1932

Abstract

is an opportunistic pathogen that causes a variety of acute and chronic infections. Usually a commensal on the host body, is capable of transforming into a virulent pathogen upon sensing favorable changes in the host immune system or stress cues. infections are hard to eradicate, because this pathogen has developed strong resistance to most conventional antibiotics; in addition, in chronic infections it commonly forms a biofilm matrix, which provides bacterial cells a protected environment to withstand various stresses including antibiotics. Given its importance as a human pathogen and its notorious antimicrobial tolerance, has been the subject of intensive investigations internationally. Research progress over the last two decades has unveiled a range of chemical communication systems in this pathogen. These diversified chemical communication systems endow a superb ability and remarkable flexibility to coordinate and modulate accordingly the transcriptional expression of various sets of genes associated with virulence and other physiologic activities in response to environmental changes. A fair understanding of the chemical signaling mechanisms with which governs virulence gene expression may hold the key to developing alternative therapeutic interventions that control and prevent bacterial infections.

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2019-09-08
2025-05-01
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Literature Cited

  1. 1. 
    Amari DT, Marques CNH, Davies DG 2013. The putative enoyl-coenzyme A hydratase DspI is required for production of the Pseudomonas aeruginosa biofilm dispersion autoinducer cis-2-decenoic acid. J. Bacteriol. 195204600–10
    [Google Scholar]
  2. 2. 
    Ballok AE, O'Toole GA. 2013. Pouring salt on a wound: Pseudomonas aeruginosa virulence factors alter Na+ and Cl flux in the lung. J. Bacteriol. 195184013–19
    [Google Scholar]
  3. 3. 
    Barbieri JT, Sun J. 2004. Pseudomonas aeruginosa ExoS and ExoT. Rev. Physiol. Biochem. Pharmacol. 15279–92
    [Google Scholar]
  4. 4. 
    Belin P, Moutiez M, Lautru S, Seguin J, Pernodet J-L, Gondry M 2012. The nonribosomal synthesis of diketopiperazines in tRNA-dependent cyclodipeptide synthase pathways. Nat. Prod. Rep. 299961–79
    [Google Scholar]
  5. 5. 
    Bomberger JM, MacEachran DP, Coutermarsh BA, Ye S, O'Toole GA, Stanton BA 2009. Long-distance delivery of bacterial virulence factors by Pseudomonas aeruginosa outer membrane vesicles. PLOS Pathog 54e1000382
    [Google Scholar]
  6. 6. 
    Boon C, Deng Y, Wang L-H, He Y, Xu J-L et al. 2008. A novel DSF-like signal from Burkholderia cenocepacia interferes with Candida albicans morphological transition. ISME J 2127–36Characterization of B. cenocepacia BDSF signal, a structural analog of DSF and its role in interspecies signaling and microbial pathogenesis.
    [Google Scholar]
  7. 7. 
    Bredenbruch F, Geffers R, Nimtz M, Buer J, Häussler S 2006. The Pseudomonas aeruginosa quinolone signal (PQS) has an iron‐chelating activity. Environ. Microbiol. 881318–29
    [Google Scholar]
  8. 8. 
    Bredenbruch F, Nimtz M, Wray V, Morr M, Müller R, Häussler S 2005. Biosynthetic pathway of Pseudomonas aeruginosa 4-hydroxy-2-alkylquinolines. J. Bacteriol. 187113630–35
    [Google Scholar]
  9. 9. 
    Bridge DR, Martin KH, Moore ER, Lee WM, Carroll JA et al. 2012. Examining the role of actin-plasma membrane association in Pseudomonas aeruginosa infection and type III secretion translocation in migratory T24 epithelial cells. Infect. Immun. 8093049–64
    [Google Scholar]
  10. 10. 
    Brint JM, Ohman DE. 1995. Synthesis of multiple exoproducts in Pseudomonas aeruginosa is under the control of RhlR-RhlI, another set of regulators in strain PAO1 with homology to the autoinducer-responsive LuxR-LuxI family. J. Bacteriol. 177247155–63
    [Google Scholar]
  11. 11. 
    Bzdrenga J, Daudé D, Rémy B, Jacquet P, Plener L et al. 2017. Biotechnological applications of quorum quenching enzymes. Chem. Biol. Interact. 267104–15
    [Google Scholar]
  12. 12. 
