Abstract
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.
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Adak S, Aulak KS, Stuehr DJ (2002) Direct evidence for nitric oxide production by a nitric-oxide synthase-like protein from Bacillus subtilis. J Biol Chem 277:16167–16171
Allie Z, Jacobs EP, Maartens A, Swart P (2003) Enzymatic cleaning of ultrafiltration membranes fouled by abattoir effluent. J Membr Sci 218:107–116
Appendini P, Hotchkiss JH (1997) Immobilization of lysozyme on food contact polymers as potential antimicrobial films. Packag Technol Sci 10:271–279
Arguello MA, Alvarez S, Riera FA, Alvarez R (2002) Enzymatic cleaning of inorganic ultrafiltration membranes fouled by whey proteins. J Agric Food Chem 50:1951–1958
Arguello MA, Alvarez S, Riera FA, Alvarez R (2003) Enzymatic cleaning of inorganic ultrafiltration membranes used for whey protein fractionation. J Membr Sci 216:121–134
Atterbury RJ, Van Bergen MAP, Ortiz F, Lovell MA, Harris JA, De Boer A, Wagenaar JA, Allen VM, Barrow PA (2007) Bacteriophage therapy to reduce Salmonella colonization of broiler chickens. Appl Environ Microbiol 73:4543–4549
Azeredo J, Oliveira R (2000) The role of exopolymers produced by Sphingomonas paucimobilis in biofilm formation and composition. Biofouling 16:17–27
Babcock GT, Wikstrom M (1992) Oxygen activation and the conservation of energy in cell respiration. Nature 356:301–309
Balaban N, Stoodley P, Fux CA, Wilson S, Costerton JW, Dell'Acqua G (2005) Prevention of staphylococcal biofilm-associated infections by the quorum sensing inhibitor RIP. CORR 437:48–54
Barraud N, Hassett DJ, Hwang SH, Rice SA, Kjelleberg S, Webb JS (2006) Involvement of nitric oxide in biofilm dispersal of Pseudomonas aeruginosa. J Bacteriol 188:7344–7353
Barraud N, Storey MV, Moore ZP, Webb JS, Rice SA, Kjelleberg S (2009) Nitric oxide-mediated dispersal in single- and multi-species biofilms of clinically and industrially relevant microorganisms. Microb Biotechnol 2:370–378
Barrios AFG, Zuo RJ, Hashimoto Y, Yang L, Bentley WE, Wood TK (2006) Autoinducer 2 controls biofilm formation in Escherichia coli through a novel motility quorum-sensing regulator (MqsR, B3022). J Bacteriol 188:305–316
Cai TB, Wang PG, Holder AA (2005) NO and NO Donors. In: Wang PG, Cai TB, Taniguchi N (ed) Nitric oxide donors. Wiley-VCH Verlag GmbH & Co. KGaA, p 1–31.
Calleja GB (1984) Microbial aggregation. CRC, Florida
Caro A, Humblot V, Methivier C, Minier M, Salmain M, Pradier CM (2009) Grafting of lysozyme and/or poly(ethylene glycol) to prevent biofilm growth on stainless steel surfaces. J Phys Chem B 113:2101–2109
Chaignon P, Sadovskaya I, Ragunah C, Ramasubbu N, Kaplan JB, Jabbouri S (2007) Susceptibility of staphylococcal biofilms to enzymatic treatments depends on their chemical composition. Appl Microbiol Biotechnol 75:125–132
Charville GW, Hetrick EM, Geer CB, Schoenfisch MH (2008) Reduced bacterial adhesion to fibrinogen-coated substrates via nitric oxide release. Biomaterials 29:4039–4044
Chen X, Schauder S, Potier N, Van Dorsselaer A, Pelczer I, Bassler BL, Hughson FM (2002) Structural identification of a bacterial quorum-sensing signal containing boron. Nature 415:545–549
Conte A, Buonocore GG, Bevilacqua A, Sinigaglia M, Del Nobile MA (2006) Immobilization of lysozyme on polyvinylalcohol films for active packaging applications. J Food Prot 69:866–870
