Metagenomic approaches to understanding phylogenetic diversity in quorum sensing

Virulence

Volumn 5, Issue 3, 2014, Pages 433-442

  Kimura, Nobutada ^a  

^a NATIONAL INSTITUTE OF ADVANCED INDUSTRIAL SCIENCE AND TECHNOLOGY AIST   (Japan)

Author keywords

Metagenomics; N acyl L homoserine lactone; Quorum quenching; Quorum sensing; Quorum sensing inhibitor; Quorum sensing signal

Indexed keywords

(5Z) 4 BROMO 5 (BROMOMETHYLENE) 3 BUTYL 2(5H) FURANONE; 4 HYDROXYINDOLE; 5 HYDROXYINDOLE; 6 HYDROXYINDOLE; 7 HYDROXYINDOLE; BETA GALACTOSIDASE; FURANONE DERIVATIVE; GAMMA BUTYROLACTONE; GREEN FLUORESCENT PROTEIN; INDOLE; INDOLE DERIVATIVE; ISATIN; LUCIFERASE; N ACYLHOMOSERINE LACTONE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR LUXI; TRANSCRIPTION FACTOR LUXR; UNCLASSIFIED DRUG;

BIOFILM; GENE EXPRESSION; METAGENOMICS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; QUORUM SENSING; REVIEW; SIGNAL TRANSDUCTION; VIRULENCE; ARCHAEON; BACTERIA; BACTERIAL PHENOMENA AND FUNCTIONS; BIODIVERSITY; CLASSIFICATION; GENETICS; METABOLISM; ORGANISMAL INTERACTION; PHYSIOLOGY; PROCEDURES;

ARCHAEA; BACTERIA; BACTERIAL PHYSIOLOGICAL PHENOMENA; BIODIVERSITY; METABOLIC NETWORKS AND PATHWAYS; METAGENOMICS; MICROBIAL INTERACTIONS; PHYLOGENY; QUORUM SENSING;

EID: 84897930904     PISSN: 21505594     EISSN: 21505608     Source Type: Journal    
DOI: 10.4161/viru.27850     Document Type: Review

References (102)

1. Williams P, Winzer K, Chan WC, Cámara M. Look who's talking: communication and quorum sensing in the bacterial world. Philos Trans R Soc Lond B Biol Sci 2007; 362:1119-34; PMID:17360280; http://dx.doi.org/10.1098/rstb.2007.2039
2. Decho AW, Norman RS, Visscher PT. Quorum sensing in natural environments: emerging views from microbial mats. Trends Microbiol 2010; 18:73-80; PMID:20060299; http://dx.doi.org/10.1016/j.tim.2009.12.008
3. Bassler BL, Wright M, Silverman MR. Multiple signalling systems controlling expression of luminescence in Vibrio harveyi: sequence and function of genes encoding a second sensory pathway. Mol Microbiol 1994; 13:273-86; PMID:7984107; http://dx.doi.org/10.1111/j.1365-2958.1994.tb00422.x
4. Whitehead NA, Barnard AM, Slater H, Simpson NJ, Salmond GP. Quorum-sensing in Gram-negative bacteria. FEMS Microbiol Rev 2001; 25:365-404; PMID: 11524130; http://dx.doi.org/10.1111/j.1574-6976.2001.tb00583.x
5. Xu L, Li H, Vuong C, Vadyvaloo V, Wang J, Yao Y, Otto M, Gao Q. Role of the luxS quorum-sensing system in biofilm formation and virulence of Staphylococcus epidermidis. Infect Immun 2006; 74:488-96; PMID:16369005; http://dx.doi.org/10.1128/IAI.74.1.488-496.2006
6. Burton EO, Read HW, Pellitteri MC, Hickey WJ. Identification of acyl-homoserine lactone signal molecules produced by Nitrosomonas europaea strain Schmidt. Appl Environ Microbiol 2005; 71:4906-9; PMID:16085894; http://dx.doi.org/10.1128/AEM.71.8.4906-4909.2005
7. Labbate M, Queck SY, Koh KS, Rice SA, Givskov M, Kjelleberg S. Quorum sensing-controlled biofilm development in Serratia liquefaciens MG1. J Bacteriol 2004; 186:692-8; PMID:14729694; http://dx.doi.org/10.1128/JB.186.3.692-698.2004
8. McLean RJC, Whiteley M, Stickler DJ, Fuqua WC. Evidence of autoinducer activity in naturally occurring biofilms. FEMS Microbiol Lett 1997; 154:259-63; PMID:9311122; http://dx.doi.org/10.1111/j.1574-6968.1997.tb12653.x
