Biotechnological applications of quorum quenching enzymes

Chemico-Biological Interactions

Volumn 267, Issue , 2017, Pages 104-115

  Bzdrenga, Janek ^a   Daudé, David ^b   Rémy, Benjamin ^a,b   Jacquet, Pauline ^a   Plener, Laure ^b   Elias, Mikael ^c   Chabrière, Eric ^a  

^a AIX MARSEILLE UNIVERSITÉ   (France)

^b AIX MARSEILLE UNIVERSITY   (France)

^c UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Biofilm; Enzyme; Lactonase; Quorum quenching; Quorum sensing; Virulence

Indexed keywords

AMIDASE; CIPROFLOXACIN; GAMMA LACTONE DERIVATIVE; GLUCONOLACTONASE; N ACYLHOMOSERINE LACTONE; OXIDOREDUCTASE; PHOSPHOTRIESTERASE; BACTERIAL PROTEIN;

AEROSOL; AGRICULTURE; ANTIBIOTIC RESISTANCE; AQUACULTURE; ARTICLE; BACTERIAL INFECTION; BACTERIAL PLANT DISEASE; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; BIOFILM; BIOFOULING; BIOTECHNOLOGY; DRUG POTENTIATION; DRUG STRUCTURE; ENZYME ENGINEERING; ENZYME INDUCTION; ENZYME MECHANISM; ENZYME RELEASE; ENZYME SYNTHESIS; GENE EXPRESSION REGULATION; GRAM NEGATIVE BACTERIUM; GRAM POSITIVE BACTERIUM; MEMBRANE REACTOR; NONHUMAN; QUORUM SENSING; SIGNAL TRANSDUCTION; WOUND DRESSING; ANIMAL; AQUATIC SPECIES; BACTERIUM; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; PLANT DISEASE;

AMIDOHYDROLASES; ANIMALS; AQUATIC ORGANISMS; BACTERIA; BACTERIAL PROTEINS; GRAM-NEGATIVE BACTERIA; PLANT DISEASES; QUORUM SENSING;

EID: 85014852102     PISSN: 00092797     EISSN: 18727786     Source Type: Journal    
DOI: 10.1016/j.cbi.2016.05.028     Document Type: Article

References (142)

1. [1] Nealson, K.H., Hastings, J.W., Bacterial bioluminescence: its control and ecological significance. Microbiol. Rev. 43 (1979), 496–518.
2. [2] Miller, M.B., Bassler, B.L., Quorum sensing in bacteria. Annu. Rev. Microbiol. 55 (2001), 165–199, 10.1146/annurev.micro.55.1.165.
3. [3] Chen, X., Schauder, S., Potier, N., Van Dorsselaer, A., Pelczer, I., Bassler, B.L., et al. Structural identification of a bacterial quorum-sensing signal containing boron. Nature 415 (2002), 545–549, 10.1038/415545a.
4. [4] Churchill, M.E.A., Chen, L., Structural basis of acyl-homoserine lactone-dependent signaling. Chem. Rev. 111 (2011), 68–85, 10.1021/cr1000817.
5. [5] Kendall, M.M., Sperandio, V., Quorum sensing by enteric pathogens. Curr. Opin. Gastroenterol. 23 (2007), 10–15, 10.1097/MOG.0b013e3280118289.
6. [6] Ryan, R.P., An, S., Allan, J.H., McCarthy, Y., Dow, J.M., The DSF family of cell-cell signals: an expanding class of bacterial virulence regulators. PLoS Pathog., 11, 2015, e1004986, 10.1371/journal.ppat.1004986.
7. [7] Flavier, A.B., Clough, S.J., Schell, M.A., Denny, T.P., Identification of 3-hydroxypalmitic acid methyl ester as a novel autoregulator controlling virulence in Ralstonia solanacearum. Mol. Microbiol. 26 (1997), 251–259.
8. [8] Winans, S.C., A new family of quorum sensing pheromones synthesized using S-adenosylmethionine and Acyl-CoAs. Mol. Microbiol. 79 (2011), 1403–1406, 10.1111/j.1365-2958.2011.07551.x.
9. [9] Lee, J., Zhang, L., The hierarchy quorum sensing network in Pseudomonas aeruginosa. Protein Cell 6 (2015), 26–41, 10.1007/s13238-014-0100-x.
10. [10] Plener, L., Lorenz, N., Reiger, M., Ramalho, T., Gerland, U., Jung, K., The phosphorylation flow of the vibrio harveyi quorum-sensing cascade determines levels of phenotypic heterogeneity in the population. J. Bacteriol. 197 (2015), 1747–1756, 10.1128/JB.02544-14.
11. [11] Jung, S.A., Chapman, C.A., Ng, W.-L., Quadruple quorum-sensing inputs control Vibrio cholerae virulence and maintain system robustness. PLoS Pathog., 11, 2015, e1004837, 10.1371/journal.ppat.1004837.
12. [12] Lee, J., Zhang, L., The hierarchy quorum sensing network in Pseudomonas aeruginosa. Protein Cell 6 (2015), 26–41, 10.1007/s13238-014-0100-x.
13. [13] Schmid, N., Pessi, G., Deng, Y., Aguilar, C., Carlier, A.L., Grunau, A., et al. The AHL- and BDSF-dependent quorum sensing systems control specific and overlapping sets of genes in Burkholderia cenocepacia H111. PLoS One, 7, 2012, e49966, 10.1371/journal.pone.0049966.
