DOI QR코드

DOI QR Code

Quorum quenching for effective control of biofouling in membrane bioreactor: A comprehensive review of approaches, applications, and challenges

  • Kose-Mutlu, Borte (National Research Center on Membrane Technologies, Istanbul Technical University) ;
  • Ergon-Can, Tulay (National Research Center on Membrane Technologies, Istanbul Technical University) ;
  • Koyuncu, Ismail (National Research Center on Membrane Technologies, Istanbul Technical University) ;
  • Lee, Chung-Hak (School of Chemical and Biological Engineering, Seoul National University)
  • Received : 2018.10.31
  • Accepted : 2019.01.14
  • Published : 2019.12.30

Abstract

In comparison to alternative advanced wastewater treatment technologies, the main problem associated with membrane bioreactor (MBR) technology, which has become prominent in recent years, is biofouling. Within these systems, biofouling is typically the result of a biofilm layer resulting from bacterial gathering. One biological system that can be employed to interrupt the process of bacterial gathering is called 'Quorum Quenching (QQ)'. Existing QQ applications can be classified using three main types: 1) bacterial/whole-cell applications, 2) direct enzyme applications, and 3) natural sourced compounds. The most common and widely recognized applications for membrane fouling control during MBR operation are bacterial and direct enzyme applications. The purpose of this review was to identify and assess biofilm formation mechanism and results, the suggestion of the QQ concept and its potential to control biofilm formation, and the means by which these QQ applications can be applied within the MBR and present QQ MBR studies.

Keywords

References

  1. Von Grebmer K, Ringler C, Rosegrant MW, Olofinbiyi T, Wiesmann D, Thompson J. Global hunger index: The challenge of hunger: Ensuring sustainable food security under land, water, and energy stresses. Intl. Food Policy Res. Inst. 2012.
  2. Lee S, Park SK, Kwon H, et al. Crossing the border between laboratory and field: Bacterial quorum quenching for anti-biofouling strategy in an MBR. Environ. Sci. Technol. 2016;50: 1788-1795. https://doi.org/10.1021/acs.est.5b04795
  3. Meng F, Chae SR, Drew A, Kraume M, Shin HS, Yang F. Recent advances in membrane bioreactors (MBRs): Membrane fouling and membrane material. Water Res. 2009;43:489-1512.
  4. Judd S. A review of fouling of membrane bioreactors in sewage treatment. Water Sci. Technol. 2004;492:229-235. https://doi.org/10.2166/wst.2004.0131
  5. Noble J. GE ZeeWeed MBR technology for pharmaceutical wastewater treatment. Membr. Technol. 2006;2006:7-9. https://doi.org/10.1016/S0958-2118(06)70790-X
  6. Chen W, Liu J. The possibility and applicability of coagulation-MBR hybrid system in reclamation of dairy wastewater. Desalination 2012;285:226-231. https://doi.org/10.1016/j.desal.2011.10.007
  7. Ortiz M, Raluy RG, Serra L, Uche J. Life cycle assessment of water treatment technologies: Wastewater and water-reuse in a small town. Desalination 2007;204:121-131. https://doi.org/10.1016/j.desal.2006.04.026
  8. Pandey A, Singh RK. Industrial waste water treatment by membrane bioreactor system. Elixir Chem. Eng. 2014;70:23772-23777.
  9. BCC Research. Global market for membrane bioreactors worth $488 million by 2013. International report. Massachusetts, USA; 2008.
  10. Grand view research. Membrane bioreactor (MBR) market analysis by product (hollow fiber, flat sheet, multi-tubular), by configuration (submerged, side stream), by application, and segment forecasts, 2018-2025. International report. California, USA; 2017.
  11. Drews A. Membrane fouling in membrane bioreactors-Characterisation, contradictions, cause and cures. J. Membr. Sci. 2010;363:1-28. https://doi.org/10.1016/j.memsci.2010.06.046
  12. Bouayed N, Dietrich N, Lafforgue C, Lee CH, Guigui C. Process-oriented review of bacterial quorum quenching for membrane biofouling mitigation in membrane bioreactors (MBRs). Membranes 2016;6:52. https://doi.org/10.3390/membranes6040052
  13. Lade H, Paul D, Kweon JH. N-Acyl homoserine lactone-mediated quorum sensing with special reference to use of quorum quenching bacteria in membrane biofouling control. BioMed Res. Int. 2014;2014:162584.
