Biological control of microbial attachment: a promising alternative for mitigating membrane biofouling

Microbial attachment to a solid surface is a universal phenomenon occurring in both natural and engineering systems and is responsible for various types of biofouling. Membrane systems have been widely applied in drinking water production, wastewater reuse, and seawater desalination. However, membrane biofouling is the bottleneck that limits the development of membrane systems. In this review, some biological control strategies of microbial attachment which would have great potential in alleviating membrane biofouling are discussed, including inhibition of quorum sensing system, nitric oxide-induced biofilm dispersal, enzymatic disruption of extracellular polysaccharides, proteins, and DNA, inhibition of microbial attachment by energy uncoupling, use of cell wall hydrolases, and disruption of biofilm by bacteriophage. It appears that biological control of microbial attachment would be a novel and promising alternative for mitigating membrane biofouling and would be a new research niche that deserves further study.

[1]  D. E. Caldwell,et al.  Lytic infection of Escherichia coli biofilms by bacteriophage T4. , 1995, Canadian journal of microbiology.

[2]  W. Waites,et al.  Effect of Flagella on Initial Attachment of Listeria monocytogenes to Stainless Steel , 2000, Applied and Environmental Microbiology.

[3]  Paola Appendini,et al.  Immobilization of lysozyme on food contact polymers as potential antimicrobial films , 1997 .

[4]  D. Boone,et al.  Isolation and characterization of disaggregatase from Methanosarcina mazei LYC , 1990, Applied and environmental microbiology.

[5]  D. Fine,et al.  Enzymatic Detachment of Staphylococcus epidermidis Biofilms , 2004, Antimicrobial Agents and Chemotherapy.

[6]  F. Riera,et al.  Enzymatic cleaning of inorganic ultrafiltration membranes used for whey protein fractionation , 2003 .

[7]  James J. Collins,et al.  Dispersing biofilms with engineered enzymatic bacteriophage , 2007, Proceedings of the National Academy of Sciences.

[8]  Peng George Wang,et al.  NO and NO Donors , 2005 .

[9]  Lian-Hui Zhang Quorum quenching and proactive host defense. , 2003, Trends in plant science.

[10]  J. Theron,et al.  DNA as an Adhesin: Bacillus cereus Requires Extracellular DNA To Form Biofilms , 2009, Applied and Environmental Microbiology.

[11]  R. Donlan,et al.  Using Bacteriophages To Reduce Formation of Catheter-Associated Biofilms by Staphylococcus epidermidis , 2006, Antimicrobial Agents and Chemotherapy.

[12]  B. Bassler,et al.  Structural identification of a bacterial quorum-sensing signal containing boron , 2002, Nature.

[13]  R. Bing,et al.  Nitric oxide donors. , 2000, Proceedings of the Society for Experimental Biology and Medicine. Society for Experimental Biology and Medicine.

[14]  Roseanne M Ford,et al.  Characterizing the adhesion of motile and nonmotile Escherichia coli to a glass surface using a parallel-plate flow chamber. , 2002, Biotechnology and bioengineering.

[15]  M. Gilles-Gonzalez,et al.  Dos, a heme-binding PAS protein from Escherichia coli, is a direct oxygen sensor. , 2000, Biochemistry.

[16]  Kathleen Marchal,et al.  Brominated Furanones Inhibit Biofilm Formation by Salmonella enterica Serovar Typhimurium , 2008, Applied and Environmental Microbiology.

[17]  L. Eberl,et al.  Influence of Polyphenols on Bacterial Biofilm Formation and Quorum-sensing , 2003, Zeitschrift fur Naturforschung. C, Journal of biosciences.

[18]  J. Russell The Energy Spilling Reactions of Bacteria and Other Organisms , 2007, Journal of Molecular Microbiology and Biotechnology.

[19]  R. Kolter,et al.  Flagellar Motility Is Critical for Listeria monocytogenes Biofilm Formation , 2007, Journal of bacteriology.

