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Acyl Homoserine Lactone in Interspecies Bacterial Signaling

  • Kanojiya, Poonam (Symbiosis School of Biological Sciences, Symbiosis International (Deemed University)) ;
  • Banerji, Rajashri (Symbiosis School of Biological Sciences, Symbiosis International (Deemed University)) ;
  • Saroj, Sunil D. (Symbiosis School of Biological Sciences, Symbiosis International (Deemed University))
  • Received : 2021.11.30
  • Accepted : 2021.12.31
  • Published : 2022.03.28

Abstract

Bacteria communicate with each other through an intricate communication mechanism known as quorum sensing (QS). QS regulates different behavioral aspects in bacteria, such as biofilm formation, sporulation, virulence gene expression, antibiotic production, and bioluminescence. Several different chemical signals and signal detection systems play vital roles in promoting highly efficient intra- and interspecies communication. Gram-negative bacteria coordinate gene regulation through the production of acyl homoserine lactones (AHLs). Gram-positive bacteria do not code for AHL production, while some gram-negative bacteria have an incomplete AHL-QS system. Despite this fact, these microbes can detect AHLs owing to the presence of LuxR solo receptors. Various studies have reported the role of AHLs in interspecies signaling. Moreover, as bacteria live in a polymicrobial community, the production of extracellular compounds to compete for resources is imperative. Thus, AHL-mediated signaling and inhibition are considered to affect virulence in bacteria. In the current review, we focus on the synthesis and regulation mechanisms of AHLs and highlight their role in interspecies bacterial signaling. Exploring interspecies bacterial signaling will further help us understand host-pathogen interactions, thereby contributing to the development of therapeutic strategies intended to target chronic polymicrobial infections.

Keywords

Acknowledgement

PK and RB are supported by the junior research fellowship program of the Symbiosis International (Deemed University). The work was supported by the Ramalingaswami fellowship program of Department of Biotechnology, India under grant BT/RLF/Reentry/41/2015.

References

  1. Rutherford ST, Bassler BL. 2012. Bacterial quorum sensing: its role in virulence and possibilities for its control. Cold Spring Harb. Perspect. Med. 2: a012427. https://doi.org/10.1101/cshperspect.a012427
  2. Waters CM, Bassler BL. 2005. Quorum sensing: cell-to-cell communication in bacteria. Annu. Rev. Cell Dev. Biol. 21: 319-346. https://doi.org/10.1146/annurev.cellbio.21.012704.131001
  3. Ryan RP, Dow JM. 2008. Diffusible signals and interspecies communication in bacteria. Microbiology 154: 1845-1858. https://doi.org/10.1099/mic.0.2008/017871-0
  4. Fajardo A, Martinez JL. 2008. Antibiotics as signals that trigger specific bacterial responses. Curr. Opin. Microbiol. 11: 161-167. https://doi.org/10.1016/j.mib.2008.02.006
  5. Miller MB, Bassler BL. 2001. Quorum sensing in bacteria. Annu. Rev. Microbiol. 55: 165-199. https://doi.org/10.1146/annurev.micro.55.1.165
  6. Parsek MR, Val DL, Hanzelka BL, Cronan Jr JE, Greenberg EP. 1999. Acyl homoserine-lactone quorum-sensing signal generation. Proc. Natl. Acad. Sci. USA 96: 4360-4365. https://doi.org/10.1073/pnas.96.8.4360
  7. Eberl L. 1999. N-acyl homoserinelactone-mediated gene regulation in gram-negative bacteria. Syst. Appl. Microbiol. 22: 493-506. https://doi.org/10.1016/S0723-2020(99)80001-0