  14. Lim AL, Bai R. Membrane fouling and cleaning in microfiltration of activated sludge wastewater. J. Membr. Sci. 2003;216:279-290. https://doi.org/10.1016/S0376-7388(03)00083-8
  15. Van den Broeck R, Krzeminski P, Van Dierdonck J, et al. Activated sludge characteristics affecting sludge filterability in municipal and industrial MBRs: Unraveling correlations using multi-component regression analysis. J. Membr. Sci.378: 330-338. https://doi.org/10.1016/j.memsci.2011.05.010
  16. Adav SS, Lee DJ. Extraction of extracellular polymeric substances from aerobic granule with compact interior structure. J. Hazard. Mater. 2008;154:1120-1126. https://doi.org/10.1016/j.jhazmat.2007.11.058
  17. Tansel B, Sager J, Garland J, Xu S, Levine L, Bisbee P. Deposition of extracellular polymeric substances (EPS) and microtopographical changes on membrane surfaces during intermittent filtration conditions. J. Membr. Sci. 2006;285:225-231. https://doi.org/10.1016/j.memsci.2006.08.031
  18. Laspidou CS, Rittmann BE. A unified theory for extracellular polymeric substances soluble microbial products and active and inert biomass. Water Res. 2002;36:2711-2720. https://doi.org/10.1016/S0043-1354(01)00413-4
  19. Jiang W, Xia S, Liang J, Zhang Z, Hermanowicz SW. Effect of quorum quenching on the reactor performance biofouling and biomass characteristics in membrane bioreactors. Water Res. 2013;47:187-196. https://doi.org/10.1016/j.watres.2012.09.050
  20. Ham SY, Kim HS, Cha E, Park JH, Park HD. Mitigation of membrane biofouling by a quorum quenching bacterium for membrane bioreactors. Biores. Technol. 2018;258:220-226. https://doi.org/10.1016/j.biortech.2018.03.007
  21. Greenberg EP. Quorum Sensing in Gram-Negative Bacteria. ASM News 1997;63:371-377.
  22. Greenberg EP. Bacterial communication and group behavior. J. Clin. Invest. 2003;112:1288-1290. https://doi.org/10.1172/JCI200320099
  23. Kim AL, Park SY, Lee CH, Lee CH, Lee JK. Quorum quenching bacteria isolated from the sludge of a wastewater treatment plant and their application for controlling biofilm formation. J. Microbiol. Biotechnol. 2014;24:1574-1582. https://doi.org/10.4014/jmb.1407.07009
  24. Parsek MR, Greenberg EP. Sociomicrobiology: The connections between quorum sensing and biofilms. Trends Microbiol. 2005;13:27-33. https://doi.org/10.1016/j.tim.2004.11.007
  25. Whitehead NA, Barnard AM, Slater H, Simpson NJ, Salmond GP. Quorum sensing in Gram-negative bacteria. FEMS Microbiol. Rev. 2001;25:365-404. https://doi.org/10.1111/j.1574-6976.2001.tb00583.x
  26. Ng WL, Bassler BL. Bacterial quorum-sensing network architectures. Annu. Rev. Genet. 2009;43:197-222. https://doi.org/10.1146/annurev-genet-102108-134304
  27. Chen X, Schauder S, Potier N, et al. Structural identification of a bacterial quorum-sensing signal containing boron. Nature 2002;415:545-549. https://doi.org/10.1038/415545a
  28. Federle MJ, Bassler L. Interspecies communication in bacteria. J. Clin. Invest. 2003;112:1291-1299. https://doi.org/10.1172/JCI20195
  29. Xavier KB, Bassler BL. Regulation of uptake and processing of the quorum-sensing autoinducer AI-2 in Escherichia coli. J. Bacteriol. 2005;187:238-248. https://doi.org/10.1128/JB.187.1.238-248.2005
  30. Dobretsov S, Teplitski M, Paul V. Mini-review: Quorum sensing in the marine environment and its relationship to biofouling. Biofouling 2009;25:413-427. https://doi.org/10.1080/08927010902853516
  31. Nealson KH, Platt T, Hastings JW. Cellular control of the synthesis and activity of the bacterial luminescent system. J. Bacteriol. 1970;104:313-322. https://doi.org/10.1128/JB.104.1.313-322.1970
  32. Eberhard A, Burlingame AL, Eberhard C, Kenyon GL, Nealson KH, Oppenheimer NJ. Structural identification of autoinducer of Photobacterium fischeri luciferase. Biochemistry. 1981;20:2444-2449. https://doi.org/10.1021/bi00512a013
  33. Pearson JP, Gray KM, Passador L, et al. Structure of the auto-inducer required for expression of Pseudomonas aeruginosa virulence genes. Proc. Natl. Acad. Sci. USA 1994;91:197-201. https://doi.org/10.1073/pnas.91.1.197
  34. Cha C, Gao P, Chen YC, Shaw PD, Farrand SK. Production of acyl-homoserine lactone quorum-sensing signals by gram-negative plant-associated bacteria. Mol. Plant Microb. Interact. 1998;11:1119-1129. https://doi.org/10.1094/MPMI.1998.11.11.1119
  35. Fuqua C, Parsek MR, Greenberg EP. Regulation of gene expression by cell-to-cell communication: Acylhomoserine lactone quorum sensing. Annu. Rev. Genet. 2001;35:439-468. https://doi.org/10.1146/annurev.genet.35.102401.090913
  36. Swift S, Lynch MJ, Fish L, et al. Quorum sensing-dependent regulation and blockade of exoprotease production in Aeromonas hydrophila. Infect. Immun. 1999;67:5192-5199. https://doi.org/10.1128/IAI.67.10.5192-5199.1999
