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Bacterial Quorum Sensing and Quorum Quenching for the Inhibition of Biofilm Formation

박테리아의 Quorum Sensing 및 생물막 형성 억제를 위한 Quorum Quenching 연구 동향

  • Lee, Jung-Kee (Department of Biomedicinal Science & Biotechnology, Paichai University)
  • 이정기 (배재대학교 바이오.의생명공학과)
  • Received : 2012.05.11
  • Accepted : 2012.06.11
  • Published : 2012.06.28

Abstract

Quorum sensing (QS) is a cell-to-cell communication system, which is used by many bacteria to regulate diverse gene expression in response to changes in population density. Bacteria recognize the differences in cell density by sensing the concentration of signal molecules such as N-acyl-homoserine lactones (AHL) and autoinducer-2 (AI-2). In particular, QS plays a key role in biofilm formation, which is a specific bacterial group behavior. Biofilms are dense aggregates of packed microbial communities that grow on surfaces, and are embedded in a self-produced matrix of extracellular polymeric substances (EPS). QS regulates biofilm dispersal as well as the production of EPS. In some bacteria, biofilm formations are regulated by c-di-GMP-mediated signaling as well as QS, thus the two signaling systems are mutually connected. Biofilms are one of the major virulence factors in pathogenic bacteria. In addition, they cause numerous problems in industrial fields, such as the biofouling of pipes, tanks and membrane bioreactors (MBR). Therefore, the interference of QS, referred to as quorum quenching (QQ) has received a great deal of attention. To inhibit biofilm formation, several strategies to disrupt bacterial QS have been reported, and many enzymes which can degrade or modify the signal molecule AHL have been studied. QQ enzymes, such as AHL-lactonase, AHL-acylase, and oxidoreductases may offer great potential for the effective control of biofilm formation and membrane biofouling in the future. This review describes the process of bacterial QS, biofilm formation, and the close relationship between them. Finally, QQ enzymes and their applications for the reduction of biofouling are also discussed.

본 총설은 N-acyl-homoserine lactone (AHL)에 기반한 quorum sensing(QS)을 비롯한 다양한 QS 시스템 및 생물막 형성과의 관련성에 대한 연구 동향을 정리하였다. 또한 anti-QS으로서 quorum quenching 전략을 이용한 생물막 억제 연구 동향에 대해 중점적으로 서술하였다. 세균의 독특한 신호전달 체계인 QS는 AHL과 같은 특정한 신호분자의 농도에 의해 세균의 집단적 행동 양식이 결정되는 세포밀도-의존성 유전자 발현 조절 메커니즘이다. QS 시스템은 미생물의 부착 및 생물막 형성에 있어 중요한 역할을 한다. AI-1이나 AI-2에 의한 QS는 생물막 형성 과정에 필요한 세포외 다당류, 단백질, 세포 외 DNA 등 주요한 구성 성분 등의 생산뿐만 아니라, 세균의 운동성 조절, 부착, 생물막 해체 과정까지도 조절하는 기능을 한다. 일부 세균의 경우 QS시스템 이외에도 second messenger로 알려진 c-di-GMP에 의한 signaling이 QS와 서로 연결되어 생물막 형성이나 병독성과 같은 타깃들을 함께 조절한다. 생물막은 병원성 세균에 의한 감염 시 여러 가지 병독성 가운데 가장 중요한 요소 중 하나이기 때문에, 생물막 형성을 조절하는 QS를 차단하기 위한 다양한 anti-quorum sensing 전략이 연구되고 있다. Anti-QS 접근 방식은 의학적 이용뿐만 아니라 물에 노출되어있는 MBR을 비롯한 많은 산업적 장치 등에서 생물막 형성으로 인한 손상 및 오염을 방지하기 위해 쓰일 수 있다. Anti-QS 전략 중 신호분자인 AHL을 무력화 시키는 quorum quenching 효소(AHL-lactonase, AHL-acylase, oxidoreductas)를 이용하여 생물막 형성을 억제할 수 있으며, 막을 이용한 수처리 공정에서 막에 발생하는 biofouling을 완화시킬 수 있는 새로운 anti-fouling 처리 기술로서 이러한 QQ 효소의적용 가능성을 보여 주고 있다.