  8. Schauder S, Bassler BL. 2001. The languages of bacteria. Genes Dev. 15: 1468-1480. https://doi.org/10.1101/gad.899601
  9. Ismail AS, Valastyan JS, Bassler BL. 2016. A host-produced autoinducer-2 mimic activates bacterial quorum sensing. Cell Host Microbe 19: 470-480. https://doi.org/10.1016/j.chom.2016.02.020
  10. Hughes DT, Sperandio V. 2008. Inter-kingdom signaling communication between bacteria and their hosts. Nat. Rev. Microbiol. 6: 111-120. https://doi.org/10.1038/nrmicro1836
  11. Sircili MP, Walters M, Trabulsi LR, Sperandio V. 2004. Modulation of enteropathogenic Escherichia coli virulence by quorum sensing. Infect. Immun. 72: 2329-2337. https://doi.org/10.1128/IAI.72.4.2329-2337.2004
  12. Verstrepen KJ, Reynolds TB, Fink GR. 2004. Origins of variation in the fungal cell surface. Nat. Rev. Microbiol. 2: 533-540. https://doi.org/10.1038/nrmicro927
  13. Lee J, Jayaraman A, Wood TK. 2007. Indole is an inter-species biofilm signal mediated by SdiA. BMC Microbiol. 7: 42. https://doi.org/10.1186/1471-2180-7-42
  14. Kuczynska-Wisnik D, Matuszewska E, Furmanek-Blaszk B, Leszczynska D, Grudowska A, Szczepaniak P, et al. 2010. Antibiotics promoting oxidative stress inhibit formation of Escherichia coli biofilm via indole signaling. Res. Microbiol. 161: 847-853. https://doi.org/10.1016/j.resmic.2010.09.012
  15. Lee JH, Lee J. 2010. Indole as an intercellular signal in microbial communities. FEMS Microbiol. Rev. 34: 426-444. https://doi.org/10.1111/j.1574-6976.2009.00204.x
  16. Davies J. 1990. What are antibiotics? Archaic functions for modern activities. Mol. Microbiol. 4: 1227-1232. https://doi.org/10.1111/j.1365-2958.1990.tb00701.x
  17. Davies J. 2007. Microbes have the last word: A drastic re-evaluation of antimicrobial treatment is needed to overcome the threat of antibiotic-resistant bacteria. EMBO Rep. 8: 616-621. https://doi.org/10.1038/sj.embor.7401022
  18. Seshasayee AS, Bertone P, Fraser GM, Luscombe NM. 2006. Transcriptional regulatory networks in bacteria: from input signals to output responses. Curr. Opin. Microbiol. 9: 511-519. https://doi.org/10.1016/j.mib.2006.08.007
  19. Yim G, Wang HH, Davies J. 2006. The truth about antibiotics. Int. J. Med. Microbiol. 296: 163-170. https://doi.org/10.1016/j.ijmm.2006.01.039
  20. Yim G, Huimi Wang H, Davies Frs J. 2007. Antibiotics as signaling molecules. Philos. Trans. R. Soc. Lond., B, Biol. Sci. 362: 1195-1200. https://doi.org/10.1098/rstb.2007.2044
  21. Eberhard A, Burlingame AL, Eberhard C, Kenyon GL, Nealson KH, Oppenheimer NJ. 1981. Structural identification of autoinducer of Photobacterium fischeri luciferase. Biochemistry 20: 2444-2449. https://doi.org/10.1021/bi00512a013
  22. Pearson JP, Gray KM, Passador L, Tucker KD, Eberhard A, Lglewski BH, et al. 1994. Structure of the autoinducer required for expression of Pseudomonas aeruginosa virulence genes. Proc. Natl. Acad. Sci. USA 91: 197-201. https://doi.org/10.1073/pnas.91.1.197
  23. Pearson JP, Passador L, Iglewski BH, Greenberg EP. 1995. A second N-acylhomoserine lactone signal produced by Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 92: 1490-1494. https://doi.org/10.1073/pnas.92.5.1490
  24. Gray KM, Pearson JP, Downie JA, Boboye BE, Freenberg EP. 1996. Cell-to-cell signaling in the symbiotic nitrogen-fixing bacterium Rhizobium leguminosarum: autoinduction of a stationary phase and rhizosphere-expressed genes. J. Bacteriol. 178: 372-376. https://doi.org/10.1128/jb.178.2.372-376.1996
  25. Eberhard A, Longin T, Widrig CA, Stranick SJ. 1991. Synthesis of the lux gene autoinducer in Vibrio fischeri is positively autoregulated. Arch. Microbiol. 155: 294-297. https://doi.org/10.1007/BF00252215