14. [14] West, S.A., Winzer, K., Gardner, A., Diggle, S.P., Quorum sensing and the confusion about diffusion. Trends Microbiol. 20 (2012), 586–594, 10.1016/j.tim.2012.09.004.
15. [15] Kaye, K.S., Pogue, J.M., Infections caused by resistant gram-negative bacteria: epidemiology and management. Pharmacotherapy 35 (2015), 949–962, 10.1002/phar.1636.
16. [16] Pimentel, D., Biological Invasions: Economic and Environmental Costs of Alien Plant, Animal, and Microbe Species. 2014, CRC Press.
17. [17] Mole, B.M., Baltrus, D.A., Dangl, J.L., Grant, S.R., Global virulence regulation networks in phytopathogenic bacteria. Trends Microbiol. 15 (2007), 363–371, 10.1016/j.tim.2007.06.005.
18. [18] Mansfield, J., Genin, S., Magori, S., Citovsky, V., Sriariyanum, M., Ronald, P., et al. Top 10 plant pathogenic bacteria in molecular plant pathology. Mol. Plant Pathol. 13 (2012), 614–629, 10.1111/j.1364-3703.2012.00804.x.
19. [19] Gauthier, D.T., Bacterial zoonoses of fishes: a review and appraisal of evidence for linkages between fish and human infections. Vet. J. Lond. Engl. 203 (2015), 27–35, 10.1016/j.tvjl.2014.10.028 1997.
20. [20] Certner, R.H., Vollmer, S.V., Evidence for autoinduction and quorum sensing in white band disease-causing microbes on Acropora cervicornis. Sci. Rep., 5, 2015, 11134, 10.1038/srep11134.
21. [21] Costerton, J.W., Stewart, P.S., Greenberg, E.P., Bacterial biofilms: a common cause of persistent infections. Science 284 (1999), 1318–1322, 10.1126/science.284.5418.1318.
22. [22] Lejars, M., Margaillan, A., Bressy, C., Fouling release coatings: a nontoxic alternative to biocidal antifouling coatings. Chem. Rev. 112 (2012), 4347–4390, 10.1021/cr200350v.
23. [23] Mattila-Sandholm, T., Wirtanen, G., Biofilm formation in the industry: a review. Food Rev. Int. 8 (1992), 573–603, 10.1080/87559129209540953.
24. [24] Coetser, S.E., Cloete, T.E., Biofouling and biocorrosion in industrial water systems. Crit. Rev. Microbiol. 31 (2005), 213–232, 10.1080/10408410500304074.
25. [25] Dürr, S., Watson, D.I., Biofouling and antifouling in aquaculture. Dürr, S., Thomason, J.C., (eds.) Biofouling, 2009, Wiley-Blackwell, 267–287 http://onlinelibrary.wiley.com/doi/10.1002/9781444315462.ch19/summary (accessed 3.12. 15).
26. [26] Dong, Y.H., Xu, J.L., Li, X.Z., Zhang, L.H., AiiA, an enzyme that inactivates the acylhomoserine lactone quorum-sensing signal and attenuates the virulence of Erwinia carotovora. Proc. Natl. Acad. Sci. U. S. A. 97 (2000), 3526–3531, 10.1073/pnas.060023897.
27. [27] Givskov, M., de Nys, R., Manefield, M., Gram, L., Maximilien, R., Eberl, L., et al. Eukaryotic interference with homoserine lactone-mediated prokaryotic signalling. J. Bacteriol. 178 (1996), 6618–6622.
28. [28] Manefield, M., Rasmussen, T.B., Henzter, M., Andersen, J.B., Steinberg, P., Kjelleberg, S., et al. Halogenated furanones inhibit quorum sensing through accelerated LuxR turnover. Microbiol. Read. Engl. 148 (2002), 1119–1127, 10.1099/00221287-148-4-1119.
29. [29] Zang, T., Lee, B.W.K., Cannon, L.M., Ritter, K.A., Dai, S., Ren, D., et al. A naturally occurring brominated furanone covalently modifies and inactivates LuxS. Bioorg. Med. Chem. Lett. 19 (2009), 6200–6204, 10.1016/j.bmcl.2009.08.095.
30. [30] Defoirdt, T., Miyamoto, C.M., Wood, T.K., Meighen, E.A., Sorgeloos, P., Verstraete, W., et al. The natural furanone (5Z)-4-bromo-5-(bromomethylene)-3-butyl-2(5H)-furanone disrupts quorum sensing-regulated gene expression in Vibrio harveyi by decreasing the DNA-binding activity of the transcriptional regulator protein luxR. Environ. Microbiol. 9 (2007), 2486–2495, 10.1111/j.1462-2920.2007.01367.x.
31. [31] Dessaux, Y., Chapelle, E., Faure, D., Quorum sensing and quorum quenching in soil ecosystems. Witzany, G., (eds.) Biocommunication Soil Microorg, 2011, Springer Berlin Heidelberg, 339–367 http://link.springer.com/chapter/10.1007/978-3-642-14512-4_13 (accessed 16.11.15).
32. [32] Shinohara, M., Nakajima, N., Uehara, Y., Purification and characterization of a novel esterase (β-hydroxypalmitate methyl ester hydrolase) and prevention of the expression of virulence by Ralstonia solanacearum. J. Appl. Microbiol. 103 (2007), 152–162, 10.1111/j.1365-2672.2006.03222.x.