9. Fuqua WC, Winans SC, Greenberg EP. Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators. J Bacteriol 1994; 176:269-75; PMID:8288518
10. Hanzelka BL, Greenberg EP. Quorum sensing in Vibrio fischeri: evidence that S-adenosylmethionine is the amino acid substrate for autoinducer synthesis. J Bacteriol 1996; 178:5291-4; PMID:8752350
11. Watson WT, Minogue TD, Val DL, von Bodman SB, Churchill ME. Structural basis and specificity of acyl-homoserine lactone signal production in bacterial quorum sensing. Mol Cell 2002; 9:685-94; PMID:11931774; http://dx.doi.org/10.1016/S1097-2765(02)00480-X
12. Hanzelka BL, Stevens AM, Parsek MR, Crone TJ, Greenberg EP. Mutational analysis of the Vibrio fischeri LuxI polypeptide: critical regions of an autoinducer synthase. J Bacteriol 1997; 179:4882-7; PMID:9244278
13. Cullinane M, Baysse C, Morrissey JP, O'Gara F. Identification of two lysophosphatidic acid acyl-transferase genes with overlapping function in Pseudomonas fluorescens. Microbiology 2005; 151: 3071-80; PMID: 16151217; http://dx.doi.org/10.1099/mic.0.27958-0
14. Beck von Bodman S, Farrand SK. Capsular polysac-charide biosynthesis and pathogenicity in Erwinia stewartii require induction by an N-acylhomoserine lactone autoinducer. J Bacteriol 1995; 177:5000-8; PMID:7665477
15. Juhas M, Wiehlmann L, Salunkhe P, Lauber J, Buer J, Tümmler B. GeneChip expression analysis of the VqsR regulon of Pseudomonas aeruginosa TB. FEMS Microbiol Lett 2005; 242:287-95; PMID: 15621450; http://dx.doi.org/10.1016/j.femsle.2004.11.020
16. Gambello MJ, Iglewski BH. Cloning and characterization of the Pseudomonas aeruginosa lasR gene, a transcriptional activator of elastase expression. J Bacteriol 1991; 173:3000-9; PMID:1902216
17. Piper KR, Beck von Bodman S, Farrand SK. Conjugation factor of Agrobacterium tumefaciens regulates Ti plasmid transfer by autoinduction. Nature 1993; 362:448-50; PMID:8464476; http://dx.doi.org/10.1038/362448a0
18. d'Angelo-Picard C, Faure D, Penot I, Dessaux Y. Diversity of N-acyl homoserine lactone-producing and -degrading bacteria in soil and tobacco rhizosphere. Environ Microbiol 2005; 7:1796-808; PMID:16232294; http://dx.doi.org/10.1111/j.1462-2920.2005.00886.x
19. Dunphy G, Miyamoto C, Meighen E. A homoserine lactone autoinducer regulates virulence of an insect-pathogenic bacterium, Xenorhabdus nematophilus (Enterobacteriaceae). J Bacteriol 1997; 179:5288-91; PMID:9286978
20. Pinto UM, Viana ED, Martins ML, Vanetti MCD. Detection of acylated homoserine lactones in gram-negative proteolytic psychrotrophic bacteria isolated from cooled raw milk. Food Contr 2007; 18:1322-7; http://dx.doi.org/10.1016/j.foodcont.2006.09.005
21. Chong G, Kimyon O, Rice SA, Kjelleberg S, Manefield M. The presence and role of bacterial quorum sensing in activated sludge. Microb Biotechnol 2012; 5:621-33; PMID:22583685; http://dx.doi.org/10.1111/j.1751-7915.2012.00348.x
22. Boyer M, Wisniewski-Dyé F. Cell-cell signalling in bacteria: not simply a matter of quorum. FEMS Microbiol Ecol 2009; 70:1-19; PMID:19689448; http://dx.doi.org/10.1111/j.1574-6941.2009.00745.x
23. Eberl L, Riedel K. Mining quorum sensing regulated proteins - Role of bacterial cell-to-cell communication in global gene regulation as assessed by proteomics. Proteomics 2011; 11: 3070-85; PMID:21548094; http://dx.doi.org/10.1002/pmic.201000814
