Influence of extracellular polymeric substances on deposition and redeposition of to surfaces Free

Abstract

In this study, the role of extracellular polymeric substances (EPS) in the initial adhesion of EPS-producing SG81 and SG81R1, a non-EPS-producing strain, to substrata with different hydrophobicity was investigated. The release of EPS by SG81 was concurrent with a decrease in surface tension of a bacterial suspension from 70 to 45 mJ m that was absent for SG81R1. Both strains adhered faster and in higher numbers to a hydrophilic than to a hydrophobic substratum, but the initial deposition rates and numbers of adhering bacteria in a stationary-end point were highest for the non-EPS-producing strain SG81R1, regardless of substratum hydrophobicity. Both strains adhered less to substrata pre-coated with isolated EPS of strain SG81. Furthermore, it was investigated whether bacteria, detached by passing air-bubbles, had left behind ‘footprints’ with an influence on adhesion of newly redepositing bacteria. Redeposition on glass was highest for non-EPS-producing SG81R1 and decreased linearly with the number of times these cycles of detachment and deposition were repeated to become similar to the redeposition of SG81 after six cycles. This indicates that SG81 leaves the substratum surface nearly completely covered with EPS after detachment, while SG81R1 releases only minor amounts of surface active EPS, completely covering the substratum after repeated cycles of detachment and adhesion. Atomic force microscopy showed a thick and irregular EPS layer (up to 32 nm) after the first detachment cycle of EPS-producing strain SG81, whereas the putatively non-EPS-producing strain SG81R1 left a 9 nm thin layer after one cycle. X-ray photoelectron spectroscopy indicated that the bacterial footprints consisted of uronic acids, the prevalence of which increased with the number of detachment and deposition cycles.

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2002-04-01
2024-03-29
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References

  1. Allison D. G., Sutherland I. W. 1987; The role of exopolysaccharides in adhesion of freshwater bacteria. J Gen Microbiol 133:1319–1327
    [Google Scholar]
  2. Azeredo J., Oliveira R. 2000; The role of exopolymer in the attachment of Sphingomonas paucimobilis . Biofouling 16:59–67 [CrossRef]
    [Google Scholar]
  3. Azeredo J., Visser J., Oliveira R. 1999; Exopolymer in bacterial adhesion: interpretation in terms of DLVO and xDVLO theories. Colloids Surf B: Biointerfaces 14:141–148 [CrossRef]
    [Google Scholar]
  4. Beech I., Hanjagsit L., Kalaji M., Neal A. L., Zinkevich V. 1999; Chemical and structural characterization of exopolymer produced by Pseudomonas sp. NCIMB 2021 in continuous culture. Microbiology 145:1491–1497 [CrossRef]
    [Google Scholar]
  5. Bos R., Van der Mei H. C., Busscher H. J. 1995; A quantitative method to study co-adhesion of micro-organisms in a parallel plate flow chamber. II: Analysis of the kinetics of co-adhesion. J Microbiol Methods 23:169–182 [CrossRef]
    [Google Scholar]
  6. Boucher J. C., Schurr M. J., Deretic V. 2000; Dual regulation of mucoidity in Pseudomonas aeruginosa and sigma factor antagonism. Mol Microbiol 36:341–351 [CrossRef]
    [Google Scholar]
  7. Busscher H. J., Weerkamp A. H., Van der Mei H. C., Van Pelt A. W. J., De Jong H. P., Arends J. 1984; Measurements of the surface free energy of bacterial cell surfaces and its relevance for adhesion. Appl Environ Microbiol 48:980–983
    [Google Scholar]
  8. Busscher H. J., Cowan M. M., Van der Mei H. C. 1992; On the relative importance of specific and non-specific approaches to oral microbial adhesion. FEMS Microbiol Lett 88:199–210 [CrossRef]
    [Google Scholar]
  9. Busscher H. J., Bos R., Van der Mei H. C. 1995; Initial microbial adhesion is a determinant for the strength of biofilm adhesion. FEMS Microbiol Lett 128:229–234 [CrossRef]
    [Google Scholar]
  10. Busscher H. J., Van Hoogmoed C. G., Geertsema-Doornbusch G. I., Van der Kuijl-Booij M., Van der Mei H. C. 1997; Streptococcus thermophilus and its biosurfactants inhibit adhesion by Candida spp. on silicone rubber. Appl Environ Microbiol 63:3810–3817
    [Google Scholar]
  11. Cheng P., Li D., Boruvka L., Rotenberg Y., Neumann A. W. 1990; Automation of axisymmetric drop shape analysis for measurements of interfacial tensions and contact angles. Colloids Surf 43:151–167 [CrossRef]
    [Google Scholar]