  37. Holden MTG, Chhabra SR, De Nys R, et al. Quorum-sensing cross talk: Isolation and chemical characterization of cyclic dipeptides from Pseudomonas aeruginosa and other Gram-negative bacteria. Mol. Microbiol. 1999;33:1254-1266. https://doi.org/10.1046/j.1365-2958.1999.01577.x
  38. Lyon GJ, Mayville P, Muir TW, Novick RP. Rational design of a global inhibitor of the virulence response in Staphylococcus aureus based in part on localization of the site of inhibition to the receptor-histidine kinase. AgrC. Proc. Natl. Acad. Sci. USA. 2000;97:13330-13335. https://doi.org/10.1073/pnas.97.24.13330
  39. Miller MB, Bassler BL. Quorum sensing in bacteria. Annu. Rev. Microbiol. 2001;55:165-199. https://doi.org/10.1146/annurev.micro.55.1.165
  40. Chen X, Schauder S, Potier N, et al. Structural identification of a bacterial quorum sensing signal containing boron. Nature 2002;415:545-549. https://doi.org/10.1038/415545a
  41. Miller ST, Xavier KB, Campagna SR, et al. Salmonella typhimurium recognizes a chemically distinct form of the bacterial quorum-sensing signal AI-2. Mol. Cell. 2004;15:677-687. https://doi.org/10.1016/j.molcel.2004.07.020
  42. Defoirdt T, Boon N, Bossier P, Verstraete W. Disruption of bacterial quorum sensing: An unexplored strategy to fight infections in aquaculture. Aquaculture 2004;240:69-88. https://doi.org/10.1016/j.aquaculture.2004.06.031
  43. Zhang LH, Dong YH. Quorum sensing and signal interference: Diverse implications. Mol. Microbiol. 2004;53:1563-1571. https://doi.org/10.1111/j.1365-2958.2004.04234.x
  44. Chong TM, Koh CL, Sam CK, Choo YM, Yin WF, Chan KG. Characterization of quorum sensing and quorum quenching soil bacteria isolated from Malaysian tropical montane forest. Sensors 2012;12:4846-4859. https://doi.org/10.3390/s120404846
  45. Lau YY, Sulaiman J, Chen JW, Yin WF, Chan GK. Quorum sensing activity of Enterobacter asburiae isolated from lettuce leaves. Sensors 2013;13:14189-14199. https://doi.org/10.3390/s131014189
  46. Tan WS, Yunos NYM, Tan PW, et al. Freshwater-borne bacteria isolated from a malaysian rainforest waterfall exhibiting quorum sensing properties. Sensors 2014;14:10527-10537. https://doi.org/10.3390/s140610527
  47. Zan J, Liu Y, Fuqua C, Hill RT. Acyl-homoserine lactone quorum sensing in the Roseobacter clade. Int. J. Mol. Sci. 2014;15: 654-669. https://doi.org/10.3390/ijms15010654
  48. Sandle T. Bacterial adhesion: An introduction. J. Valid. Technol. 2013;19:1-10.
  49. Lade H, Paul D, Kweon JH. Isolation and molecular characterization of biofouling bacteria and profiling of quorum sensing signal molecules from membrane bioreactor activated sludge. Int. J. Mol. Sci. 2014;152:2255-2273. https://doi.org/10.3390/ijms15022255
  50. Madigan MT, Martinko JM, Stahl DA, Clark DP. Brock biology of microorganisms. 13th ed. USA: Benjamin Cummings Publishers; 2010. p.14-15
  51. Yeon KM, Cheong WS, Oh HS, et al. Quorum sensing: A new biofouling control paradigm in a membrane bioreactor for advanced wastewater treatment. Environ. Sci. Technol. 2009;432:380-385.
  52. Fuqua C, Winans SC. Conserved cis-acting promoter elements are required for density-dependent transcription of Agrobacterium tumefaciens conjugal transfer genes. J. Bacteriol. 1996;178:435-440. https://doi.org/10.1128/JB.178.2.435-440.1996
  53. Kawaguchi T, Chen YP, Norman RS, Decho AW. Rapid screening of quorum-sensing signal N-Acyl homoserine lactones by an in vitro cell-free assay. Appl. Environ. Microbiol. 2008;74:3667-3671. https://doi.org/10.1128/AEM.02869-07
  54. Hannah R, Stroke I, Betz N. Beta-Glo(R) Assay System: A luminescent $\beta$-galactosidase assay for multiple cell types and media. Cell Note. 2003;6:16-18.
  55. Oh HS, Kim SR, Cheong WS, Lee CH, Lee JK. Biofouling inhibition in MBR by Rhodococcus sp. BH4 isolated from real MBR plant. Appl. Microbiol. Biotechnol. 2013;9723:10223-10231. https://doi.org/10.1007/s00253-013-4933-7
  56. Zhu J, Chai Y, Zhong Z, Li S, Winans SC. Agrobacterium bioassay strain for ultrasensitive detection of N-acylhomoserine lactone-type quorum-sensing molecules: detection of autoinducers in Mesorhizobium huakuii. Appl. Environ. Microbiol. 2003;69:6949-6953. https://doi.org/10.1128/AEM.69.11.6949-6953.2003
  57. Steindler L, Venturi V. Detection of quorum-sensing N-acyl homoserine lactone signal molecules by bacterial biosensors. FEMS Microbiol. Lett. 2006;26:1-9. https://doi.org/10.1016/0378-1097(85)90114-4
  58. Rajamani S, Sayre R. Biosensors for the detection and quantification of AI-2 class quorum-sensing compounds. In: Quorum Sensing. New York: Humana Press; 2018. p. 73-88.