  26. Gilson L, Kuo A, Dunlap PV. 1995. AinS and a new family of autoinducer synthesis proteins. J. Bacteriol. 177: 6946-6951. https://doi.org/10.1128/jb.177.23.6946-6951.1995
  27. Schaefer AL, Val DL, Hanzelka BL, Cronan JE, Jr, Greenberg EP. 1996. Generation of cell-to-cell signals in quorum sensing: acyl homoserine lactone synthase activity of a purified Vibrio fischeri LuxI protein. Proc. Natl. Acad. Sci. USA 93: 9505-9509. https://doi.org/10.1073/pnas.93.18.9505
  28. Pearson JP, Van Delden C, Iglewski BH. 1999. Active efflux and diffusion are involved in transport of Pseudomonas aeruginosa cell-to-cell signals. J. Bacteriol. 181: 1203-1210. https://doi.org/10.1128/jb.181.4.1203-1210.1999
  29. Evans K, Passador L, Srikumar R, Tsang E, Nezezon J, Poole K. 1998. Influence of the MexAB-OprM multidrug efflux system on quorum sensing in Pseudomonas aeruginosa. J. Bacteriol. 180: 5443-5437. https://doi.org/10.1128/jb.180.20.5443-5447.1998
  30. Alcalde-Rico M, Hernando-Amado S, Blanco P, Martinez JL. 2016. Multidrug efflux pumps at the crossroad between antibiotic resistance and bacterial virulence. Front. Microbiol. 7: 1483. https://doi.org/10.3389/fmicb.2016.01483
  31. Hanzelka BL, Parsek MR, Val DL, Dunlap PV, Cronan Jr JE, Greenberg EP. 1999. Acylhomoserine lactone synthase activity of the Vibrio fischeri AinS protein. J. Bacteriol. 181: 5766-5770. https://doi.org/10.1128/jb.181.18.5766-5770.1999
  32. Parsek MR, Greenberg EP. 2000. Acyl-homoserine lactone quorum sensing in gram-negative bacteria: a signaling mechanism involved in associations with higher organisms. Proc. Natl. Acad. Sci. USA 97: 8789-8793. https://doi.org/10.1073/pnas.97.16.8789
  33. Mok KC, Wingreen NS, Bassler BL. 2003. Vibrio harveyi quorum sensing: a coincidence detector for two autoinducers controls gene expression. EMBO J. 22: 870-881. https://doi.org/10.1093/emboj/cdg085
  34. Henke JM, Bassler BL. 2004. Three parallel quorum-sensing systems regulate gene expression in Vibrio harveyi. J. Bacteriol. 186: 6902-6914. https://doi.org/10.1128/JB.186.20.6902-6914.2004
  35. Cao JG, Meighen EA. 1989. Purification and structural identification of an autoinducer for the luminescence system of Vibrio harveyi. J. Biol. Chem. 264: 21670-21676. https://doi.org/10.1016/S0021-9258(20)88238-6
  36. Surette MG, Miller MB, Bassler BL. 1999. Quorum sensing in Escherichia coli, Salmonella Typhimurium, and Vibrio harveyi: a new family of genes responsible for autoinducer production. Proc. Natl. Acad. Sci. USA 96: 1639-1644. https://doi.org/10.1073/pnas.96.4.1639
  37. Chen X, Schauder S, Potier N, Van Dorsselaer A, Pelczer I, Bassler BL, et al. 2002. Structural identification of a bacterial quorum-sensing signal containing boron. Nature 415: 545-549. https://doi.org/10.1038/415545a
  38. Bassler BL, Wright M, Silverman MR. 1994. Multiple signaling systems controlling expression of luminescence in Vibrio harveyi: sequence and function of genes encoding a second sensory pathway. Mol. Microbiol. 13: 273-286. https://doi.org/10.1111/j.1365-2958.1994.tb00422.x
  39. Freeman JA, Bassler BL. 1999. A genetic analysis of the function of LuxO, a two-component response regulator involved in quorum sensing in Vibrio harveyi. Mol. Microbiol. 31: 665-677. https://doi.org/10.1046/j.1365-2958.1999.01208.x
  40. Freeman JA, Bassler BL. 1999. Sequence and function of LuxU: a Two-component phosphorelay protein that regulates quorum sensing in Vibrio harveyi. J. Bacteriol. 181: 899-906. https://doi.org/10.1128/jb.181.3.899-906.1999