Corbin BD, McLean RJC, Aron GM (2001) Bacteriophage T4 multiplication in a glucose-limited Escherichia coli biofilm. Can J Microbiol 47:680–684
Cubonava L, Majernik A, Smigan P (2004) Biochemical characteristics of a mutant of the methanoarchaeon Methanothermobacter thermautotrophicus resistant to the protonophoric uncoupler TCS. Folia Microbiol 49:147–150
Curtin JJ, Donlan RM (2006) Using bacteriophages to reduce formation of catheter-associated biofilms by Staphylococcus epidermidis. Antimicrob Agents Chemother 50:1268–1275
Delgado-Nixon VM, Gonzalez G, Gilles-Gonzalez MA (2000) Dos, a heme-binding PAS protein from Escherichia coli, is a direct oxygen sensor. Biochem 39:2685–2691
Denys R, Wright AD, Konig GM, Sticher O (1993) New halogenated furanones from the marine alga delisea-pulchara (cf. fimbriata). Tetrahedron 49:11213–11220
Dobretsov S, Teplitski M, Paul V (2009) Mini-review: quorum sensing in the marine environment and its relationship to biofouling. Biofouling 25:413–427
Dong YH, Zhang LH (2005) Quorum sensing and quorum-quenching enzymes. J Microbiol 43:101–109
Doolittle MM, Cooney JJ, Caldwell DE (1995) Lytic infection of Escherichia coli biofilms by bacteriophage T4. Can J Microbiol 41:12–18
Doolittle MM, Cooney JJ, Caldwell DE (1996) Tracing the interaction of bacteriophage with bacterial biofilms using fluorescent and chromogenic probes. J Ind Microbiol 16:331–341
Ellwood DC, Keevil CW, Marsh PD, Brown CM, Wardell JN (1982) Surface-associated growth. Philos Trans R Soc London Ser B-Biol Sci 297:517–532
Feldner J, Bredt W, Razin S (1981) Role of energy-metabolism in Mycoplasma pneumoniae attachment to glass surface. Infect Immun 31:107–113
Flemming HC, Schaule G, McDonogh R (1992) Biofouling on membranes—a short review. In: Melo LF, Bott TR, Fletcher M, Capdeville B (eds) Biofilms—Science and Technology. NATO ASI series, Alvor, Portugal, pp 487–497
Fletcher M (1977) Effects of culture concentration and age, time and temperature on bacterial attachment to polystyrene. Can J Microbiol 23:1–6
Fredheim EGA, Klingenberg C, Rohde H, Frankenberger S, Gaustad P, Flaegstad T, Sollid JE (2009) Biofilm formation by Staphylococcus haemolyticus. J Clin Microbiol 47:1172–1180
Goldman G, Starosvetsky J, Armon R (2009) Inhibition of biofilm formation on UF membrane by use of specific bacteriophages. J Membr Sci 342:145–152
Gonzalez JE, Keshavan ND (2006) Messing with bacterial quorum sensing. Microbiol Mol Biol Rev 70:859–875
Gorski A, Miedzybrodzki R, Borysowski J, Weber-Dabrowska B, Lobocka M, Fortuna W, Letkiewicz S, Zimecki M, Filby G (2009) Bacteriophage therapy for the treatment of infections. Curr Opin Investig Drugs 10:766–774
Gram L, deNys R, Maximilien R, Givskov M, Steinberg P, Kjelleberg S (1996) Inhibitory effects of secondary metabolites from the red alga Delisea pulchra on swarming motility of Proteus mirabilis. Appl Environ Microbiol 62:4284–4287
Gusarov I, Starodubtseva M, Wang ZQ, McQuade L, Lippard SJ, Stuehr DJ, Nudler E (2008) Bacterial nitric-oxide synthases operate without a dedicated redox partner. J Biol Chem 283:13140–13147
Hanlon GW, Denyer SP, Olliff CJ, Ibrahim LJ (2001) Reduction in exopolysaccharide viscosity as an aid to bacteriophage penetration through Pseudomonas aeruginosa biofilms. Appl Environ Microbiol 67:2746–2753
