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

Since many years, membrane biofouling has been described as the Achilles heel of membrane fouling. In the present study, an ecological assay was performed using model systems with increasing complexity: a monospecies assay using Pseudomonas aeruginosa or Escherichia coli separately, a duospecies assay using both microorganisms, and a multispecies assay using activated sludge with or without spiked P. aeruginosa. The microbial adhesion and biofilm formation were evaluated in terms of bacterial cell densities, species richness, and bacterial community composition on polyvinyldifluoride, polyethylene, and polysulfone membranes. The data show that biofouling formation was strongly influenced by the kind of microorganism, the interactions between the organisms, and the changes in environmental conditions whereas the membrane effect was less important. The findings obtained in this study suggest that more knowledge in species composition and microbial interactions is needed in order to understand the complex biofouling process. This is the first report describing the microbial interactions with a membrane during the biofouling development.

[1]  H. De Wever,et al.  Diverse and distinct bacterial communities induced biofilm fouling in membrane bioreactors operated under different conditions. , 2008, Environmental science & technology.

[2]  K. Mathee,et al.  Comparative transcriptome analyses of Pseudomonas aeruginosa , 2009, Human Genomics.

[3]  Matthias Wessling,et al.  Influence of membrane properties on fouling in submerged membrane bioreactors , 2010 .

[4]  Jin Li,et al.  Role of Pseudomonas aeruginosa biofilm in the initial adhesion, growth and detachment of Escherichia coli in porous media. , 2008, Environmental science & technology.

[5]  Daniel B. Oerther,et al.  Identifying pioneer bacterial species responsible for biofouling membrane bioreactors. , 2006, Environmental microbiology.

[6]  F. Ollevier,et al.  Receptor‐mediated uptake of Legionella pneumophila by Acanthamoeba castellanii and Naegleria lovaniensis , 2007, Journal of applied microbiology.

[7]  H. Ridgway,et al.  Biofouling potentials of microporous polysulfone membranes containing a sulfonated polyether-ethersulfone/polyethersulfone block copolymer: correlation of membrane surface properties with bacterial attachment , 1999 .

[8]  J. Garnett,et al.  Interactions in Bacterial Biofilm Development: A Structural Perspective , 2012, Current protein & peptide science.

[9]  Pieter Vandezande,et al.  Solvent resistant nanofiltration: separating on a molecular level. , 2008, Chemical Society reviews.

[10]  Noboru Takiguchi,et al.  Pseudomonas aeruginosa as a model microorganism for investigation of chemotactic behaviors in ecosystem. , 2008, Journal of bioscience and bioengineering.

[11]  Anthony G. Fane,et al.  Adhesion of waste water bacteria to reverse osmosis membranes , 1998 .

[12]  H. Flemming,et al.  Biofouling in water systems – cases, causes and countermeasures , 2002, Applied Microbiology and Biotechnology.

[13]  Byoung-In Sang,et al.  Correlation between microbial community structure and biofouling in a laboratory scale membrane bioreactor with synthetic wastewater , 2012 .

[14]  Guillaume Delaplace,et al.  Cell adhesion and related fouling mechanism on a tubular ceramic microfiltration membrane using Bacillus cereus spores , 2011 .

[15]  C. M. Brown,et al.  Surface-associated growth. , 1982, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[16]  K. Jarvis,et al.  Longus pilus of enterotoxigenic Escherichia coli and its relatedness to other type-4 pili--a minireview. , 1997, Gene.

[17]  P. Nielsen,et al.  Microbial Ecology of Activated Sludge , 2010 .

[18]  Jan Lepš,et al.  Multivariate Analysis of Ecological Data using CANOCO , 2003 .

[19]  M. Bilad,et al.  Treatment of molasses wastewater in a membrane bioreactor: Influence of membrane pore size , 2010 .

[20]  M. Madigan,et al.  Brock Biology of Microorganisms , 1996 .

[21]  O. Nybroe,et al.  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. , 2001, Journal of microbiological methods.

[22]  L. Meester,et al.  Bacterial community analysis of activated sludge: an evaluation of four commonly used DNA extraction methods , 2010, Applied Microbiology and Biotechnology.

[23]  Seoktae Kang,et al.  Effect of Membrane Surface Properties During the Fast Evaluation of Cell Attachment , 2006 .

[24]  Ehud Banin,et al.  Multi-species biofilms: living with friendly neighbors. , 2012, FEMS microbiology reviews.

[25]  Daniel B. Oerther,et al.  Effect of activated sludge properties and membrane operation conditions on fouling characteristics in membrane bioreactors. , 2006, Chemosphere.

[26]  B. M. Veeregowda,et al.  Biofilms: A survival strategy of bacteria , 2003 .

[27]  Y. Watanabe,et al.  Membrane biofouling in pilot-scale membrane bioreactors (MBRs) treating municipal wastewater: impact of biofilm formation. , 2007, Environmental science & technology.

[28]  Blaise R. Boles,et al.  Self-generated diversity produces "insurance effects" in biofilm communities. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[29]  I. Vankelecom,et al.  Analysis of the microbial community structure in a membrane bioreactor during initial stages of filtration , 2012, Biofouling.