    Cai Z, Yuan Z-H, Zhang H, Pan Y, Wu Y et al. 2017. Fatty acid DSF binds and allosterically activates histidine kinase RpfC of phytopathogenic bacterium Xanthomonas campestris pv. campestris to regulate quorum-sensing and virulence. PLOS Pathog 134e1006304
    [Google Scholar]
  13. 13. 
    Cámara M, Williams P, Hardman A 2002. Controlling infection by tuning in and turning down the volume of bacterial small-talk. Lancet Infect. Dis. 211667–76
    [Google Scholar]
  14. 14. 
    Campbell J, Lin Q, Geske GD, Blackwell HE 2009. New and unexpected insights into the modulation of LuxR-type quorum sensing by cyclic dipeptides. ACS Chem. Biol. 4121051–59
    [Google Scholar]
  15. 15. 
    Cornforth DM, Foster KR. 2013. Competition sensing: the social side of bacterial stress responses. Nat. Rev. Microbiol. 114285
    [Google Scholar]
  16. 16. 
    Costerton JW, Stewart PS, Greenberg EP 1999. Bacterial biofilms: a common cause of persistent infections. Science 28454181318–22
    [Google Scholar]
  17. 17. 
    Cowell BA, Evans DJ, Fleiszig SMJ 2005. Actin cytoskeleton disruption by ExoY and its effects on Pseudomonas aeruginosa invasion. FEMS Microbiol. Lett. 250171–76
    [Google Scholar]
  18. 18. 
    Cuzick A, Stirling FR, Lindsay SL, Evans TJ 2006. The type III pseudomonal exotoxin U activates the c-Jun NH2-terminal kinase pathway and increases human epithelial interleukin-8 production. Infect. Immun. 7474104–13
    [Google Scholar]
  19. 19. 
    Dasgupta N, Ashare A, Hunninghake GW, Yahr TL 2006. Transcriptional induction of the Pseudomonas aeruginosa type III secretion system by low Ca2+ and host cell contact proceeds through two distinct signaling pathways. Infect. Immun 7463334–41P. aeruginosa utilizes a complex set of regulatory pathways for T3SS expression via ExsC in response to calcium and host factors.
    [Google Scholar]
  20. 20. 
    Dasgupta N, Lykken GL, Wolfgang MC, Yahr TL 2004. A novel anti-anti-activator mechanism regulates expression of the Pseudomonas aeruginosa type III secretion system. Mol. Microbiol. 531297–308
    [Google Scholar]
  21. 21. 
    Davies DG, Marques CNH. 2009. A fatty acid messenger is responsible for inducing dispersion in microbial biofilms. J. Bacteriol. 19151393–403
    [Google Scholar]
  22. 22. 
    de Bentzmann S, Polette M, Zahm J-M, Hinnrasky J, Kileztky C et al. 2000. Pseudomonas aeruginosa virulence factors delay airway epithelial wound repair by altering the actin cytoskeleton and inducing overactivation of epithelial matrix metalloproteinase-2. Lab. Investig. 802209–19
    [Google Scholar]
  23. 23. 
    de Kievit TR, Kakai Y, Register JK, Pesci EC, Iglewski BH 2002. Role of the Pseudomonas aeruginosa las and rhl quorum-sensing systems in rhlI regulation. FEMS Microbiol. Lett. 2121101–6
    [Google Scholar]
  24. 24. 
    Dekimpe V, Deziel E. 2009. Revisiting the quorum-sensing hierarchy in Pseudomonas aeruginosa: the transcriptional regulator RhlR regulates LasR-specific factors. Microbiology 1553712–23Host factors reorganize the hierarchical las-pqs-rhl-QS system from a las-dependent to a las-independent pathway.
    [Google Scholar]
  25. 25. 
    Deng Y, Wu J, Tao F, Zhang LH 2011. Listening to a new language: DSF-based quorum sensing in Gram-negative bacteria. Chem. Rev. 111160–73
    [Google Scholar]
  26. 26. 
    Déziel E, Lépine F, Milot S, He J, Mindrinos MN et al. 2004. Analysis of Pseudomonas aeruginosa 4-hydroxy-2-alkylquinolines (HAQs) reveals a role for 4-hydroxy-2-heptylquinoline in cell-to-cell communication. PNAS 10151339–44
    [Google Scholar]
  27. 27. 
    Diaz MH, Shaver CM, King JD, Musunuri S, Kazzaz JA, Hauser AR 2008. Pseudomonas aeruginosa induces localized immunosuppression during pneumonia. Infect. Immun. 76104414–21
    [Google Scholar]
  28. 28. 