Hardie KR, Heurlier K (2008) Establishing bacterial communities by ‘word of mouth’: LuxS and autoinducer 2 in biofilm development. Nat Rev Microbiol 6:635–643
Hentzer M, Givskov M (2003) Pharmacological inhibition of quorum sensing for the treatment of chronic bacterial infections. J Clin Invest 112:1300–1307
Hentzer M, Riedel K, Rasmussen TB, Heydorn A, Andersen JB, Parsek MR, Rice SA, Eberl L, Molin S, Hoiby N, Kjelleberg S, Givskov M (2002) Inhibition of quorum sensing in Pseudomonas aeruginosa biofilm bacteria by a halogenated furanone compound. Microbiology 148:87–102
Hentzer M, Wu H, Andersen JB, Riedel K, Rasmussen TB, Bagge N, Kumar N, Schembri MA, Song ZJ, Kristoffersen P, Manefield M, Costerton JW, Molin S, Eberl L, Steinberg P, Kjelleberg S, Hoiby N, Givskov M (2003) Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitors. Embo J 22:3803–3815
Hermansson M (1999) The DLVO theory in microbial adhesion. Colloids Surf B-Biointerfaces 14:105–119
Herzberg M, Kang S, Elimelech M (2009) Role of extracellular polymeric substances (EPS) in biofouling of reverse osmosis membranes. Environ Sci Technol 43:4393–4398
Huber B, Eberl L, Feucht W, Polster J (2003) Influence of polyphenols on bacterial biofilm formation and quorum-sensing. Zeitschrift Fur Naturforschung C-a J Biosci 58:879–884
Hume EBH, Baveja J, Muir B, Schubert TL, Kumar N, Kjelleberg S, Griesser HJ, Thissen H, Read R, Poole-Warren LA, Schindhelm K, Willcox MDP (2004) The control of Staphylococcus epidermidis biofilm formation and in vivo infection rates by covalently bound furanones. Biomaterials 25:5023–5030
Izano EA, Shah SM, Kaplan JB (2009) Intercellular adhesion and biocide resistance in nontypeable Haemophilus influenzae biofilms. Microb Pathog 46:207–213
Jain A, Nishad KK, Bhosle NB (2007) Effects of DNP on the cell surface properties of marine bacteria and its implication for adhesion to surfaces. Biofouling 23:171–177
Janssens JCA, Steenackers H, Robijns S, Gellens E, Levin J, Zhao H, Hermans K, De Coster D, Verhoeven TL, Marchal K, Vanderleyden J, De Vos DE, De Keersmaecker SCJ (2008) Brominated furanones inhibit biofilm formation by Salmonella enterica serovar Typhimurium. Appl Environ Microbiol 74:6639–6648
Jiang B, Liu Y (2010) Energy uncoupling inhibits aerobic granulation. Appl Microbiol Biotechnol 85:589–595
Jolliffe LK, Doyle RJ, Streips UN (1981) The energized membrane and cellular autolysis in Bacillus subtilis. Cell 25:753–763
Jones JB, Jackson LE, Balogh B, Obradovic A, Iriarte FB, Momol MT (2007) Bacteriophages for plant disease control. Annu Rev Phytopathol 45:245–262
Kaplan JB, Ragunath C, Velliyagounder K, Fine DH, Ramasubbu N (2004) Enzymatic detachment of Staphylococcus epidermidis biofilms. Antimicrob Agents Chemother 48:2633–2636
Kim C, Kim J, Park HY, Park HJ, Lee JH, Kim CK, Yoon J (2008) Furanone derivatives as quorum-sensing antagonists of Pseudomonas aeruginosa. Appl Microbiol Biotechnol 80:37–47
Klebensberger J, Rui O, Fritz E, Schink B, Philipp B (2006) Cell aggregation of Pseudomonas aeruginosa strain PAO1 as an energy-dependent stress response during growth with sodium dodecyl sulfate. Arch Microbiol 185:417–427
Kogure K, Ikemoto E, Morisaki H (1998) Attachment of Vibrio alginolyticus to glass surfaces is dependent on swimming speed. J Bacteriol 180:932–937
Le-Clech P, Chen V, Fane TAG (2006) Fouling in membrane bioreactors used in wastewater treatment. J Membr Sci 284:17–53
