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Korean Society for Biochemistry and Molecular Biology (생화학분자생물학회)
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Microbial linguistics: perspectives and applications of microbial cell-to-cell communication

  • Mitchell, Robert J. (School of Nano-Bioscience and Chemical Engineering, Ulsan National Institute of Science and Technology (UNIST)) ;
  • Lee, Sung-Kuk (School of Nano-Bioscience and Chemical Engineering, Ulsan National Institute of Science and Technology (UNIST)) ;
  • Kim, Tae-Sung (School of Mechanical and Advanced Materials Engineering, Ulsan National Institute of Science and Technology (UNIST)) ;
  • Ghim, Cheol-Min (School of Nano-Bioscience and Chemical Engineering, Ulsan National Institute of Science and Technology (UNIST))
  • Received : 2011.01.12
  • Published : 2011.01.31
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Abstract

Inter-cellular communication via diffusible small molecules is a defining character not only of multicellular forms of life but also of single-celled organisms. A large number of bacterial genes are regulated by the change of chemical milieu mediated by the local population density of its own species or others. The cell density-dependent "autoinducer" molecules regulate the expression of those genes involved in genetic competence, biofilm formation and persistence, virulence, sporulation, bioluminescence, antibiotic production, and many others. Recent innovations in recombinant DNA technology and micro-/nano-fluidics systems render the genetic circuitry responsible for cell-to-cell communication feasible to and malleable via synthetic biological approaches. Here we review the current understanding of the molecular biology of bacterial intercellular communication and the novel experimental protocols and platforms used to investigate this phenomenon. A particular emphasis is given to the genetic regulatory circuits that provide the standard building blocks which constitute the syntax of the biochemical communication network. Thus, this review gives focus to the engineering principles necessary for rewiring bacterial chemo-communication for various applications, ranging from population-level gene expression control to the study of host-pathogen interactions.

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References

  1. Bhattacharyya, R. P., Remenyi, A., Yeh, B. J. and Lim, W. A. (2006) Domains, motifs, and scaffolds: the role of modular interactions in the evolution and wiring of cell signaling circuits. Ann. Rev. Biochem. 75, 655-680. https://doi.org/10.1146/annurev.biochem.75.103004.142710
  2. Bassler, B. L. and Losick, R. (2006) Bacterially speaking. Cell 125, 237-246. https://doi.org/10.1016/j.cell.2006.04.001
  3. Wagner, V. E., Bushnell, D., Passador, L., Brooks, A. I. and Iglewski, B. H. (2003) Microarray analysis of Pseudomonas aeruginosa quorum-sensing regulons: effects of growth phase and environment. J. Bacteriol. 185, 2080-2095. https://doi.org/10.1128/JB.185.7.2080-2095.2003
  4. You, L., Cox, R. S., Weiss, R. and Arnold, F. H. (2004) Programmed population control by cell-cell communication and regulated killing. Nature 428, 868-871. https://doi.org/10.1038/nature02491
  5. Choudhary, S. and Schmidt-Dannert, C. (2010) Applications of quorum sensing in biotechnology. Appl. Microbiol. Biotechnol. 86, 1267-1279. https://doi.org/10.1007/s00253-010-2521-7
  6. Rasmussen, T. B. and Givskov, M. (2006) Quorum-sensing inhibitors as anti-pathogenic drugs. Int. J. Med. Microbiol. 296, 149-161.
  7. Lerat, E. and Moran, N. A. (2004) Evolutionary history of quorum-sensing systems in bacteria. Mol. Biol. Evol. 21, 903-913. https://doi.org/10.1093/molbev/msh097
  8. Fuqua, W. C., Winans, S. C. and Greenberg, E. P. (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
  9. Hense, B. A., Kuttler, C., Müller, J., Rothballer, M., Hartmann, A. and Kreft, J. U. (2007) Does efficiency sensing unify diffusion and quorum sensing? Nat. Rev. Microbiol. 5, 230-239. https://doi.org/10.1038/nrmicro1600
  10. Nealson, K. H., Platt, T. and Hastings, J. W. (1970) Cellular control of the synthesis and activity of the bacterial luminescent system. J. Bacteriol. 104, 313-322.