[20]  Menachem Elimelech,et al.  Role of extracellular polymeric substances (EPS) in biofouling of reverse osmosis membranes. , 2009, Environmental science & technology.

[21]  J. V. D. Graaf,et al.  Enzymatic cleaning in ultrafiltration of wastewater treatment plant effluent , 2005 .

[22]  Yu Liu,et al.  Involvement of ATP and autoinducer‐2 in aerobic granulation , 2010, Biotechnology and bioengineering.

[23]  G. Bitton,et al.  INT–dehydrogenase test for activated sludge process control , 1986, Biotechnology and bioengineering.

[24]  L. Poole-Warren,et al.  The control of Staphylococcus epidermidis biofilm formation and in vivo infection rates by covalently bound furanones. , 2004, Biomaterials.

[25]  L. Jolliffe,et al.  The energized membrane and cellular autolysis in Bacillus subtilis , 1981, Cell.

[26]  Mark H Schoenfisch,et al.  Reduced bacterial adhesion to fibrinogen-coated substrates via nitric oxide release. , 2008, Biomaterials.

[27]  J. Mattick,et al.  Extracellular DNA required for bacterial biofilm formation. , 2002, Science.

[28]  Joo-Hwa Tay,et al.  The effects of extracellular polymeric substances on the formation and stability of biogranules , 2004, Applied Microbiology and Biotechnology.

[29]  Jeremy S. Webb,et al.  Nitric oxide‐mediated dispersal in single‐ and multi‐species biofilms of clinically and industrially relevant microorganisms , 2009, Microbial biotechnology.

[30]  J. Wagenaar,et al.  Bacteriophage Therapy To Reduce Salmonella Colonization of Broiler Chickens , 2007, Applied and Environmental Microbiology.

[31]  Melanie Loiselle,et al.  The Use of Cellulase in Inhibiting Biofilm Formation from Organisms Commonly Found on Medical Implants , 2003, Biofouling.

[32]  J. Kato,et al.  Inhibition of Quorum Sensing in Serratia marcescens AS-1 by Synthetic Analogs of N-Acylhomoserine Lactone , 2007, Applied and Environmental Microbiology.

[33]  V. Paul,et al.  Mini-review: quorum sensing in the marine environment and its relationship to biofouling , 2009, Biofouling.

[34]  Christian Melander,et al.  Controlling Bacterial Biofilms , 2009 .

[35]  Robert Armon,et al.  Inhibition of biofilm formation on UF membrane by use of specific bacteriophages , 2009 .

[36]  B. Brüne,et al.  Superoxide and nitric oxide–participation in cell communication , 2002, Cell Death and Differentiation.

[37]  F. Götz,et al.  Inhibition of Staphylococcal Biofilm Formation by Nitrite , 2007, Journal of bacteriology.

[38]  N. Bhosle,et al.  Effects of DNP on the cell surface properties of marine bacteria and its implication for adhesion to surfaces , 2007, Biofouling.

[39]  L. Hancock,et al.  Regulation of Autolysis-Dependent Extracellular DNA Release by Enterococcus faecalis Extracellular Proteases Influences Biofilm Development , 2008, Journal of bacteriology.

[40]  S. Kjelleberg,et al.  Inhibitory Effects of Secondary Metabolites from the Red Alga Delisea pulchra on Swarming Motility of Proteus mirabilis , 1996, Applied and environmental microbiology.

[41]  T. Standiford,et al.  Nitric oxide is required for effective innate immunity against Klebsiella pneumoniae , 1997, Infection and immunity.

[42]  B. Schink,et al.  Cell aggregation of Pseudomonas aeruginosa strain PAO1 as an energy-dependent stress response during growth with sodium dodecyl sulfate , 2006, Archives of Microbiology.

[43]  J. Costerton,et al.  Prevention of Staphylococcal Biofilm-associated Infections by the Quorum Sensing Inhibitor RIP , 2005, Clinical orthopaedics and related research.