  59. Culhane K, Jiang K, Neumann A, Pinchuk AO. Laser-fabricated plasmonic nanostructures for surface-enhanced Raman spectroscopy of bacteria quorum sensing molecules. MRS Adv. 2017;2:2287-2294. https://doi.org/10.1557/adv.2017.98
  60. Wopperer J, Cardona ST, Huber B, Jacobi CA, Valvano MA, Eberl L. A quorum-quenching approach to investigate the conservation of quorum-sensing-regulated functions within the Burkholderia cepacia complex. Appl. Environ. Microbiol. 2006;72:1579-1587. https://doi.org/10.1128/AEM.72.2.1579-1587.2006
  61. Garcia-Aljaro C, Eberl L, Riedel K, Blanch AR. Detection of quorum-sensing-related molecules in Vibrio scophthalmi. BMC Microbiol. 2008;8:138. https://doi.org/10.1186/1471-2180-8-138
  62. Uroz S, Dessaux Y, Oger P. Quorum sensing and quorum quenching: The yin and yang of bacterial communication. ChemBioChem 2009;10:205-216. https://doi.org/10.1002/cbic.200800521
  63. Whiteley M, Diggle SP, Greenberg EP. Progress in and promise of bacterial quorum sensing research. Nature 2017;551:31-320. https://doi.org/10.1038/551031a
  64. Geske GD, O'Neill JC, Blackwell HE. Expanding dialogues: From natural autoinducers to non-natural analogues that modulate quorum sensing in Gram-negative bacteria. Chem. Soc. Rev. 2008;37:1432-1447. https://doi.org/10.1039/b703021p
  65. Parveen N, Cornell KA. Methylthioadenosine/S-adenosylhomocysteine nucleosidase a critical enzyme for bacterial metabolism. Mol. Microbiol. 2011;79:7-20. https://doi.org/10.1111/j.1365-2958.2010.07455.x
  66. Rasmussen TB, Givskov M. Quorum-sensing inhibitors as anti-pathogenic drugs. Int. J. Med. Microbiol. 2006;152:149-161. https://doi.org/10.1016/j.ijmm.2006.02.005
  67. Dong YH, Xu JL, Li XZ, Zhang LH. AiiA, an enzyme that inactivates the acylhomoserine lactone quorum sensing signal and attenuates the virulence of Erwinia carotovora. Proc. Natl. Acad. Sci. USA 2000;97:3526-3531. https://doi.org/10.1073/pnas.97.7.3526
  68. Dong YH, Wang LH, Xu JL, Zhang HB, Zhang XF, Zhang LH. Quenching quorum-sensing-dependent bacterial infection by an N-acyl homoserine lactonase. Nature 2001;411:813-817. https://doi.org/10.1038/35081101
  69. Leadbetter JR, Greenberg EP. Metabolism of acyl-homoserine lactone quorum-sensing signals by Variovorax paradoxus. J. Bacteriol. 2000;182:6921-6926. https://doi.org/10.1128/JB.182.24.6921-6926.2000
  70. Zhang HB, Wang LH, Zhang LH. Genetic control of quorum-sensing signal turnover in Agrobacterium tumefaciens. Proc. Natl. Acad. Sci. 2002;99:4638-4643. https://doi.org/10.1073/pnas.022056699
  71. Fetzner S. Quorum quenching enzymes. J. Biotechnol. 2015;201:2-14. https://doi.org/10.1016/j.jbiotec.2014.09.001
  72. Kiran GS, Hassan S, Sajayan A, Selvin J. Quorum quenching compounds from natural sources. Bioresour. Bioproc. Biotechnol. 2017;351-364.
  73. Draganov DI, Stetson PL, Watson CE, Billecke SS, La Du BN. Rabbit serum paraoxonase 3 (PON3); is a high density lipoprotein-associated lactonase and protects low density lipoprotein against oxidation. J. Biol. Chem. 2000;275:33435-33442. https://doi.org/10.1074/jbc.M004543200
  74. Teiber JF, Draganov DI, La Du BN. Lactonase and lactonizing activities of human serum paraoxonase (PON1) and rabbit serum PON3. Biol. Chem. Pharmacol. 2003;66:887-896. https://doi.org/10.1016/S0006-2952(03)00401-5
  75. Chun CK, Ozer EA, Welsh MJ, Zabner J, Greenberg EP. Inactivation of pseudomonas aeruginosa quorum sensing signal by human airway epithelia. Proc. Natl. Acad. Sci. USA 2004;101:3587-3590. https://doi.org/10.1073/pnas.0308750101
  76. Chowdhary PK, Keshavan N, Nguyen HQ, Peterson JA, Gonzales JE, Haines DC. Bacillus megaterium CYP102A1 oxidation of acyl homoserine lactones and acyl homoserines. Biol. Chem. 2007;46:14429-14437.