Keywords

References

  1. Aguilar, C., A. Carlier, K. Riedel, and L. Eberl. 2010. Cell-cell communication in biofilms of Gram-Negative bacteria. p. 23-40. In R. Kramer, and K. Jung (eds.), Bacterial Signaling, WILEY-VCH.
  2. Allesen-Holm, M., K. B. Barken, L. Yang, M. Klausen, J. S. Webb, S. Kjelleberg, S. Molin, M. Givskov, and T. Tolker-Nielsen. 2006. A characterization of DNA release in Pseudomonas aeruginosa and biofilms. Mol. Microbiol. 59: 1114-1128. https://doi.org/10.1111/j.1365-2958.2005.05008.x
  3. Bainton, N. J., P. Stead, S. R. Chhabra, B. W. Bycroft, G. P. Salmond, G. S. Stewart, and P. Williams. 1992. N-(3-oxohexanoyl)-L-homoserine lactone regulates carbapenem antibiotic production in Erwinia carotovora. Biochem. J. 288: 997-1004. https://doi.org/10.1042/bj2880997
  4. Barrios, A. F. G., R. J. Zuo, Y. Hashimoto, L. Yang, W. E. Bentley, T. K. Wood. 2006. Autoinducer 2 controls biofilm formation in Escherichia coli through a novel motility quorum-sensing regulator (MqsR, B3022). J. Bacteriol. 188: 305-3116. https://doi.org/10.1128/JB.188.1.305-316.2006
  5. Bassler, B. L., M. Wright, R. E. Showalter, and M. R. Silverman. 1993. Intercellular signalling in Vibrio harveyi: sequence and function of genes regulating expression of luminescence. Mol. Microbiol. 9: 773-786. https://doi.org/10.1111/j.1365-2958.1993.tb01737.x
  6. Bokhove, M., P. N. Jimenez, W. J. Quax, and B. W. Dijkstra. 2010. The quorum-quenching N-acyl homoserine lactone acylase PvdQ is an Ntn-hydrolase with an unusual substrate-binding pocket. Proc. Natl. Acad. Sci. USA 107: 686-691. https://doi.org/10.1073/pnas.0911839107
  7. Boles, B. R., M. Thoendel, and P. K. Singh. 2005. Rhamnolipids mediated detachment of Pseudomonas aeruginosa from biofilms. Mol. Microbiol. 57: 1210-1223. https://doi.org/10.1111/j.1365-2958.2005.04743.x
  8. Camps, J., I. Pujol, F. Ballester, J. Joven, and J. M. Simo. 2011. Paraoxonases as potential antibiofilm agents: Their relationship with quorum-sensing signals in Gram-negative bacteria. Antimicrob. Agents Chemother. 55: 1325-1331. https://doi.org/10.1128/AAC.01502-10
  9. Chen, X., S. Schauder, N. Potier, A. Van Dorsselaer, I. Pelczer, B. L. Bassler, and F. M. Hughson. 2002. Structural identification of a bacterial quorum-sensing signal containing boron. Nature 415: 545-549. https://doi.org/10.1038/415545a
  10. Choudhary, S., and C. Schmidt-Dannert. 2010. Applications of quorum sensing in biotechnology. Appl. Microbiol. Biotechnol. 86: 1267-1279. https://doi.org/10.1007/s00253-010-2521-7
  11. Chow, J. Y., L. Wu, and W. S. Yew. 2009. Directed evolution of a quorum-quenching lactonase from Mycobacterium avium subsp. paratuberculosis K-10 in the amidohydrolase superfamily. Biochemistry 48: 4344-4353. https://doi.org/10.1021/bi9004045
  12. Chowdhary, P. K., N. Keshavan, H. Q. Nguyen, J. A. Peterson, J. E. Gonzalez, and D. C. Haines. 2007. Bacillus megaterium CYP102A1 oxidation of acyl homoserine lactones and acyl homoserines. Biochemistry 46: 14429-14437. https://doi.org/10.1021/bi701945j
  13. Cotter, P. A. and S. Stibitz. 2007. c-di-GMP-mediated regulation of virulence and biofilm formation. Curr. Opin. Microbiol. 10: 17-23. https://doi.org/10.1016/j.mib.2006.12.006
  14. Davies, D. 2003. Understanding biofilm resistance to antibacterial agents. Nat. Rev. Drug Discov. 2: 114-122. https://doi.org/10.1038/nrd1008
  15. Davies, D. G., M. R. Parsek, J. P. Pearson, B. H. Iglewski, J. W. Costerton, and E. P. Greenberg. 1998. The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 280: 295-298. https://doi.org/10.1126/science.280.5361.295
