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http://dx.doi.org/10.5352/JLS.2016.26.12.1487

Quorum Quenching Enzymes and Biofouling Control  

Jeon, Young Jae (Department of Microbiology, Pukyong National University)
Jeong, Won-Geom (Department of Microbiology, Pukyong National University)
Heo, Hye-Sook (Department of Microbiology, Pukyong National University)
Publication Information
Journal of Life Science / v.26, no.12, 2016 , pp. 1487-1497 More about this Journal
Abstract
Bacterial cell to cell communication strategies called quorum sensing (QS) using small diffusible signaling molecules (auto-inducers) govern the expression of various genes dependent on their population density manner. As a consequence of synthesis and response to the signaling molecules, individual planktonic cells synchronized group behaviors to control a diverse array of phenotypes such as maturation of biofilm, production of extra-polymeric substances (EPS), virulence, bioluminescence and antibiotic production. Many studies indicated that biofilm formations are associated with QS signaling molecules such as acyl-homoserine lactones (AHLs) mainly used by several Gram negative bacteria. The biofilm maturation causes undesirable biomass accumulation in various surface environments anywhere water is present called biofouling, which results in serious eco-technological problems. Numerous molecules that interfere the bacterial QS called quorum quenching (QQ), have been discovered from various microorganisms, and their functions and mechanisms associated with QS have also been elucidated. To resolve biofouling problems related to various industries, the novel approach based on QS interference has been emerged attenuating multi-drug resisting bacteria appearance and environmental toxicities, which may provide potential advantages over the conventional anti-biofouling approaches. Therefore this paper presents recent information related to bacterial quorum sensing system, quorum quenching enzymes that can control the QS signaling, and lastly discuss the anti-biofouling approaches using the quorum quenching.
Keywords
Acyl-homoserine lactone; anti-biofouling; biofouling; quorum quenching enzymes; quorum sensing (QS);
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1 Sio, C. F., Otten, L. G., Cool, R. H., Diggle, S. P., Braun, P. G., Bos, R., Daykin, M., Camara, M., Williams, P. and Quax, W. J. 2006. Quorum quenching by an N-acyl-homoserine lactone acylase from Pseudomonas aeruginosa PAO1. Infect. Immun. 74, 1673-1682.   DOI
2 Steidle, A., Allesen-Holm, M., Riedel, K., Berg, G., Givskov, M., Molin, S. and Eberl, L. 2002. Identification and characterization of an N-acylhomoserine lactone-dependent quorum- sensing system in Pseudomonas putida strain IsoF. Appl. Environ. Microbiol. 68, 6371-6382.   DOI
3 Swain, G. and Shinjo, N. 2014. Comparing biofouling control treatments for use on aquaculture nets. Int. J. Mol. Sci. 15, 22142-22154.   DOI
4 Swift, S., Karlyshev, A. V., Fish, L., Durant, E. L., Winson, M. K., Chhabra, S. R., Williams, P., Macintyre, S. and Stewart, G. 1997. Quorum sensing in Aeromonas hydrophila and Aeromonas salmonicida: Identification of the LuxRI homologs AhyRI and AsaRI and their cognate N-acylhomoserine lactone signal molecules. J. Bacteriol. 179, 5271-5281.   DOI
5 Tait, K., Joint, I., Daykin, M., Milton, D. L., Williams, P. and Camara, M. 2005. Disruption of quorum sensing in seawater abolishes attraction of zoospores of the green alga Ulva to bacterial biofilms. Environ. Microbiol. 7, 229-240.   DOI
6 Uroz, S., Oger, P. M., Chapelle, E., Adeline, M. T., Faure, D. and Dessaux, Y. 2008. A Rhodococcus qsdA-encoded enzyme defines a novel class of large-spectrum quorumquenching lactonases. Appl. Environ. Microbiol. 74, 1357-1366.   DOI
