About this Journal Submit a Manuscript Table of Contents
BioMed Research International
Volume 2013 (2013), Article ID 470867, 12 pages
http://dx.doi.org/10.1155/2013/470867
Research Article

Microbial Adhesion and Biofilm Formation on Microfiltration Membranes: A Detailed Characterization Using Model Organisms with Increasing Complexity

1Centre for Surface Chemistry and Catalysis, KU Leuven, Kasteelpark Arenberg 23, P.O. Box 2461, 3001 Heverlee, Belgium
2Laboratory of Aquatic Ecology and Evolutionary Biology, KU Leuven, Charles Deberiotstraat 32, 3000 Leuven, Belgium

Received 2 April 2013; Accepted 24 June 2013

Academic Editor: Dimitrios Karpouzas

Copyright © 2013 L. Vanysacker et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. J. A. Garnett and S. Matthews, “Interactions in bacterial biofilm development: a structural perspective,” Current Protein and Peptide Science, vol. 13, no. 8, pp. 739–755, 2012. View at Publisher · View at Google Scholar
  2. H.-C. Flemming, “Biofouling in water systems—cases, causes and countermeasures,” Applied Microbiology and Biotechnology, vol. 59, no. 6, pp. 629–640, 2002. View at Publisher · View at Google Scholar · View at Scopus
  3. R. M. Donlan, “Biofilms: microbial life on surfaces,” Emerging Infectious Diseases, vol. 8, no. 9, pp. 881–890, 2002. View at Scopus
  4. H.-C. Flemming, G. Schaule, T. Griebe, J. Schmitt, and A. Tamachkiarowa, “Biofouling—the Achilles heel of membrane processes,” Desalination, vol. 113, no. 2-3, pp. 215–225, 1997. View at Scopus
  5. P. Blanpain-Avet, C. Faille, G. Delaplace, and T. Bénézech, “Cell adhesion and related fouling mechanism on a tubular ceramic microfiltration membrane using Bacillus cereus spores,” Journal of Membrane Science, vol. 385-386, no. 1, pp. 200–216, 2011. View at Publisher · View at Google Scholar · View at Scopus
  6. C. J. Seneviratne, Y. Wang, L. Jin, S. S. W. Wong, T. D. K. Herath, and L. P. Samaranayake, “Unraveling the resistance of microbial biofilms: has proteomics been helpful?” Proteomics, vol. 12, no. 4-5, pp. 651–665, 2012. View at Publisher · View at Google Scholar · View at Scopus
  7. B. Prakash, B. M. Veeregowda, and G. Krishnappa, “Biofilms: a survival strategy of bacteria,” Current Science, vol. 85, no. 9, pp. 1299–1307, 2003. View at Scopus
  8. S. Elias and E. Banin, “Multi-species biofilms: living with friendly neighbors,” FEMS Microbiology Reviews, vol. 36, pp. 990–1004, 2012. View at Publisher · View at Google Scholar · View at Scopus
  9. O. Rendueles and J.-M. Ghigo, “Multi-species biofilms: how to avoid unfriendly neighbors,” FEMS Microbiology Reviews, vol. 36, pp. 972–989, 2012. View at Publisher · View at Google Scholar · View at Scopus
  10. S. Judd, The MBR Book: Principles and Applications of Membrane Bioreactors For Water and wasteWater Treatment, Elsevier Science, Oxford, UK, 2006.