Lee JH, Kaplan JB, Lee WY (2008) Microfluidic devices for studying growth and detachment of Staphylococcus epidermidis biofilms. Biomed Microdevices 10:489–498
Lemon KP, Higgins DE, Kolter R (2007) Flagellar motility is critical for Listeria monocytogenes biofilm formation. J Bacteriol 189:4418–4424
Leroy C, Delbarre-Ladrat C, Ghillebaert F, Compere C, Combes D (2008a) Effects of commercial enzymes on the adhesion of a marine biofilm-forming bacterium. Biofouling 24:11–22
Leroy C, Delbarre-Ladrat C, Ghillebaert F, Compere C, Combes D (2008b) Influence of subtilisin on the adhesion of a marine bacterium which produces mainly proteins as extracellular polymers. J Appl Microbiol 105:791–799
Lewis K, Naroditskaya V, Ferrante A, Fokina I (1994) Bacterial-resistance to uncouplers. J Bioenerg Biomembranes 26:639–646
Liao BQ, Bagley DM, Kraemer HE, Leppard GG, Liss SN (2004) A review of biofouling and its control in membrane separation bioreactors. Water Environ Res 76:425–436
Liu Y, Tay JH (2002) The essential role of hydrodynamic shear force in the formation of biofilm and granular sludge. Water Res 36:1653–1665
Liu YQ, Liu Y, Tay JH (2004) The effects of extracellular polymeric substances on the formation and stability of biogranules. Appl Microbiol Biotechnol 65:143–148
Loiselle M, Anderson KW (2003) The use of cellulase in inhibiting biofilm formation from organisms commonly found on medical implants. Biofouling 19:77–85
Lonn-Stensrud J, Petersen FC, Benneche T, Aamdal SA (2007) Synthetic bromated furanone inhibits autoinducer-2-mediated communication and biofilm formation in oral streptococci. Oral Microbiol Immunol 22:340–346
Lopez JM, Koopman B, Bitton G (1986) INT-dehydrogenase test for activated sludge process control. Biotechnol Bioeng 28:1080–1085
Lu TK, Collins JJ (2007) Dispersing biofilms with engineered enzymatic bacteriophage. Proc Natl Acad Sci 104:11197–11202
Maartens A, Swart P, Jacobs EP (1996) An enzymatic approach to the cleaning of ultrafiltration membranes fouled in abattoir effluent. J Membr Sci 119:9–16
Mc Grath S (2007) Bacteriophage: genetics and molecular biology. Caister Acedemic
McClaine JW, Ford RM (2002) Characterizing the adhesion of motile and nonmotile Escherichia coli to a glass surface using a parallel-plate flow chamber. Biotechnol Bioeng 78:179–189
McNab R, Ford SK, El-Sabaeny A, Barbieri B, Cook GS, Lamont RJ (2003) LuxS-based signaling in Streptococcus gordonii: autoinducer 2 controls carbohydrate metabolism and biofilm formation with Porphyromonas gingivalis. J Bacteriol 185:274–284
Mitchell P (1961) Chemiosmotic coupling in oxidative and photosynthetic phosphorylation. Biochem J 79:P23
Morohoshi T, Shiono T, Takidouchi K, Kato M, Kato N, Kato J, Ikeda T (2007) Inhibition of quorum sensing in Serratia marcescens AS-1 by synthetic analogs of N-acylhomoserine lactone. Appl Environ Microbiol 73:6339–6344
Paul K, Erhardt M, Hirano T, Blair DF, Hughes KT (2008) Energy source of flagellar type[thinsp]III secretion. Nature 451:489–492
Paul D, Kim YS, Ponnusamy K, Kweon JH (2009) Application of quorum quenching to inhibit biofilm formation. Environ Eng Sci 26:1319–1324
Petersen FC, Tao L, Scheie AA (2005) DNA binding–uptake system: a link between cell-to-cell communication and biofilm formation. J Bacteriol 187:4392–4400