  16. Dickschat, J. S. 2010. Quorum sensing and bacterial biofilms. Nat. Prod. Rep. 27: 343-369. https://doi.org/10.1039/b804469b
  17. Dobretsov, S., M. Teplitski, and V. Paul. 2009. Mini-review: quorum sensing in the marine environment and its relationship to biofouling. Biofouling 25: 413-427. https://doi.org/10.1080/08927010902853516
  18. Dong, Y. H., J. L. Xu, X. Z. Li, and L. H. Zhang. 2000. AiiA, an enzyme that inactivates the acylhomoserine lactone quorum-sensing signal and attenuates the virulence of Erwinia carotovora. Proc. Natl. Acad. Sci. USA 97: 3526-3531. https://doi.org/10.1073/pnas.97.7.3526
  19. Dong, Y. H., L. H. Wang, J. L. Xu, H. B. Zhang, X. F. Zhang, and L. H. Zhang. 2001. Quenching quorum-sensing-dependent bacterial infection by an N-acyl homoserine lactonase. Nature 411: 813-817. https://doi.org/10.1038/35081101
  20. Flemming, H. C., T. R. Neu, and D. J. Wozniak. 2007. The EPS Matrix: The "House of Biofilm Cells". J. Bacteriol. 189: 7945-7947. https://doi.org/10.1128/JB.00858-07
  21. Fuqua, W. C., S. C. Winans, and E. P. Greenberg. 1994. Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators. J. Bacteriol. 176: 269-275. https://doi.org/10.1128/jb.176.2.269-275.1994
  22. Fux, C. A., P. Stoodley, L. Hall-Stoodley, and J. W. Costerton. 2003. Bacterial biofilms: a diagnostic and therapeutic challenge. Expert Rev. Anti Infect. Ther. 1: 667-683. https://doi.org/10.1586/14787210.1.4.667
  23. Hall-Stoodley, L., J. W. Costerton, and P. Stoodley. 2004. Bacterial biofilms: From the natural environment to infectious diseases. Nat. Rev. Microbiol. 2: 95-108. https://doi.org/10.1038/nrmicro821
  24. Hammer, B., and B. L. Bassler. 2008. Signal integration in the Vibrio Harveyi and Vibrio cholerae quorum-sensing circuits. p. 323-332. In S. C. Winans and B. L. Bassler (eds.), Chemical Communication Among Bacteria, ASM Press, USA.
  25. Hentzer, M, K. Riedel, T. B. Rasmussen, A. Heydorn, J. B. Anderson, M. R. Parsek, S. A. Rice, L. Eberl, S. Molin, N. Hoiby, S. Kjelleberg, and M. Givskov. 2002. Inhibition of quorum sensing in Pseudomonas aeruginosa biofilm bacteria by a halogenated furanone compound. Microbiology 148: 87-101. https://doi.org/10.1099/00221287-148-1-87
  26. Hong, S. H., M. Hegde, J. Kim, X. Wang, A. Jayaraman, and T. K. Wood. 2012. Synthetic quorum-sensing circuit to control consortial biofilm formation and dispersal in a microfluidic device. Nat. Commun. 3: 613. doi: 10.1038/ncomms1616.
  27. Huang J. J., A. Petersen, M. Whiteley, and J. R. Leadbetter. 2006. Identification of QuiP, the product of gene PA1032, as the second acyl-homoserine lactone acylase of Pseudomonas aeruginosa PAO1. Appl. Environ. Microbiol. 72: 1190-1197. https://doi.org/10.1128/AEM.72.2.1190-1197.2006
  28. Jenal, U. 2004. Cyclic di-guanosine-monophosphate comes of age: a novel secondary messenger involved in modulating cell surface structures in bacteria? Curr. Opin. Microbiol. 7: 185-191. https://doi.org/10.1016/j.mib.2004.02.007
  29. Jiang, P., L. Jingbao, F. Han, G. Duan, X. Lu, Y. Gu, and W. Yu. 2011. Antibiofilm activity of exopolysaccharide from marine bacterium Vibrio sp. QY101. PLoS ONE 6: e18514. https://doi.org/10.1371/journal.pone.0018514
  30. Kalia, V. C., S. C. Raju, and H. J. Purohit. 2011. Genomic analysis reveals versatile organisms for quorum quenching enzymes: Acyl-homoserine lactone-acylase and -lactonase. Open Microbiol. J. 5: 1-13.