  11. Eberhard, A. (1972) Inhibition and activation of bacterial luciferase synthesis. J. Bacteriol. 109, 1101-1105.
  12. 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. https://doi.org/10.1021/bi00512a013
  13. Shaw, P. D., Ping, G., Daly, S. L., Cha, C., Cronan, J. E. Jr., Rinehart, K. L. and Farrand, S. K. (1997) Detecting and characterizing N-acyl-homoserine lactone signal molecules by thin-layer chromatography. Proc. Natl. Acad. Sci. U.S.A. 94, 6036-6041. https://doi.org/10.1073/pnas.94.12.6036
  14. McClean, K. H., Winson, M. K., Fish, L., Taylor, A., Chhabra, S. R., Camara, M., Daykin, M., Lamb, J. H., Swift, S., Bycroft, B. W., Stewart, G. S. and Williams P. (1997) Quorum sensing and Chromobacterium violaceum: exploitation of violacein production and inhibition for the detection of N-acylhomoserine lactones. Microbiology 143, 3703-3711. https://doi.org/10.1099/00221287-143-12-3703
  15. Blosser, R. S. and Gray, K. M. (2000) Extraction of violacein from Chromobacterium violaceum provides a new quantitative bioassay for N-acyl homoserine lactone autoinducers. J. Microbiol. Methods 40, 47-55. https://doi.org/10.1016/S0167-7012(99)00136-0
  16. Charlton, T. S., de Nys, R., Netting, A., Kumar, N., Hentzer, M., Givskov, M. and Kjelleberg, S. (2000) A novel and sensitive method for the quantification of N-3-oxoacyl homoserine lactones using gas chromatographymass spectrometry: application to a model bacterial biofilm. Environ. Microbiol. 2, 530-541. https://doi.org/10.1046/j.1462-2920.2000.00136.x
  17. Winson, M. K, Swift, S., Fish, L., Throup, J. P., Jørgensen, F., Chhabra, S. R., Bycroft, B. W., Williams, P. and Stewart, G. S. (1998) Construction and analysis of luxCDABE-based plasmid sensors for investigating N-acyl homoserine lactone-mediated quorum sensing. FEMS Microbiol. Lett. 163, 185-192. https://doi.org/10.1111/j.1574-6968.1998.tb13044.x
  18. Andersen, J. B., Heydorn, A., Hentzer, M., Eberl, L., Geisenberger, O., Christensen, B. B., Molin, S. and Givskov, M. (2001) gfp-based N-acyl homoserine-lactone sensor systems for detection of bacterial communication. Appl. Environ. Microbiol. 67, 575-585. https://doi.org/10.1128/AEM.67.2.575-585.2001
  19. Ji, G., Beavis, R. and Novick, R. P. (1997) Bacterial interference caused by autoinducing peptide variants. Science 276, 2027-2030. https://doi.org/10.1126/science.276.5321.2027
  20. Mayville, P., Ji, G., Beavis, R., Yang, H., Goger, M., Novick, R. P. and Muir, T. W. (1999) Structure-activity analysis of synthetic autoinducing thiolactone peptides from Staphylococcus aureus responsible for virulence. Proc. Natl. Acad. Sci. U.S.A. 96, 1218-1223. https://doi.org/10.1073/pnas.96.4.1218
  21. Xavier, K. B., and Bassler, B. L. (2003) LuxS quorum sensing: more than just a numbers game. Curr. Opin. Microbiol. 6, 191-197. https://doi.org/10.1016/S1369-5274(03)00028-6
  22. Vendeville, A., Winzer, K., Heurlier, K., Tang, C. M. and Hardie, K. R. (2005) Making 'sense' of metabolism: autoinducer-2, LuxS and pathogenic bacteria. Nat. Rev. Microbiol. 3, 383-396. https://doi.org/10.1038/nrmicro1146
  23. Schauder, S., Shokat, K., Surette, M. G. and Bassler, B. L. (2001) The LuxS family of bacterial autoinducers: biosynthesis of a novel quorum-sensing signal molecule. Mol. Microbiol. 41, 463-476. https://doi.org/10.1046/j.1365-2958.2001.02532.x