    Diggle SP, Cornelis P, Williams P, Cámara M 2006. 4-Quinolone signalling in Pseudomonas aeruginosa: old molecules, new perspectives. Int. J. Med. Microbiol. 296283–91
    [Google Scholar]
  29. 29. 
    Diggle SP, Griffin AS, Campbell GS, West SA 2007. Cooperation and conflict in quorum-sensing bacterial populations. Nature 4507168411–14The impact of evolutionary dynamics on QS-mediated community lifestyle in bacterial populations of genetically varying cells.
    [Google Scholar]
  30. 30. 
    Diggle SP, Winzer K, Chhabra SR, Worrall KE, Cámara M, Williams P 2003. The Pseudomonas aeruginosa quinolone signal molecule overcomes the cell density‐dependency of the quorum sensing hierarchy, regulates rhl‐dependent genes at the onset of stationary phase and can be produced in the absence of LasR. Mol. Microbiol. 50129–43
    [Google Scholar]
  31. 31. 
    Diggle SP, Winzer K, Lazdunski A, Williams P, Cámara M 2002. Advancing the quorum in Pseudomonas aeruginosa: MvaT and the regulation of N-acylhomoserine lactone production and virulence gene expression. J. Bacteriol. 184102576–86
    [Google Scholar]
  32. 32. 
    Dong Y-H, Wang L-H, Xu J-L, Zhang H-B, Zhang X-F, Zhang L-H 2001. Quenching quorum-sensing-dependent bacterial infection by an N-acyl homoserine lactonase. Nature 4116839813–17
    [Google Scholar]
  33. 33. 
    Dong Y-H, Wang L-H, Zhang L-H 2007. Quorum-quenching microbial infections: mechanisms and implications. Philos. Trans. R. Soc. B Biol. Sci. 36214831201–11
    [Google Scholar]
  34. 34. 
    Dong Y-H, Zhang L-H. 2005. Quorum sensing and quorum-quenching enzymes. J. Microbiol. 431101–9
    [Google Scholar]
  35. 35. 
    Drenkard E, Ausubel FM. 2002. Pseudomonas biofilm formation and antibiotic resistance are linked to phenotypic variation. Nature 4166882740
    [Google Scholar]
  36. 36. 
    El-Halfawy OM, Valvano MA. 2015. Antimicrobial heteroresistance: An emerging field in need of clarity. Clin. Microbiol. Rev. 281191–207
    [Google Scholar]
  37. 37. 
    Engel J, Balachandran P. 2009. Role of Pseudomonas aeruginosa type III effectors in disease. Curr. Opin. Microbiol. 1261–66
    [Google Scholar]
  38. 38. 
    Frimmersdorf E, Horatzek S, Pelnikevich A, Wiehlmann L, Schomburg D 2010. How Pseudomonas aeruginosa adapts to various environments: a metabolomic approach. Environ. Microbiol. 1261734–47
    [Google Scholar]
  39. 39. 
    Fuqua WC, Winans SC, Greenberg EP 1994. Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators. J. Bacteriol. 1762269
    [Google Scholar]
  40. 40. 
    Gallagher LA, McKnight SL, Kuznetsova MS, Pesci EC, Manoil C 2002. Functions required for extracellular quinolone signaling by Pseudomonas aeruginosa. J. Bacteriol 184236472–80
    [Google Scholar]
  41. 41. 
    Gilbert KB, Kim TH, Gupta R, Greenberg EP, Schuster M 2009. Global position analysis of the Pseudomonas aeruginosa quorum‐sensing transcription factor LasR. Mol. Microbiol. 7361072–85
    [Google Scholar]
  42. 42. 
    Glessner A, Smith RS, Iglewski BH, Robinson JB 1999. Roles of Pseudomonas aeruginosa las and rhl quorum-sensing systems in control of twitching motility. J. Bacteriol. 18151623–29
    [Google Scholar]
  43. 43. 
    Gondry M, Jacques IB, Thai R, Babin M, Canu N et al. 2018. A comprehensive overview of the cyclodipeptide synthase family enriched with the characterization of 32 new enzymes. Front. Microbiol. 946
    [Google Scholar]
  44. 44. 
    González O, Ortíz-Castro R, Díaz-Pérez C, Díaz-Pérez AL, Magaña-Dueñas V et al. 2017. Non-ribosomal peptide synthases from Pseudomonas aeruginosa play a role in cyclodipeptide biosynthesis, quorum-sensing regulation, and root development in a plant host. Microb. Ecol. 733616–29
    [Google Scholar]
  45. 45. 