24. Nakazawa H, Arakaki A, Narita-Yamada S, Yashiro I, Jinno K, Aoki N, Tsuruyama A, Okamura Y, Tanikawa S, Fujita N, et al. Whole genome sequence of Desulfovibrio magneticus strain RS-1 revealed common gene clusters in magnetotactic bacteria. Genome Res 2009; 19:1801-8; PMID:19675025; http://dx.doi.org/10.1101/gr.088906.108
25. Shelobolina ES, Vrionis HA, Findlay RH, Lovley DR. Geobacter uraniireducens sp. nov., isolated from subsurface sediment undergoing uranium bioreme-diation. Int J Syst Evol Microbiol 2008; 58:1075-8; PMID:18450691; http://dx.doi.org/10.1099/ij s.0.65377-0
26. Simmons SL, Dibartolo G, Denef VJ, Goltsman DS, Thelen MP, Banfield JF. Population genomic analysis of strain variation in Leptospirillum group II bacteria involved in acid mine drainage formation. PLoS Biol 2008; 6:e177; PMID:18651792; http://dx.doi.org/10.1371/journal.pbio.0060177
27. Rappé MS, Giovannoni SJ. The uncultured microbial majority. Annu Rev Microbiol 2003; 57:369-94; PMID:14527284; http://dx.doi.org/10.1146/annurev.micro.57.030502.090759
28. Zhang G, Zhang F, Ding G, Li J, Guo X, Zhu J, Zhou L, Cai S, Liu X, Luo Y, et al. Acyl homoserine lactone-based quorum sensing in a methanogenic archaeon. ISME J 2012; 6:1336-44; PMID:22237544; http://dx.doi.org/10.1038/ismej.2011.203
29. Gray KM, Garey JR. The evolution of bacterial LuxI and LuxR quorum sensing regulators. Microbiology 2001; 147:2379-87; PMID:11496014
30. Amann RI, Ludwig W, Schleifer KH. Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 1995; 59:143-69; PMID:7535888
31. Kellenberger E. Exploring the unknown. The silent revolution of microbiology. EMBO Rep 2001; 2:5-7; PMID:11252724; http://dx.doi.org/10.1093/embo-reports/kve014
32. Handelsman J, Rondon MR, Brady SF, Clardy J, Goodman RM. Molecular biological access to the chemistry of unknown soil microbes: a new frontier for natural products. Chem Biol 1998; 5:R245-R249; PMID:9818143; http://dx.doi.org/10.1016/S1074-5521(98)90108-9
33. Kimura N. Metagenomics: Access to unculturable microbes in the environment. Microbes Environ 2006; 21:201-15; http://dx.doi.org/10.1264/jsme2.21.201
34. Kimura N, Sakai K, Nakamura K. Isolation and characterization of a 4-nitrotoluene-oxidizing enzyme from activated sludge by a metagenomic approach. Microbes Environ 2010; 25:133-9; PMID: 21576 86 4; http://dx.doi.org/10.1264/jsme2.ME10110
35. Fujita MJ, Kimura N, Sakai A, Ichikawa Y, Hanyu T, Otsuka M. Cloning and heterologous expression of the vibrioferrin biosynthetic gene cluster from a marine metagenomic library. Biosci Biotechnol Biochem 2011; 75:2283-7; PMID: 2214 6715; http://dx.doi.org/10.1271/bbb.110379
36. Fujita MJ, Kimura N, Yokose H, Otsuka M. Heterologous production of bisucaberin using a bio-synthetic gene cluster cloned from a deep sea metage-nome. Mol Biosyst 2012; 8:482-5; PMID:22051782; http://dx.doi.org/10.1039/c1mb05431g
37. Streit WR, Daniel R, Jaeger KE. Prospecting for biocatalysts and drugs in the genomes of non-cultured microorganisms. Curr Opin Biotechnol 2004; 15: 285-90; PMID: 15296926; http://dx.doi.org/10.1016/j.copbio.2004.05.006
38. Schmeisser C, Steele H, Streit WR. Metagenomics, biotechnology with non-culturable microbes. Appl Microbiol Biotechnol 2007; 75:955-62; PMID:17396253; http://dx.doi.org/10.1007/s00253-007-0945-5