  24. Sun, J., Daniel, R., Wagner-Döbler, I. and Zeng, A. P. (2004) Is autoinducer-2 a universal signal for interspecies communication: a comparative genomic and phylogenetic analysis of the synthesis and signal transduction pathways. BMC Evol. Biol. 4, 36. https://doi.org/10.1186/1471-2148-4-36
  25. Pottathil, M. and Lazazzera, B. A. (2003) The extracellular Phr peptide-Rap phosphatase signaling circuit of Bacillus subtilis. Front. Biosci. 8, d32-45. https://doi.org/10.2741/913
  26. Aceves-Diez, A. E., Robles-Burgueño, R. and de la Torre, M. (2007) SKPDT is a signaling peptide that stimulates sporulation and cry1Aa expression in Bacillus thuringiensis but not in Bacillus subtilis. Appl. Microbiol. Biotechnol. 76, 203-209. https://doi.org/10.1007/s00253-007-0982-0
  27. Pierson, L. S. 3rd, Wood, D. W. and Pierson, E. A. (1998) Homoserine lactone-mediated gene regulation in plant-associated bacteria. Ann. Rev. Phytopathol. 36, 207-225. https://doi.org/10.1146/annurev.phyto.36.1.207
  28. d'Angelo-Picard, C., Faure, D., Penot, I. and Dessaux, Y. (2005) Diversity of N-acyl homoserine lactone-producing and degrading bacteria in soil and tobacco rhizosphere. Environ. Microbiol. 7, 1796-1808. https://doi.org/10.1111/j.1462-2920.2005.00886.x
  29. Wang, Y. J. and Leadbetter, J. R. (2005) Rapid acyl-homoserine lactone quorum signal biodegradation in diverse soils. Appl. Environ. Microbiol. 71, 1291-1299. https://doi.org/10.1128/AEM.71.3.1291-1299.2005
  30. Schaefer, A. L., Hanzelka, B. L., Parsek, M. R. and Greenberg, E. P. (2000) Detection, purification, and structural elucidation of the acylhomoserine lactone inducer of Vibrio fischeri luminescence and other related molecules. Methods Enzymol. 305, 288-301. https://doi.org/10.1016/S0076-6879(00)05495-1
  31. Dong, Y. H., Xu, J. L., Li, X. Z. and Zhang, L. H. (2000) 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, 3526-3531. https://doi.org/10.1073/pnas.060023897
  32. Dong, Y. H., Wang, L. H., Xu, J. L., Zhang, H. B., Zhang, X. F. and Zhang, L. H. (2001) Quenching quorum-sensing-dependent bacterial infection by an N-acyl homoserine lactonase. Nature 411, 813-817. https://doi.org/10.1038/35081101
  33. Dong, Y. H., Gusti, A. R., Zhang, Q., Xu, J. L. and Zhang, L. H. (2002) Identification of quorum-quenching N-acyl homoserine lactonases from Bacillus species. Appl. Environ. Microbiol. 68, 1754-1759. https://doi.org/10.1128/AEM.68.4.1754-1759.2002
  34. Zhang, H. B., Wang, L. H. and Zhang, L. H. (2002) Genetic control of quorum-sensing signal turnover in Agrobacterium tumefaciens. Proc. Natl. Acad. Sci. U.S.A. 99, 4638-4643. https://doi.org/10.1073/pnas.022056699
  35. 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. https://doi.org/10.1099/mic.0.26269-0
  36. Leadbetter, J. R. and Greenberg, E. P. (2000) Metabolism of acyl-homoserine lactone quorum-sensing signals by Variovorax paradoxus. J. Bacteriol. 182, 6921-6926. https://doi.org/10.1128/JB.182.24.6921-6926.2000
  37. Huang, J. J., Han, J. I., Zhang, L. H. and Leadbetter, J. R. (2003) Utilization of acyl-homoserine lactone quorum signals for growth by a soil pseudomonad and Pseudomonas aeruginosa PAO1. Appl. Environ. Microbiol. 69, 5941-5949. https://doi.org/10.1128/AEM.69.10.5941-5949.2003