  77. Uroz S, Chabra SR, Camara M, Williams P, Oger P, Dessaux Y. N-acylhomoserine lactone quorum-sensing molecules are modified and degraded by Rhodococcus erythropolis W2 by both amidolytic and novel oxidoreductase activities. Microbiology 2005;151:3313-3322. https://doi.org/10.1099/mic.0.27961-0
  78. Yang F, Wang LH, Wang J, Dong YH, Hu JY, Zhang LH. Quorum quenching enzyme activity is widely conserved in the sera of mammalian species. FEBS Lett. 2005;579:3713-3717. https://doi.org/10.1016/j.febslet.2005.05.060
  79. Gotz C, Fakete A, Gebefuegi I, et al. Uptake, degradation and chiral discrimination of N-acyl-D/L-homoserine lactones by barley (Hordeum vulgare) and yam bean (Pachyrhizus erosus) plants. Anal. Bioanal. Chem. 2007;389:1447-1457. https://doi.org/10.1007/s00216-007-1579-2
  80. Ogawa K, Nakajima-Kambe T, Nakahara T, Kokufuta E. Coimmobilization of gluconolactonase with glucose oxidase for improvement in kinetic property of enzymatically induced volume collapse in ionic gels. Biomacromolecules 2002;3:625-631. https://doi.org/10.1021/bm025512f
  81. Ulrich RL. Quorum quenching: Enzymatic disruption of N-acylhomoserine lactone-mediated bacterial communication in Burkholderia thailandensis. Appl. Environ. Microbiol. 2004;70:6173-6180. https://doi.org/10.1128/AEM.70.10.6173-6180.2004
  82. Dong YH, Gusti AR, Zhang Q, Xu JL, Zhang LH. Identification of quorum-quenching N-acyl homoserine lactonases from Bacillus species. Appl. Environ. Microbiol. 2002;68:1754-1759. https://doi.org/10.1128/AEM.68.4.1754-1759.2002
  83. Carlier A, Uroz S, Smadja B, et al. The Ti plasmid of Agrobacterium tumefaciens harbors an attM-Paralogous gene, aiiB, also encoding N-acyl homoserine lactonase activity. Appl. Environ. Microbiol. 2003;69:4989-4993. https://doi.org/10.1128/AEM.69.8.4989-4993.2003
  84. Liu D, Thomas PW, Momb J, et al. Structure and specificity of a quorum-quenching lactonase (AiiB) from Agrobacterium tumefaciens. Biochemistry 2007;46:11789-11799. https://doi.org/10.1021/bi7012849
  85. Chow JY, Xue B, Lee KH, et al. Directed evolution of a thermostable quorum-quenching lactonase from the amidohydrolase superfamily. J. Biol. Chem. 2010;285:40911-40920. https://doi.org/10.1074/jbc.M110.177139
  86. Wang WZ, Morohoshi T, Ikenoya M, Someya N, Ikeda T. AiiM, a novel class of N-acylhomoserine lactonase from the leaf-associated bacterium microbacterium testaceum. Appl. Environ. Microbiol. 2010;76:2524-2530. https://doi.org/10.1128/AEM.02738-09
  87. Chow JY, Wu L, Yew WS. Directed evolution of a quorum-quenching lactonase from Mycobacterium avium sub sp. paratuberculosis K-10 in the amidohydrolase superfamily. Biochemistry 2009;48:4344-4353. https://doi.org/10.1021/bi9004045
  88. Afriat L, Roodveldt C, Manco G, Tawfik DS. The latent promiscuity of newly identified microbial lactonases is linked to a recently diverged phosphotriesterase. Biochemistry 2006;45:13677-13686. https://doi.org/10.1021/bi061268r
  89. Mei GY, Yan XX, Turak A, Luo ZQ, Zhang LQ. AidH, an alpha/beta-hydrolase fold family member from an Ochrobactrum sp. strain is a novel N-acylhomoserine lactonase. Appl. Environ. Microbiol. 2010;76:4933-4942. https://doi.org/10.1128/AEM.00477-10
  90. Morohoshi T, Tominaga Y, Someya N, Ikeda T. Complete genome sequence and characterization of the N-acylhomoserine lactone-degrading gene of the potato leaf-associated solibacillus silvestris. J. Biosci. Bioeng. 2012;113:20-25. https://doi.org/10.1016/j.jbiosc.2011.09.006
  91. Merone L, Mandrich L, Rossi M, Manco G. A thermostable phosphotriesterase from the archaeon sulfolobus solfataricus: Cloning overexpression and properties. Extremophiles 2005;9:297-305. https://doi.org/10.1007/s00792-005-0445-4
  92. Elias M, Dupuy J, Merone L, et al. Structural basis for natural lactonase and promiscuous phosphotriesterase activities. J. Mol. Biol. 2008;379:1017-1028. https://doi.org/10.1016/j.jmb.2008.04.022
  93. Uroz S, Oger PM, Chapelle E, Adeline MT, Faure D, Dessaux Y. A Rhodococcus qsdA-encoded enzyme defines a novel class of large-spectrum quorum-quenching lactonases. Appl. Environ. Microbiol. 2008;74:1357-1366. https://doi.org/10.1128/AEM.02014-07
  94. Riaz K, Elmerich C, Moreira D, Raffoux A, Dessaux Y, Faure D. A metagenomic analysis of soil bacteria extends the diversity of quorum-quenching lactonases. Environ. Microbiol. 2008;10:560-570. https://doi.org/10.1111/j.1462-2920.2007.01475.x
  95. Park SY, Lee SJ, Oh TK, et al. AhlD, an N-acylhomoserine lactonase in Arthrobacter sp., and predicted homologues in other bacteria. Microbiology 2003;149:1541-1550. https://doi.org/10.1099/mic.0.26269-0
  96. Park SY, Hwang BJ, Shin MH, Kim JA, Kim HK, Lee JK. N-acylhomoserine lactonase-producing Rhodococcus spp. with different AHL-degrading activities. FEMS Microbiol. Lett. 2006;261:102-108. https://doi.org/10.1111/j.1574-6968.2006.00336.x
  97. Lynch MJ, Swift S, Kirke DF, Keevil CW, Dodd CE, Williams P. The regulation of biofilm development by quorum sensing in Aeromonas hydrophila. Environ. Microbiol. 2002;4:18-28. https://doi.org/10.1046/j.1462-2920.2002.00264.x
  98. Paul D, Kim YS, Ponnusamy K, Kwon JH. Application of quorum quenching to inhibit biofilm formation. Environ. Eng. Sci. 2009;26:1319-1324. https://doi.org/10.1089/ees.2008.0392
  99. Sauer K, Camper AK. Characterization of phenotypic changes in Pseudomonas putida in response to surface associated growth. J. Bacteriol. 2001;183:6579-6589. https://doi.org/10.1128/JB.183.22.6579-6589.2001
  100. Xu F, Byun T, Deussen HJ, Duke KR. Degradation of N-acylhomoserine lactones the bacterial quorum sensing molecules by acylase. J. Biotechnol. 2003;101:89-96. https://doi.org/10.1016/S0168-1656(02)00305-X
  101. Kim SR, Oh HS, Jo SJ, et al. Biofouling control with bead-entrapped quorum quenching bacteria in membrane bioreactors: Physical and biological effects. Environ. Sci. Technol. 2013;472:836-842.