  31. Kappachery, S., D. Paul, J. Yoon, and J. H. Kweon. 2010. Vanillin, a potential agent to prevent biofouling of reverse osmosis membrane. Biofouling 26: 667-672. https://doi.org/10.1080/08927014.2010.506573
  32. de Kievit, T. R., and B. H. Iglewski. 2000. Bacterial quorum sensing in pathogenic relationships. Infect. Immun. 68: 4839-4849. https://doi.org/10.1128/IAI.68.9.4839-4849.2000
  33. Kim, M. H., W. C. Choi, H. O. Kang, J. S. Lee, B. S. Kang, K. J. Kim, Z. S. Derewenda, T. K. Oh, C. H. Lee, and J. K. Lee. 2005. The molecular structure and catalytic mechanism of a quorum-quenching N-acyl-L-homoserine lactone hydrolase. Proc. Natl. Acad. Sci. USA 102: 17606-17611. https://doi.org/10.1073/pnas.0504996102
  34. Kjelleberg, S. and S. Molin. 2002. Is there a role for quorum sensing signals in bacterial biofilms? Curr. Opin. Microbiol. 5: 254-258. https://doi.org/10.1016/S1369-5274(02)00325-9
  35. Landini P., D. Antoniani, J. G. Burgess, and R. Nijland. 2010. Molecular mechanisms of compounds affecting bacterial biofilm formation and dispersal. Appl. Microbiol. Biotechnol. 86: 813-823. https://doi.org/10.1007/s00253-010-2468-8
  36. Lazar, V. 2011. Quorum sensing in biofilms - How to destroy the bacterial citadels or their cohesion/power? Anaerobe 17: 280-285. https://doi.org/10.1016/j.anaerobe.2011.03.023
  37. Lee, S. J., S. Y. Park, J. J. Lee, D. Y. Yum, B. T. Koo, and J. K. Lee. 2002. Genes encoding the N-Acyl homoserine lactonedegrading enzyme are widespread in many subspecies of Bacillus thuringiensis. Appl. Environ. Microbiol. 68: 3919-3924. https://doi.org/10.1128/AEM.68.8.3919-3924.2002
  38. Lin Y. H., J. L. Xu, J. Hu, L. H. Wang, S. L. Ong, J. R. Leadbetter, and L. H. Zhang. 2003. Acyl-homoserine lactone acylase from Ralstonia strain XJ12B represents a novel and potent class of quorum-quenching enzymes. Mol. Microbiol. 47: 849-860. https://doi.org/10.1046/j.1365-2958.2003.03351.x
  39. Manefield, M., T. B. Rasmussen, M. Henzter, J. B. Andersen, P. Steinberg, S. Kjelleberg, and M. Givskov. 2002. Halogenated furanones inhibit quorum sensing through accelerated LuxR turnover. Microbiology 148: 1119-1127. https://doi.org/10.1099/00221287-148-4-1119
  40. Medina G., K. Juarez, and G. Soberan-Chavez. 2003. The Pseudomonas aeruginosa rhlAB operon is not expressed during the logarithmic phase of growth even in the presence of its activator RhlR and the autoinducer N-butyryl-homoserine lactone. J. Bacteriol. 185: 377-380. https://doi.org/10.1128/JB.185.1.377-380.2003
  41. Mei, G. Y., X. X. Yan, A. Turak, Z. Q. Luo, and L. Q. Zhang. 2010. AidH, an alpha/beta-hydrolase fold family member from an Ochrobactrum sp. strain, is a novel N-acylhomoserine lactonase. Appl. Environ. Microbiol. 76: 4933-4942. https://doi.org/10.1128/AEM.00477-10
  42. Miller, M. B., and B. L. Bassler. 2001. Quorum sensing in bacteria. Annu. Rev. Microbiol. 55: 165-199. https://doi.org/10.1146/annurev.micro.55.1.165
  43. Momb, J., D. W. Yoon, and W. Fast. 2010. Enzymic disruption of N-aroyl-L-homoserine lactone-based quorum sensing. ChemBioChem 11: 1535-1537. https://doi.org/10.1002/cbic.201000191
  44. Nadell, C. D., J. B. Xavier, and K. R. Foster. 2009. The sociobiology of biofilms. FEMS Microbiol. Rev. 33: 206-224. https://doi.org/10.1111/j.1574-6976.2008.00150.x
  45. Natrah, F. M., T. Defoirdt, P. Sorgeloos, and P. Bossier. 2011. Disruption of bacterial cell-to-cell communication by marine organisms and its relevance to aquaculture. Mar. Biotechnol. 13: 109-126. https://doi.org/10.1007/s10126-010-9346-3
  46. Nealson, K. H., and J. W. Hastings. 1979. Bacterial bioluminescence: its control and ecological significance. Microbiol. Rev. 43: 496-518.