Poele ST, van der Graaf J (2005) Enzymatic cleaning in ultrafiltration of wastewater treatment plant effluent. Desalination 179:73–81
Ponnusamy K, Paul D, Kweon JH (2009) Inhibition of quorum sensing mechanism and Aeromonas hydrophila biofilm formation by vanillin. Environ Eng Sci 26:1359–1364
Qin ZQ, Ou YZ, Yang LA, Zhu YL, Tolker-Nielsen T, Molin S, Qu D (2007) Role of autolysin-mediated DNA release in biofilm formation of Staphylococcus epidermidis. Microbiology-Sgm 153:2083–2092
Ramesh A, Lee DJ, Wang ML, Hsu JP, Juang RS, Hwang KJ, Liu JC, Tseng SJ (2006) Biofouling in membrane bioreactor. Sep Sci Technol 41:1345–1370
Rasmussen TB, Givskov M (2006) Quorum sensing inhibitors: a bargain of effects. Microbiology-Sgm 152:895–904
Ren DC, Sims JJ, Wood TK (2001) Inhibition of biofilm formation and swarming of Escherichia coli by (5Z)-4-bromo-5(bromomethylene)-3-butyl-2(5H)-furanone. Environ Microbiol 3:731–736
Ren DC, Bedzyk LA, Ye RW, Thomas SM, Wood TK (2004) Differential gene expression shows natural brominated furanones interfere with the autoinducer-2 bacterial signaling system of Escherichia coli. Biotechnol Bioeng 88:630–642
Richards JJ, Melander C (2009) Controlling bacterial biofilms. Chembiochem 10:2287–2294
Rodionov DA, Dubchak IL, Arkin AP, Alm EJ, Gelfand MS (2005) Dissimilatory metabolism of nitrogen oxides in bacteria: comparative reconstruction of transcriptional networks. PloS Comput Biol 1:415–431
Romling U, Gomelsky M, Galperin MY (2005) C-di-GMP: the dawning of a novel bacterial signalling system. Mol Microbiol 57:629–639
Russell JB (2007) The energy spilling reactions of bacteria and other organisms. J Mol Microbiol Biotechnol 13:1–11
Ryan RP, Fouhy Y, Lucey JF, Dow JM (2006) Cyclic Di-GMP signaling in bacteria: recent advances and new puzzles. J Bacteriol 188:8327–8334
Samaranayake YH, Cheung BPK, Parahitiyawa N, Seneuiratne CJ, Yau JYY, Yeung KWS, Samaranayake LP (2009) Synergistic activity of lysozyme and antifungal agents against Candida albicans biofilms on denture acrylic surfaces. Arch Oral Biol 54:115–126
Sarti P, Abigliano L, Gorlach A, Brune B (2002) Superoxide and nitric oxide participation in cell communication. Cell Death Differ 9:1160–1162
Sauer K, Camper AK, Ehrlich GD, Costerton JW, Davies DG (2002) Pseudomonas aeruginosa displays multiple phenotypes during development as a biofilm. J Bacteriol 184:1140–1154
Schlag S, Nerz C, Birkenstock TA, Altenberend F, Gotz F (2007) Inhibition of staphylococcal biofilm formation by nitrite. J Bacteriol 189:7911–7919
Smith KM, Bu YG, Suga H (2003) Induction and inhibition of Pseudomonas aeruginosa quorum sensing by synthetic autoinducer analogs. Chem Biol 10:81–89
Stevenson B, Babb K (2002) LuxS-mediated quorum sensing in Borrelia burgdorferi, the Lyme disease spirochete. Infect Immun 70:4099–4105
Thomas VC, Thurlow LR, Boyle D, Hancock LE (2008) Regulation of autolysis-dependent extracellular DNA release by Enterococcus faecalis extracellular proteases influences biofilm development. J Bacteriol 190:5690–5698
Trevors JT (1984) The measurement of electron transport system (ETS) activity in freshwater sediment. Water Res 18:581–584
Tsai WC, Strieter RM, Zisman DA, Wilkowski JM, Bucknell KA, Chen GH, Standiford TJ (1997) Nitric oxide is required for effective innate immunity against Klebsiella pneumoniae. Infect Immun 65:1870–1875