33. [33] Newman, K.L., Chatterjee, S., Ho, K.A., Lindow, S.E., Virulence of plant pathogenic bacteria attenuated by degradation of fatty acid cell-to-cell signaling factors. Mol. Plant-Microbe Interact. MPMI 21 (2008), 326–334, 10.1094/MPMI-21-3-0326.
34. [34] Carlier, A., Uroz, S., Smadja, B., Fray, R., Latour, X., Dessaux, Y., et al. The Ti plasmid of Agrobacterium tumefaciens harbors an attM-paralogous gene, aiiB, also encoding N-Acyl homoserine lactonase activity. Appl. Environ. Microbiol. 69 (2003), 4989–4993.
35. [35] Zhang, H.-B., Wang, L.-H., Zhang, L.-H., Genetic control of quorum-sensing signal turnover in Agrobacterium tumefaciens. Proc. Natl. Acad. Sci. U. S. A. 99 (2002), 4638–4643, 10.1073/pnas.022056699.
36. [36] Dong, Y.-H., Zhang, X.-F., Xu, J.-L., Zhang, L.-H., Insecticidal Bacillus thuringiensis silences Erwinia carotovora virulence by a new form of microbial antagonism, signal interference. Appl. Environ. Microbiol. 70 (2004), 954–960.
37. [37] Zhang, L., Ruan, L., Hu, C., Wu, H., Chen, S., Yu, Z., et al. Fusion of the genes for AHL-lactonase and S-layer protein in Bacillus thuringiensis increases its ability to inhibit soft rot caused by Erwinia carotovora. Appl. Microbiol. Biotechnol. 74 (2007), 667–675, 10.1007/s00253-006-0696-8.
38. [38] Palma, L., Muñoz, D., Berry, C., Murillo, J., Caballero, P., Bacillus thuringiensis toxins: an overview of their biocidal activity. Toxins 6 (2014), 3296–3325, 10.3390/toxins6123296.
39. [39] Dong, Y.H., Wang, L.H., Xu, J.L., Zhang, H.B., Zhang, X.F., Zhang, L.H., Quenching quorum-sensing-dependent bacterial infection by an N-acyl homoserine lactonase. Nature 411 (2001), 813–817, 10.1038/35081101.
40. [40] D'Angelo-Picard, C., Chapelle, E., Ratet, P., Faure, D., Dessaux, Y., Transgenic plants expressing the quorum quenching lactonase AttM do not significantly alter root-associated bacterial populations. Res. Microbiol. 162 (2011), 951–958, 10.1016/j.resmic.2011.01.009.
41. [41] Molina, L., Constantinescu, F., Michel, L., Reimmann, C., Duffy, B., Défago, G., Degradation of pathogen quorum-sensing molecules by soil bacteria: a preventive and curative biological control mechanism. FEMS Microbiol. Ecol. 45 (2003), 71–81, 10.1016/S0168-6496(03)00125-9.
42. [43] FAO, FAO Global Aquaculture Production Database Updated to 2013 – Summary Information. 2015.
43. [44] Defoirdt, T., Boon, N., Bossier, P., Verstraete, W., Disruption of bacterial quorum sensing: an unexplored strategy to fight infections in aquaculture. Aquaculture 240 (2004), 69–88, 10.1016/j.aquaculture.2004.06.031.
44. [45] Subasinghe, R., Fish health and quarantine. FAO Fish. Circ., 45, 1997.
45. [46] Mortazavi, A.L., Poppin’ the prophylactics: an analysis of antibiotics in aquaculture. J. Glob. Health., 2014 http://www.ghjournal.org/poppin-the-prophylactics-an-analysis-of-antibiotics-in-aquaculture/.
46. [47] Cabello, F.C., Godfrey, H.P., Tomova, A., Ivanova, L., Dölz, H., Millanao, A., et al. Antimicrobial use in aquaculture re-examined: its relevance to antimicrobial resistance and to animal and human health. Environ. Microbiol. 15 (2013), 1917–1942, 10.1111/1462-2920.12134.
47. [48] Buschmann, A.H., Tomova, A., López, A., Maldonado, M.A., Henríquez, L.A., Ivanova, L., et al. Salmon aquaculture and antimicrobial resistance in the marine environment. PLoS One, 7, 2012, e42724, 10.1371/journal.pone.0042724.
48. [49] Romero, J., Gloria, C., Navarrete, P., Antibiotics in aquaculture – use, abuse and alternatives. Carvalho, E., (eds.) Health Environ. Aquac., 2012, InTech http://www.intechopen.com/books/health-and-environment-in-aquaculture/antibiotics-in-aquaculture-use-abuse-and-alternatives (accessed 20.11. 15).
49. [50] Heuer, O.E., Kruse, H., Grave, K., Collignon, P., Karunasagar, I., Angulo, F.J., Human health consequences of use of antimicrobial agents in aquaculture. Clin. Infect. Dis. Off. Publ. Infect. Dis. Soc. Am. 49 (2009), 1248–1253, 10.1086/605667.
50. [51] Defoirdt, T., Sorgeloos, P., Bossier, P., Alternatives to antibiotics for the control of bacterial disease in aquaculture. Curr. Opin. Microbiol. 14 (2011), 251–258, 10.1016/j.mib.2011.03.004.