  47. Ng, F. S., D. M. Wright, and S. Y. Seah. 2011. Characterization of a phosphotriesterase-like lactonase from Sulfolobus solfataricus and its immobilization for disruption of quorum sensing. Appl. Environ. Microbiol. 77: 1181-1186. https://doi.org/10.1128/AEM.01642-10
  48. Oh, H. S., K. M. Yeon, C. S. Yang, S. R. Kim, C. H. Lee, S. Y. Park, J. Y. Han, and J. K. Lee. 2012. Control of membrane biofouling in MBR for wastewater treatment by quorum quenching bacteria encapsulated in microporous membrane. Environ. Sci. Technol. 46: 4877-4884. https://doi.org/10.1021/es204312u
  49. Park, S. Y., S. J. Lee, T. K. Oh, J. W. Oh, B. T. Koo, D. Y. Yum, and J. K. Lee. 2003. AhlD, an N-acylhomoserine lactonase in Arthrobacter sp., and predicted homologues in other bacteria. Microbiology 149: 1541-1550. https://doi.org/10.1099/mic.0.26269-0
  50. Park, S. Y., H. O. Kang, H. S. Jang, J. K. Lee, B. T. Koo, and D. Y. Yum. 2005. Identification of extracellular N-acylhomoserine lactone acylase from Streptomyces sp. and its application to quorum quenching. Appl. Environ. Microbiol. 71: 2632-2641. https://doi.org/10.1128/AEM.71.5.2632-2641.2005
  51. Park, S. Y, B. J. Hwang, M. H. Shin, J. A. Kim, H. K. Kim and J. K. Lee. 2006. N-Acylhomoserine lactonase (AHLase) producing Rhodococcus sp. with different AHL-degrading activities. FEMS Microbiol. Lett. 261: 102-108. https://doi.org/10.1111/j.1574-6968.2006.00336.x
  52. Pesavento, C. and R. Hengge. 2010. c-di-GMP signaling. p. 377-394. In R. Kramer and K. Jung (eds.), Bacterial Signaling, WILEY-VCH.