  12. Christensen B. E., Characklis W. G. 1990; Physical properties of biofilms. In Biofilms pp 93–130 Edited by Characklis W. G., Marshall K. C. New York: Wiley;
    [Google Scholar]
  13. Cooksey K. E. 1992; Extracellular polymers in biofilms. In Biofilms: Science and Technology . pp 137–147 Edited by Melo L. F., Fletcher M., Bott T. R. Dordrecht: Kluwer;
  14. Cooksey K. E., Wigglesworth-Cooksey B. 1995; Adhesion of bacteria and diatoms to surfaces in the sea: a review. Aquat Microbiol Ecol 9:87–96 [CrossRef]
    [Google Scholar]
  15. Costerton J. W., Marrie C. B., Cheng K.-J. 1985; Phenomena of bacterial adhesion. In Bacterial Adhesion pp 3–43 Edited by Savage D. C., Fletcher M. New York: Plenum;
    [Google Scholar]
  16. Danielsson A., Norkrans B., Bjornsson A. 1977; On bacterial adhesion – the effect of certain enzymes on adhered cells of a marine Pseudomonas sp. Bot Mar 20:13–17
    [Google Scholar]
  17. DeFlaun M. F., Tanzer A. S., McAteer A. L., Marshall B., Levy S. B. 1990; Development of an adhesion assay and characterization of an adhesion-deficient mutant of Pseudomonas fluorescens . Appl Environ Microbiol 56:112–119
    [Google Scholar]
  18. Dũfrene Y. F., Rouxhet P. G. 1996; X-ray photoelectron spectroscopy analysis of the surface composition of Azospirillum brasilense in relation with growth conditions. Colloids Surf B: Biointerfaces 7:271–279 [CrossRef]
    [Google Scholar]
  19. Dũfrene Y. F., Boonaert J.-P., Rouxhet P. G. 1996a; Adhesion of Azospirillum brasilense : role of the proteins at the cell-support interface. Colloids Surf B: Biointerfaces 7:113–128 [CrossRef]
    [Google Scholar]
  20. Dũfrene Y. F., Vermeiren H., Vanderleyden J., Rouxhet P. G. 1996b; Direct evidence for the involvement of extracellular proteins in the adhesion of Azospirillum brasilense . Microbiology 142:855–865 [CrossRef]
    [Google Scholar]
  21. Escher A., Characklis W. G. 1990; Modeling the initial events in biofilm accumulation. In Biofilms pp 445–486 Edited by Characklis W. G., Marshall K. C. New York: Wiley;
    [Google Scholar]
  22. Flemming H.-C., Wingender J. 2001; Relevance of microbial polymeric substances (EPSs) – part I: structural and ecological aspects. Water Sci Technol 43:1–8
    [Google Scholar]
  23. Fletcher M., Floodgate G. D. 1973; An electron-microscopic demonstration of an acidic polysaccharide involved in the adhesion of a marine bacterium to solid surface. J Gen Microbiol 74:325–334 [CrossRef]
    [Google Scholar]
  24. Gómez-Suárez C., Noordmans J., Van der Mei H. C., Busscher H. J. 1999; Removal of colloidal particles from quartz collector surfaces as stimulated by the passage of air–liquid interfaces. Langmuir 15:5123–5127 [CrossRef]
    [Google Scholar]
  25. Gómez-Suárez C., Busscher H. J., Van der Mei H. C. 2001; Analysis of bacterial detachment from substratum surfaces by the passage of air–liquid interfaces. Appl Environ Microbiol 67:2531–2537 [CrossRef]
    [Google Scholar]
  26. Grobe S., Wingender J., Trüper H. G. 1995; Characterization of mucoid Pseudomonas aeruginosa strains isolated from technical water systems. J Appl Bacteriol 79:94–102 [CrossRef]
    [Google Scholar]
  27. Habash M. H., Van der Mei H. C., Reid G., Busscher H. J. 1997; Adhesion of Pseudomonas aeruginosa to silicone rubber in a parallel plate flow chamber in the absence and presence of nutrient broth. Microbiology 143:2569–2574 [CrossRef]
    [Google Scholar]
  28. Haynes C. A., Norde W. 1994; Globular proteins at solid/liquid interfaces. Colloids Surf B: Biointerfaces 2:517–566 [CrossRef]
    [Google Scholar]
  29. Heinemann C., Van Hylckama Vlieg J. E. T., Janssen D. B., Busscher H. J., Van der Mei H. C., Reid G. 2000; Purification and characterization of a surface-binding protein from Lactobacillus fermentum RC-14 that inhibits adhesion of Enterococcus faecalis 1131. FEMS Microbiol Lett 190:177–180 [CrossRef]
    [Google Scholar]
  30. Hiemenz P. C. 1977; Electrophoresis and other electrokinetic phenomena. In Principles of Colloid and Surface Chemistry pp 452–487 Edited by Lagowski J. J. New York: Marcel Dekker;
    [Google Scholar]
  31. Landa A. S., Van der Mei H. C., Van Rij G., Busscher H. J. 1998; Efficacy of ophthalmic solutions to detach adhering Pseudomonas aeruginosa from contact lenses. Cornea 17:293–300 [CrossRef]
    [Google Scholar]
  32. McGroarty J. A., Reid G. 1988; Detection of a lactobacillus substance that inhibits Escherichia coli . Can J Microbiol 34:974–978 [CrossRef]
    [Google Scholar]