  102. Yeon KM, Lee CH, Kim J. Magnetic enzyme carrier for effective biofouling control in the membrane bioreactor based on enzymatic quorum quenching. Environ. Sci. Technol. 2009;43:7403-7409. https://doi.org/10.1021/es901323k
  103. Lin YH, Xu JL, Hu J, et al. Acyl‐homoserine lactone acylase from Ralstonia strain XJ12B represents a novel and potent class of quorum‐quenching enzymes. Mol. Microbiol. 2003;47:849-860. https://doi.org/10.1046/j.1365-2958.2003.03351.x
  104. Romero M, Diggle SP, Heeb S, Camara M, Otero A. Quorum quenching activity in Anabaena sp. PCC 7120: Identification of AiiC a novel AHL-acylase. FEMS Microbiol. Lett. 2008;280:73-80. https://doi.org/10.1111/j.1574-6968.2007.01046.x
  105. Huang JJ, Han JI, Zhang LH, Leadbetter JR. Utilization of acyl-homoserine lactone quorum signals for growth by a soil pseudomonad and Pseudomonas aeruginosa PAO1. Appl. Environ. Microbiol. 2003;69:5941-5949. https://doi.org/10.1128/AEM.69.10.5941-5949.2003
  106. Sio CF, Otten LG, Cool RH, et al. Quorum quenching by an N-acyl-homoserine lactone acylase from Pseudomonas aeruginosa PAO1. Infect. Immun. 2006;74:1673-1682. https://doi.org/10.1128/IAI.74.3.1673-1682.2006
  107. Shepherd RW, Lindow SE. Two dissimilar N-acyl-homoserine lactone acylases of Pseudomonas syringae influence colony and biofilm morphology. Appl. Environ. Microbiol. 2009;75:45-53. https://doi.org/10.1128/AEM.01723-08
  108. Chen CN, Chen CJ, Liao CT, Lee CY. A probable aculeacin A acylase from the ralstonia solanacearum GMI1000 is N-acyl-homoserine lactone acylase with quorum quenching activity. BMC Microbiol. 2009;9:89. https://doi.org/10.1186/1471-2180-9-89
  109. Morohoshi T, Nakazawa S, Ebata A, Kato N, Ikeda T. Identification and characterization of N-acylhomoserine lactone-acylase from the fish intestinal Shewanella sp. strain MIB015. Biosci. Biotechnol. Biochem. 2008;72:1887-1893. https://doi.org/10.1271/bbb.80139
  110. Park SY, Kang HO, Jang HS, Lee JK, Koo BT, Yum DY. Identification of extracellular N-acylhomoserine lactone acylase from a Streptomyces sp. and its application to quorum quenching. Appl. Environ. Microbiol. 2005;71:2632-2641. https://doi.org/10.1128/AEM.71.5.2632-2641.2005
  111. Chan KG, Atkinson S, Mathee K, et al. Characterization of N-acylhomoserine lactone-degrading bacteria associated with the zingiber officinale ginger; rhizosphere: Co-existence of quorum quenching and quorum sensing in Acinetobacter and Burkholderia. BMC Microbiol. 2011;11:51. https://doi.org/10.1186/1471-2180-11-51
  112. Cheong WS, Lee CH, Moon YH, et al. Isolation and identification of indigenous quorum quenching bacteria pseudomonas sp. 1A1 for biofouling control in MBR. Ind. Eng. Chem. Res. 2013;52:10554-10560. https://doi.org/10.1021/ie303146f
  113. Uroz S, Oger P, Chhabra SR, Camara M, Williams P, Dessaux Y. N-acyl homoserine lactones are degraded via an amidolytic activity in Comamonas sp. strain D1. Arch. Microbiol. 2006;187:249-256. https://doi.org/10.1007/s00203-006-0186-5
  114. Lithgow JK, Wilkinson A, Hardman A, et al. The regulatory locus cinRI in Rhizobium leguminosarum controls a network of quorum-sensing loci. Mol. Microbiol. 2000;37:81-97. https://doi.org/10.1046/j.1365-2958.2000.01960.x
  115. Bassler BL, Losick R. Bacterially speaking. Cell 2006;125:237-246. https://doi.org/10.1016/j.cell.2006.04.001
  116. Koch B, Liljefors T, Persson T, Nielsen J, Kjelleberg S, Givskov M. The LuxR Receptor: The sites of interaction with quorum-sensing signals and inhibitors. Microbiology 2005;151:3589-3602. https://doi.org/10.1099/mic.0.27954-0
  117. Chen G, Swern LR, Swern DL, et al. A strategy for antagonizing quorum sensing. Mol. Cell 2011;42:199-209. https://doi.org/10.1016/j.molcel.2011.04.003
  118. Jimenez PN, Koch G, Thompson JA, Xavier KB, Cool RH, Quax WJ. The multiple signaling systems regulating virulence in pseudomonas aeruginosa. Microbiol. Molecul. Bio. Rev. 2012;76:46-65. https://doi.org/10.1128/MMBR.05007-11
  119. Kim JH, Choi DC, Yeon KM, Kim SR, Lee CH. Enzyme-immobilized nanofiltration membrane to mitigate biofouling based on quorum quenching. Environ. Sci. Technol. 2011;45:1601-1607. https://doi.org/10.1021/es103483j
  120. Oh HS, Yeon KM, Yang CS, et al. Control of membrane biofouling in MBR for wastewater treatment by quorum quenching bacteria encapsulated in microporous membrane. Environ. Sci. Technol. 2012;46:4877-4884. https://doi.org/10.1021/es204312u