  53. Rasmussen, T. B. and M. Givskov. 2006. Quorum sensing inhibitors: a bargain of effects. Microbiology 152: 895-904. https://doi.org/10.1099/mic.0.28601-0
  54. Reimmann, C., N. Ginet, L. Michel, C. Keel, P. Michaux, V. Krishnapillai, M. Zala, K. Heurlier, K. Triandafillu, H. Harms, G. Defago, and D. Haas. 2002. Genetically programmed autoinducer destruction reduces virulence gene expression and swarming motility in Pseudomonas aeruginosa PAO1. Microbiology 148: 923-932. https://doi.org/10.1099/00221287-148-4-923
  55. Reverchon, S., B. Chantegrel, C. Deshayes, A. Doutheau, and N. Cotte-Pattat. 2002. New synthetic analogues of N-acyl homoserine lactones as agonists or antagonists of transcriptional regulators involved in bacterial quorum sensing. Bioorg. Med. Chem. Lett. 12: 1153-1157. https://doi.org/10.1016/S0960-894X(02)00124-5
  56. Rickard A. H., R. J. Palmer Jr., D. S. Blehert, S. R. Campagna, M. F. Semmelhack, P. G. Egland, B. L. Bassler, and P. E. Kolenbrander. 2006. Autoinducer 2: a concentration-dependent signal for mutualistic bacterial biofilm growth. Mol. Microbiol. 60: 1446-1456. https://doi.org/10.1111/j.1365-2958.2006.05202.x
  57. Romero, M., A. B. Martin-Cuadrado, A. Roca-Rivada, A. M. Cabello, and A. Otero. 2011. Quorum quenching in cultivable bacteria from dense marine coastal microbial communities. FEMS Microbiol. Ecol. 75: 205-217. https://doi.org/10.1111/j.1574-6941.2010.01011.x
  58. Romling, U., M. Gomelsky, and M. Y. Galperin. 2005. C-di-GMP: the dawning of a novel bacterial signaling system. Mol. Microbiol. 57: 629-639. https://doi.org/10.1111/j.1365-2958.2005.04697.x
  59. Ross, P., H. Weinhouse, Y. Aloni, D. Michaeli, P. Weinberger-Ohana, R. Mayer, S. Braun, E. de Vroom, G. A. van der Marel, J. H. van Boom, and M. Benziman. 1987. Regulation of cellulose synthesis in Acetobacter xylinum by cyclic diguanylic acid. Nature 325: 279-281. https://doi.org/10.1038/325279a0
  60. Roy, V., R. Fernandes, C. Y. Tsao, and W. E. Bentley. 2010. Cross species quorum quenching using a native AI-2 processing enzyme. ACS Chem. Biol. 5: 223-232. https://doi.org/10.1021/cb9002738
  61. Salmond, G. P., B. W. Bycroft, G. S. Stewart, and P. Williams. 1995. The bacterial 'enigma': cracking the code of cell-cell communication. Mol. Microbiol. 16: 615-624. https://doi.org/10.1111/j.1365-2958.1995.tb02424.x
  62. Schipper, C., C. Hornung, P. Bijtenhoorn, M. Quitschau, S. Grond, and W. R. Streit. 2009. Metagenome-derived clones encoding two novel lactonase family proteins involved in biofilm inhibition in Psudomonas aeruginosa. Appl. Environ. Microbiol. 75: 224-233. https://doi.org/10.1128/AEM.01389-08
  63. Shrout J. D., and R. Nerenberg. 2012. Monitoring bacterial twitter: does quorum sensing determine the behavior of water and wastewater treatment biofilms? Environ. Sci. Technol. 46: 1995-2005. https://doi.org/10.1021/es203933h
  64. Sintim, H. O., J. A. Smith, J. Wang, S. Nakayama, and L. Yan. 2010. Paradigm shift in discovering next-generation anti-infective agents: targeting quorum sensing, c-di-GMP signaling and biofilm formation in bacteria with small molecules. Future Med. Chem. 2: 1005-1035. https://doi.org/10.4155/fmc.10.185
  65. Smith, K. M., Y. G. Bu, and H. Suga. 2003. Induction and inhibition of Pseudomonas aeruginosa quorum sensing by synthetic autoinducer analogs. Chem. Biol. 10: 81-89. https://doi.org/10.1016/S1074-5521(03)00002-4
  66. Stewart, P. S. and J. W. Costerton. 2001. Antibiotic resistance of bacteria in biofilms. Lancet 358: 135-138. https://doi.org/10.1016/S0140-6736(01)05321-1
  67. Taga, M. E., and B. L. Bassler. 2003. Chemical communication among bacteria. Proc. Natl. Acad. Sci. USA 100: 14549-14554. https://doi.org/10.1073/pnas.1934514100