  41. Defoirdt T, Bossier P, Sorgeloos P, Verstraete W. 2005. The impact of mutations in the quorum sensing systems of Aeromonas hydrophila, Vibrio anguillarum and Vibrio harveyi on their virulence towards gnotobiotically cultured Artemia franciscana. Environ. Microbiol. 7: 1239-1247. https://doi.org/10.1111/j.1462-2920.2005.00807.x
  42. Silby MW, Winstanley C, Godfrey SA, Levy SB, Jackson RW. 2011. Pseudomonas genomes: diverse and adaptable. FEMS Microbiol. Rev. 35: 652-680. https://doi.org/10.1111/j.1574-6976.2011.00269.x
  43. Schuster M, Greenberg EP. 2006. A network of networks: quorum-sensing gene regulation in Pseudomonas aeruginosa. Int. J. Med. Microbiol. 296: 73-81. https://doi.org/10.1016/j.ijmm.2006.01.036
  44. Williams P, Camara M. 2009. Quorum sensing and environmental adaptation in Pseudomonas aeruginosa: a tale of regulatory networks and multifunctional signal molecules. Curr. Opin. Microbiol. 12: 182-191. https://doi.org/10.1016/j.mib.2009.01.005
  45. Schuster M, Lostroh CP, Ogi T, Greenberg EP. 2003. Identification, timing, and signal specificity of Pseudomonas aeruginosa quorum-controlled genes: a transcriptome analysis. J. Bacteriol. 185: 2066-2079. https://doi.org/10.1128/JB.185.7.2066-2079.2003
  46. Wagner VE, Bushnell D, Passador L, Brooks AI, Lglewski BH. 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
  47. Crump JA, Collignon PJ. 2000. Intravascular catheter-associated infections. Eur. J. Clin. Microbiol. Infect. Dis. 19: 1-8. https://doi.org/10.1007/s100960050001
  48. Wargo MJ, Hogan DA. 2006. Fungal-bacterial interactions: a mixed bag of mingling microbes. Curr. Opin. Microbiol. 9: 359-364. https://doi.org/10.1016/j.mib.2006.06.001
  49. Duan K, Dammel C, Stein J, Rabin H, Surette MG. 2003. Modulation of Pseudomonas aeruginosa gene expression by host microflora through interspecies communication. Mol. Microbiol. 50: 1477-1491. https://doi.org/10.1046/j.1365-2958.2003.03803.x
  50. Hogan DA, Vik A, Kolter R. 2004. A Pseudomonas aeruginosa quorum-sensing molecule influences Candida albicans morphology. Mol. Microbiol. 54: 1212-1223. https://doi.org/10.1111/j.1365-2958.2004.04349.x
  51. Trejo-Hernandez A, Andrade-Dominguez A, Hernandez M, Encarnacion S. 2014. Interspecies competition triggers virulence and mutability in Candida albicans-Pseudomonas aeruginosa mixed biofilms. ISME J. 8: 1974-1988. https://doi.org/10.1038/ismej.2014.53
  52. Roux D, Gaudry S, Dreyfuss D, El-Benna J, de Prost N, Denamur E, et al. 2009. Candida albicans impairs macrophage function and facilitates Pseudomonas aeruginosa pneumonia in rat. Crit. Care Med. 37: 1062-1067. https://doi.org/10.1097/CCM.0b013e31819629d2
  53. Cugini C, Calfee MW, Farrow III JM, Morales DK, Pesci EC, Hogan DA. 2007. Farnesol, a common sesquiterpene, inhibits PQS production in Pseudomonas aeruginosa. Mol. Microbiol. 65: 896-906. https://doi.org/10.1111/j.1365-2958.2007.05840.x
  54. Tashiro Y, Yawata Y, Toyofuku M, Uchiyama H, Nomura N. 2013. Interspecies interaction between Pseudomonas aeruginosa and other microorganisms. Microbes Environ. 28: 13-24. https://doi.org/10.1264/jsme2.ME12167
  55. Hoffman LR, Deziel E, d'Argenio DA, Lepine F, Emerson J, McNamara S, et al. 2006. Selection for Staphylococcus aureus small-colony variants due to growth in the presence of Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 103: 19890-19895. https://doi.org/10.1073/pnas.0606756104
  56. Fishbain J, Peleg AY. 2010. Treatment of Acinetobacter infections. Clin. Infect. Dis. 51: 79-84. https://doi.org/10.1086/653120