  121. Jahangir D, Oh HS, Kim SR, Park PK, Lee CH, Lee JK. Specific location of encapsulated quorum quenching bacteria for biofouling control in an external submerged membrane bioreactor. J. Membr. Sci. 2012;411-412,130-136. https://doi.org/10.1016/j.memsci.2012.04.022
  122. Cheong WS, Kim SR, Oh HS, et al. Design of quorum quenching microbial vessel to enhance cell viability for biofouling control in membrane bioreactor. J. Microbiol. Biotechnol. 2014;24:97-105. https://doi.org/10.4014/jmb.1311.11008
  123. Kose-Mutlu B, Ergon-Can T, Koyuncu I, Lee CH. Quorum quenching MBR operations for biofouling control under different operation conditions and using different immobilization media. Desalin. Water Treat. 2015;17696-17706.
  124. Lee B, Yeon KM, Shim J, et al. Effective antifouling using quorum-quenching acylase stabilized in magnetically- separable mesoporous silica. Biomacromolecules 2014;15:1153-1159. https://doi.org/10.1021/bm401595q
  125. Kim SR, Lee KB, Kim JE, et al. Macroencapsulation of quorum quenching bacteria by polymeric membrane layer and its application to MBR for biofouling control. J. Membr. Sci. 2015;437:109-117.
  126. Lee KB, Lee SK, Lee SH, et al. Fungal quorum quenching: A paradigm shift for energy savings in membrane bioreactor (MBR) for wastewater treatment. Environ. Sci. Technol. 2016;50:10914-10922. https://doi.org/10.1021/acs.est.6b00313
  127. Lee SK, Lee SH, Lee KB, et al. Effect of shape and size of quorum quenching medium on biofouling control in membrane bioreactors for wastewater treatment. J. Microbiol. Biotechnol. 2016;26:1746-1754. https://doi.org/10.4014/jmb.1605.05021
  128. Lee SH, Lee S, Lee K, et al. More efficient media design for enhanced biofouling control in a membrane bioreactor: quorum quenching bacteria entrapping hollow cylinder. Environ. Sci. Technol. 2016;50:8596-8604. https://doi.org/10.1021/acs.est.6b01221
  129. Nahm CH, Choi DC, Kwon H, et al. Application of quorum quenching bacteria entrapping sheets to enhance biofouling control in a membrane bioreactor with a hollow fiber module. J. Membr. Sci. 2017;526:264-271. https://doi.org/10.1016/j.memsci.2016.12.046
  130. Lee J, Lee I, Nam J, Hwang DS, Yeon KM, Kim J. Immobilization and stabilization of acylase on carboxylated polyaniline nanofibers for highly effective antifouling application via quorum quenching. ACS Appl. Mater. Interf. 2017;9:15424-15432. https://doi.org/10.1021/acsami.7b01528
  131. Hong KW, Koh CL, Sam CK, Yin WF, Chan KG. Quorum quenching revisited-from signal decays to signalling confusion. Sensors. 2012;12:4661-4696. https://doi.org/10.3390/s120404661
  132. Patankar AV, Gonzalez JE. Orphan LuxR regulators of quorum sensing. FEMS Microbiol. Rev. 2009;33:739-756. https://doi.org/10.1111/j.1574-6976.2009.00163.x
  133. Sandoz KM, Mitzimberg SM, Schuster M. Social cheating in Pseudomonas aeruginosa quorum sensing. Proceed. Nat. Acad. Sci. 2007;104:15876-15881. https://doi.org/10.1073/pnas.0705653104
  134. Beatson SA, Whitchurch CB, Semmler AB, Mattick JS. Quorum sensing is not required for twitching motility in Pseudomonas aeruginosa. J. Bacteriol. 2002;184:3598-3604. https://doi.org/10.1128/JB.184.13.3598-3604.2002
  135. Choi Y, Park HY, Park SJ, et al. Growth phase-differential quorum sensing regulation of anthranilate metabolism in pseudomonas aeruginosa. Mol. Cell. 2011;32:57-65. https://doi.org/10.1007/s10059-011-2322-6
  136. Bardill JP, Zhao X, Hammer BK. The Vibrio cholerae quorum sensing response is mediated by Hfq‐dependent sRNA/mRNA base pairing interactions. Mol. Microbiol. 2011;80:1381-1394. https://doi.org/10.1111/j.1365-2958.2011.07655.x
  137. Defoirdt T, Boon N, Bossier P. Can bacteria evolve resistance to quorum sensing disruption? PLoS Pathogens. 2010;6, e1000989. https://doi.org/10.1371/journal.ppat.1000989
  138. Estrela AB, Abraham WR. Combining biofilm-controlling compounds and antibiotics as a promising new way to control biofilm infections. Pharmaceuticals 2010;3:1374-1393. https://doi.org/10.3390/ph3051374
  139. Clatworthy AE, Pierson E, Hung DT. Targeting virulence: A new paradigm for antimicrobial therapy. Nat. Chem. Biol. 2007;3:541-548. https://doi.org/10.1038/nchembio.2007.24