  11. K. E. Shannon, D.-Y. Lee, J. T. Trevors, and L. A. Beaudette, “Application of real-time quantitative PCR for the detection of selected bacterial pathogens during municipal wastewater treatment,” Science of the Total Environment, vol. 382, no. 1, pp. 121–129, 2007. View at Publisher · View at Google Scholar · View at Scopus
  12. M. Cardinale, L. Brusetti, P. Quatrini et al., “Comparison of different primer sets for use in automated ribosomal intergenic spacer analysis of complex bacterial communities,” Applied and Environmental Microbiology, vol. 70, no. 10, pp. 6147–6156, 2004. View at Publisher · View at Google Scholar · View at Scopus
  13. M. T. Suzuki, L. T. Taylor, and E. F. DeLong, “Quantitative analysis of small-subunit rRNA genes in mixed microbial populations via 5'-nuclease assays,” Applied and Environmental Microbiology, vol. 66, no. 11, pp. 4605–4614, 2000. View at Publisher · View at Google Scholar · View at Scopus
  14. K. N. Timmis, “Pseudomonas putida: a cosmopolitan opportunist par excellence,” Environmental Microbiology, vol. 4, no. 12, pp. 779–781, 2002. View at Publisher · View at Google Scholar · View at Scopus
  15. Q. Lin and W. Jianlong, “Biodegradation characteristics of quinoline by Pseudomonas putida,” Bioresource Technology, vol. 101, no. 19, pp. 7683–7686, 2010. View at Publisher · View at Google Scholar · View at Scopus
  16. C. Beloin, A. Roux, and J.-M. Ghigo, “Escherichia coli biofilms,” Current Topics in Microbiology and Immunology, vol. 322, pp. 249–289, 2008. View at Publisher · View at Google Scholar · View at Scopus
  17. E. L. Golovlev, “The mechanism of formation of Pseudomonas aeruginosa biofilm, a type of structured population,” Microbiology, vol. 71, no. 3, pp. 249–254, 2002. View at Publisher · View at Google Scholar · View at Scopus
  18. J. Kato, H.-E. Kim, N. Takiguchi, A. Kuroda, and H. Ohtake, “Pseudomonas aeruginosa as a model microorganism for investigation of chemotactic behaviors in ecosystem,” Journal of Bioscience and Bioengineering, vol. 106, no. 1, pp. 1–7, 2008. View at Publisher · View at Google Scholar · View at Scopus
  19. B. Koch, L. E. Jensen, and O. Nybroe, “A panel of Tn7-based vectors for insertion of the gfp marker gene or for delivery of cloned DNA into Gram-negative bacteria at a neutral chromosomal site,” Journal of Microbiological Methods, vol. 45, no. 3, pp. 187–195, 2001. View at Publisher · View at Google Scholar · View at Scopus
  20. P. Declerck, J. Behets, B. De Keersmaecker, and F. Ollevier, “Receptor-mediated uptake of Legionella pneumophila by Acanthamoeba castellanii and Naegleria lovaniensis,” Journal of Applied Microbiology, vol. 103, no. 6, pp. 2697–2703, 2007. View at Publisher · View at Google Scholar · View at Scopus
  21. A. Piasecka, C. Souffreau, K. Vandepitte et al., “Analysis of the microbial community structure in a membrane bioreactor during initial stages of filtration,” Biofouling, vol. 28, no. 2, pp. 225–238, 2012. View at Publisher · View at Google Scholar · View at Scopus
  22. P. Vandezande, L. E. M. Gevers, and I. F. J. Vankelecom, “Solvent resistant nanofiltration: separating on a molecular level,” Chemical Society Reviews, vol. 37, no. 2, pp. 365–405, 2008. View at Publisher · View at Google Scholar · View at Scopus
  23. M. Mulder, “Preparation of synthetic membranes,” in Basic Principles of Membrane Technology, M. Mulder, Ed., pp. 71–154, Kluwer Academic Publishers, Dordrecht, The Netherlands, 1996.
  24. M. R. Bilad, P. Declerck, A. Piasecka, L. Vanysacker, X. Yan, and I. F. J. Vankelecom, “Treatment of molasses wastewater in a membrane bioreactor: Influence of membrane pore size,” Separation and Purification Technology, vol. 78, no. 2, pp. 105–112, 2011. View at Publisher · View at Google Scholar · View at Scopus
  25. P. van der Marel, A. Zwijnenburg, A. Kemperman, M. Wessling, H. Temmink, and W. van der Meer, “Influence of membrane properties on fouling in submerged membrane bioreactors,” Journal of Membrane Science, vol. 348, no. 1-2, pp. 66–74, 2010. View at Publisher · View at Google Scholar · View at Scopus
  26. M. R. Bilad, D. Vandamme, I. Foubert, K. Muylaert, and I. F. J. Vankelecom, “Harvesting microalgal biomass using submerged microfiltration membranes,” Bioresource Technology, vol. 111, pp. 343–352, 2012. View at Publisher · View at Google Scholar · View at Scopus
  27. S. B. S. Ghayeni, P. J. Beatson, R. P. Schneider, and A. G. Fane, “Adhesion of waste water bacteria to reverse osmosis membranes,” Journal of Membrane Science, vol. 138, no. 1, pp. 29–42, 1998. View at Publisher · View at Google Scholar · View at Scopus
  28. T. Knoell, J. Safarik, T. Cormack, R. Riley, S. W. Lin, and H. Ridgway, “Biofouling potentials of microporous polysulfone membranes containing a sulfonated polyether-ethersulfone/polyethersulfone block copolymer: correlation of membrane surface properties with bacterial attachment,” Journal of Membrane Science, vol. 157, no. 1, pp. 117–138, 1999. View at Publisher · View at Google Scholar · View at Scopus
  29. M. Pasmore, P. Todd, S. Smith et al., “Effects of ultrafiltration membrane surface properties on Pseudomonas aeruginosa biofilm initiation for the purpose of reducing biofouling,” Journal of Membrane Science, vol. 194, no. 1, pp. 15–32, 2001. View at Publisher · View at Google Scholar · View at Scopus
  30. L. Eshed, S. Yaron, and C. G. Dosoretz, “Effect of permeate drag force on the development of a biofouling layer in a pressure-driven membrane separation system,” Applied and Environmental Microbiology, vol. 74, no. 23, pp. 7338–7347, 2008. View at Publisher · View at Google Scholar · View at Scopus
  31. D. C. Ellwood, C. W. Keevil, P. D. Marsh, C. M. Brown, and J. N. Wardell, “Surface-associated growth,” Philosophical Transactions of the Royal Society B, vol. 297, no. 1088, pp. 517–532, 1982. View at Scopus
  32. M. R. Bilad, P. Declerck, A. Piasecka, L. Vanysacker, X. Yan, and I. F. J. Vankelecom, “Development and validation of a high-throughput membrane bioreactor (HT-MBR),” Journal of Membrane Science, vol. 379, no. 1-2, pp. 146–153, 2011. View at Publisher · View at Google Scholar · View at Scopus
  33. M. Hamilton, The Biofilm Laboratory: Step-By-Step Protocols for Experimental Design, Analysis, and Data Interpretation, Cytergy, Bozeman, Mont, USA, 2003.