  68. Teplitski, M., U. Mathesius, and K. P. Rumbaugh. 2011. Perception and degradation of N-acyl homoserine lactone quorum sensing signals by mammalian and plant cells. Chem. Rev. 111: 100-116. https://doi.org/10.1021/cr100045m
  69. Uroz, S., S. R. Chhabra, M. Camara, P. Williams, P. Oger, and Y. Dessaux. 2005. N-acylhomoserine lactone quorum-sensing molecules are modified and degraded by Rhodococcus erythropolis W2 by both amidolytic and novel oxidoreductase activities. Microbiology 151: 3313-22. https://doi.org/10.1099/mic.0.27961-0
  70. Uroz, S., P. Oger, S. R. Chhabra, M. Camara, P. Williams, and Y. Dessaux. 2007. N-acyl homoserine lactones are degraded via an amidolytic activity in Comamonas sp. Strain D1. Arch. Microbiol. 187: 249-256. https://doi.org/10.1007/s00203-006-0186-5
  71. Uroz, S., P. Oger, E. Chapelle, M. Adeline, D. Faure, and Y. Dessaux. 2008. A Rhodococcus qsdA-encoded enzyme defines a novel class of large-spectrum quorum-quenching lactonases. Appl. Environ. Microbiol. 74: 1357-1366. https://doi.org/10.1128/AEM.02014-07
  72. Wahjudi, M., E. Papaioannou, O. Hendrawati, A. H. van Assen, R. van Merkerk, R. H. Cool, G. J. Poelarends, and W. J. Quax. 2011. PA0305 of Pseudomonas aeruginosa is a quorum quenching acylhomoserine lactone acylase belonging to the Ntn hydrolase superfamily. Microbiology 157: 2042-2055. https://doi.org/10.1099/mic.0.043935-0
  73. Wang, L. H., Y. H Dong, and L. H. Zhang. 2008. Quorum Quenching: Impact and Mechanisms. p. 379-392. In S. C. Winans and B. L. Bassler (eds.), Chemical Communication Among Bacteria, ASM Press, USA.
  74. Watnick, P. and R. Kolter. 2000. Biofilm, city of microbes. J. Bacteriol. 182: 2675-2679. https://doi.org/10.1128/JB.182.10.2675-2679.2000
  75. Whitchurch, C.B., T. Tolker-Nielsen, P. C. Ragas, and J. S. Mattick. 2002. Extracellular DNA required for bacterial biofilm formation. Science 295:1487. https://doi.org/10.1126/science.295.5559.1487
  76. Whitehead, N. A., A. M. Barnard, H. Slater, N. J. Simpson, and G. P. Salmond. 2001. Quorum-sensing in Gram-negative bacteria. FEMS Microbiol. Rev. 25: 365-404. https://doi.org/10.1111/j.1574-6976.2001.tb00583.x
  77. Whitehead, N. A., M. Welch, and G. P. Salmond. 2001. Silencing the majority. Nat. Biotechnol. 19: 735-736. https://doi.org/10.1038/90780
  78. Wood, T. K., S. H. Hong, and Q. Ma. 2011. Engineering biofilm formation and dispersal. Trends Biotechnol. 29: 87-94. https://doi.org/10.1016/j.tibtech.2010.11.001
  79. Xavier, K. B. and B. L. Bassler. 2005. Interference with AI-2-mediated bacterial cell-cell communication. Nature 437: 750-753. https://doi.org/10.1038/nature03960
  80. Xiong, Y., and Y. Liu. 2010. Biological control of microbial attachment: a promising alternative for mitigating membrane biofouling. Appl. Microbiol. Biotechnol. 86: 825-837. https://doi.org/10.1007/s00253-010-2463-0
  81. Yang, L., K. B. Barken, M. E. Skindersoe, A. B. Christensen, M. Givskov, and T. Tolker-Nielsen. 2007. Effect of iron on DNA release and biofilm development by Pseudomonas aeruginosa. Microbiology 153: 1318-1328. https://doi.org/10.1099/mic.0.2006/004911-0
  82. Yeon, K. M., W. S. Cheong, H. S. Oh, W. N. Lee, B. K. Whang, C. H. Lee, H. Beyenal and Z. Lewandowski. 2009. Quorum Sensing: A New biofouling Control Paradigm in a Memenbrane Bioreactor for Advanced Wastewater Treatment. Environ. Sci. Technol. 43: 380-385. https://doi.org/10.1021/es8019275
  83. Zuo, R. 2007. Biofilms: strategies for metal corrosion inhibition employing microorganisms. Appl. Microbiol. Biotechnol. 76: 1245-1253. https://doi.org/10.1007/s00253-007-1130-6

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