39. Kimura N, Sakai K, Nakamura K. Isolation and characterization of a 4-nitrotoluene-oxidizing enzyme from activated sludge by a metagenomic approach. Microbes Environ 2010; 25:133-9; PMID: 21576 86 4; http://dx.doi.org/10.1264/jsme2.ME10110
40. Craig JW, Chang FY, Kim JH, Obiajulu SC, Brady SF. Expanding small-molecule functional metage-nomics through parallel screening of broad-host-range cosmid environmental DNA libraries in diverse proteobacteria. Appl Environ Microbiol 2010; 76:1633-41; PMID:20081001; http://dx.doi.org/10.1128/AEM.02169-09
41. Williamson LL, Borlee BR, Schloss PD, Guan C, Allen HK, Handelsman J. Intracellular screen to identify metagenomic clones that induce or inhibit a quorum-sensing biosensor. Appl Environ Microbiol 2005; 71:6335-44; PMID:16204555; http://dx.doi.org/10.1128/AEM.71.10.6335-6344.2005
42. Hao Y, Winans SC, Glick BR, Charles TC. Identification and characterization of new LuxR/LuxI-type quorum sensing systems from metagenomic libraries. Environ Microbiol 2010; 12:105-17; PMID:19735279; http://dx.doi.org/10.1111/j.1462-2920.2009.02049.x
43. Handelsman J. Metagenomics: application of genom-ics to uncultured microorganisms. Microbiol Mol Biol Rev 2004; 68:669-85; PMID: 155 9 0 7 7 9; http://dx.doi.org/10.1128/MMBR.68.4.669-685.2004
44. Guan C, Ju J, Borlee BR, Williamson LL, Shen B, Raffa KF, Handelsman J. Signal mimics derived from a metagenomic analysis of the gypsy moth gut microbiota. Appl Environ Microbiol 2007; 73:3669-76; PMID:1743500 0; http://dx.doi.org/10.1128/AEM.02617-06
45. Valle A, Bailey MJ, Whiteley AS, Manefield M. N-acyl-l-homoserine lactones (AHLs) affect microbial community composition and function in activated sludge. Environ Microbiol 2004; 6:424-33; PMID: 15008819; http://dx.doi.org/10.1111/j.1462-2920.2004.00581.x
46. Schauder S, Shokat K, Surette MG, Bassler BL. The LuxS family of bacterial autoinducers: biosynthesis of a novel quorum-sensing signal molecule. Mol Microbiol 2001; 41:463-76; PMID:11489131; http://dx.doi.org/10.1046/j.1365-2958.2001.02532.x
47. Onaka H, Ando N, Nihira T, Yamada Y, Beppu T, Horinouchi S. Cloning and characterization of the A-factor receptor gene from Streptomyces griseus. J Bacteriol 1995; 177:6083-92; PMID:7592371
48. Schaefer AL, Greenberg EP, Oliver CM, Oda Y, Huang JJ, Bittan-Banin G, Peres CM, Schmidt S, Juhaszova K, Sufrin JR, et al. A new class of homo-serine lactone quorum-sensing signals. Nature 2008; 454:595-9; PMID:18563084; http://dx.doi.org/10.1038/nature07088
49. Wang D, Ding X, Rather PN. Indole can act as an extracellular signal in Escherichia coli. J Bacteriol 2001; 183:4210-6; PMID:11418561; http://dx.doi.org/10.1128/JB.183.14.4210-4216.2001
50. Anyanful A, Dolan-Livengood JM, Lewis T, Sheth S, Dezalia MN, Sherman MA, Kalman LV, Benian GM, Kalman D. Paralysis and killing of Caenorhabditis elegans by enteropathogenic Escherichia coli requires the bacterial tryptophanase gene. Mol Microbiol 2005; 57:988-1007; PMID:16091039; http://dx.doi.org/10.1111/j.1365-2958.2005.04739.x
51. Lee J, Attila C, Cirillo SLG, Cirillo JD, Wood TK. Indole and 7-hydroxyindole diminish Pseudomonas aeruginosa virulence. Microb Biotechnol 2009; 2:75-90; PMID:21261883; http://dx.doi.org/10.1111/j.1751-7915.2008.00061.x