    Gooderham WJ, Hancock REW. 2009. Regulation of virulence and antibiotic resistance by two-component regulatory systems in Pseudomonas aeruginosa. FEMS Microbiol. Rev 332279–94
    [Google Scholar]
  46. 46. 
    Goodman AL, Kulasekara B, Rietsch A, Boyd D, Smith RS, Lory S 2004. A signaling network reciprocally regulates genes associated with acute infection and chronic persistence in Pseudomonas aeruginosa. Dev. Cell 75745–54
    [Google Scholar]
  47. 47. 
    Goytia M, Shafer WM. 2010. Polyamines can increase resistance of Neisseria gonorrhoeae to mediators of the innate human host defense. Infect. Immun. 7873187–95
    [Google Scholar]
  48. 48. 
    Grandclément C, Tannière M, Moréra S, Dessaux Y, Faure D 2016. Quorum quenching: role in nature and applied developments. FEMS Microbiol. Rev. 40186–116
    [Google Scholar]
  49. 49. 
    Hawver LA, Jung SA, Ng W-L 2016. Specificity and complexity in bacterial quorum-sensing systems. FEMS Microbiol. Rev. 405738–52
    [Google Scholar]
  50. 50. 
    He Y, Xu M, Lin K, Ng YA, Wen C et al. 2006. Genome scale analysis of diffusible signal factor regulon in Xanthomonas campestris pv. campestris: identification of novel cell-cell communication‐dependent genes and functions. Mol. Microbiol. 592610–22
    [Google Scholar]
  51. 51. 
    He Y-W, Wu J, Cha J-S, Zhang L-H 2010. Rice bacterial blight pathogen Xanthomonas oryzae pv. oryzae produces multiple DSF-family signals in regulation of virulence factor production. BMC Microbiol 10187
    [Google Scholar]
  52. 52. 
    He Y-W, Zhang L-H. 2008. Quorum sensing and virulence regulation in Xanthomonas campestris. FEMS Microbiol. Rev 325842–57
    [Google Scholar]
  53. 53. 
    Hernández-Padilla L, Vázquez-Rivera D, Sánchez-Briones LA, Díaz-Pérez AL, Moreno-Rodríguez J et al. 2017. The antiproliferative effect of cyclodipeptides from Pseudomonas aeruginosa PAO1 on HeLa cells involves inhibition of phosphorylation of Akt and S6k kinases. Molecules 221024
    [Google Scholar]
  54. 54. 
    Hogardt M, Roeder M, Schreff AM, Eberl L, Heesemann J 2004. Expression of Pseudomonas aeruginosa exoS is controlled by quorum sensing and RpoS. Microbiology 150843–51
    [Google Scholar]
  55. 55. 
    Holden MTG, Ram Chhabra S, De Nys R, Stead P, Bainton NJ et al. 1999. Quorum‐sensing cross talk: isolation and chemical characterization of cyclic dipeptides from Pseudomonas aeruginosa and other gram‐negative bacteria. Mol. Microbiol. 3361254–66
    [Google Scholar]
  56. 56. 
    Igarashi K, Kashiwagi K. 2000. Polyamines: mysterious modulators of cellular functions. Biochem. Biophys. Res. Commun. 2713559–64
    [Google Scholar]
  57. 57. 
    Igarashi K, Kashiwagi K. 2010. Modulation of cellular functions by polyamines. Int. J. Biochem. Cell Biol. 42139–51
    [Google Scholar]
  58. 58. 
    Iyer R, Williams C, Miller C 2003. Arginine-agmatine antiporter in extreme acid resistance in Escherichia coli. J. Bacteriol 185226556–61
    [Google Scholar]
  59. 59. 
    Jensen V, Löns D, Zaoui C, Bredenbruch F, Meissner A et al. 2006. RhlR expression in Pseudomonas aeruginosa is modulated by the Pseudomonas quinolone signal via PhoB-dependent and-independent pathways. J. Bacteriol. 188248601–6
    [Google Scholar]
  60. 60. 
    Jimenez PN, Koch G, Thompson JA, Xavier KB, Cool RH, Quax WJ 2012. The multiple signaling systems regulating virulence in Pseudomonas aeruginosa. Microbiol. Mol. Biol. Rev 76146–65
    [Google Scholar]
  61. 61. 
    Journet L, Hughes KT, Cornelis GR 2005. Type III secretion: a secretory pathway serving both motility and virulence. Mol. Membr. Biol. 221–241–50
    [Google Scholar]
  62. 62. 