7 Del Vecchio, P., Elias, M., Merone, L., Graziano, G., Dupuy, J., Mandrich, L., Carullo, P., Fournier, B., Rochu, D. and Rossi, M. 2009. Structural determinants of the high thermal stability of Ssopox from the hyperthermophilic archaeon Sulfolobus solfataricus. Extremophiles 13, 461-470.   DOI
8 Dobretsov, S., Dahms, H. U., YiLi, H., Wahl, M. and Qian, P. Y. 2007. The effect of quorum-sensing blockers on the formation of marine microbial communities and larval attachment. FEMS Microbiol. Ecol. 60, 177-188.   DOI
9 Dobretsov, S., Teplitski, M., Bayer, M., Gunasekera, S., Proksch, P. and Paul, V. J. 2011. Inhibition of marine biofouling by bacterial quorum sensing inhibitors. Biofouling 27, 893-905.   DOI
10 Dong, Y. H., Zhang, X. F., Xu, J. L. and Zhang, L. H. 2004. Insecticidal Bacillus thuringiensis silences Erwinia carotovora virulence by a new form of microbial antagonism, signal interference. Appl. Environ. Microbiol. 70, 954-960.   DOI
11 Dong, Y. H., Wang, L. H., Xu, J. L., Zhang, H. B., Zhang, X. F. and Zhang, L. H. 2001. Quenching quorum-sensingdependent bacterial infection by an N-acyl homoserine lactonase. Nature 411, 813-817.   DOI
12 Dong, Y. H. and Zhang, L. H. 2005. Quorum sensing and quorum-quenching enzymes. J. Microbiol. 43, 101-109.
13 Givskov, M., de Nys, R., Manefield, M., Gram, L., Maximilien, R., Eberl, L., Molin, S., Steinberg, P. D. and Kjelleberg, S. 1996. Eukaryotic interference with homoserine lactonemediated prokaryotic signalling. J. Bacteriol. 178, 6618-6622.   DOI
14 Eberhard, A., Burlingame, A. L., Eberhard, C., Kenyon, G. L., Nealson, K. H. and Oppenheimer, N. J. 1981. Structural identification of autoinducer of Photobacterium fischeri Luciferase. Biochemistry 20, 2444-2449.   DOI
15 Davies, D. G., Parsek, M. R., Pearson, J. P., Iglewski, B. H., Costerton, J. W. and Greenberg, E. P. 1998. The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 280, 295-298.   DOI
16 Elias, M., Dupuy, J., Merone, L., Mandrich, L., Porzio, E., Moniot, S., Rochu, D., Lecomte, C., Rossi, M. and Masson, P. 2008. Structural basis for natural lactonase and promiscuous phosphotriesterase activities. J. Mol. Biol. 379, 1017-1028.   DOI
17 Elias, M. and Tawfik, D. S. 2012. Divergence and convergence in enzyme evolution: Parallel evolution of paraoxonases from quorum-quenching lactonases. J. Biol. Chem. 287, 11-20.   DOI
18 Givskov, M., de Nys, R., Manefield, M., Gram, L., Maximilien, R., Eberl, L., Molin, S., Steinberg, P. D. and Kjelleberg, S. 1996. Eukaryotic interference with homoserine lactone-mediated prokaryotic signalling. J. Bacteriol. 178, 6618-6622.   DOI
19 Gould, T. A., Herman, J., Krank, J., Murphy, R. C. and Churchill, M. E. 2006. Specificity of acyl-homoserine lactone synthases examined by mass spectrometry. J. Bacteriol. 188, 773-783.   DOI
20 Grandclement, C., Tannieres, M., Morera, S., Dessaux, Y. and Faure, D. 2016. Quorum quenching: Role in nature and applied developments. FEMS Microbiol. Rev. 40, 86-116.   DOI
21 Jiang, W., Xia, S., Liang, J., Zhang, Z. and Hermanowicz, S. W. 2013. Effect of quorum quenching on the reactor performance, biofouling and biomass characteristics in membrane bioreactors. Water Res. 47, 187-196.   DOI
22 Harding, J. L. and Reynolds, M. M. 2014. Combating medical device fouling. Trends Biotechnol. 32, 140-146.   DOI
23 Hiblot, J., Gotthard, G., Chabriere, E. and Elias, M. 2012. Structural and enzymatic characterization of the lactonase sis lac from Sulfolobus islandicus. PLoS One 7, e47028.   DOI
24 Hoch, J. A. 1993. Regulation of the phosphorelay and the initiation of sporulation in bacillus subtilis. Annu. Rev. Microbiol. 47, 441-465.   DOI
25 Huang, J., Shi, Y., Zeng, G., Gu, Y., Chen, G., Shi, L., Hu, Y., Tang, B. and Zhou, J. 2016. Acyl-homoserine lactonebased quorum sensing and quorum quenching hold promise to determine the performance of biological wastewater treatments: An overview. Chemosphere 157, 137-151.   DOI