52. Hirakawa H, Kodama T, Takumi-Kobayashi A, Honda T, Yamaguchi A. Secreted indole serves as a signal for expression of type III secretion system translocators in enterohaemorrhagic Escherichia coli O157:H7. Microbiology 2009; 155:541-50; PMID:19202102; http://dx.doi.org/10.1099/mic.0.020420-0
53. Mueller RS, Beyhan S, Saini SG, Yildiz FH, Bartlett DH. Indole acts as an extracellular cue regulating gene expression in Vibrio cholerae. J Bacteriol 2009; 191:3504-16; PMID:19329638; http://dx.doi.org/10.1128/JB.01240-08
54. Martino PD, Fursy R, Bret L, Sundararaju B, Phillips RS. Indole can act as an extracellular signal to regulate biofilm formation of Escherichia coli and other indole-producing bacteria. Can J Microbiol 2003; 49:443-9; PMID:14569285; http://dx.doi.org/10.1139/w03-056
55. Lee J, Jayaraman A, Wood TK. Indole is an inter-species biofilm signal mediated by SdiA. BMC Microbiol 2007; 7:42; PMID: 175118 76; http://dx.doi.org/10.1186/1471-2180-7-42
56. Lindum PW, Anthoni U, Christophersen C, Eberl L, Molin S, Givskov M. N-Acyl-L-homoserine lactone autoinducers control production of an extracellular lipopeptide biosurfactant required for swarming motility of Serratia liquefaciens MG1. J Bacteriol 1998; 180:6384-8; PMID:9829950
57. Xu L, Li H, Vuong C, Vadyvaloo V, Wang J, Yao Y, Otto M, Gao Q. Role of the luxS quorum-sensing system in biofilm formation and virulence of Staphylococcus epidermidis. Infect Immun 2006; 74:488-96; PMID:16369005; http://dx.doi.org/10.1128/IAI.74.1.488-496.2006
58. Burr T, Barnard AM, Corbett MJ, Pemberton CL, Simpson NJ, Salmond GP. Identification of the central quorum sensing regulator of virulence in the enteric phytopathogen, Erwinia caro-tovora: the VirR repressor. Mol Microbiol 2006; 59:113-25; PMID:16359322; http://dx.doi.org/10.1111/j.1365-2958.2005.04939.x
59. Givskov M, Ostling J, Eberl L, Lindum PW, Christensen AB, Christiansen G, Molin S, Kjelleberg S. Two separate regulatory systems participate in control of swarming motility of Serratia liquefaciens MG1. J Bacteriol 1998; 180:742-5; PMID:9457883
60. Labbate M, Queck SY, Koh KS, Rice SA, Givskov M, Kjelleberg S. Quorum sensing-controlled biofilm development in Serratia liquefaciens MG1. J Bacteriol 2004; 186:692-8; PMID:14729694; http://dx.doi.org/10.1128/JB.186.3.692-698.2004
61. Hammer BK, Bassler BL. Quorum sensing controls biofilm formation in Vibrio cholerae. Mol Microbiol 2003; 50:101-4; PMID:14507367; http://dx.doi.org/10.1046/j.1365-2958.2003.03688.x
62. Leadbetter JR, Greenberg EP. Metabolism of acyl-homoserine lactone quorum-sensing signals by Variovorax paradoxus. J Bacteriol 2000; 182:6921-6; PMID:11092851; http://dx.doi.org/10.1128/JB.182.24.6921-6926.2000
63. Huang JJ, Han JI, Zhang LH, Leadbetter JR. Utilization of acyl-homoserine lactone quorum signals for growth by a soil pseudomonad and Pseudomonas aeruginosa PAO1. Appl Environ Microbiol 2003; 69:5941-9; PMID:14532048; http://dx.doi.org/10.1128/AEM.69.10.5941-5949.2003
64. Hu JY, Fan Y, Lin YH, Zhang HB, Ong SL, Dong N, Xu JL, Ng WJ, Zhang LH. Microbial diversity and prevalence of virulent pathogens in biofilms developed in a water reclamation system. Res Microbiol 2003; 154:623-9; PMID:14596899; http://dx.doi.org/10.1016/j.resmic.2003.09.004
65. Flagan S, Ching WK, Leadbetter JR. Arthrobacter strain VAI-A utilizes acyl-homoserine lactone inac-tivation products and stimulates quorum signal bio-degradation by Variovorax paradoxus. Appl Environ Microbiol 2003; 69:909-16; PMID: 125 71011; http://dx.doi.org/10.1128/AEM.69.2.909-916.2003