[30]  W. Jianlong,et al.  Biodegradation characteristics of quinoline by Pseudomonas putida. , 2010, Bioresource technology.

[31]  Simon Judd,et al.  The MBR Book: Principles and Applications of Membrane Bioreactors for Water and Wastewater Treatment , 2006 .

[32]  Yang Li,et al.  Surface hydrophilization of microporous polypropylene membrane by grafting zwitterionic polymer for anti-biofouling , 2010 .

[33]  A. Fane,et al.  Microbial behaviors involved in cake fouling in membrane bioreactors under different solids retention times. , 2011, Bioresource technology.

[34]  J. Ghigo,et al.  Multi-species biofilms: how to avoid unfriendly neighbors. , 2012, FEMS microbiology reviews.

[35]  C. Bowman,et al.  Effects of ultrafiltration membrane surface properties on Pseudomonas aeruginosa biofilm initiation for the purpose of reducing biofouling , 2001 .

[36]  S. White,et al.  RNAi-mediated chromatin silencing in fission yeast. , 2008, Current topics in microbiology and immunology.

[37]  W. Dunne,et al.  Bacterial Adhesion: Seen Any Good Biofilms Lately? , 2002, Clinical Microbiology Reviews.

[38]  M. Schembri,et al.  Global gene expression in Escherichia coli biofilms , 2003, Molecular microbiology.

[39]  Kenneth N Timmis,et al.  Pseudomonas putida: a cosmopolitan opportunist par excellence. , 2002, Environmental microbiology.

[40]  L. Samaranayake,et al.  Unraveling the resistance of microbial biofilms: Has proteomics been helpful? , 2012, Proteomics.

[41]  N. Ren,et al.  Linking microbial community structure to membrane biofouling associated with varying dissolved oxygen concentrations. , 2011, Bioresource technology.

[42]  J. Trevors,et al.  Application of real-time quantitative PCR for the detection of selected bacterial pathogens during municipal wastewater treatment. , 2007, The Science of the total environment.

[43]  J. Ghigo,et al.  Escherichia coli biofilms. , 2008, Current topics in microbiology and immunology.

[44]  C. Sorlini,et al.  Comparison of Different Primer Sets for Use in Automated Ribosomal Intergenic Spacer Analysis of Complex Bacterial Communities , 2004, Applied and Environmental Microbiology.

[45]  E. Golovlev The Mechanism of Formation of Pseudomonas aeruginosa Biofilm, a Type of Structured Population , 2002, Microbiology.

[46]  M. Banks,et al.  Bacterial species dominance within a binary culture biofilm , 1991, Applied and environmental microbiology.

[47]  D. Allison,et al.  Immigration and emigration of Burkholderia cepacia and Pseudomonas aeruginosa between and within mixed biofilm communities , 2004, Journal of applied microbiology.

[48]  A. Aertsen,et al.  Bacterial interactions in biofilms , 2009, Critical reviews in microbiology.

[49]  Xiaojiao Wang,et al.  The effect of organic loading on bacterial community composition of membrane biofilms in a submerged polyvinyl chloride membrane bioreactor. , 2010, Bioresource technology.

[50]  E. Delong,et al.  Quantitative Analysis of Small-Subunit rRNA Genes in Mixed Microbial Populations via 5′-Nuclease Assays , 2000, Applied and Environmental Microbiology.

[51]  K. Fukushi,et al.  Bacterial Community Structure on Membrane Surface and Characteristics of Strains Isolated from Membrane Surface in Submerged Membrane Bioreactor , 2006 .

[52]  R. Donlan,et al.  Biofilms: Microbial Life on Surfaces , 2002, Emerging infectious diseases.

[53]  M R Bilad,et al.  Harvesting microalgal biomass using submerged microfiltration membranes. , 2012, Bioresource technology.

[54]  A. Aertsen,et al.  Role of Quorum Sensing and Antimicrobial Component Production by Serratia plymuthica in Formation of Biofilms, Including Mixed Biofilms with Escherichia coli , 2006, Applied and Environmental Microbiology.

[55]  Jiti Zhou,et al.  Factors affecting the membrane performance in submerged membrane bioreactors , 2006 .

[56]  C. Dosoretz,et al.  Effect of Permeate Drag Force on the Development of a Biofouling Layer in a Pressure-Driven Membrane Separation System , 2008, Applied and Environmental Microbiology.

[57]  T. Wood,et al.  Indole Production Promotes Escherichia coli Mixed-Culture Growth with Pseudomonas aeruginosa by Inhibiting Quorum Signaling , 2011, Applied and Environmental Microbiology.

[58]  M. Mulder Preparation of Synthetic Membranes , 1996 .

[59]  T. Wood,et al.  Motility influences biofilm architecture in Escherichia coli , 2006, Applied Microbiology and Biotechnology.

[60]  Hans-Curt Flemming,et al.  Biofouling—the Achilles heel of membrane processes☆ , 1997 .

[61]  M. Bilad,et al.  Development and validation of a high-throughput membrane bioreactor (HT-MBR) , 2011 .