  140. Kalia VC. Quorum sensing and its biotechnological applications. Springer Nature; 2018. p. 119-131.
  141. Ran T, Zhou CS, Xu LW, et al. Initial detection of the quorum sensing autoinducer activity in the rumen of goats in vivo and in vitro. J. Integ. Agri. 2016;15:2343-2352. https://doi.org/10.1016/S2095-3119(16)61417-X

Cited by

  1. In situ versus pre-quorum quenching of microbial signaling for enhanced biofouling control in membrane bioreactors vol.592, 2019, https://doi.org/10.1016/j.memsci.2019.117387
  2. Regulatory Mechanisms and Promising Applications of Quorum Sensing-Inhibiting Agents in Control of Bacterial Biofilm Formation vol.11, 2019, https://doi.org/10.3389/fmicb.2020.589640
  3. Impact of Encapsulated Quorum-Quenching Bacterial Dose and Feed Type on Biofouling Control in Membrane Bioreactors vol.146, pp.2, 2019, https://doi.org/10.1061/(asce)ee.1943-7870.0001640
  4. Application of cell entrapping beads for Quorum Quenching technique in submerged membrane bioreactor vol.81, pp.4, 2019, https://doi.org/10.2166/wst.2020.149
  5. Hydrodynamics Characterization of the Impact of Free-Moving Particles in an Air-Lift Membrane Bioreactor vol.59, pp.16, 2019, https://doi.org/10.1021/acs.iecr.9b06749
  6. A brief review of anaerobic membrane bioreactors emphasizing recent advancements, fouling issues and future perspectives vol.270, 2019, https://doi.org/10.1016/j.jenvman.2020.110909
  7. Recent developments in social network disruption approaches to manage bacterial plant diseases vol.150, 2020, https://doi.org/10.1016/j.biocontrol.2020.104376
  8. Bacterial Biofilm Inhibition: A Focused Review on Recent Therapeutic Strategies for Combating the Biofilm Mediated Infections vol.12, 2019, https://doi.org/10.3389/fmicb.2021.676458
  9. Industrial Cooling Systems and Antibiofouling Strategies: A Comprehensive Review vol.60, pp.8, 2019, https://doi.org/10.1021/acs.iecr.0c05985
  10. A review of the current in-situ fouling control strategies in MBR: Biological versus physicochemical vol.98, 2021, https://doi.org/10.1016/j.jiec.2021.03.042
  11. A review of the current in-situ fouling control strategies in MBR: Biological versus physicochemical vol.98, 2021, https://doi.org/10.1016/j.jiec.2021.03.042
  12. Novel Bifunctional Acylase from Actinoplanes utahensis: A Versatile Enzyme to Synthesize Antimicrobial Compounds and Use in Quorum Quenching Processes vol.10, pp.8, 2021, https://doi.org/10.3390/antibiotics10080922
  13. Quorum sensing in synthetic biology: A review vol.28, 2019, https://doi.org/10.1016/j.coisb.2021.100378
  14. Silt density index as a fouling propensity parameter of various membrane materials using dissolved organic matter vol.44, 2021, https://doi.org/10.1016/j.jwpe.2021.102391
  15. Quorum quenching, biological characteristics, and microbial community dynamics as key factors for combating fouling of membrane bioreactors vol.4, pp.1, 2021, https://doi.org/10.1038/s41545-021-00110-9
  16. Mitigation of membrane biofouling using quorum-quenching bacteria in a continuously operated membrane bioreactor vol.166, 2019, https://doi.org/10.1016/j.ibiod.2021.105339
  17. Live membrane filters with immobilized quorum quenching bacterial strains for anti-biofouling vol.641, 2019, https://doi.org/10.1016/j.memsci.2021.119895
  18. Quorum quenching strategy for biofouling control in membrane photobioreactor vol.288, pp.p3, 2022, https://doi.org/10.1016/j.chemosphere.2021.132667
  19. Enzyme-based control of membrane biofouling for water and wastewater purification: A comprehensive review vol.25, 2019, https://doi.org/10.1016/j.eti.2021.102106