66. Uroz S, D'Angelo-Picard C, Carlier A, Elasri M, Sicot C, Petit A, Oger P, Faure D, Dessaux Y. Novel bacteria degrading N-acylhomoserine lactones and their use as quenchers of quorum-sensing-regulated functions of plant-pathogenic bacteria. Microbiology 2003; 149:1981-9; PMID:12904538; http://dx.doi.org/10.1099/mic.0.26375-0
67. Lin YH, Xu JL, Hu J, Wang LH, Ong SL, Leadbetter JR, Zhang LH. Acyl-homoserine lactone acylase from Ralstonia strain XJ12B represents a novel and potent class of quorum-quenching enzymes. Mol Microbiol 2003; 47:849-60; PMID:12535081; http://dx.doi.org/10.1046/j.1365-2958.2003.03351.x
68. Park SY, Lee SJ, Oh TK, Oh JW, Koo BT, Yum DY, Lee JK. AhlD, an N-acylhomoserine lactonase in Arthrobacter sp., and predicted homologues in other bacteria. Microbiology 2003; 149:1541-50; PMID:12777494; http://dx.doi.org/10.1099/mic.0.26269-0
69. Yoon JH, Lee JK, Jung SY, Kim JA, Kim HK, Oh TK. Nocardioides kongjuensis sp. nov., an N-acylhomoserine lactone-degrading bacterium. Int J Syst Evol Microbiol 2006; 56:1783-7; PMID:16902008; http://dx.doi.org/10.1099/ijs.0.64120-0
70. Romero M, Avendaño-Herrera R, Magariños B, Cámara M, Otero A. Acylhomoserine lactone production and degradation by the fish pathogen Tenacibaculum maritimum, a member of the Cytophaga-Flavobacterium-Bacteroides (CFB) group. FEMS Microbiol Lett 2010; 304:131-9; PMID:20377642; http://dx.doi.org/10.1111/j.1574-6968.2009.01889.x
71. Romero M, Diggle SP, Heeb S, Cámara M, Otero A. Quorum quenching activity in Anabaena sp. PCC 7120: identification of AiiC, a novel AHL-acylase. FEMS Microbiol Lett 2008; 280:73-80; PMID:18194337; http://dx.doi.org/10.1111/j.1574-6968.2007.01046.x
72. Huang JJ, Han JI, Zhang LH, Leadbetter JR. Utilization of acyl-homoserine lactone quorum signals for growth by a soil pseudomonad and Pseudomonas aeruginosa PAO1. Appl Environ Microbiol 2003; 69:5941-9; PMID:14532048; http://dx.doi.org/10.1128/AEM.69.10.5941-5949.2003
73. Sio CF, Otten LG, Cool RH, Diggle SP, Braun PG, Bos R, Daykin M, Cámara M, Williams P, Quax WJ. Quorum quenching by an N-acyl-homoserine lactone acylase from Pseudomonas aeruginosa PAO1. Infect Immun 2006; 74:1673-82; PMID:16495538; http://dx.doi.org/10.1128/IAI.74.3.1673-1682.2006
74. Dong YH, Xu JL, Li XZ, Zhang LH. 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 2000; 97:3526-31; PMID:10716724; http://dx.doi.org/10.1073/pnas.97.7.3526
75. Lee SJ, Park SY, Lee JJ, Yum DY, Koo BT, Lee JK. Genes encoding the N-acyl homoserine lactone-degrading enzyme are widespread in many subspecies of Bacillus thuringiensis. Appl Environ Microbiol 2002; 68: 3919-24; PMID:12147491; http://dx.doi.org/10.1128/AEM.68.8.3919-3924.2002
76. Wang WZ, Morohoshi T, Ikenoya M, Someya N, Ikeda T. AiiM, a novel class of N-acylhomoserine lactonase from the leaf-associated bacterium Microbacterium testaceum. Appl Environ Microbiol 2010; 76:2524-30; PMID:20173075; http://dx.doi.org/10.1128/AEM.02738-09
77. Park SY, Hwang BJ, Shin MH, Kim JA, Kim HK, Lee JK. N-acylhomoserine lactonase producing Rhodococcus spp. with different AHL-degrading activities. FEMS Microbiol Lett 2006; 261:102-8; PMID:16842366; http://dx.doi.org/10.1111/j.1574-6968.2006.00336.x