[44]  A. Majerník,et al.  Biochemical characteristics of a mutant of the methanoarchaeonMethanothermobacter thermautotrophicus resistant to the protonophoric uncoupler TCS , 2008, Folia Microbiologica.

[45]  Lian-Hui Zhang,et al.  Quorum sensing and quorum-quenching enzymes. , 2005, Journal of microbiology.

[46]  D. Hassett,et al.  Involvement of Nitric Oxide in Biofilm Dispersal of Pseudomonas aeruginosa , 2006, Journal of bacteriology.

[47]  W. Zumft The biological role of nitric oxide in bacteria , 2004, Archives of Microbiology.

[48]  K. Lewis,et al.  Bacterial resistance to uncouplers , 1994, Journal of bioenergetics and biomembranes.

[49]  S. Kjelleberg,et al.  Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitors , 2003, The EMBO journal.

[50]  S. Molin,et al.  Synthetic furanones inhibit quorum-sensing and enhance bacterial clearance in Pseudomonas aeruginosa lung infection in mice. , 2004, The Journal of antimicrobial chemotherapy.

[51]  J. Rogalski,et al.  Hydrolysis of mutan and prevention of its formation in streptococcal films by fungal α-D-glucanases , 2004 .

[52]  J. Kaplan,et al.  Intercellular adhesion and biocide resistance in nontypeable Haemophilus influenzae biofilms. , 2009, Microbial pathogenesis.

[53]  Pierre Le-Clech,et al.  Fouling in membrane bioreactors used in wastewater treatment , 2006 .

[54]  D. Bagley,et al.  A Review of Biofouling and its Control in Membrane Separation Bioreactors , 2004, Water environment research : a research publication of the Water Environment Federation.

[55]  T. Wood,et al.  A naturally occurring brominated furanone covalently modifies and inactivates LuxS. , 2009, Bioorganic & medicinal chemistry letters.

[56]  K. Kogure,et al.  Attachment of Vibrio alginolyticus to Glass Surfaces Is Dependent on Swimming Speed , 1998, Journal of bacteriology.

[57]  A. Conte,et al.  Immobilization of lysozyme on polyvinylalcohol films for active packaging applications. , 2006, Journal of food protection.

[58]  R. Nys,et al.  New halogenated furanones from the marine alga delisea pulchra (cf. fimbriata) , 1993 .

[59]  Malte Hermansson,et al.  The DLVO theory in microbial adhesion , 1999 .

[60]  F. Petersen,et al.  DNA Binding-Uptake System: a Link between Cell-to-Cell Communication and Biofilm Formation , 2005, Journal of bacteriology.

[61]  C. Pradier,et al.  Grafting of lysozyme and/or poly(ethylene glycol) to prevent biofilm growth on stainless steel surfaces. , 2009, The journal of physical chemistry. B.

[62]  P. Mitchell CHEMIOSMOTIC COUPLING IN OXIDATIVE AND PHOTOSYNTHETIC PHOSPHORYLATION , 1966, Biological reviews of the Cambridge Philosophical Society.

[63]  J. Trevors The measurement of electron transport system (ETS) activity in freshwater sediment , 1984 .

[64]  F. Petersen,et al.  Synthetic bromated furanone inhibits autoinducer-2-mediated communication and biofilm formation in oral streptococci. , 2007, Oral microbiology and immunology.

[65]  Thomas K. Wood,et al.  Autoinducer 2 Controls Biofilm Formation in Escherichia coli through a Novel Motility Quorum-Sensing Regulator (MqsR, B3022) , 2006, Journal of bacteriology.

[66]  D. Stuehr,et al.  Direct Evidence for Nitric Oxide Production by a Nitric-oxide Synthase-like Protein from Bacillus subtilis * , 2002, The Journal of Biological Chemistry.

[67]  Zhiqiang Qin,et al.  Role of autolysin-mediated DNA release in biofilm formation of Staphylococcus epidermidis. , 2007, Microbiology.