51. [52] Verschuere, L., Rombaut, G., Sorgeloos, P., Verstraete, W., Probiotic bacteria as biological control agents in aquaculture. Microbiol. Mol. Biol. Rev. MMBR 64 (2000), 655–671.
52. [53] Irianto, A., Austin, B., Probiotics in aquaculture. J. Fish. Dis. 25 (2002), 633–642.
53. [54] Anderson, D.P., Immunostimulants, adjuvants, and vaccine carriers in fish: applications to aquaculture. Annu. Rev. Fish. Dis., 1992, 281–307.
54. [55] Ringø, E., Olsen, R.E., Jensen, I., Romero, J., Lauzon, H.L., Application of vaccines and dietary supplements in aquaculture: possibilities and challenges. Rev. Fish. Biol. Fish. 24 (2014), 1005–1032, 10.1007/s11160-014-9361-y.
55. [56] Adams, A., Thompson, K.D., Biotechnology offers revolution to fish health management. Trends Biotechnol. 24 (2006), 201–205, 10.1016/j.tibtech.2006.03.004.
56. [57] Magnadottir, B., Immunological control of fish diseases. Mar. Biotechnol. 12 (2010), 361–379, 10.1007/s10126-010-9279-x.
57. [58] Gudding, R., Van Muiswinkel, W.B., A history of fish vaccination. Fish. Shellfish Immunol. 35 (2013), 1683–1688, 10.1016/j.fsi.2013.09.031.
58. [59] Cao, Y., He, S., Zhou, Z., Zhang, M., Mao, W., Zhang, H., et al. Orally administered thermostable N-Acyl homoserine lactonase from bacillus sp. strain ai96 attenuates aeromonas hydrophila infection in zebrafish. Appl. Environ. Microbiol. 78 (2012), 1899–1908, 10.1128/AEM.06139-11.
59. [60] Vinoj, G., Vaseeharan, B., Thomas, S., Spiers, A.J., Shanthi, S., Quorum-quenching activity of the AHL-Lactonase from Bacillus licheniformis DAHB1 inhibits vibrio biofilm formation in vitro and reduces shrimp intestinal colonisation and mortality. Mar. Biotechnol. 16 (2014), 707–715, 10.1007/s10126-014-9585-9.
60. [61] Chen, R., Zhou, Z., Cao, Y., Bai, Y., Yao, B., Research High yield expression of an AHL-lactonase from Bacillus sp. B546 in Pichia pastoris and its application to reduce Aeromonas hydrophila mortality in aquaculture. Microb. Cell Factories, 9, 2010, 39.
61. [62] Romero, M., Muras, A., Mayer, C., Buján, N., Magariños, B., Otero, A., In vitro quenching of fish pathogen Edwardsiella tarda AHL production using marine bacterium Tenacibaculum sp. strain 20J cell extracts. Dis. Aquat. Organ 108 (2014), 217–225, 10.3354/dao02697.
62. [63] Tinh, N.T.N., Asanka Gunasekara, R.A.Y.S., Boon, N., Dierckens, K., Sorgeloos, P., Bossier, P., N-acyl homoserine lactone-degrading microbial enrichment cultures isolated from Penaeus vannamei shrimp gut and their probiotic properties in Brachionus plicatilis cultures: probiotic properties of AHL-degrading enrichment cultures. FEMS Microbiol. Ecol. 62 (2007), 45–53, 10.1111/j.1574-6941.2007.00378.x.
63. [64] Bourne, D.G., Høj, L., Webster, N.S., Swan, J., Hall, M.R., Biofilm development within a larval rearing tank of the tropical rock lobster, Panulirus ornatus. Aquaculture 260 (2006), 27–38, 10.1016/j.aquaculture.2006.06.023.
64. [65] Drews, A., Membrane fouling in membrane bioreactors—Characterisation, contradictions, cause and cures. J. Membr. Sci. 363 (2010), 1–28, 10.1016/j.memsci.2010.06.046.
65. [66] Yeon, K.-M., Cheong, W.-S., Oh, H.-S., Lee, W.-N., Hwang, B.-K., Lee, C.-H., et al. Quorum sensing: a new biofouling control paradigm in a membrane bioreactor for advanced wastewater treatment. Environ. Sci. Technol. 43 (2009), 380–385, 10.1021/es8019275.
66. [67] Xiong, Y., Liu, Y., Biological control of microbial attachment: a promising alternative for mitigating membrane biofouling. Appl. Microbiol. Biotechnol. 86 (2010), 825–837, 10.1007/s00253-010-2463-0.
67. [68] Wang, Z., Ma, J., Tang, C.Y., Kimura, K., Wang, Q., Han, X., Membrane cleaning in membrane bioreactors: a review. J. Membr. Sci. 468 (2014), 276–307, 10.1016/j.memsci.2014.05.060.
68. [69] Ponnusamy, K., Kappachery, S., Thekeettle, M., Song, J.H., Kweon, J.H., Anti-biofouling property of vanillin on Aeromonas hydrophila initial biofilm on various membrane surfaces. World J. Microbiol. Biotechnol. 29 (2013), 1695–1703, 10.1007/s11274-013-1332-2.
69. [70] Siddiqui, M.F., Sakinah, M., Ismail, A.F., Matsuura, T., Zularisam, A.W., The anti-biofouling effect of Piper betle extract against Pseudomonas aeruginosa and bacterial consortium. Desalination 288 (2012), 24–30, 10.1016/j.desal.2011.11.060.