26 Huang, J. J., Petersen, A., Whiteley, M. and Leadbetter, J. R. 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.
27 Kalishwaralal, K., BarathManiKanth, S., Pandian, S. R. K., Deepak, V. and Gurunathan, S. 2010. Silver nanoparticles impede the biofilm formation by Pseudomonas aeruginosa and Staphylococcus epidermidis. Colloids Surfaces B. 79, 340-344.   DOI
28 Karlsson, T., Turkina, M. V., Yakymenko, O., Magnusson, K. E. and Vikstrom, E. 2012. The Pseudomonas aeruginosa N-acylhomoserine lactone quorum sensing molecules target IQGAP1 and modulate epithelial cell migration. PLoS Pathog. 8, e1002953.   DOI
29 Kim, M. H., Choi, W. C., Kang, H. O., Lee, J. S., Kang, B. S., Kim, K. J., Derewenda, Z. S., Oh, T. K., Lee, C. H. and Lee, J. K. 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.   DOI
30 Kim, J. H., Choi, D. C., Yeon, K. M., Kim, S. R. and Lee, C. H. 2011. Enzyme-immobilized nanofiltration membrane to mitigate biofouling based on quorum quenching. Environ. Sci. Technol. 45, 1601-1607.   DOI
31 Lade, H., Paul, D. and Kweon, J. H. 2014. Isolation and molecular characterization of biofouling bacteria and profiling of quorum sensing signal molecules from membrane bioreactor activated sludge. Int. J. Biol. Sci. 15, 2255-2273.
32 Kim, S. R., Oh, H. S., Jo, S. J., Yeon, K. M., Lee, C. H., Lim, D. J., Lee, C. H. and Lee, J. K. 2013. Biofouling control with bead-entrapped quorum quenching bacteria in membrane bioreactors: Physical and biological effects. Environ. Sci. Technol. 47, 836-842.   DOI
33 Kristensen, J. B., Meyer, R. L., Laursen, B. S., Shipovskov, S., Besenbacher, F. and Poulsen, C. H. 2008. Antifouling enzymes and the biochemistry of marine settlement. Biotech. Adv. 26, 471-481.   DOI
34 Labbate, M., Queck, S. Y., Koh, K. S., Rice, S. A., Givskov, M. and Kjelleberg, S. 2004. Quorum sensing-controlled biofilm development in Serratia liquefaciens MG1. J. Bacteriol. 186, 692-698.   DOI
35 Lade, H., Paul, D. and Kweon, J. H. 2014. Quorum quenching mediated approaches for control of membrane biofouling. Int. J. Biol. Sci. 10, 550-565.   DOI
36 Leadbetter, J. R. and Greenberg, E. 2000. Metabolism of acyl- homoserine lactone quorum-sensing signals by Variovorax paradoxus. J. Bacteriol. 182, 6921-6926.   DOI
37 Lin, Y. H., Xu, J. L., Hu, J., Wang, L. H., Ong, S. L., Leadbetter, J. R. and Zhang, L. H. 2003. Acyl-homoserine lactone acylase from Ralstonia strain XJ12B represents a novel and potent class of quorum-quenching enzymes. Mol. Microbiol. 47, 849-860.   DOI
38 Lee, S., Park, S. K., Kwon, H., Lee, S. H., Lee, K., Nahm, C. H., Jo, S. J., Oh, H. S., Park, P. K., Choo, K. H., Lee, C. H. and Yi, T. 2016. Crossing the border between laboratory and field: Bacterial quorum quenching for anti-biofouling strategy in an MBR. Environ. Sci. Technol. 50, 1788-1795.   DOI
39 Lewenza, S., Conway, B., Greenberg, E. and Sokol, P. A. 1999. Quorum sensing in Burkholderia cepacia: Identification of the LuxRI homologs CepRI. J. Bacteriol. 181, 748-756.