  57. Weinstein RA, Gaynes R, Edwards JR. 2005. Overview of nosocomial infections caused by gram-negative bacilli. Clin. Infect. Dis. 41: 848-854. https://doi.org/10.1086/432803
  58. Nucleo E, Steffanoni L, Fugazza G, Migliavacca R, Giacobone E, Navarra A, et al. 2009. Growth in glucose-based medium and exposure to subinhibitory concentrations of imipenem induce biofilm formation in a multidrug-resistant clinical isolate of Acinetobacter baumannii. BMC Microbiol. 9: 270. https://doi.org/10.1186/1471-2180-9-270
  59. Tomaras AP, Dorsey CW, Edelmann RE, Actis L. 2003. Attachment to and biofilm formation on abiotic surfaces by Acinetobacter baumannii: involvement of a novel chaperone-usher pili assembly system. Microbiology 149: 3473-3484. https://doi.org/10.1099/mic.0.26541-0
  60. Dent LL, Marshall DR, Pratap S, Hulette RB. 2010. Multidrug resistant Acinetobacter baumannii: a descriptive study in a city hospital. BMC Infect. Dis. 10: 196. https://doi.org/10.1186/1471-2334-10-196
  61. Bhargava N, Sharma P, Capalash N. 2012. N-acyl homoserine lactone mediated interspecies interactions between A. baumannii and P. aeruginosa. Biofouling 28: 813-822. https://doi.org/10.1080/08927014.2012.714372
  62. Niu C, Clemmer KM, Bonomo RA, Rather PN. 2008. Isolation and characterization of an autoinducer synthase from Acinetobacter baumannii. J. Bacteriol. 190: 3386-3392. https://doi.org/10.1128/JB.01929-07
  63. Savka MA, Le PT, Burr TJ. 2011. LasR receptor for detection of long-chain quorum-sensing signals: identification of N-acyl-homoserine lactones encoded by the avsI locus of Agrobacterium vitis. Curr. Microbiol. 62: 101-110. https://doi.org/10.1007/s00284-010-9679-1
  64. Govan JR, Deretic V. 1996. Microbial pathogenesis in cystic fibrosis: mucoid Pseudomonas aeruginosa and Burkholderia cepacia. Microbiol. Rev. 60: 539-574. https://doi.org/10.1128/mr.60.3.539-574.1996
  65. Tummler B, Kiewitz C. 1999. Cystic fibrosis: an inherited susceptibility to bacterial respiratory infections. Mol. Med. Today 5: 351-358. https://doi.org/10.1016/S1357-4310(99)01506-3
  66. Saiman LI, Cacalano GR, Prince AL. 1990. Pseudomonas cepacia adherence to respiratory epithelial cells is enhanced by Pseudomonas aeruginosa. Infect. Immun. 58: 2578-2584. https://doi.org/10.1128/iai.58.8.2578-2584.1990
  67. Isles A, Maclusky I, Corey M, Gold R, Prober C, Fleming P, et al. 1984. Pseudomonas cepacia infection in cystic fibrosis: an emerging problem. J. Pediatr. 104: 206-210. https://doi.org/10.1016/s0022-3476(84)80993-2
  68. Lewenza S, Conway B, Greenberg EP, Sokol PA. 1999. Quorum sensing in Burkholderia cepacia: identification of the LuxRI homologs CepRI. J. Bacteriol. 181: 748-756. https://doi.org/10.1128/jb.181.3.748-756.1999
  69. Gotschlich A, Huber B, Geisenberger O, Togl A, Steidle A, Riedel K, et al. 2001. Synthesis of multiple N-acylhomoserine lactones is wide-spread among the members of the Burkholderia cepacia complex. Syst. Appl. Microbiol. 24: 1-4. https://doi.org/10.1078/0723-2020-00013
  70. McKenney D, Brown KE, Allison DG. 1995. Influence of Pseudomonas aeruginosa exoproducts on virulence factor production in Burkholderia cepacia: evidence of interspecies communication. J. Bacteriol. 177: 6989-6992. https://doi.org/10.1128/jb.177.23.6989-6992.1995
  71. Riedel K, Hentzer M, Geisenberger O, Huber B, Steidle A, Wu H, et al. 2001. N-acylhomoserine-lactone-mediated communication between Pseudomonas aeruginosa and Burkholderia cepacia in mixed biofilms. Microbiology 147: 3249-3262. https://doi.org/10.1099/00221287-147-12-3249