    Korgaonkar A, Trivedi U, Rumbaugh KP, Whiteley M 2013. Community surveillance enhances Pseudomonas aeruginosa virulence during polymicrobial infection. PNAS 11031059–64P. aeruginosa senses cellular factors from other bacteria to stimulate the production of multiple virulence factors.
    [Google Scholar]
  63. 63. 
    Kwon DH, Lu C-D. 2006. Polyamines induce resistance to cationic peptide, aminoglycoside, and quinolone antibiotics in Pseudomonas aeruginosa PAO1. Antimicrob. Agents Chemother. 5051615–22
    [Google Scholar]
  64. 64. 
    Kwon DH, Lu CD. 2006. Polyamines increase antibiotic susceptibility in bacteria. Antimicrob. Agents Chemother. 5051623–27
    [Google Scholar]
  65. 65. 
    Langan KM, Kotsimbos T, Peleg AY 2015. Managing Pseudomonas aeruginosa respiratory infections in cystic fibrosis. Curr. Opin. Infect. Dis. 286547–56
    [Google Scholar]
  66. 66. 
    Laskowski MA, Osborn E, Kazmierczak BI 2004. A novel sensor kinase-response regulator hybrid regulates type III secretion and is required for virulence in Pseudomonas aeruginosa. Mol. Microbiol 5441090–103
    [Google Scholar]
  67. 67. 
    Latifi A, Winson MK, Foglino M, Bycroft BW, Stewart GSAB et al. 1995. Multiple homologues of LuxR and LuxI control expression of virulence determinants and secondary metabolites through quorum sensing in Pseudomonas aeruginosa PAO1. Mol. Microbiol. 172333–43
    [Google Scholar]
  68. 68. 
    Lee J, Wu J, Deng Y, Wang J, Wang C et al. 2013. A cell-cell communication signal integrates quorum sensing and stress response. Nat. Chem. Biol. 95339–43
    [Google Scholar]
  69. 69. 
    Lee J, Zhang L. 2015. The hierarchy quorum sensing network in Pseudomonas aeruginosa. Protein Cell 6126–41The versatility of the P. aeruginosa QS circuit in responding to environmental and host stress factors to enhance virulence.
    [Google Scholar]
  70. 70. 
    Liu L, Li T, Cheng XJ, Peng CT, Li CC et al. 2018. Structural and functional studies on Pseudomonas aeruginosa DspI: Implications for its role in DSF biosynthesis. Sci. Rep. 813928
    [Google Scholar]
  71. 71. 
    Lund-Palau H, Turnbull AR, Bush A, Bardin E, Cameron L et al. 2016. Pseudomonas aeruginosa infection in cystic fibrosis: pathophysiological mechanisms and therapeutic approaches. Expert Rev. Respir. Med. 106685–97
    [Google Scholar]
  72. 72. 
    Manago A, Becker KA, Carpinteiro A, Wilker B, Soddemann M et al. 2015. Pseudomonas aeruginosa pyocyanin induces neutrophil death via mitochondrial reactive oxygen species and mitochondrial acid sphingomyelinase. Antioxid. Redox Signal. 22131097–110
    [Google Scholar]
  73. 73. 
    Martin LW, Robson CL, Watts AM, Gray AR, Wainwright CE et al. 2018. Expression of Pseudomonas aeruginosa antibiotic resistance genes varies greatly during infections in cystic fibrosis patients. Antimicrob. Agents Chemother. 6211e01789–18
    [Google Scholar]
  74. 74. 
    Mashburn LM, Whiteley M. 2005. Membrane vesicles traffic signals and facilitate group activities in a prokaryote. Nature 4377057422–25
    [Google Scholar]
  75. 75. 
    McCaw ML, Lykken GL, Singh PK, Yahr TL 2002. ExsD is a negative regulator of the Pseudomonas aeruginosa type III secretion regulon. Mol. Microbiol. 4641123–33
    [Google Scholar]
  76. 76. 
    Michael AJ. 2016. Biosynthesis of polyamines and polyamine-containing molecules. Biochem. J. 473152315–29
    [Google Scholar]
  77. 77. 
    Mishra A, Choi J, Choi S-J, Baek K-H 2017. Cyclodipeptides: an overview of their biosynthesis and biological activity. Molecules 2210):1796
    [Google Scholar]
  78. 78. 
