microcosm: maladaptation, compensation and ecological success. PLoS One 2, e740 [CrossRef]
    [Google Scholar]
  24. Spiers, A. J. & Rainey, P. B. ( 2005; ). The Pseudomonas fluorescens SBW25 Wrinkly Spreader biofilm requires attachment factor, cellulose fibre and LPS interactions to maintain strength and integrity. Microbiology 151, 2829–2839.[CrossRef]
    [Google Scholar]
  25. Spiers, A. J., Kahn, S. G., Travisano, M., Bohannon, J. & Rainey, P. B. ( 2002; ). Phenotypic evolution in Pseudomonas fluorescens. 1. Determinants of Wrinkly Spreader fitness and the cause of an evolutionary transition. Genetics 161, 33–46.
    [Google Scholar]
  26. Spiers, A. J., Bohannon, J., Gehrig, S. & Rainey, P. B. ( 2003; ). Biofilm formation at the air–liquid interface by the Pseudomonas fluorescens SBW25 Wrinkly Spreader requires an acetylated form of cellulose. Mol Microbiol 50, 15–27.[CrossRef]
    [Google Scholar]
  27. Spiers, A. J., Arnold, D. L., Moon, C. D. & Timms-Wilson, T. M. ( 2006; ). A survey of A–L biofilm formation and cellulose expression amongst soil and plant-associated Pseudomonas isolates. In Microbial Ecology of Aerial Plant Surfaces, pp. 121–132. Edited by M. J. Bailey, A. K. Lilley, T. M. Timms-Wilson & P. T. N. Spencer-Phillips. Wallingford, UK: CABI.
  28. Stoodley, P., Cargo, R., Rupp, C. J., Wilson, S. & Klapper, I. ( 2002; ). Biofilm material properties as related to shear-induced deformation and detachment phenomena. J Ind Microbiol Biotechnol 29, 361–367.[CrossRef]
    [Google Scholar]
  29. Sutherland, I. W. ( 2001; ). Biofilm exopolysaccharides: a strong and sticky framework. Microbiology 147, 3–9.
    [Google Scholar]
  30. Ude, S., Arnold, D. L., Moon, C. D., Timms-Wilson, T. & Spiers, A. J. ( 2006; ). Biofilm formation and cellulose expression among diverse environmental Pseudomonas isolates. Environ Microbiol 8, 1997–2011.[CrossRef]
    [Google Scholar]
  31. Van Hamme, J. D., Singh, A. & Ward, O. P. ( 2006; ). Physiological aspects. Part 1 in a series of papers devoted to surfactants in microbiology and biotechnology. Biotechnol Adv 24, 604–620.[CrossRef]
    [Google Scholar]
  32. Villavicencio, E. ( 2000; ). Biofilm analysis of Pseudomonas fluorescens SBW25. The role of cellulose in biofilm development. MSc thesis, Technical University of Denmark, Lyngby, Denmark.
  33. Zhang, X. X. & Rainey, P. B. ( 2007; ). The role of a P1-type ATPase from Pseudomonas fluorescens SBW25 in copper homeostasis and plant colonization. Mol Plant Microbe Interact 20, 581–588.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.025064-0
Loading
/content/journal/micro/10.1099/mic.0.025064-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error