70. [71] Siddiqui, M.F., Sakinah, M., Singh, L., Zularisam, A.W., Targeting N-acyl-homoserine-lactones to mitigate membrane biofouling based on quorum sensing using a biofouling reducer. J. Biotechnol. 161 (2012), 190–197, 10.1016/j.jbiotec.2012.06.029.
71. [72] Kim, J.-H., Choi, D.-C., Yeon, K.-M., Kim, S.-R., Lee, C.-H., Enzyme-immobilized nanofiltration membrane to mitigate biofouling based on quorum quenching. Environ. Sci. Technol. 45 (2011), 1601–1607, 10.1021/es103483j.
72. [73] Jiang, W., Xia, S., Liang, J., Zhang, Z., Hermanowicz, S.W., Effect of quorum quenching on the reactor performance, biofouling and biomass characteristics in membrane bioreactors. Water Res. 47 (2013), 187–196, 10.1016/j.watres.2012.09.050.
73. [74] Kim, H.-W., Oh, H.-S., Kim, S.-R., Lee, K.-B., Yeon, K.-M., Lee, C.-H., et al. Microbial population dynamics and proteomics in membrane bioreactors with enzymatic quorum quenching. Appl. Microbiol. Biotechnol. 97 (2012), 4665–4675, 10.1007/s00253-012-4272-0.
74. [75] Lee, B., Yeon, K.-M., Shim, J., Kim, S.-R., Lee, C.-H., Lee, J., et al. Effective antifouling using quorum-quenching acylase stabilized in magnetically-separable mesoporous silica. Biomacromolecules 15 (2014), 1153–1159, 10.1021/bm401595q.
75. [76] Oh, H.-S., Yeon, K.-M., Yang, C.-S., Kim, S.-R., Lee, C.-H., Park, S.Y., et al. Control of membrane biofouling in MBR for wastewater treatment by quorum quenching bacteria encapsulated in microporous membrane. Environ. Sci. Technol. 46 (2012), 4877–4884, 10.1021/es204312u.
76. [77] Kim, S.-R., Oh, H.-S., Jo, S.-J., Yeon, K.-M., Lee, C.-H., Lim, D.-J., et al. Biofouling control with bead-entrapped quorum quenching bacteria in membrane bioreactors: physical and biological effects. Environ. Sci. Technol. 47 (2013), 836–842, 10.1021/es303995s.
77. [78] Weerasekara, N.A., Choo, K.-H., Lee, C.-H., Hybridization of physical cleaning and quorum quenching to minimize membrane biofouling and energy consumption in a membrane bioreactor. Water Res. 67 (2014), 1–10, 10.1016/j.watres.2014.08.049.
78. [79] Maqbool, T., Khan, S.J., Waheed, H., Lee, C.-H., Hashmi, I., Iqbal, H., Membrane biofouling retardation and improved sludge characteristics using quorum quenching bacteria in submerged membrane bioreactor. J. Membr. Sci. 483 (2015), 75–83, 10.1016/j.memsci.2015.02.011.
79. [80] Kim, S.-R., Lee, K.-B., Kim, J.-E., Won, Y.-J., Yeon, K.-M., Lee, C.-H., et al. Macroencapsulation of quorum quenching bacteria by polymeric membrane layer and its application to MBR for biofouling control. J. Membr. Sci. 473 (2015), 109–117, 10.1016/j.memsci.2014.09.009.
80. [81] Kristensen, J.B., Meyer, R.L., Laursen, B.S., Shipovskov, S., Besenbacher, F., Poulsen, C.H., Antifouling enzymes and the biochemistry of marine settlement. Biotechnol. Adv. 26 (2008), 471–481, 10.1016/j.biotechadv.2008.05.005.
81. [82] Cordeiro, A.L., Werner, C., Enzymes for antifouling strategies. J. Adhes. Sci. Technol. 25 (2011), 2317–2344, 10.1163/016942411X574961.
82. [83] Ciriminna, R., Bright, F.V., Pagliaro, M., Ecofriendly antifouling marine coatings. ACS Sustain. Chem. Eng. 3 (2015), 559–565, 10.1021/sc500845n.
83. [84] Olsen, S.M., Pedersen, L.T., Laursen, M.H., Kiil, S., Dam-Johansen, K., Enzyme-based antifouling coatings: a review. Biofouling 23 (2007), 369–383, 10.1080/08927010701566384.
84. [85] Tait, K., Joint, I., Daykin, M., Milton, D.L., Williams, P., Camara, M., Disruption of quorum sensing in seawater abolishes attraction of zoospores of the green alga Ulva to bacterial biofilms. Environ. Microbiol. 7 (2005), 229–240, 10.1111/j.1462-2920.2004.00706.x.
85. [86] Dobretsov, S., Dahms, H.-U., YiLi, H., Wahl, M., Qian, P.-Y., The effect of quorum-sensing blockers on the formation of marine microbial communities and larval attachment: antifouling activity of QS blockers. FEMS Microbiol. Ecol. 60 (2007), 177–188, 10.1111/j.1574-6941.2007.00285.x.
86. [87] Dobretsov, S., Teplitski, M., Bayer, M., Gunasekera, S., Proksch, P., Paul, V.J., Inhibition of marine biofouling by bacterial quorum sensing inhibitors. Biofouling 27 (2011), 893–905, 10.1080/08927014.2011.609616.