  38. 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. https://doi.org/10.1046/j.1365-2958.2003.03351.x
  39. Surette, M. G. and Bassler, B. L. (1998) Quorum sensing in Escherichia coli and Salmonella typhimurium. Proc. Natl. Acad. Sci. U.S.A. 95, 7046-7050. https://doi.org/10.1073/pnas.95.12.7046
  40. Surette, M. G. and Bassler, B. L. (1999) Regulation of autoinducer production in Salmonella typhimurium. Mol. Microbiol. 31, 585-595. https://doi.org/10.1046/j.1365-2958.1999.01199.x
  41. Xavier, K. B. and Bassler, B. L. (2005) Regulation of uptake and processing of the quorum-sensing autoinducer AI-2 in Escherichia coli. J. Bacteriol. 187, 238-248. https://doi.org/10.1128/JB.187.1.238-248.2005
  42. Xavier, K. B. and Bassler, B. L. (2005) Interference with AI-2-mediated bacterial cell-cell communication. Nature 437, 750-753. https://doi.org/10.1038/nature03960
  43. Redfield, R. J. (2002) Is quorum sensing a side effect of diffusion sensing? Trends Microbiol. 10, 365-370. https://doi.org/10.1016/S0966-842X(02)02400-9
  44. Keller, L. and Surette, M. G. (2006) Communication in bacteria: an ecological and evolutionary perspective. Nat. Rev. Microbiol. 4, 249-258. https://doi.org/10.1038/nrmicro1383
  45. Klausen, M., Gjermansen, M., Kreft, J. U. and Tolker-Nielsen, T. (2006) Dynamics of development and dispersal in sessile microbial communities: examples from Pseudomonas aeruginosa and Pseudomonas putida model biofilms. FEMS Microbiol. Lett. 261, 1-11. https://doi.org/10.1111/j.1574-6968.2006.00280.x
  46. Weibel, D. B., DiLuzio, W. R. and Whitesides, G. M. (2007) Microfabrication meets microbiology. Nat. Rev. Microbiol. 5, 209-218. https://doi.org/10.1038/nrmicro1616
  47. Ghim, C.-M., Kim, T. S. Mitchell, R. J. and Lee, S. K. (2010) Synthetic biology for biofuels: building designer microbes from the scratch. Biotech. Bioproc. Eng. 15, 11-21. https://doi.org/10.1007/s12257-009-3065-5
  48. Gulati, S., Rouilly, V., Niu, X., Chappell, J., Kitney, R. I., Edel, J. B., Freemont, P. S. and deMello, A. J. (2009) Opportunities for microfluidic technologies in synthetic biology. J. Roy. Soc. Interface 6, S493-506. https://doi.org/10.1098/rsif.2009.0083.focus
  49. Ingham, C. J., Sprenkels, A., Bomer, J., Molenaar, D., van den Berg, A., van Hylckama Vlieg, J. E. T. and de Vos, W. M. (2007) The micro-petri dish, a million-well growth chip for the culture and high-throughput screening of microorganisms. Proc. Natl. Acad. Sci. U.S.A. 104, 18217-18222. https://doi.org/10.1073/pnas.0701693104
  50. Velve-Casquillas, G., Le Berre, M., Piel, M. and Tran, P. T. (2010) Microfluidic tools for cell biological research. Nano Today 5, 28-47. https://doi.org/10.1016/j.nantod.2009.12.001
  51. Calvert, P. (2007) Printing cells. Science 318, 208-209. https://doi.org/10.1126/science.1144212
  52. Cohen, D. J., Morfino, R. C. and Maharbiz, M. M. (2009) A modified consumer inkjet for spatiotemporal control of gene expression. PLoS One 4, e7086. https://doi.org/10.1371/journal.pone.0007086
  53. Merrin, J., Leibler, S. and Chuang, J. S. (2007) Printing multistrain bacterial patterns with a piezoelectric inkjet printer. PLoS One 2, e663. https://doi.org/10.1371/journal.pone.0000663
  54. Xu, T., Petridou, S., Lee, E. H., Roth, E. A., Vyavahare, N. R., Hickman, J. J. and Boland, T. (2004) Construction of high-density bacterial colony arrays and patterns by the ink-jet method. Biotech. Bioeng. 85, 29-33. https://doi.org/10.1002/bit.10768