78. Park SY, Kang HO, Jang HS, Lee JK, Koo BT, Yum DY. Identification of extracellular N-acylhomoserine lactone acylase from a Streptomyces sp. and its application to quorum quenching. Appl Environ Microbiol 2005; 71:2632-41; PMID:158 70355; http://dx.doi.org/10.1128/AEM.71.5.2632-2641.2005
79. Uroz S, Oger PM, Chapelle E, Adeline MT, Faure D, Dessaux Y. A Rhodococcus qsdA-encoded enzyme defines a novel class of large-spectrum quorum-quenching lactonases. Appl Environ Microbiol 2008; 74:1357-66; PMID:18192419; http://dx.doi.org/10.1128/AEM.02014-07
80. Uroz S, Chhabra SR, Cámara M, Williams P, Oger P, Dessaux Y. N-Acylhomoserine lactone quorum-sensing molecules are modified and degraded by Rhodococcus erythropolis W2 by both amidolytic and novel oxidoreductase activities. Microbiology 2005; 151:3313-22; PMID:16207914; http://dx.doi.org/10.1099/mic.0.27961-0
81. Zelinski T, Kula MR. A kinetic study and application of a novel carbonyl reductase isolated from Rhodococcus erythropolis. Bioorg Med Chem 1994; 2:421-8; PMID:8000863; http://dx.doi.org/10.1016/0968-0896(94)80010-3
82. Zelinski T, Peters J, Kula MR. Purification and characterization of a novel carbonyl reductase isolated from Rhodococcus erythropolis. J Biotechnol 1994; 33:283-92; PMID:7764739; http://dx.doi.org/10.1016/0168-1656(94)90076-0
83. Kalia VC, Raju SC, Purohit HJ. Genomic analysis reveals versatile organisms for quorum quenching enzymes: acyl-homoserine lactone-acylase and-lactonase. Open Microbiol J 2011; 5:1-13; PMID: 21660112; http://dx.doi.org/10.2174/1874285801105010001
84. Riaz K, Elmerich C, Moreira D, Raffoux A, Dessaux Y, Faure D. A metagenomic analysis of soil bacteria extends the diversity of quorum-quenching lactonases. Environ Microbiol 2008; 10:560-70; PMID:18201196; http://dx.doi.org/10.1111/j.1462-2920.2007.01475.x
85. Tannières M, Beury-Cirou A, Vigouroux A, Mondy S, Pellissier F, Dessaux Y, Faure D. A metage-nomic study highlights phylogenetic proximity of quorum-quenching andxenobiotic-degrading ami-dases of the AS-family. PLoS One 2013; 8:e65473; PMID:23762380; http://dx.doi.org/10.1371/jour-nal.pone.0065473
86. Christensen QH, Grove TL, Booker SJ, Greenberg EP. A high-throughput screen for quorum-sensing inhibitors that target acyl-homoserine lactone syn-thases. Proc Natl Acad Sci U S A 2013; 110:13815-20; PMID: 23924613; http://dx.doi.org/10.1073/pnas.1313098110
87. Müh U, Schuster M, Heim R, Singh A, Olson ER, Greenberg EP. Novel Pseudomonas aeruginosa quorum-sensing inhibitors identified in an ultra-high-throughput screen. Antimicrob Agents Chemother 2006; 50:3674-9; PMID:16966394; http://dx.doi.org/10.1128/AAC.00665-06
88. Ni N, Li M, Wang J, Wang B. Inhibitors and antagonists of bacterial quorum sensing. Med Res Rev 2009; 29: 65-124; PMID:18956421; http://dx.doi.org/10.1002/med.20145
89. Chen G, Swem LR, Swem DL, Stauff DL, O'Loughlin CT, Jeffrey PD, Bassler BL, Hughson FM. A strategy for antagonizing quorum sensing. Mol Cell 2011; 42:199-209; PMID:21504831; http://dx.doi.org/10.1016/j.molcel.2011.04.003
90. Lee J, Bansal T, Jayaraman A, Bentley WE, Wood TK. Enterohemorrhagic Escherichia coli biofilms are inhibited by 7-hydroxyindole and stimulated by isatin. Appl Environ Microbiol 2007; 73:4100-9; PMID:17483266; http://dx.doi.org/10.1128/AEM.00360-07