87. [88] Sievert, D.M., Ricks, P., Edwards, J.R., Schneider, A., Patel, J., Srinivasan, A., et al. National healthcare safety network (NHSN) team and participating NHSN facilities, antimicrobial-resistant pathogens associated with healthcare-associated infections: summary of data reported to the national healthcare safety network at the centers for disease control and prevention, 2009-2010. Infect. Control Hosp. Epidemiol. Off. J. Soc. Hosp. Epidemiol. Am. 34 (2013), 1–14, 10.1086/668770.
88. [89] Ng, W.-L., Bassler, B.L., Bacterial quorum-sensing network architectures. Annu. Rev. Genet. 43 (2009), 197–222, 10.1146/annurev-genet-102108-134304.
89. [90] Antunes, L.C.M., Ferreira, R.B.R., Buckner, M.M.C., Finlay, B.B., Quorum sensing in bacterial virulence. Microbiology 156 (2010), 2271–2282, 10.1099/mic.0.038794-0.
90. [91] Antonova, E.S., Hammer, B.K., Genetics of natural competence in vibrio cholerae and other vibrios. Microbiol. Spectr., 3, 2015, 10.1128/microbiolspec.VE-0010-2014.
91. [92] Ng, F.S.W., Wright, D.M., Seah, S.Y.K., Characterization of a phosphotriesterase-like lactonase from sulfolobus solfataricus and its immobilization for disruption of quorum sensing. Appl. Environ. Microbiol. 77 (2011), 1181–1186, 10.1128/AEM.01642-10.
92. [93] Jacobsen, S.M., Stickler, D.J., Mobley, H.L.T., Shirtliff, M.E., Complicated catheter-associated urinary tract infections due to Escherichia coli and Proteus mirabilis. Clin. Microbiol. Rev. 21 (2008), 26–59, 10.1128/CMR.00019-07.
93. [94] Walz, J.M., Avelar, R.L., Longtine, K.J., Carter, K.L., Mermel, L.A., Heard, S.O., 5-FU Catheter Study Group, Anti-infective external coating of central venous catheters: a randomized, noninferiority trial comparing 5-fluorouracil with chlorhexidine/silver sulfadiazine in preventing catheter colonization. Crit. Care Med. 38 (2010), 2095–2102, 10.1097/CCM.0b013e3181f265ba.
94. [95] Ivanova, K., Fernandes, M.M., Mendoza, E., Tzanov, T., Enzyme multilayer coatings inhibit Pseudomonas aeruginosa biofilm formation on urinary catheters. Appl. Microbiol. Biotechnol. 99 (2015), 4373–4385, 10.1007/s00253-015-6378-7.
95. [96] Ivanova, K., Fernandes, M.M., Francesko, A., Mendoza, E., Guezguez, J., Burnet, M., et al. Quorum-quenching and matrix-degrading enzymes in multilayer coatings synergistically prevent bacterial biofilm formation on urinary catheters. ACS Appl. Mater. Interfaces 7:49 (2015), 27066–27077, 10.1021/acsami.5b09489.
96. [97] Gupta, P., Chhibber, S., Harjai, K., Efficacy of purified lactonase and ciprofloxacin in preventing systemic spread of Pseudomonas aeruginosa in murine burn wound model, Burns J. Int. Soc. Burn Inj. 41:1 (February 2015), 153–162, 10.1016/j.burns.2014.06.009.
97. [98] Guttenplan, S.B., Kearns, D.B., Regulation of flagellar motility during biofilm formation. FEMS Microbiol. Rev. 37 (2013), 849–871, 10.1111/1574-6976.12018.
98. [99] Hraiech, S., Hiblot, J., Lafleur, J., Lepidi, H., Papazian, L., Rolain, J.-M., et al. Inhaled lactonase reduces pseudomonas aeruginosa quorum sensing and mortality in rat pneumonia. PLoS One, 9, 2014, e107125, 10.1371/journal.pone.0107125.
99. [100] Afriat, L., Roodveldt, C., Manco, G., Tawfik, D.S., The latent promiscuity of newly identified microbial lactonases is linked to a recently diverged phosphotriesterase†. Biochem. (Mosc.) 45 (2006), 13677–13686, 10.1021/bi061268r.
100. [101] Afriat-Jurnou, L., Jackson, C.J., Tawfik, D.S., Reconstructing a missing link in the evolution of a recently diverged phosphotriesterase by active-site loop remodeling. Biochem. (Mosc.) 51 (2012), 6047–6055, 10.1021/bi300694t.
101. [102] Elias, M., Tawfik, D.S., Divergence and convergence in enzyme evolution: parallel evolution of paraoxonases from quorum-quenching lactonases. J. Biol. Chem. 287 (2011), 11–20, 10.1074/jbc.R111.257329.
102. [103] Elias, M., Dupuy, J., Merone, L., Mandrich, L., Porzio, E., Moniot, S., et al. Structural basis for natural lactonase and promiscuous phosphotriesterase activities. J. Mol. Biol. 379 (2008), 1017–1028, 10.1016/j.jmb.2008.04.022.
103. [104] Hiblot, J., Bzdrenga, J., Champion, C., Chabriere, E., Elias, M., Crystal structure of VmoLac, a tentative quorum quenching lactonase from the extremophilic crenarchaeon Vulcanisaeta moutnovskia. Sci. Rep., 5, 2015, 8372, 10.1038/srep08372.