  55. Kim, H. J., Boedicker, J. Q., Choi, J. W. and Ismagilov, R. F. (2008) Defined spatial structure stabilizes a synthetic multispecies bacterial community. Proc. Natl. Acad. Sci. U.S.A. 105, 18188-18193. https://doi.org/10.1073/pnas.0807935105
  56. Lee, S. H., Heinz, A. J., Shin, S., Jung, Y. G., Choi, S. E., Park, W., Roe, J. H. and Kwon, S. (2010) Capillary based patterning of cellular communities in laterally open channels. Anal. Chem. 82, 2900-2906. https://doi.org/10.1021/ac902903q
  57. Yaguchi, T., Lee, S., Choi, W. S., Kim, D., Kim, T., Mitchell, R. J. and Takayama, S. (2010) Micropatterning bacterial suspensions using aqueous two phase systems. Analyst 135, 2848-2852. https://doi.org/10.1039/c0an00464b
  58. Boedicker, J. Q., Vincent, M. E. and Ismagilov, R. F. (2009) Microfluidic confinement of single cells of bacteria in small volumes initiates high-density behavior of quorum sensing and growth and reveals its variability. Angewandte Chemie - Int. Ed. 48, 5908-5911. https://doi.org/10.1002/anie.200901550
  59. Chen, M. T. and Weiss, R. (2005) Artificial cell-cell communication in yeast Saccharomyces cerevisiae using signaling elements from Arabidopsis thaliana. Nat. Biotechnol. 23, 1551-1555. https://doi.org/10.1038/nbt1162
  60. Choi, W. S., Ha, D., Park, S. and Kim, T. S. (2011) Synthetic multicellular cell-to-cell communication in inkjet printed bacterial cell systems. Biomaterials doi:10.1016/j.biomaterials.2010.12.014.
  61. Basu, S., Gerchman, Y., Collins, C. H., Arnold, F. H. and Weiss, R. (2005) A synthetic multicellular system for programmed pattern formation. Nature 434, 1130-1134. https://doi.org/10.1038/nature03461
  62. Brenner, K., Karig, D. K., Weiss, R. and Arnold, F. H. (2007) Engineered bidirectional communication mediates a consensus in a microbial biofilm consortium. Proc. Natl. Acad. Sci. U.S.A. 104, 17300-17304. https://doi.org/10.1073/pnas.0704256104
  63. Ingham, C., Bomer, J., Sprenkels, A., van den Berg, A., de Vos, W. and van Hylckama Vlieg, J. (2010) High-resolution microcontact printing and transfer of massive arrays of microorganisms on planar and compartmentalized nanoporous aluminium oxide. Lab on a Chip 10, 1410-1416. https://doi.org/10.1039/b925796a
  64. Xu, L. P., Robert, L., Ouyang, Q., Taddei, F., Chen, Y., Lindner, A. B. and Baigl, D. (2007) Microcontact printing of living bacteria arrays with cellular resolution. Nano Lett. 7, 2068-2072. https://doi.org/10.1021/nl070983z
  65. Holz, C., Opitz, D., Mehlich, J., Ravoo, B. J. and Maier, B. (2009) Bacterial motility and clustering guided by microcontact printing. Nano Lett. 9, 4553-4557. https://doi.org/10.1021/nl903153c
  66. Eun, Y. J. and Weibel, D. B. (2009) Fabrication of microbial biofilm arrays by geometric control of cell adhesion. Langmuir 25, 4643-4654. https://doi.org/10.1021/la803985a
  67. Shou, W., Ram, S. and Vilar, J. M. G. (2007) Synthetic cooperation in engineered yeast populations. Proc. Natl. Acad. Sci. U.S.A. 104, 1877-1882. https://doi.org/10.1073/pnas.0610575104
  68. Balagadde, F. K., Song, H., Ozaki, J., Collins, C. H., Barnet, M., Arnold, F. H., Quake, S. R. and You, L. (2008) A synthetic Escherichia coli predator-prey ecosystem. Mol. Sys. Biol. 4, e187.