40 Lewis, A. L. 2000. Phosphorylcholine-based polymers and their use in the prevention of biofouling. Colloids Surf. B. Biointerfaces 18, 261-275.   DOI
41 Littlechild, J. A. 2015. Archaeal enzymes and applications in industrial biocatalysts. Archaea 10, 2015.
42 Liu, D., Thomas, P. W., Momb, J., Hoang, Q. Q., Petsko, G. A., Ringe, D. and Fast, W. 2007. Structure and specificity of a quorum-quenching lactonase (AiiB) from Agrobacterium tumefaciens. Biochemistry 46, 11789-11799.   DOI
43 Manefield, M., Welch, M., Givskov, M., Salmond, G. P. and Kjelleberg, S. 2001. Halogenated furanones from the red alga, Delisea pulchra, inhibit carbapenem antibiotic synthesis and exoenzyme virulence factor production in the phytopathogen Erwinia carotovora. FEMS Microbiol. Lett. 205, 131-138.   DOI
44 Yeon, K. M., Cheong, W. S., Oh, H. S., Lee, W. N., Hwang, B. K., Lee, C. H., Beyenal, H. and Lewandowski, Z. 2009. Quorum sensing: A new biofouling control paradigm in a membrane bioreactor for advanced wastewater treatment. Environ. Sci. Technol. 43, 380-385.   DOI
45 Watson, W. T., Minogue, T. D., Val, D. L., von Bodman, S. B. and Churchill, M. E. 2002. Structural basis and specificity of acyl-homoserine lactone signal production in bacterial quorum sensing. Mol. Cell 9, 685-694.   DOI
46 Martin-Rodriguez, A. J., Babarro, J. M. F., Lahoz, F., Sanson, M., Martin, V. S., Norte, M. and Fernandez, J. J. 2015. From broad-spectrum biocides to quorum sensing disruptors and mussel repellents: Antifouling profile of alkyl triphenylphosphonium salts. PLoS ONE 10, e0123652.   DOI
47 McClean, K. H., Winson, M. K., Fish, L., Taylor, A., Chhabra, S. R., Camara, M., Daykin, M., Lamb, J. H., Swift, S. and Bycroft, B. W. 1997. Quorum sensing and Chromobacterium violaceum: Exploitation of violacein production and inhibition for the detection of N-acylhomoserine lactones. Microbiology 143, 3703-3711.   DOI
48 Mei, G. Y., Yan, X. X., Turak, A., Luo, Z. Q. and Zhang, L. Q. 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.   DOI
49 Weerasekara, N. A., Choo, K. H. and Lee, C. H. 2014. Hybridization of physical cleaning and quorum quenching to minimize membrane biofouling and energy consumption in a membrane bioreactor. Water Res. 67, 1-10.   DOI
50 Xu, F., Byun, T., Dussen, H. J. and Duke, K. R. 2003. Degradation of N-acylhomoserine lactones, the bacterial quorum-sensing molecules, by acylase. J. Biotechnol. 101, 89-96.   DOI
51 Yeon, K. M., Lee, C. H. and Kim, J. 2009. Magnetic enzyme carrier for effective biofouling control in the membrane bioreactor based on enzymatic quorum quenching. Environ. Sci. Technol. 43, 7403-7409.   DOI
52 Yeon, K. M., Park, J. S., Lee, C. H. and Kim, S. M. 2005. Membrane coupled high-performance compact reactor: A new MBR system for advanced wastewater treatment. Water Res. 39, 1954-1961.   DOI
53 Zhang, K., Zheng, X., Shen, D. S., Wang, M. Z., Feng, H. J., He, H. Z., Wang, S. and Wang, J. H. 2015. Evidence for existence of quorum sensing in a bioaugmented system by acylated homoserine lactone-dependent quorum quenching. Environ. Sci. Pollut. Res. Int. 22, 6050-6056.   DOI
54 Zhang, W. and Li, C. 2015. Exploiting quorum sensing interfering strategies in gram-negative bacteria for the enhancement of environmental applications. Front. Microbiol. 6, 1535.