[68]  G. Babcock,et al.  Oxygen activation and the conservation of energy in cell respiration , 1992, Nature.

[69]  T. Wood,et al.  Inhibition of biofilm formation and swarming of Escherichia coli by (5Z)-4-bromo-5-(bromomethylene)-3-butyl-2(5H)-furanone. , 2001, Environmental microbiology.

[70]  S. Lippard,et al.  Bacterial Nitric-oxide Synthases Operate without a Dedicated Redox Partner* , 2008, Journal of Biological Chemistry.

[71]  Joo-Hwa Tay,et al.  Inhibition of free ammonia to the formation of aerobic granules , 2004 .

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

[73]  Biofouling on Membranes — A Short Review , 1992 .

[74]  Haluk Beyenal,et al.  Quorum sensing: a new biofouling control paradigm in a membrane bioreactor for advanced wastewater treatment. , 2009, Environmental science & technology.

[75]  J. Kaplan,et al.  Susceptibility of staphylococcal biofilms to enzymatic treatments depends on their chemical composition , 2007, Applied Microbiology and Biotechnology.

[76]  T. B. Rasmussen,et al.  Quorum sensing inhibitors: a bargain of effects. , 2006, Microbiology.

[77]  Leo Eberl,et al.  Inhibition of quorum sensing in Pseudomonas aeruginosa biofilm bacteria by a halogenated furanone compound. , 2002, Microbiology.

[78]  M. Fletcher The effects of culture concentration and age, time, and temperature on bacterial attachment to polystyrene , 1977 .

[79]  S. Denyer,et al.  Reduction in Exopolysaccharide Viscosity as an Aid to Bacteriophage Penetration through Pseudomonas aeruginosa Biofilms , 2001, Applied and Environmental Microbiology.

[80]  Bacteriophage T4 multiplication in a glucose-limited Escherichia coli biofilm. , 2001 .

[81]  Juan E. González,et al.  Messing with Bacterial Quorum Sensing , 2006, Microbiology and Molecular Biology Reviews.

[82]  Yu Liu,et al.  Energy uncoupling inhibits aerobic granulation , 2009, Applied Microbiology and Biotechnology.

[83]  Yu Liu,et al.  Control of microbial attachment by inhibition of ATP and ATP‐mediated autoinducer‐2 , 2010, Biotechnology and bioengineering.

[84]  D. Combes,et al.  Influence of subtilisin on the adhesion of a marine bacterium which produces mainly proteins as extracellular polymers , 2008, Journal of applied microbiology.

[85]  M. Hentzer,et al.  Pharmacological inhibition of quorum sensing for the treatment of chronic bacterial infections. , 2003, The Journal of clinical investigation.

[86]  K. Winzer,et al.  Look who's talking: communication and quorum sensing in the bacterial world , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[87]  E. P. Jacobs,et al.  Enzymatic cleaning of ultrafiltration membranes fouled by abattoir effluent. , 2003 .

[88]  B. Stevenson,et al.  LuxS-Mediated Quorum Sensing in Borrelia burgdorferi, the Lyme Disease Spirochete , 2002, Infection and Immunity.

[89]  A. Obradović,et al.  Bacteriophages for plant disease control. , 2007, Annual review of phytopathology.

[90]  P. Swart,et al.  An enzymatic approach to the cleaning of ultrafiltration membranes fouled in abattoir effluent , 1996 .

[91]  L. Samaranayake,et al.  Synergistic activity of lysozyme and antifungal agents against Candida albicans biofilms on denture acrylic surfaces. , 2009, Archives of oral biology.

[92]  L. Melo,et al.  Biofilms--science and technology , 1992 .

[93]  Rosário Oliveira,et al.  The Role of Exopolymers Produced by Sphingomonas paucimobilis in Biofilm Formation and Composition , 2000 .