  69. Nealson, K. H. and Hastings, J. W. (1979) Bacterial bioluminescence: its control and ecological significance. Microbiol. Rev. 43, 496-518.
  70. Basu, S., Mehreja, R., Thiberge, S., Chen, M. T. and Weiss, R. (2004) Spatiotemporal control of gene expression with pulse-generating networks. Proc. Natl. Acad. Sci. U.S.A. 101, 6355-6360. https://doi.org/10.1073/pnas.0307571101
  71. Pai, A., Tanouchi, Y., Collins, C. and You, L. (2009) Engineering multicellular systems by cell-cell communication. Curr. Opin. Biotechnol. 20, 461-470. https://doi.org/10.1016/j.copbio.2009.08.006
  72. Levskaya, A., Chevalier, A. A., Tabor, J. J., Simpson, Z. B., Lavery, L. A., Levy, M., Davidson, E. A., Scouras, A., Ellington, A. D., Marcotte, E. M. and Voigt, C. A. (2005) Engineering E. coli to see light. Nature 438, 441-442. https://doi.org/10.1038/nature04405
  73. Tabor, J. J., Levskaya, A. and Voigt, C. A. (2010) Multichromatic control of gene expression in Escherichia coli. J. Mol. Biol. doi:10.1016/j.jmb.2010.10.038.
  74. Lu, T. K., Khalil, A. S. and Collins, J. J. (2009) Next-generation synthetic gene networks. Nat. Biotechnol. 27, 1139-1150. https://doi.org/10.1038/nbt.1591
  75. Levskaya, A., Weiner, O. D., Lim, W. A. and Voigt, C. A. (2009) Spatiotemporal control of cell signalling using a light-switchable protein interaction. Nature 461, 997-1001. https://doi.org/10.1038/nature08446
  76. Eiteman, M. A., Lee, S. A. and Altman, E. (2008) A co-fermentation strategy to consume sugar mixtures effectively. J. Biol. Engin. 2, 3. https://doi.org/10.1186/1754-1611-2-3
  77. Brenner, K., You, L. and Arnold, F. H. (2008) Engineering microbial consortia: a new frontier in synthetic biology. Trends Biotechnol. 26, 483-489. https://doi.org/10.1016/j.tibtech.2008.05.004
  78. Minami, H., Kim, J. S., Ikezawa, N., Takemura, T., Katayama, T., Kumagai, H. and Sato, F. (2008) Microbial production of plant benzylisoquinoline alkaloids. Proc. Natl. Acad. Sci. U.S.A. 105, 7393-7398. https://doi.org/10.1073/pnas.0802981105
  79. Hoang, T. T. and Schweizer, H. P. (1999) Characterization of Pseudomonas aeruginosa enoyl-acyl carrier protein reductase (FabI): a target for the antimicrobial triclosan and its role in acylated homoserine lactone synthesis. J. Bacteriol. 181, 5489-5497.