104. [105] Xue, B., Chow, J.Y., Baldansuren, A., Yap, L.L., Gan, Y.H., Dikanov, S.A., et al. Structural evidence of a productive active site architecture for an evolved quorum-quenching GKL Lactonase. Biochem. (Mosc.) 52 (2013), 2359–2370, 10.1021/bi4000904.
105. [106] Bzdrenga, J., Hiblot, J., Gotthard, G., Champion, C., Elias, M., Chabriere, E., SacPox from the thermoacidophilic crenarchaeon Sulfolobus acidocaldarius is a proficient lactonase. BMC Res. Notes, 7, 2014, 333, 10.1186/1756-0500-7-333.
106. [107] Hiblot, J., Gotthard, G., Chabriere, E., Elias, M., Structural and enzymatic characterization of the lactonase SisLac from sulfolobus islandicus. PLoS One, 7, 2012, e47028, 10.1371/journal.pone.0047028.
107. [108] Vecchio, P., Elias, M., Merone, L., Graziano, G., Dupuy, J., Mandrich, L., et al. Structural determinants of the high thermal stability of SsoPox from the hyperthermophilic archaeon Sulfolobus solfataricus. Extremophiles 13 (2009), 461–470, 10.1007/s00792-009-0231-9.
108. [109] Hiblot, J., Gotthard, G., Elias, M., Chabriere, E., Differential active site loop conformations mediate promiscuous activities in the lactonase SsoPox. PLoS One, 8, 2013, e75272, 10.1371/journal.pone.0075272.
109. [110] Hiblot, J., Gotthard, G., Chabriere, E., Elias, M., Characterisation of the organophosphate hydrolase catalytic activity of SsoPox. Sci. Rep., 2, 2012, 10.1038/srep00779.
110. [111] Hiblot, J., Gotthard, G., Champion, C., Chabriere, E., Elias, M., Crystallization and preliminary X-ray diffraction analysis of the lactonase VmoLac from Vulcanisaeta moutnovskia. Acta Crystallogr. Sect. F. Struct. Biol. Cryst. Commun. 69 (2013), 1235–1238, 10.1107/S1744309113024846.
111. [112] Chow, J.Y., Wu, L., Yew, W.S., Directed Evolution of a Quorum-Quenching Lactonase from Mycobacterium avium subsp. paratuberculosis K-10 in the amidohydrolase superfamily. Biochem. (Mosc.) 48 (2009), 4344–4353, 10.1021/bi9004045.
112. [113] Chow, J.Y., Xue, B., Lee, K.H., Tung, A., Wu, L., Robinson, R.C., et al. Directed evolution of a thermostable quorum-quenching lactonase from the amidohydrolase superfamily. J. Biol. Chem. 285 (2010), 40911–40920, 10.1074/jbc.M110.177139.
113. [114] Dong, Y.-H., Xu, J.-L., Li, X.-Z., Zhang, L.-H., AiiA, an enzyme that inactivates the acylhomoserine lactone quorum-sensing signal and attenuates the virulence of Erwinia carotovora. Proc. Natl. Acad. Sci. 97 (2000), 3526–3531, 10.1073/pnas.97.7.3526.
114. [115] Liu, D., Thomas, P.W., Momb, J., Hoang, Q.Q., Petsko, G.A., Ringe, D., et al. Structure and specificity of a quorum-quenching lactonase (AiiB) from Agrobacterium tumefaciens†,‡. Biochem. (Mosc.) 46 (2007), 11789–11799, 10.1021/bi7012849.
115. [116] Merone, L., Mandrich, L., Rossi, M., Manco, G., A thermostable phosphotriesterase from the archaeon Sulfolobus solfataricus: cloning, overexpression and properties. Extremophiles 9 (2005), 297–305, 10.1007/s00792-005-0445-4.
116. [117] Elias, M., Dupuy, J., Merone, L., Lecomte, C., Rossi, M., Masson, P., et al. Crystallization and preliminary X-ray diffraction analysis of the hyperthermophilic Sulfolobus solfataricus phosphotriesterase. Acta Crystallogr. Sect. F. Struct. Biol. Cryst. Commun. 63 (2007), 553–555, 10.1107/S1744309107023512.
117. [118] Elias, M., Dupuy, J., Merone, L., Mandrich, L., Porzio, E., Moniot, S., et al. Structural basis for natural lactonase and promiscuous phosphotriesterase activities. J. Mol. Biol. 379 (2008), 1017–1028, 10.1016/j.jmb.2008.04.022.
118. [119] Alanis, A.J., Resistance to antibiotics: are we in the post-antibiotic era?. Arch. Med. Res. 36 (2005), 697–705, 10.1016/j.arcmed.2005.06.009.
119. [120] Wright, G.D., Bacterial resistance to antibiotics: enzymatic degradation and modification. Adv. Drug Deliv. Rev. 57 (2005), 1451–1470, 10.1016/j.addr.2005.04.002.
120. [121] Kumar, A., Schweizer, H.P., Bacterial resistance to antibiotics: active efflux and reduced uptake. Adv. Drug Deliv. Rev. 57 (2005), 1486–1513, 10.1016/j.addr.2005.04.004.
121. [122] Hentzer, M., Wu, H., Andersen, J.B., Riedel, K., Rasmussen, T.B., Bagge, N., et al. Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitors. EMBO J. 22 (2003), 3803–3815, 10.1093/emboj/cdg366.