  34. L. Vanysacker, S. A. J. Declerck, B. Hellemans, L. De Meester, I. Vankelecom, and P. Declerck, “Bacterial community analysis of activated sludge: an evaluation of four commonly used DNA extraction methods,” Applied Microbiology and Biotechnology, vol. 88, no. 1, pp. 299–307, 2010. View at Publisher · View at Google Scholar · View at Scopus
  35. J. Lepš and P. Šmilauer, Multivariate Analysis of Ecological Data Using CANOCO, Cambridge University Press, Cambridge, Mass, USA, 2003.
  36. W. M. Dunne Jr., “Bacterial adhesion: seen any good biofilms lately?” Clinical Microbiology Reviews, vol. 15, no. 2, pp. 155–166, 2002. View at Publisher · View at Google Scholar · View at Scopus
  37. S. Kang, E. M. V. Hoek, H. Choi, and H. Shin, “Effect of membrane surface properties during the fast evaluation of cell attachment,” Separation Science and Technology, vol. 41, no. 7, pp. 1475–1487, 2006. View at Publisher · View at Google Scholar · View at Scopus
  38. Y.-F. Yang, Y. Li, Q.-L. Li, L.-S. Wan, and Z.-K. Xu, “Surface hydrophilization of microporous polypropylene membrane by grafting zwitterionic polymer for anti-biofouling,” Journal of Membrane Science, vol. 362, no. 1-2, pp. 255–264, 2010. View at Publisher · View at Google Scholar · View at Scopus
  39. P. Moons, C. W. Michiels, and A. Aertsen, “Bacterial interactions in biofilms bacterial interactions in biofilms,” Critical Reviews in Microbiology, vol. 35, no. 3, pp. 157–168, 2009. View at Publisher · View at Google Scholar · View at Scopus
  40. M. K. Banks and J. D. Bryers, “Bacterial species dominance within a binary culture biofilm,” Applied and Environmental Microbiology, vol. 57, no. 7, pp. 1974–1979, 1991. View at Scopus
  41. M. T. Madigan, M. T. Madigan, and T. D. Brock, Brock Biology of Microorganisms, Pearson, San Francisco, Calif, USA, 2009.
  42. T. K. Wood, A. F. González Barrios, M. Herzberg, and J. Lee, “Motility influences biofilm architecture in Escherichia coli,” Applied Microbiology and Biotechnology, vol. 72, no. 2, pp. 361–367, 2006. View at Publisher · View at Google Scholar · View at Scopus
  43. J. A. Girón, O. G. Gómez-Duarte, K. G. Jarvis, and J. B. Kaper, “Longus pilus of enterotoxigenic Escherichia coli and its relatedness to other type-4 pili—a minireview,” Gene, vol. 192, no. 1, pp. 39–43, 1997. View at Publisher · View at Google Scholar · View at Scopus
  44. M. A. Schembri, K. Kjærgaard, and P. Klemm, “Global gene expression in Escherichia coli biofilms,” Molecular Microbiology, vol. 48, no. 1, pp. 253–267, 2003. View at Publisher · View at Google Scholar · View at Scopus
  45. Y. Liu and J. Li, “Role of Pseudomonas aeruginosa biofilm in the initial adhesion, growth and detachment of Escherichia coli in porous media,” Environmental Science and Technology, vol. 42, no. 2, pp. 443–449, 2008. View at Publisher · View at Google Scholar · View at Scopus
  46. A. G. Al-Bakri, P. Gilbert, and D. G. Allison, “Immigration and emigration of Burkholderia cepacia and Pseudomonas aeruginosa between and within mixed biofilm communities,” Journal of Applied Microbiology, vol. 96, no. 3, pp. 455–463, 2004. View at Publisher · View at Google Scholar · View at Scopus
  47. P. Moons, R. Van Houdt, A. Aertsen, K. Vanoirbeek, Y. Engelborghs, and C. W. Michiels, “Role of quorum sensing and antimicrobial component production by Serratia plymuthica in formation of biofilms, including mixed biofilms with Escherichia coli,” Applied and Environmental Microbiology, vol. 72, no. 11, pp. 7294–7300, 2006. View at Publisher · View at Google Scholar · View at Scopus
  48. W. Chu, T. R. Zere, M. M. Weber et al., “Indole production promotes Escherichia coli mixed-culture growth with Pseudomonas aeruginosa by inhibiting quorum signaling,” Applied and Environmental Microbiology, vol. 78, no. 2, pp. 411–419, 2012. View at Publisher · View at Google Scholar · View at Scopus