    Ochsner UA, Reiser J. 1995. Autoinducer-mediated regulation of rhamnolipid biosurfactant synthesis in Pseudomonas aeruginosa. PNAS 92146424–28
    [Google Scholar]
  79. 79. 
    Olejnickova K, Hola V, Ruzicka F 2014. Catheter-related infections caused by Pseudomonas aeruginosa: virulence factors involved and their relationships. Pathog. Dis. 72287–94
    [Google Scholar]
  80. 80. 
    Pearson JP, Feldman M, Iglewski BH, Prince A 2000. Pseudomonas aeruginosa cell-to-cell signaling is required for virulence in a model of acute pulmonary infection. Infect. Immun. 6874331–34
    [Google Scholar]
  81. 81. 
    Pesci EC, Milbank JBJ, Pearson JP, McKnight S, Kende AS et al. 1999. Quinolone signaling in the cell-to-cell communication system of Pseudomonas aeruginosa. PNAS 962011229–34
    [Google Scholar]
  82. 82. 
    Pesci EC, Pearson JP, Seed PC, Iglewski BH 1997. Regulation of las and rhl quorum sensing in Pseudomonas aeruginosa. J. Bacteriol 179103127–32
    [Google Scholar]
  83. 83. 
    Rahmani-Badi A, Sepehr S, Fallahi H, Heidari-Keshel S 2015. Dissection of the cis-2-decenoic acid signaling network in Pseudomonas aeruginosa using microarray technique. Front. Microbiol. 6383
    [Google Scholar]
  84. 84. 
    Rojas Murcia N, Lee X, Waridel P, Maspoli A, Imker HJ et al. 2015. The Pseudomonas aeruginosa antimetabolite l-2-amino-4-methoxy-trans-3-butenoic acid (AMB) is made from glutamate and two alanine residues via a thiotemplate-linked tripeptide precursor. Front. Microbiol. 6170
    [Google Scholar]
  85. 85. 
    Romling U, Galperin MY, Gomelsky M 2013. Cyclic di-GMP: the first 25 years of a universal bacterial second messenger. Microbiol. Mol. Biol. Rev. 7711–52
    [Google Scholar]
  86. 86. 
    Ryan RP, Fouhy Y, Garcia BF, Watt SA, Niehaus K et al. 2008. Interspecies signalling via the Stenotrophomonas maltophilia diffusible signal factor influences biofilm formation and polymyxin tolerance in Pseudomonas aeruginosa. Mol. Microbiol 68175–86
    [Google Scholar]
  87. 87. 
    Ryan RP, Fouhy Y, Lucey JF, Crossman LC, Spiro S et al. 2006. Cell-cell signaling in Xanthomonas campestris involves an HD-GYP domain protein that functions in cyclic di-GMP turnover. PNAS 103176712–17
    [Google Scholar]
  88. 88. 
    Ryan RP, McCarthy Y, Watt SA, Niehaus K, Dow JM 2009. Intraspecies signaling involving the diffusible signal factor BDSF (cis-2-dodecenoic acid) influences virulence in Burkholderia cenocepacia. J. Bacteriol 191155013–19
    [Google Scholar]
  89. 89. 
    Saliba AM, Nascimento DO, Silva MCA, Assis MC, Gayer CRM et al. 2005. Eicosanoid-mediated proinflammatory activity of Pseudomonas aeruginosa ExoU. Cell. Microbiol. 7121811–22
    [Google Scholar]
  90. 90. 
    Schuster M, Greenberg EP. 2006. A network of networks: quorum-sensing gene regulation in Pseudomonas aeruginosa. Int. J. Med. Microbiol 296273–81
    [Google Scholar]
  91. 91. 
    Shen D-K, Filopon D, Chaker H, Boullanger S, Derouazi M et al. 2008. High-cell-density regulation of the Pseudomonas aeruginosa type III secretion system: implications for tryptophan catabolites. Microbiology 15482195–208
    [Google Scholar]
  92. 92. 
    Sitkiewicz I, Stockbauer KE, Musser JM 2007. Secreted bacterial phospholipase A2 enzymes: better living through phospholipolysis. Trends Microbiol 15263–69
    [Google Scholar]
  93. 93. 
    Sousa AM, Pereira MO. 2014. Pseudomonas aeruginosa diversification during infection development in cystic fibrosis lungs—a review. Pathogens 33680–703
    [Google Scholar]
  94. 94. 
    Stacy A, McNally L, Darch SE, Brown SP, Whiteley M 2016. The biogeography of polymicrobial infection. Nat. Rev. Microbiol. 14293Spatial variations in the microbial environment influence bacterial virulence and survival during infection.