122. [123] Waters, C.M., Bassler, B.L., Quorum sensing: cell-to-cell communication in bacteria. Annu. Rev. Cell Dev. Biol. 21 (2005), 319–346, 10.1146/annurev.cellbio.21.012704.131001.
123. [124] Romero, M., Acuna, L., Otero, A., Patents on quorum quenching: interfering with bacterial communication as a strategy to fight infections. Recent Pat. Biotechnol. 6 (2012), 2–12, 10.2174/187220812799789208.
124. [125] Uroz, S., Dessaux, Y., Oger, P., Quorum sensing and quorum quenching: the yin and yang of bacterial communication. Chembiochem Eur. J. Chem. Biol. 10 (2009), 205–216, 10.1002/cbic.200800521.
125. [126] Diggle, S.P., Griffin, A.S., Campbell, G.S., West, S.A., Cooperation and conflict in quorum-sensing bacterial populations. Nature 450 (2007), 411–414, 10.1038/nature06279.
126. [127] Defoirdt, T., Boon, N., Bossier, P., Can bacteria evolve resistance to quorum sensing disruption?. PLoS Pathog., 6, 2010, e1000989, 10.1371/journal.ppat.1000989.
127. [128] García-Contreras, R., Maeda, T., Wood, T.K., Resistance to quorum-quenching compounds. Appl. Environ. Microbiol. 79 (2013), 6840–6846, 10.1128/AEM.02378-13.
128. [129] García-Contreras, R., Nuñez-López, L., Jasso-Chávez, R., Kwan, B.W., Belmont, J.A., Rangel-Vega, A., et al. Quorum sensing enhancement of the stress response promotes resistance to quorum quenching and prevents social cheating. ISME J. 9 (2015), 115–125, 10.1038/ismej.2014.98.
129. [130] Maeda, T., García-Contreras, R., Pu, M., Sheng, L., Garcia, L.R., Tomás, M., et al. Quorum quenching quandary: resistance to antivirulence compounds. ISME J. 6 (2012), 493–501, 10.1038/ismej.2011.122.
130. [131] Sandoz, K.M., Mitzimberg, S.M., Schuster, M., Social cheating in Pseudomonas aeruginosa quorum sensing. Proc. Natl. Acad. Sci. U. S. A. 104 (2007), 15876–15881, 10.1073/pnas.0705653104.
131. [132] Tay, S.B., Yew, W.S., Development of quorum-based anti-virulence therapeutics targeting Gram-negative bacterial pathogens. Int. J. Mol. Sci. 14 (2013), 16570–16599, 10.3390/ijms140816570.
132. [133] Gerdt, J.P., Blackwell, H.E., Competition studies confirm two major barriers that can preclude the spread of resistance to quorum-sensing inhibitors in bacteria. ACS Chem. Biol. 9 (2014), 2291–2299, 10.1021/cb5004288.
133. [134] Collins, C.H., Arnold, F.H., Leadbetter, J.R., Directed evolution of Vibrio fischeri LuxR for increased sensitivity to a broad spectrum of acyl-homoserine lactones. Mol. Microbiol. 55 (2005), 712–723, 10.1111/j.1365-2958.2004.04437.x.
134. [135] Hawkins, A.C., Arnold, F.H., Stuermer, R., Hauer, B., Leadbetter, J.R., Directed evolution of Vibrio fischeri LuxR for improved response to butanoyl-homoserine lactone. Appl. Environ. Microbiol. 73 (2007), 5775–5781, 10.1128/AEM.00060-07.
135. [136] Mah, T.F., O'Toole, G.A., Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol. 9 (2001), 34–39.
136. [137] Stewart, P.S., Costerton, J.W., Antibiotic resistance of bacteria in biofilms. Lancet Lond. Engl. 358 (2001), 135–138.
137. [138] Drenkard, E., Ausubel, F.M., Pseudomonas biofilm formation and antibiotic resistance are linked to phenotypic variation. Nature 416 (2002), 740–743, 10.1038/416740a.
138. [139] Stewart, P.S., Mechanisms of antibiotic resistance in bacterial biofilms. Int. J. Med. Microbiol. IJMM 292 (2002), 107–113, 10.1078/1438-4221-00196.
139. [140] Mah, T.-F., Pitts, B., Pellock, B., Walker, G.C., Stewart, P.S., O'Toole, G.A., A genetic basis for Pseudomonas aeruginosa biofilm antibiotic resistance. Nature 426 (2003), 306–310, 10.1038/nature02122.
140. [141] Høiby, N., Bjarnsholt, T., Givskov, M., Molin, S., Ciofu, O., Antibiotic resistance of bacterial biofilms. Int. J. Antimicrob. Agents 35 (2010), 322–332, 10.1016/j.ijantimicag.2009.12.011.
141. [142] Breidenstein, E.B.M., de la Fuente-Núñez, C., Hancock, R.E.W., Pseudomonas aeruginosa: all roads lead to resistance. Trends Microbiol. 19 (2011), 419–426, 10.1016/j.tim.2011.04.005.
142. [143] Kiran, S., Sharma, P., Harjai, K., Capalash, N., Enzymatic quorum quenching increases antibiotic susceptibility of multidrug resistant Pseudomonas aeruginosa. Iran. J. Microbiol. 3 (2011), 1–12.