55 Morohoshi, T., Inaba, T., Kato, N., Kanai, K. and Ikeda, T. 2004. Identification of quorum-sensing signal molecules and the luxri homologs in fish pathogen Edwardsiella tarda. J. Biosci. Bioeng. 98, 274-281.   DOI
56 Meng, X., Shi, Y., Ji, W., Meng, X., Zhang, J., Wang, H., Lu, C., Sun, J. and Yan, Y. 2011. Application of a bacteriophage lysin to disrupt biofilms formed by the animal pathogen Streptococcus suis. Appl. Environ. Microbiol. 77, 8272-8279.   DOI
57 Mohanty, S., Mishra, S., Jena, P., Jacob, B., Sarkar, B. and Sonawane, A. 2012. An investigation on the antibacterial, cytotoxic, and antibiofilm efficacy of starch-stabilized silver nanoparticles. Nanomedicine 8, 916-924.   DOI
58 Momb, J., Wang, C., Liu, D., Thomas, P. W., Petsko, G. A., Guo, H., Ringe, D. and Fast, W. 2008. Mechanism of the quorum-quenching lactonase (AiiA) from Bacillus thuringiensis. Substrate modeling and active site mutations. Biochemistry 47, 7715-7725.   DOI
59 Oh, H. S., Yeon, K. M., Yang, C. S., Kim, S. R., Lee, C. H., Park, S. Y., Han, J. Y. and Lee, J. K. 2012. Control of membrane biofouling in mbr for wastewater treatment by quorum quenching bacteria encapsulated in microporous membrane. Environ. Sci. Technol. 46, 4877-4884.   DOI
60 Ng, F. S., Wright, D. M. and Seah, S. Y. 2011. Characterization of a phosphotriesterase-like lactonase from Sulfolobus solfataricus and its immobilization for disruption of quorum sensing. Appl. Environ. Microbiol. 77, 1181-1186.   DOI
61 Olsen, S. M., Pedersen, L. T., Laursen, M., Kiil, S. and Dam-Johansen, K. 2007. Enzyme-based antifouling coatings: A review. Biofouling 23, 369-383.   DOI
62 Paggi, R. A., Martone, C. B., Fuqua, C. and De Castro, R. E. 2003. Detection of quorum sensing signals in the haloalkaliphilic archaeon Natronococcus occultus. FEMS Microbiol. Lett. 221, 49-52.   DOI
63 Bzdrenga, J., Daude, D., Remy, B., Jacquet, P., Plener, L., Elias, M. and Chabriere, E. 2016. Biotechnological applications of quorum quenching enzymes. Chem. Biol. Interact. (In press)
64 Park, S. H., Kang, J. Y., Kim, D. H., Ahn, T. and Yun, C. H. 2012. The flavin-containing reductase domain of cytochrome P450 BM3 acts as a surrogate for mammalian NADPG-P450 reductase. Biomol. Ther. 20, 562.   DOI
65 Park, S. Y., Lee, S. J., Oh, T. K., Oh, J. W., Koo, B. T., Yum, D. Y. and Lee, J. K. 2003. Ahld, an N-acylhomoserine lactonase in Arthrobacter sp., and predicted homologues in other bacteria. Microbiology 149, 1541-1550.   DOI
66 Park, S. Y., Hwang, B. J., Shin, M. H., Kim, J. A., Kim, H. K. and Lee, J. K. 2006. N-acylhomoserine lactonase producing Rhodococcus spp. with different AHL-degrading activities. FEMS Microbiol. Lett. 261, 102-108.   DOI
67 Beck von Bodman, S. and Farrand, S. K. 1995. Capsular polysaccharide biosynthesis and pathogenicity in Erwinia stewartii require induction by an N-acylhomoserine lactone autoinducer. J. Bacteriol. 177, 5000-5008.   DOI