91. Tashiro Y, Toyofuku M, Nakajima-Kambe T, Uchiyama H, Nomura N. Bicyclic compounds repress membrane vesicle production and Pseudomonas quinolone signal synthesis in Pseudomonas aeruginosa. FEMS Microbiol Lett 2010; 304:123-30; PMID:20146747; http://dx.doi.org/10.1111/j.1574-6968.2010.01897.x
92. Ren D, Bedzyk LA, Ye RW, Thomas SM, Wood TK. Stationary-phase quorum-sensing signals affect autoinducer-2 and gene expression in Escherichia coli. Appl Environ Microbiol 2004; 70:2038-43; PMID:15066794; http://dx.doi.org/10.1128/AEM.70.4.2038-2043.2004
93. Henne A, Daniel R, Schmitz RA, Gottschalk G. Construction of environmental DNA libraries in Escherichia coli and screening for the presence of genes conferring utilization of 4-hydroxy-butyrate. Appl Environ Microbiol 1999; 65:3901-7; PMID:10473393
94. Lämmle K, Zipper H, Breuer M, Hauer B, Buta C, Brunner H, Rupp S. Identification of novel enzymes with different hydrolytic activities by metagenome expression cloning. J Biotechnol 2007; 127:575-92; PMID: 16963141; http://dx.doi.org/10.1016/j.jbiotec.2006.07.036
95. Courtois S, Cappellano CM, Ball M, Francou FX, Normand P, Helynck G, Martinez A, Kolvek SJ, Hopke J, Osburne MS, et al. Recombinant environmental libraries provide access to microbial diversity for drug discovery from natural products. Appl Environ Microbiol 2003; 69:49-55; PMID: 12513976; http://dx.doi.org/10.1128/AEM.69.1.49-55.2003
96. Entcheva P, Liebl W, Johann A, Hartsch T, Streit WR. Direct cloning from enrichment cultures, a reliable strategy for isolation of complete operons and genes from microbial consortia. Appl Environ Microbiol 2001; 67:89-99; PMID:11133432; http://dx.doi.org/10.1128/AEM.67.1.89-99.2001
97. Knietsch A, Waschkowitz T, Bowien S, Henne A, Daniel R. Construction and screening of metage-nomic libraries derived from enrichment cultures: generation of a gene bank for genes conferring alcohol oxidoreductase activity on Escherichia coli. Appl Environ Microbiol 2003; 69:1408-16; PMID:12620823; http://dx.doi.org/10.1128/AEM.69.3.1408-1416.2003
98. Voget S, Leggewie C, Uesbeck A, Raasch C, Jaeger KE, Streit WR. Prospecting for novel biocatalysts in a soil metagenome. Appl Environ Microbiol 2003; 69:6235-42; PMID:14532085; http://dx.doi.org/10.1128/AEM.69.10.6235-6242.2003
99. Nasuno E, Kimura N, Fujita MJ, Nakatsu CH, Kamagata Y, Hanada S. Phylogenetically novel LuxI/LuxR-type quorum sensing systems isolated using a metagenomic approach. Appl Environ Microbiol 2012; 78: 8067-74; PMID:22983963; http://dx.doi.org/10.1128/AEM.01442-12
100. Suenaga H, Ohnuki T, Miyazaki K. Functional screening of a metagenomic library for genes involved in microbial degradation of aromatic compounds. Environ Microbiol 2007; 9:2289-97; PMID:17686025; http://dx.doi.org/10.1111/j.1462-2920.2007.01342.x
101. Gloux K, Leclerc M, Iliozer H, L'Haridon R, Manichanh C, Corthier G, Nalin R, Blottière HM, Doré J. Development of high-throughput pheno-typing of metagenomic clones from the human gut microbiome for modulation of eukaryotic cell growth. Appl Environ Microbiol 2007; 73:3734-7; PMID:17400773; http://dx.doi.org/10.1128/AEM.02204-06
102. Wynendaele E, Bronselaer A, Nielandt J, D'Hondt M, Stalmans S, Bracke N, Verbeke F, Van De Wiele C, De Tré G, De Spiegeleer B. Quorumpeps database: chemical space, microbial origin and functionality of quorum sensing peptides. Nucleic Acids Res 2013; 41:D655-D659; PMID:23180797; http://dx.doi.org/10.1093/nar/gks1137