Browse > Article
http://dx.doi.org/10.5483/BMBRep.2011.44.1.1

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))
Publication Information
BMB Reports / v.44, no.1, 2011 , pp. 1-10 More about this Journal
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.
Keywords
Microbial community; Microchemostat; Quorum sensing; Synthetic biology;
Citations & Related Records
Times Cited By KSCI : 2  (Citation Analysis)
Times Cited By Web Of Science : 4  (Related Records In Web of Science)
Times Cited By SCOPUS : 8
연도 인용수 순위
1 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.   DOI   ScienceOn
2 Ghim, C.-M. and Almaas, E. (2009) Two-component genetic switch as a synthetic module with tunable stability. Phys. Rev. Lett. 103, 028101.   DOI   ScienceOn
3 Ghim, C.-M. and Almaas, E. (2008) Genetic noise control via protein oligomerization. BMC Syst. Biol. 2, 94.   DOI   ScienceOn
4 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.   DOI   ScienceOn
5 Uroz, S., Dessaux, Y. and Oger, P. (2009) Quorum sensing and quorum quenching: the Yin and Yang of bacterial communication. Chembiochem 10, 205-216.   DOI   ScienceOn
6 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.
7 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.   DOI   ScienceOn
8 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.   DOI   ScienceOn
9 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.   DOI
10 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.   DOI
11 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.   DOI   ScienceOn
12 Hu, B., Du, J., Zou, R-. Y. and Yuan, Y-. J. (2010) An environment-sensitive synthetic microbial ecosystem. PLos One 5, e10619.   DOI   ScienceOn
13 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.   DOI
14 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.   DOI   ScienceOn
15 Lu, T. K., Khalil, A. S. and Collins, J. J. (2009) Next-generation synthetic gene networks. Nat. Biotechnol. 27, 1139-1150.   DOI   ScienceOn
16 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.   DOI   ScienceOn
17 Eiteman, M. A., Lee, S. A. and Altman, E. (2008) A co-fermentation strategy to consume sugar mixtures effectively. J. Biol. Engin. 2, 3.   DOI   ScienceOn
18 Brenner, K., You, L. and Arnold, F. H. (2008) Engineering microbial consortia: a new frontier in synthetic biology. Trends Biotechnol. 26, 483-489.   DOI   ScienceOn
19 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.   DOI   ScienceOn
20 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.
21 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.   DOI
22 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.   DOI   ScienceOn
23 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.   DOI   ScienceOn
24 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.   DOI   ScienceOn
25 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.   DOI   ScienceOn
26 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.   DOI   ScienceOn
27 Eun, Y. J. and Weibel, D. B. (2009) Fabrication of microbial biofilm arrays by geometric control of cell adhesion. Langmuir 25, 4643-4654.   DOI   ScienceOn
28 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.   DOI   ScienceOn
29 Nealson, K. H. and Hastings, J. W. (1979) Bacterial bioluminescence: its control and ecological significance. Microbiol. Rev. 43, 496-518.
30 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.