68 Bijtenhoorn, P., Mayerhofer, H., Muller-Dieckmann, J., Utpatel, C., Schipper, C., Hornung, C., Szesny, M., Grond, S., Thurmer, A. and Brzuszkiewicz, E. 2011. A novel metagenomic short-chain dehydrogenase/reductase attenuates Pseudomonas aeruginosa biofilm formation and virulence on caenorhabditis elegans. PLoS One 6, e26278.   DOI
69 Carius, L., Carius, A. B., McIntosh, M. and Grammel, H. 2013. Quorum sensing influences growth and photosynthetic membrane production in high-cell-density cultivations of Rhodospirillum rubrum. BMC Microbiol. 13, 1.   DOI
70 Carlier, A., Uroz, S., Smadja, B., Fray, R., Latour, X., Dessaux, Y. and Faure, D. 2003. The Ti plasmid of Agrobacterium tumefaciens harbors an attM-paralogous gene, aiiB, also encoding n-acyl homoserine lactonase activity. Appl. Environ. Microbiol. 69, 4989-4993.   DOI
71 Riaz, K., Elmerich, C., Moreira, D., Raffoux, A., Dessaux, Y. and Faure, D. 2008. A metagenomic analysis of soil bacteria extends the diversity of quorum‐quenching lactonases. Environ. Microbiol. 10, 560-570.   DOI
72 Zhang, Y., An, J., Ye, W., Yang, G., Qian, Z. G., Chen, H. F., Cui, L. and Feng, Y. 2012. Enhancing the promiscuous phosphotriesterase activity of a thermostable lactonase (GkaP) for the efficient degradation of organophosphate pesticides. Appl. Environ. Microbiol. 78, 6647-6655.   DOI
73 Zhang, Y., Liu, J., Tang, K., Yu, M., Coenye, T. and Zhang, X. H. 2015. Genome analysis of Flaviramulus ichthyoenteri Th78(T) in the family Flavobacteriaceae: Insights into its quorum quenching property and potential roles in fish intestine. BMC Genomics 16, 38.   DOI
74 Park, S. Y., Kang, H. O., Jang, H. S., Lee, J. K., Koo, B. T. and Yum, D. Y. 2005. Identification of extracellular N-acylhomoserine lactone acylase from a Streptomyces sp. and its application to quorum quenching. Appl. Environ. Microbiol. 71, 2632-2641.   DOI
75 Pierson, L. S., Keppenne, V. D. and Wood, D. W. 1994. Phenazine antibiotic biosynthesis in Pseudomonas aureofaciens 30-84 is regulated by PhzR in response to cell density. J. Bacteriol. 176, 3966-3974.   DOI
76 Rai, N., Rai, R. and Venkatesh, K. 2015. Quorum sensing biosensors, pp. 173-183. In: Kalia, V. C. (eds), Quorum sensing vs quorum quenching: A battle with no end in sight, Springer.
77 Riedel, K., Hentzer, M., Geisenberger, O., Huber, B., Steidle, A., Wu, H., Hoiby, N., Givskov, M., Molin, S. and Eberl, L. 2001. N-acylhomoserine-lactone-mediated communication between Pseudomonas aeruginosa and Burkholderia cepacia in mixed biofilms. Microbiology 147, 3249-3262.   DOI
78 Romero, M., Diggle, S. P., Heeb, S., Camara, M. and Otero, A. 2008. Quorum quenching activity in Anabaena sp. PCC 7120: Identification of AiiC, a novel AHL-acylase. FEMS Microbiol. Lett. 280, 73-80.   DOI
79 Rivas, M., Seeger, M., Holmes, D. S. and Jedlicki, E. 2005. A Lux-like quorum sensing system in the extreme acidophile Acidithiobacillus ferrooxidans. Biol. Res. 38, 283-297.