  72. Carapetis JR, Steer AC, Mulholland EK, Weber M. 2005. The global burden of group A streptococcal diseases. Lancet Infect. Dis. 5: 685-694. https://doi.org/10.1016/S1473-3099(05)70267-X
  73. Jimenez JC, Federle MJ. 2014. Quorum sensing in group A Streptococcus. Front. Cell. Infect. Microbiol. 4: 127. https://doi.org/10.3389/fcimb.2014.00127
  74. Saroj SD, Holmer L, Berengueras JM, Jonsson AB. 2017. Inhibitory role of acyl homoserine lactones in hemolytic activity and viability of Streptococcus pyogenes M6 S165. Sci. Rep. 7: 44902. https://doi.org/10.1038/srep44902
  75. Saroj SD, Maudsdotter L, Tavares R, Jonsson AB. 2016. Lactobacilli interfere with Streptococcus pyogenes hemolytic activity and adherence to host epithelial cells. Front. Microbiol. 7: 1176. https://doi.org/10.3389/fmicb.2016.01176
  76. Banerji R, Saroj SD. 2021. Interspecies signalling affects virulence related morphological characteristics of Streptococcus pyogenes M3. FEMS Microbiol. Lett. 368: fnab079. https://doi.org/10.1093/femsle/fnab079
  77. Banerji R, Saroj SD. 2021. Exposure to acyl homoserine lactone enhances survival of Streptococcus pyogenes in murine macrophages. Microb. Ecol. doi: 10.1007/s00248-021-01926-1. Online ahead of print.
  78. Subramoni S, Venturi V. 2009. LuxR-family 'solos': bachelor sensors/regulators of signaling molecules. Microbiology 155: 1377-1385. https://doi.org/10.1099/mic.0.026849-0
  79. Case RJ, Labbate M, Kjelleberg S. 2008. AHL-driven quorum-sensing circuits: their frequency and function among the proteobacteria. ISME J. 2: 345-349. https://doi.org/10.1038/ismej.2008.13
  80. Fuqua C, Greenberg EP. 2002. Listening in on bacteria: acyl-homoserine lactone signaling. Nat. Rev. Mol. Cell Biol. 3: 685-695. https://doi.org/10.1038/nrm907
  81. Lintz MJ, Oinuma KI, Wysoczynski CL, Greenberg EP, Churchill MEA. 2011. Crystal structure of QscR, a Pseudomonas aeruginosa quorum sensing signal receptor. Proc. Natl. Acad. Sci. USA 108: 15763-15768. https://doi.org/10.1073/pnas.1112398108
  82. Ahmer BM. 2004. Cell-to-cell signaling in Escherichia coli and Salmonella enterica. Mol. Microbiol. 52: 933-945. https://doi.org/10.1111/j.1365-2958.2004.04054.x
  83. Chugani SA, Whiteley M, Lee KM, D'Argenio D, Manoil C, Greenberg EP. 2001. QscR, a modulator of quorum-sensing signal synthesis and virulence in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 98: 2752-2757. https://doi.org/10.1073/pnas.051624298
  84. Janssens JC, Metzger K, Daniels R, Ptacek D, Verhoeven T, Habel LW, et al. 2007. Synthesis of N-acyl homoserine lactone analogues reveals strong activators of SdiA, the Salmonella enterica serovar Typhimurium LuxR homologue. Appl. Environ. Microbiol. 73: 535-544. https://doi.org/10.1128/AEM.01451-06
  85. Michael B, Smith JN, Swift S, Heffron F, Ahmer BM. 2001. SdiA of Salmonella enterica is a LuxR homolog that detects mixed microbial communities. J. Bacteriol. 183: 5733-5742. https://doi.org/10.1128/JB.183.19.5733-5742.2001
  86. Yao Y, Martinez-Yamout MA, Dickerson TJ, Brogan AP, Wright PE, Dyson HJ. 2006. Structure of the Escherichia coli quorum sensing protein SdiA: activation of the folding switch by acyl homoserine lactones. J. Mol. Biol. 355: 262-273. https://doi.org/10.1016/j.jmb.2005.10.041
  87. Rahmati S, Yang S, Davidson AL, Zechiedrich EL. 2002. Control of the AcrAB multidrug efflux pump by quorum-sensing regulator SdiA. Mol. Microbiol. 43: 677-685. https://doi.org/10.1046/j.1365-2958.2002.02773.x