  33. Neu T. R. 1992; Microbial ‘footprints’ and the general ability of micro-organisms to label interfaces. Can J Microbiol 38:1005–1008 [CrossRef]
    [Google Scholar]
  34. Neu T. R., Marshall K. C. 1990; Bacterial polymers: physico-chemical aspects of their interactions at interfaces. J Biomater Appl 5:107–133 [CrossRef]
    [Google Scholar]
  35. Neu T. R., Marshall K. C. 1991; Microbial footprints – a new approach to adhesive polymers. Biofouling 3:101–112 [CrossRef]
    [Google Scholar]
  36. Nielsen P. H., Jahn A., Palmgren R. 1997; Conceptual model for production and composition of exopolymers in biofilms. Water Sci Technol 36:11–19 [CrossRef]
    [Google Scholar]
  37. Omar A. S., Wecksser J., Mayer H. 1983; Different polysaccharides in the external layers (capsule and slime) of the cell envelope of Rhodopseudomonas capsulata Sp11. Arch Microbiol 136:291–296 [CrossRef]
    [Google Scholar]
  38. Pringle J. H., Fletcher M., Ellwood D. C. 1983; Selection of attachment mutants during the continuous culture of Pseudomonas fluorescens and relationship between attachment ability and surface composition. J Gen Microbiol 129:2557–2569
    [Google Scholar]
  39. Rouxhet P. G., Mozes N., Dengis P. B., Dũfrene Y. F., Gerin P. A., Genet M. J. 1994; Application of X-ray photoelectron spectroscopy to micro-organisms. Colloids Surf B: Biointerfaces 2:347–369 [CrossRef]
    [Google Scholar]
  40. Schmitt J., Flemming H.-C. 1999; Water binding in biofilms. Water Sci Technol 39:77–82
    [Google Scholar]
  41. Schmitt J., Fringeli U. P., Flemming H.-C. 1997; Structural and temporal behavior of biofilms investigated by FTIR-ATR spectroscopy. In Proceedings of the 11th Conference on Fourier Transform SpectroscopyAmerican Institute of Physics Press
    [Google Scholar]
  42. Strathmann J., Wingender J., Flemming H.-C. 2002; Application of fluorescently labelled lectins for the visualisation and biochemical characterisation of polysaccharides in biofilms of Pseudomonas aeruginosa . J Microbiol Methods in press
    [Google Scholar]
  43. Sutherland I. W. 1977; Bacterial exopolysaccharides, their nature and production. In Surface Carbohydrates of the Prokaryotic Cell pp 27–96 Edited by Sutherland I. W. London, New York, San Francisco: Academic Press;
    [Google Scholar]
  44. Sutherland I. W. 1997; Microbial biofilm exopolysaccharides – superglues or velcro? In Biofilms, Community Interactions and Control . pp 33–39 Edited by Wimpenny J. W., Handley P., Gilbert P., Lappin-Scott H. M., Jones M. Cardiff: Bioline;
  45. Urzi C., Lisi S., Criseo G., Pernice A. 1991; Adhesion and degradation of marble by Micrococcus strain isolated from it. Geomicrobiol J 9:81–90 [CrossRef]
    [Google Scholar]
  46. Vandevivere P., Kirchman D. L. 1993; Attachment stimulates exopolysaccharide synthesis by a bacterium. Appl Environ Microbiol 59:3280–3286
    [Google Scholar]
  47. Van Hoogmoed C. G., Van der Kuijl-Booij M., Van der Mei H. C., Busscher H. J. 2000; Inhibition of Streptococcus mutans NS adhesion to glass with and without a salivary conditioning film by biosurfactant-realizing Streptococcus mitis strains. Appl Environ Microbiol 66:659–663 [CrossRef]
    [Google Scholar]
  48. Van Loosdrecht M., Norde W., Lyklema L., Zehnder J. 1990; Hydrophobic and electrostatic parameters in bacterial adhesion. Aquat Sci 51:103–114
    [Google Scholar]
  49. Van Oss C. J., Gillman M. K. 1972; Phagocytosis as a surface phenomenon. I. Contact angles and phagocytosis of non-opsonized bacteria. J Reticuloendothel Soc 12:283–292
    [Google Scholar]
  50. Van Wagenen R. J., Andrade J. D. 1980; Flat plate streaming potential investigations: hydrodynamics and electrokinetic equivalency. J Colloid Interface Sci 76:305–314 [CrossRef]
    [Google Scholar]
  51. Velraeds M. M. C., Van de Belt-Gritter B., Van der Mei H. C., Reid G., Busscher H. J. 1998a; Interference in initial adhesion of uropathogenic bacteria and yeasts to silicone rubber by a Lactobacillus acidophilus biosurfactant. J Med Microbiol 47:1081–1085 [CrossRef]
    [Google Scholar]
  52. Velraeds M. M. C., Van der Mei H. C., Reid G., Busscher H. J. 1998b; Physicochemical and biochemical characterization of biosurfactants released by Lactobacillus strains. Colloids Surf B: Biointerfaces 8:51–61
    [Google Scholar]
  53. Williams V., Fletcher M. 1996; Pseudomonas fluorescens adhesion and transport through porous media are affected by lipopolysaccharides composition. Appl Environ Microbiol 62:100–104
    [Google Scholar]
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