Vatanyoopaisarn S, Nazli A, Dodd CER, Rees CED, Waites WM (2000) Effect of flagella on initial attachment of Listeria monocytogenes to stainless steel. Appl Environ Microbiol 66:860–863
Vilain S, Pretorius JM, Theron J, Brozel VS (2009) DNA as an adhesin: Bacillus cereus requires extracellular DNA to form biofilms. Appl Environ Microbiol 75:2861–2868
Visvanathan C, Ben Aim R, Parameshwaran K (2000) Membrane separation bioreactors for wastewater treatment. Crit Rev Environ Sci Technol 30:1–48
Whitchurch CB, Tolker-Nielsen T, Ragas PC, Mattick JS (2002) Extracellular DNA required for bacterial biofilm formation. Science 295:1487–1487
Wiater A, Szczodrak J, Rogalski J (2004) Hydrolysis of mutan and prevention of its formation in streptococcal films by fungal alpha-d-glucanases. Process Biochem 39:1481–1489
Williams P, Winzer K, Chan WC (2007) Look who's talking: communication and quorum sensing in the bacteria world. Philos Trans 362:1119–1134
Wu JF, Xi CW (2009) Evaluation of different methods for extracting extracellular DNA from the biofilm matrix. Appl Environ Microbiol 75:5390–5395
Wu H, Song Z, Hentzer M, Andersen JB, Molin S, Givskov M, Hoiby N (2004) Synthetic furanones inhibit quorum-sensing and enhance bacterial clearance in Pseudomonas aeruginosa lung infection in mice. J Antimicrob Chemother 53:1054–1061
Xavier KB, Bassler BL (2003) LuxS quorum sensing: more than just a numbers game. Curr Opin Microbiol 6:191–197
Xiong YH, Liu Y (2010) Involvement of ATP and autoinducer-2 in the aerobic granulation. Biotechnol Bioeng 105:51–58
Xu HJ (2009) Control of microbial attachment by inhibition of ATP and ATP-mediated autoinducer-2. PhD Interim Examination Report. Nanyang Technological University, Singapore
Xu R, Wang HF (2009) Lysozyme-liposome synthesis and its capability on biofilm removal. Available via Sciencepaper Online. http://www.paper.edu.cn/en/paper.php?serial_number=200907-165
Xu F, Byun T, Dussen HJ, Duke KR (2003) Degradation of N-acylhomoserine lactones, the bacterial quorum-sensing molecules, by acylase. J Biotechnol 101:89–96
Xun LY, Mah RA, Boone DR (1990) Isolation and characterization of disaggregatase from Methanosarcina mazei LYC. Appl Environ Microbiol 56:3693–3698
Yang SF, Tay JH, Liu Y (2004) Inhibition of free ammonia to the formation of aerobic granules. Biochem Eng J 17:41–48
Yeon K-M, Cheong W-S, Oh H-S, Lee W-N, Hwang B-K, Lee C-H, Beyenal H, Lewandowski Z (2009) Quorum sensing: a new biofouling control paradigm in a membrane bioreactor for advanced wastewater treatment. Environ Sci Technol 43:380–385
Zang TZ, Lee BWK, Cannon LM, Ritter KA, Dai SJ, Ren DC, Wood TK, Zhou ZS (2009) A naturally occurring brominated furanone covalently modifies and inactivates LuxS. Bioorg Med Chem Lett 19:6200–6204
Zhang LH (2003) Quorum quenching and proactive host defense. Trends Plant Sci 8:238–244
Zubay G (1998) Biochemistry. WCB, McGraw-Hill
Zumft WG (1993) The biological role of nitric-oxide in bacteria. Arch Microbiol 160:253–264
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Xiong, Y., Liu, Y. Biological control of microbial attachment: a promising alternative for mitigating membrane biofouling. Appl Microbiol Biotechnol 86, 825–837 (2010). https://doi.org/10.1007/s00253-010-2463-0
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DOI: https://doi.org/10.1007/s00253-010-2463-0