[94]  Inna Dubchak,et al.  Dissimilatory Metabolism of Nitrogen Oxides in Bacteria: Comparative Reconstruction of Transcriptional Networks , 2005, PLoS Comput. Biol..

[95]  F. Riera,et al.  Enzymatic cleaning of inorganic ultrafiltration membranes fouled by whey proteins. , 2002, Journal of agricultural and food chemistry.

[96]  Feng Xu,et al.  Degradation of N-acylhomoserine lactones, the bacterial quorum-sensing molecules, by acylase. , 2003, Journal of biotechnology.

[97]  D. E. Caldwell,et al.  Tracing the interaction of bacteriophage with bacterial biofilms using fluorescent and chromogenic probes , 1996, Journal of Industrial Microbiology.

[98]  S. Razin,et al.  Role of energy metabolism in Mycoplasma pneumoniae attachment to glass surfaces , 1981, Infection and immunity.

[99]  Bonnie L Bassler,et al.  LuxS quorum sensing: more than just a numbers game. , 2003, Current opinion in microbiology.

[100]  Duu-Jong Lee,et al.  Biofouling in Membrane Bioreactor , 2006 .

[101]  K. Hughes,et al.  Energy source of flagellar type III secretion , 2008, Nature.

[102]  H. Rohde,et al.  Biofilm Formation by Staphylococcus haemolyticus , 2009, Journal of Clinical Microbiology.

[103]  D. Sinderen,et al.  Bacteriophage: genetics and molecular biology. , 2007 .

[104]  J. M. Dow,et al.  Cyclic Di-GMP Signaling in Bacteria: Recent Advances and New Puzzles , 2006, Journal of bacteriology.

[105]  Chettiyappan Visvanathan,et al.  Membrane Separation Bioreactors for Wastewater Treatment , 2000 .

[106]  J. Costerton,et al.  Pseudomonas aeruginosa Displays Multiple Phenotypes during Development as a Biofilm , 2002, Journal of bacteriology.

[107]  R. Lamont,et al.  LuxS-Based Signaling in Streptococcus gordonii: Autoinducer 2 Controls Carbohydrate Metabolism and Biofilm Formation with Porphyromonas gingivalis , 2003, Journal of bacteriology.

[108]  Joon-Hee Lee,et al.  Furanone derivatives as quorum-sensing antagonists of Pseudomonas aeruginosa , 2008, Applied Microbiology and Biotechnology.

[109]  Joo-Hwa Tay,et al.  The essential role of hydrodynamic shear force in the formation of biofilm and granular sludge. , 2002, Water research.

[110]  J. Kweon,et al.  Inhibition of Quorum Sensing Mechanism and Aeromonas hydrophila Biofilm Formation by Vanillin , 2009 .

[111]  Woo Y. Lee,et al.  Microfluidic devices for studying growth and detachment of Staphylococcus epidermidis biofilms , 2008, Biomedical microdevices.

[112]  Dacheng Ren,et al.  Differential gene expression shows natural brominated furanones interfere with the autoinducer-2 bacterial signaling system of Escherichia coli. , 2004, Biotechnology and bioengineering.

[113]  Michael Y. Galperin,et al.  C‐di‐GMP: the dawning of a novel bacterial signalling system , 2005, Molecular microbiology.

[114]  C. Xi,et al.  Evaluation of Different Methods for Extracting Extracellular DNA from the Biofilm Matrix , 2009, Applied and Environmental Microbiology.

[115]  W. Fortuna,et al.  Bacteriophage therapy for the treatment of infections. , 2009, Current opinion in investigational drugs.

[116]  K. Hardie,et al.  Establishing bacterial communities by 'word of mouth': LuxS and autoinducer 2 in biofilm development , 2008, Nature Reviews Microbiology.

[117]  J. Kweon,et al.  Application of Quorum Quenching to Inhibit Biofilm Formation , 2009 .

[118]  D. Combes,et al.  Effects of commercial enzymes on the adhesion of a marine biofilm-forming bacterium , 2008, Biofouling.