  49. R. J. Seviour, Microbial Ecology of Activated Sludge, IWA, London, UK, 2010.
  50. D.-W. Gao, Y. Fu, Y. Tao et al., “Linking microbial community structure to membrane biofouling associated with varying dissolved oxygen concentrations,” Bioresource Technology, vol. 102, no. 10, pp. 5626–5633, 2011. View at Publisher · View at Google Scholar · View at Scopus
  51. L.-N. Huang, H. De Wever, and L. Diels, “Diverse and distinct bacterial communities induced biofilm fouling in membrane bioreactors operated under different conditions,” Environmental Science and Technology, vol. 42, no. 22, pp. 8360–8366, 2008. View at Publisher · View at Google Scholar · View at Scopus
  52. P. Jinhua, K. Fukushi, and K. Yamamoto, “Bacterial community structure on membrane surface and characteristics of strains isolated from membrane surface in submerged membrane bioreactor,” Separation Science and Technology, vol. 41, no. 7, pp. 1527–1549, 2006. View at Publisher · View at Google Scholar · View at Scopus
  53. S. Lim, S. Kim, K.-M. Yeon, B.-I. Sang, J. Chun, and C.-H. Lee, “Correlation between microbial community structure and biofouling in a laboratory scale membrane bioreactor with synthetic wastewater,” Desalination, vol. 287, pp. 209–215, 2012. View at Publisher · View at Google Scholar · View at Scopus
  54. K. Zhang, H. Choi, D. D. Dionysiou, G. A. Sorial, and D. B. Oerther, “Identifying pioneer bacterial species responsible for biofouling membrane bioreactors,” Environmental Microbiology, vol. 8, no. 3, pp. 433–440, 2006. View at Publisher · View at Google Scholar · View at Scopus
  55. Y. Miura, Y. Watanabe, and S. Okabe, “Membrane biofouling in pilot-scale membrane bioreactors (MBRs) treating municipal wastewater: impact of biofilm formation,” Environmental Science and Technology, vol. 41, no. 2, pp. 632–638, 2007. View at Publisher · View at Google Scholar · View at Scopus
  56. B. Wu, S. Yi, and A. G. Fane, “Microbial behaviors involved in cake fouling in membrane bioreactors under different solids retention times,” Bioresource Technology, vol. 102, no. 3, pp. 2511–2516, 2011. View at Publisher · View at Google Scholar · View at Scopus
  57. S. Xia, J. Li, S. He et al., “The effect of organic loading on bacterial community composition of membrane biofilms in a submerged polyvinyl chloride membrane bioreactor,” Bioresource Technology, vol. 101, no. 17, pp. 6601–6609, 2010. View at Publisher · View at Google Scholar · View at Scopus
  58. J. Zhang, H. C. Chua, J. Zhou, and A. G. Fane, “Factors affecting the membrane performance in submerged membrane bioreactors,” Journal of Membrane Science, vol. 284, no. 1-2, pp. 54–66, 2006. View at Publisher · View at Google Scholar · View at Scopus
  59. H. Choi, K. Zhang, D. D. Dionysiou, D. B. Oerther, and G. A. Sorial, “Effect of activated sludge properties and membrane operation conditions on fouling characteristics in membrane bioreactors,” Chemosphere, vol. 63, no. 10, pp. 1699–1708, 2006. View at Publisher · View at Google Scholar · View at Scopus
  60. B. R. Boles, M. Thoendel, and P. K. Singh, “Self-generated diversity produces “insurance effects” in biofilm communities,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 47, pp. 16630–16635, 2004. View at Publisher · View at Google Scholar · View at Scopus
  61. D. Balasubramanian and K. Mathee, “Comparative transcriptome analyses of Pseudomonas aeruginosa,” Human Genomics, vol. 3, no. 4, pp. 349–361, 2009. View at Scopus