80 Romero, M., Avendano-Herrera, R., Magarinos, B., Camara, M. and Otero, A. 2010. Acylhomoserine lactone production and degradation by the fish pathogen Tenacibaculum maritimum, a member of the Cytophaga-Flavobacterium-Bacteroides (CFB) group. FEMS Microbiol. Lett. 304, 131-139.   DOI
81 Chun, C. K., Ozer, E. A., Welsh, M. J., Zabner, J. and Greenberg, E. 2004. Inactivation of a Pseudomonas aeruginosa quorum-sensing signal by human airway epithelia. Proc. Natl. Acad. Sci. USA 101, 3587-3590.   DOI
82 Choi, O., Yu, C. P., Fernandez, G. E. and Hu, Z. 2010. Interactions of nanosilver with Escherichia coli cells in planktonic and biofilm cultures. Water Res. 44, 6095-6103.   DOI
83 Chow, J. Y., Xue, B., Lee, K. H., Tung, A., Wu, L., Robinson, R. C. and Yew, W. S. 2010. Directed evolution of a thermostable quorum-quenching lactonase from the amidohydrolase superfamily. J. Biol. Chem. 285, 40911-40920.   DOI
84 Chowdhary, P. K., Keshavan, N., Nguyen, H. Q., Peterson, J. A., Gonzalez, J. E. and Haines, D. C. 2007. Bacillus megaterium CYP102A1 oxidation of acyl homoserine lactones and acyl homoserines. Biochemistry 46, 14429-14437.   DOI
85 Ciriminna, R., Bright, F. V. and Pagliaro, M. 2015. Ecofriendly antifouling marine coatings. ACS Sustainable Chem. Eng. 3, 559-565.   DOI
86 Coenye, T., Brackman, G., Rigole, P., De Witte, E., Honraet, K., Rossel, B. and Nelis, H. J. 2012. Eradication of Propionibacterium acnes biofilms by plant extracts and putative identification of icariin, resveratrol and salidroside as active compounds. Phytomedicine 19, 409-412.   DOI
87 Cordeiro, A. L. and Werner, C. 2011. Enzymes for antifouling strategies. J. Adhes. Sci. Technol. 25, 2317-2344.   DOI
88 Schultz, M., Bendick, J., Holm, E. and Hertel, W. 2011. Economic impact of biofouling on a naval surface ship. Biofouling 27, 87-98.   DOI
89 Romero, M., Martin-Cuadrado, A. B., Roca-Rivada, A., Cabello, A. M. and Otero, A. 2011. Quorum quenching in cultivable bacteria from dense marine coastal microbial communities. FEMS Microbiol. Ecol. 75, 205-217.   DOI
90 Sadekuzzaman, M., Yang, S., Mizan, M. F. R. and Ha, S. D. 2015. Current and recent advanced strategies for combating biofilms. Compr. Rev. Food Sci. Food Saf. 14, 491-509.   DOI
91 Schultz, M. P. 2007. Effects of coating roughness and biofouling on ship resistance and powering. Biofouling 23, 331-341.   DOI
92 Seo, M. J., Lee, B. S., Pyun, Y. R. and Park, H. 2011. Isolation and characterization of N-acylhomoserine lactonase from the thermophilic bacterium, Geobacillus caldoxylosilyticus YS-8. Biosci. Biotechnol. Biochem. 75, 1789-1795.   DOI
93 Sharif, D. I., Gallon, J., Smith, C. J. and Dudley, E. 2008. Quorum sensing in cyanobacteria: N-octanoyl-homoserine lactone release and response, by the epilithic colonial cyanobacterium Gloeothece PCC6909. ISME J. 2, 1171-1182.   DOI
94 Singh, R. P., Desouky, S. E. and Nakayama, J. 2016. Quorum quenching strategy targeting gram-positive pathogenic bacteria. Adv. Exp. Med. Biol. 901, 109-130.   DOI
95 Czajkowski, R., Krzyzanowska, D., Karczewska, J., Atkinson, S., Przysowa, J., Lojkowska, E., Williams, P. and Jafra, S. 2011. Inactivation of AHLs by Ochrobactrum sp. A44 depends on the activity of a novel class of AHL acylase. Environ. Microbiol. Rep. 3, 59-68.   DOI
96 Siddiqui, M. F., Rzechowicz, M., Harvey, W., Zularisam, A. W. and Anthony, G. F. 2015. Quorum sensing based membrane biofouling control for water treatment: A review. J. Water Process Eng. 7, 112-122.   DOI