    [Google Scholar]
  95. 95. 
    Stewart PS. 2002. Mechanisms of antibiotic resistance in bacterial biofilms. Int. J. Med. Microbiol. 2922107–13
    [Google Scholar]
  96. 96. 
    Stintzi A, Evans K, Meyer J, Poole K 1998. Quorum-sensing and siderophore biosynthesis in Pseudomonas aeruginosa: lasRllasI mutants exhibit reduced pyoverdine biosynthesis. FEMS Microbiol. Lett. 1662341–45
    [Google Scholar]
  97. 97. 
    Ström K, Sjögren J, Broberg A, Schnürer J 2002. Lactobacillus plantarum MiLAB 393 produces the antifungal cyclic dipeptides cyclo(l-Phe-l-Pro) and cyclo(l-Phe-trans-4-OH-l-Pro) and 3-phenyllactic acid. Appl. Environ. Microbiol. 6894322–27
    [Google Scholar]
  98. 98. 
    Tao F, He Y-W, Wu D-H, Swarup S, Zhang L-H 2010. The cyclic nucleotide monophosphate domain of Xanthomonas campestris global regulator Clp defines a new class of cyclic di-GMP effectors. J. Bacteriol. 19241020–29
    [Google Scholar]
  99. 99. 
    Toyofuku M, Nakajima-Kambe T, Uchiyama H, Nomura N 2010. The effect of a cell-to-cell communication molecule, Pseudomonas quinolone signal (PQS), produced by P. aeruginosa on other bacterial species. Microbes Environ 2511–7
    [Google Scholar]
  100. 100. 
    Turner KH, Everett J, Trivedi U, Rumbaugh KP, Whiteley M 2014. Requirements for Pseudomonas aeruginosa acute burn and chronic surgical wound infection. PLOS Genet 107e1004518
    [Google Scholar]
  101. 101. 
    Twomey KB, O'Connell OJ, McCarthy Y, Dow JM, O'Toole GA et al. 2012. Bacterial cis-2-unsaturated fatty acids found in the cystic fibrosis airway modulate virulence and persistence of Pseudomonas aeruginosa. ISME J 65939–50
    [Google Scholar]
  102. 102. 
    Vázquez-Rivera D, González O, Guzmán-Rodríguez J, Díaz-Pérez AL, Ochoa-Zarzosa A et al. 2015. Cytotoxicity of cyclodipeptides from Pseudomonas aeruginosa PAO1 leads to apoptosis in human cancer cell lines. Biomed. Res. Int. 2015197608
    [Google Scholar]
  103. 103. 
    Ventre I, Goodman AL, Vallet-Gely I, Vasseur P, Soscia C et al. 2006. Multiple sensors control reciprocal expression of Pseudomonas aeruginosa regulatory RNA and virulence genes. PNAS 1031171–76
    [Google Scholar]
  104. 104. 
    Venturi V. 2006. Regulation of quorum sensing in Pseudomonas. FEMS Microbiol. Rev 302274–91
    [Google Scholar]
  105. 105. 
    Vílchez R, Lemme A, Ballhausen B, Thiel V, Schulz S et al. 2010. Streptococcus mutans inhibits Candida albicans hyphal formation by the fatty acid signaling molecule trans‐2‐decenoic acid (SDSF). ChemBioChem 11111552–62
    [Google Scholar]
  106. 106. 
    Wade DS, Calfee MW, Rocha ER, Ling EA, Engstrom E et al. 2005. Regulation of Pseudomonas quinolone signal synthesis in Pseudomonas aeruginosa. J. Bacteriol 187134372–80
    [Google Scholar]
  107. 107. 
    Wang C, Liu X, Wang J, Zhou J, Cui Z, Zhang LH 2016. Design and characterization of a polyamine derivative inhibiting the expression of type III secretion system in Pseudomonas aeruginosa. Sci. Rep 630949Demonstrates a rational design of polyamine derivative for dampening T3SS-mediated virulence by blocking spermidine transporters.
    [Google Scholar]
  108. 108. 
    Wang J, Dong Y, Zhou T, Liu X, Deng Y et al. 2013. Pseudomonas aeruginosa cytotoxicity is attenuated at high cell density and associated with the accumulation of phenylacetic acid. PLOS ONE 83e60187The bacterial metabolite PAA inhibits T3SS expression and mediates acute-chronic infection switch in P. aeruginosa.
    [Google Scholar]
  109. 109. 