  88. Chan KG, Liu YC, Chang CY. 2015. Inhibiting N-acyl-homoserine lactone synthesis and quenching Pseudomonas quinolone quorum sensing to attenuate virulence. Front. Microbiol. 6: 1173. https://doi.org/10.3389/fmicb.2015.01173
  89. Hoang TT, Schweizer HP. 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. https://doi.org/10.1128/jb.181.17.5489-5497.1999
  90. Singh V, Evans GB, Lenz DH, Mason JM, Clinch K, Mee S, et al. 2005. Femtomolar transition state analogue inhibitors of 5'-methylthioadenosine/S-adenosylhomocysteine nucleosidase from Escherichia coli. J. Biol. Chem. 280: 18265-18273. https://doi.org/10.1074/jbc.M414472200
  91. Singh V, Shi W, Almo SC, Evans GB, Furneaux RH, Tyler PC, et al. 2006. Structure and inhibition of a quorum sensing target from Streptococcus pneumoniae. Biochemistry 45: 12929-12941. https://doi.org/10.1021/bi061184i
  92. Taga ME, Bassler BL. 2003. Chemical communication among bacteria. Proc. Natl. Acad. Sci. USA 100(suppl 2): 14549-14554. https://doi.org/10.1073/pnas.1934514100
  93. Eberl L, Winson MK, Sternberg C, Stewart GS, Christiansen G, Chhabra SR, et al. 1996. Involvement of N-acyl-l-homoserine lactone autoinducers in controlling the multicellular behaviour of Serratia liquefaciens. Mol. Microbiol. 20: 127-136. https://doi.org/10.1111/j.1365-2958.1996.tb02495.x
  94. Lindum PW, Anthoni U, Christophersen C, Eberl L, Molin S, Givskov M. 1998. N-Acyl-L-homoserine lactone autoinducers control production of an extracellular lipopeptide biosurfactant required for swarming motility of Serratia liquefaciens MG1. J. Bacteriol. 180: 6384-6388. https://doi.org/10.1128/jb.180.23.6384-6388.1998
  95. Manefield M, de Nys R, Naresh K, Roger R, Givskov M, Peter S, et al. 1999. Evidence that halogenated furanones from Delisea pulchra inhibit acylated homoserine lactone (AHL)-mediated gene expression by displacing the AHL signal from its receptor protein. Microbiology 145: 283-291. https://doi.org/10.1099/13500872-145-2-283
  96. Borchardt SA, Allain EJ, Michels JJ, Stearns GW, Kelly RF, McCoy WF. 2001. Reaction of acylated homoserine lactone bacterial signaling molecules with oxidized halogen antimicrobials. Appl. Environ. Microbiol. 67: 3174-3179. https://doi.org/10.1128/AEM.67.7.3174-3179.2001
  97. Lee SJ, Park SY, Lee JJ, Yum DY, Koo BT, Lee JK. 2002. Genes encoding the N-acyl homoserine lactone-degrading enzyme are widespread in many subspecies of Bacillus thuringiensis. Appl. Environ. Microbiol. 68: 3919-3924. https://doi.org/10.1128/AEM.68.8.3919-3924.2002
  98. Givskov M, Ostling J, Eberl L, Lindum PW, Christensen AB, Christiansen G, et al. 1998. Two separate regulatory systems participate in control of swarming motility of Serratia liquefaciens MG1. J. Bacteriol. 180: 742-745. https://doi.org/10.1128/jb.180.3.742-745.1998
  99. Eberl L, Molin S, Givskov M. 1999. Surface motility of Serratia liquefaciens MG1. J. Bacteriol. 181: 1703-1712. https://doi.org/10.1128/jb.181.6.1703-1712.1999
  100. Bernheimer AW, Schwartz LL. 1964. Lysosomal disruption by bacterial toxins. J. Bacteriol. 87: 1100-1104. https://doi.org/10.1128/jb.87.5.1100-1104.1964
  101. Keiser H, Weissmann G, Bernheimer AW. 1964. STUDIES ON LYSOSOMES: IV. Solubilization of enzymes during mitochondrial swelling and disruption of lysosomes by streptolysin S and other hemolytic agents. J. Cell Biol. 22: 101-113. https://doi.org/10.1083/jcb.22.1.101
  102. Lowery CA, Dickerson TJ, Janda KD. 2008. Interspecies and interkingdom communication mediated by bacterial quorum sensing. Chem. Soc. Rev. 37: 1337-1346. https://doi.org/10.1039/b702781h