  80. Manefield, M., Rasmussen, T. B., Henzter, M., Andersen,J. B., Steinberg, P., Kjelleberg, S. and Givskov, M. (2002) Halogenated furanones inhibit quorum sensing through accelerated LuxR turnover. Microbiology 148, 1119-1127. https://doi.org/10.1099/00221287-148-4-1119
  81. Raina, S., De Vizio, D., Odell, M., Clements, M., Vanhulle, S. and Keshavarz, T. (2009) Microbial quorum sensing: a tool or a target for antimicrobial therapy? Biotechnol. Appl. Bioc. 54, 65-84. https://doi.org/10.1042/BA20090072
  82. Uroz, S., Dessaux, Y. and Oger, P. (2009) Quorum sensing and quorum quenching: the Yin and Yang of bacterial communication. Chembiochem 10, 205-216. https://doi.org/10.1002/cbic.200800521
  83. Lesic, B., Lepine, F., Deziel, E., Zhang, J., Zhang, Q., Padfield, K., Castonguay, M. H., Milot, S., Stachel, S., Tzika, A. A., Tompkins, R. G. and Rahme, L. G. (2007) Inhibitors of pathogen intercellular signals as selective anti-infective compounds. PLoS Pathog. 3, 1229-1239.
  84. Yeon, K. M., Cheon, W. S., Oh, H. S., Lee, W. N., Hwang, H. 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. https://doi.org/10.1021/es8019275
  85. Mae, A., Montesano, M., Koiv, V. and Palva, E. T. (2001) Transgenic plants producing the bacterial pheromone N-acyl-homoserine lactone exhibit enhanced resistance to the bacterial phytopathogen Erwinia carotovora. Mol. Plant Microbe. Interact. 14, 1035-1042. https://doi.org/10.1094/MPMI.2001.14.9.1035
  86. Yates, E. A., Phillip, B., Buckley, C., Atkinson, S., Chhabra, S. R., Sockett, R. E., Goldner, M., Dessaux, Y., Cámara, M., Smith, H. and Williams, P. (2002) N-acylhomoserine lactones undergo lactonolysis in a pH, temperature and acyl chain length dependent manner during growth of Yersinia pseudotuberculosis and Pseudomonas aeruginosa. Infect. Immun. 70, 5635-5646. https://doi.org/10.1128/IAI.70.10.5635-5646.2002
  87. Byers, J. T., Lucas, C., Salmond, G. P. C. and Welch, M. (2002) Non-enzymatic turnover of an Erwinia carotovora quorum-sensing signaling molecule. J. Bacteriol. 184, 1163-1171. https://doi.org/10.1128/jb.184.4.1163-1171.2002
  88. Hu, B., Du, J., Zou, R-. Y. and Yuan, Y-. J. (2010) An environment-sensitive synthetic microbial ecosystem. PLos One 5, e10619. https://doi.org/10.1371/journal.pone.0010619
  89. Bulter, T., Lee, S.-G., Wong, W. W., Fung, E., Connor, M. R. and Liao, J. C. (2004) Design of artificial cell-cell communication using gene and metabolic networks. Proc. Natl. Acad. Sci. U.S.A. 101, 2299-2304. https://doi.org/10.1073/pnas.0306484101
  90. Garcia-Ojalvo, J., Elowitz, M. B. and Strogatz, S. H. (2004) Modeling a synthetic multicellular clock: repressilators coupled by quorum sensing. Proc. Natl. Acad. Sci. U.S.A. 101, 10955-10960. https://doi.org/10.1073/pnas.0307095101
  91. Ghim, C.-M. and Almaas, E. (2009) Two-component genetic switch as a synthetic module with tunable stability. Phys. Rev. Lett. 103, 028101. https://doi.org/10.1103/PhysRevLett.103.028101
  92. Ghim, C.-M. and Almaas, E. (2008) Genetic noise control via protein oligomerization. BMC Syst. Biol. 2, 94. https://doi.org/10.1186/1752-0509-2-94
  93. Ghim, C.-M, Lee, S. K., Takayama, S. and Mitchell, R. J. (2010) The art of reporter proteins in science: past, present and future applications. BMB Reports 43, 451-460. https://doi.org/10.5483/BMBRep.2010.43.7.451

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