    Wang J, Wang J, Zhang L 2018. Immunological blocking of spermidine‐mediated host-pathogen communication provides effective control against Pseudomonas aeruginosa infection. Microb. Biotechnol. In press
    [Google Scholar]
  110. 110. 
    Wang LH, He YW, Gao YF, Wu JE, Dong YH et al. 2004. A bacterial cell-cell communication signal with cross-kingdom structural analogs. Mol. Microbiol. 51903–12
    [Google Scholar]
  111. 111. 
    Whiteley M, Diggle SP, Greenberg EP 2017. Progress in and promise of bacterial quorum sensing research. Nature 5517680313–20
    [Google Scholar]
  112. 112. 
    Williams P, Cámara M. 2009. Quorum sensing and environmental adaptation in Pseudomonas aeruginosa: a tale of regulatory networks and multifunctional signal molecules. Curr. Opin. Microbiol. 122182–91
    [Google Scholar]
  113. 113. 
    Winson MK, Camara M, Latifi A, Foglino M, Chhabra SR et al. 1995. Multiple N-acyl-l-homoserine lactone signal molecules regulate production of virulence determinants and secondary metabolites in Pseudomonas aeruginosa. PNAS 92209427–31
    [Google Scholar]
  114. 114. 
    Winstanley C, O'Brien S, Brockhurst MA 2016. Pseudomonas aeruginosa evolutionary adaptation and diversification in cystic fibrosis chronic lung infections. Trends Microbiol 245327–37
    [Google Scholar]
  115. 115. 
    Winzer K, Williams P. 2001. Quorum sensing and the regulation of virulence gene expression in pathogenic bacteria. Int. J. Med. Microbiol. 2912131–43
    [Google Scholar]
  116. 116. 
    Wolfgang MC, Lee VT, Gilmore ME, Lory S 2003. Coordinate regulation of bacterial virulence genes by a novel adenylate cyclase-dependent signaling pathway. Dev. Cell. 42253–63
    [Google Scholar]
  117. 117. 
    Wu D, Lim SC, Dong Y, Wu J, Tao F et al. 2012. Structural basis of substrate binding specificity revealed by the crystal structures of polyamine receptors SpuD and SpuE from Pseudomonas aeruginosa. J. Mol. Biol 4165697–712
    [Google Scholar]
  118. 118. 
    Xiao G, He J, Rahme LG 2006. Mutation analysis of the Pseudomonas aeruginosa mvfR and pqsABCDE gene promoters demonstrates complex quorum-sensing circuitry. Microbiology 15261679–86
    [Google Scholar]
  119. 119. 
    Yahr TL, Wolfgang MC. 2006. Transcriptional regulation of the Pseudomonas aeruginosa type III secretion system. Mol. Microbiol. 623631–40
    [Google Scholar]
  120. 120. 
    Youard ZA, Wenner N, Reimmann C 2011. Iron acquisition with the natural siderophore enantiomers pyochelin and enantio-pyochelin in Pseudomonas species. Biometals 243513–22
    [Google Scholar]
  121. 121. 
    Zaborin A, Romanowski K, Gerdes S, Holbrook C, Lepine F et al. 2009. Red death in Caenorhabditis elegans caused by Pseudomonas aeruginosa PAO1. PNAS 106156327–32Phosphate stress exacerbates bacterial virulence by integrating QS with stress response mediated by phoB-pqs-pyoverdine pathway.
    [Google Scholar]
  122. 122. 
    Zhang LH. 2003. Quorum quenching and proactive host defense. Trends Plant Sci 8238–44
    [Google Scholar]
  123. 123. 
    Zhou L, Wang J, Zhang L-H 2007. Modulation of bacterial Type III secretion system by a spermidine transporter dependent signaling pathway. PLOS ONE 212e1291
    [Google Scholar]
  124. 124. 
    Zhou L, Zhang L-H, Cámara M, He Y-W 2017. The DSF family of quorum sensing signals: diversity, biosynthesis, and turnover. Trends Microbiol 254293–303The advancements in the field of DSF-based QS signaling and its impact on bacterial lifestyle.
    [Google Scholar]
  125. 125. 
    Zolfaghar I, Angus AA, Kang PJ, To A, Evans DJ, Fleiszig SMJ 2005. Mutation of retS, encoding a putative hybrid two-component regulatory protein in Pseudomonas aeruginosa, attenuates multiple virulence mechanisms. Microbes Infect 7131305–16
    [Google Scholar]
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