31 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.   DOI   ScienceOn
32 Pai, A., Tanouchi, Y., Collins, C. and You, L. (2009) Engineering multicellular systems by cell-cell communication. Curr. Opin. Biotechnol. 20, 461-470.   DOI   ScienceOn
33 Merrin, J., Leibler, S. and Chuang, J. S. (2007) Printing multistrain bacterial patterns with a piezoelectric inkjet printer. PLoS One 2, e663.   DOI
34 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.   DOI   ScienceOn
35 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.   DOI   ScienceOn
36 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.   DOI   ScienceOn
37 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.   DOI   ScienceOn
38 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.   DOI   ScienceOn
39 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.   DOI   ScienceOn
40 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.   DOI   ScienceOn
41 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.   DOI   ScienceOn
42 Redfield, R. J. (2002) Is quorum sensing a side effect of diffusion sensing? Trends Microbiol. 10, 365-370.   DOI   ScienceOn
43 Keller, L. and Surette, M. G. (2006) Communication in bacteria: an ecological and evolutionary perspective. Nat. Rev. Microbiol. 4, 249-258.   DOI   ScienceOn
44 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.   DOI   ScienceOn
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.   DOI   ScienceOn
46 Weibel, D. B., DiLuzio, W. R. and Whitesides, G. M. (2007) Microfabrication meets microbiology. Nat. Rev. Microbiol. 5, 209-218.   DOI   ScienceOn
47 Calvert, P. (2007) Printing cells. Science 318, 208-209.   DOI   ScienceOn
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.   DOI   ScienceOn
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.   DOI   ScienceOn
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.   DOI   ScienceOn
51 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.   DOI   ScienceOn
52 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.   DOI   ScienceOn
53 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   ScienceOn
54 Leadbetter, J. R. and Greenberg, E. P. (2000) Metabolism of acyl-homoserine lactone quorum-sensing signals by Variovorax paradoxus. J. Bacteriol. 182, 6921-6926.   DOI
55 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.   DOI
56 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.   DOI   ScienceOn
57 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   ScienceOn
58 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.   DOI
59 Surette, M. G. and Bassler, B. L. (1999) Regulation of autoinducer production in Salmonella typhimurium. Mol. Microbiol. 31, 585-595.   DOI   ScienceOn
60 Xavier, K. B. and Bassler, B. L. (2005) Interference with AI-2-mediated bacterial cell-cell communication. Nature 437, 750-753.   DOI   ScienceOn
61 Pottathil, M. and Lazazzera, B. A. (2003) The extracellular Phr peptide-Rap phosphatase signaling circuit of Bacillus subtilis. Front. Biosci. 8, d32-45.   DOI
62 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.   DOI   ScienceOn
63 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.   DOI   ScienceOn
64 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.   DOI   ScienceOn
65 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.   DOI   ScienceOn
66 Wang, Y. J. and Leadbetter, J. R. (2005) Rapid acyl-homoserine lactone quorum signal biodegradation in diverse soils. Appl. Environ. Microbiol. 71, 1291-1299.   DOI   ScienceOn
67 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.   DOI
68 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.   DOI   ScienceOn
69 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.   DOI
70 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.   DOI
71 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.   DOI   ScienceOn
72 Ji, G., Beavis, R. and Novick, R. P. (1997) Bacterial interference caused by autoinducing peptide variants. Science 276, 2027-2030.   DOI   ScienceOn
73 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.   DOI   ScienceOn
74 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.   DOI
75 Xavier, K. B., and Bassler, B. L. (2003) LuxS quorum sensing: more than just a numbers game. Curr. Opin. Microbiol. 6, 191-197.   DOI   ScienceOn
76 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.   DOI   ScienceOn
77 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.   DOI   ScienceOn
78 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.   DOI   ScienceOn
79 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.
80 Eberhard, A. (1972) Inhibition and activation of bacterial luciferase synthesis. J. Bacteriol. 109, 1101-1105.
81 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   ScienceOn
82 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.   DOI   ScienceOn
83 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.   DOI   ScienceOn
84 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.   DOI   ScienceOn
85 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.   DOI   ScienceOn
86 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.   DOI   ScienceOn
87 Bassler, B. L. and Losick, R. (2006) Bacterially speaking. Cell 125, 237-246.   DOI   ScienceOn
88 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.   DOI
89 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.   DOI   ScienceOn
90 Choudhary, S. and Schmidt-Dannert, C. (2010) Applications of quorum sensing in biotechnology. Appl. Microbiol. Biotechnol. 86, 1267-1279.   DOI
91 Rasmussen, T. B. and Givskov, M. (2006) Quorum-sensing inhibitors as anti-pathogenic drugs. Int. J. Med. Microbiol. 296, 149-161.
92 Lerat, E. and Moran, N. A. (2004) Evolutionary history of quorum-sensing systems in bacteria. Mol. Biol. Evol. 21, 903-913.   DOI   ScienceOn
93 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.   DOI