Unravelling the Genome-Wide Contributions of Specific 2-Alkyl-4-Quinolones and PqsE to Quorum Sensing in Pseudomonas aeruginosa

PLoS Pathogens

Volumn 12, Issue 11, 2016, Pages

  Rampioni, Giordano ^a,b   Falcone, Marilena ^a,c   Heeb, Stephan ^b   Frangipani, Emanuela ^a,b   Fletcher, Matthew P ^b   Dubern, Jean Frédéric ^b   Visca, Paolo ^a   Leoni, Livia ^a   Cámara, Miguel ^b   Williams, Paul ^b  

^a ROMA TRE UNIVERSITY   (Italy)

^b UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^c UNIVERSITY OF MILAN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

4 QUINOLONE DERIVATIVE; TRANSCRIPTOME;

BIOFILM; DNA MICROARRAY; GENE EXPRESSION REGULATION; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHYSIOLOGY; POLYMERASE CHAIN REACTION; PSEUDOMONAS AERUGINOSA; QUORUM SENSING; SIGNAL TRANSDUCTION; VIRULENCE;

4-QUINOLONES; BIOFILMS; GENE EXPRESSION REGULATION, BACTERIAL; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; POLYMERASE CHAIN REACTION; PSEUDOMONAS AERUGINOSA; QUORUM SENSING; SIGNAL TRANSDUCTION; TRANSCRIPTOME; VIRULENCE;

EID: 84995960832     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1006029     Document Type: Article

References (54)

1. El Zowalaty ME, Al Thani AA, Webster TJ, El Zowalaty AE, Schweizer HP, Nasrallah GK, et al. Pseudomonas aeruginosa: arsenal of resistance mechanisms, decades of changing resistance profiles, and future antimicrobial therapies. Future Microbiol. 2015;10:1683–706. doi: 10.2217/fmb.15.4826439366
2. Gellatly SL, Hancock RE, Pseudomonas aeruginosa: new insights into pathogenesis and host defences. Pathog Dis. 2013;67:159–73. doi: 10.1111/2049-632X.1203323620179
3. Dubern JF, Cigana C, De Simone M, Lazenby J, Juhas M, Schwager S, et al. Integrated whole-genome screening for Pseudomonas aeruginosa virulence genes using multiple disease models reveals that pathogenicity is host specific. Environ Microbiol. 2015;17:4379–93. doi: 10.1111/1462-2920.1286325845292
4. Kirisits MJ, Parsek MR, Does Pseudomonas aeruginosa use intercellular signalling to build biofilm communities?Cell Microbiol. 2006;8:1841–9. doi: 10.1111/j.1462-5822.2006.00817.x17026480
5. Williams P, Cámara M, Quorum sensing and environmental adaptation in Pseudomonas aeruginosa: a tale of regulatory networks and multifunctional signal molecules. Curr Opin Microbiol. 2009;12:182–91. doi: 10.1016/j.mib.2009.01.00519249239
6. Hazan R, He J, Xiao G, Dekimpe V, Apidianakis Y, Lesic B, et al. Homeostatic interplay between bacterial cell-cell signaling and iron in virulence. PLoS Pathog. 2010;6(3):e1000810. doi: 10.1371/journal.ppat.100081020300606
7. Lee J, Zhang L, The hierarchy quorum sensing network in Pseudomonas aeruginosa. Protein Cell. 2015;6:26–41. doi: 10.1007/s13238-014-0100-x25249263
8. Rampioni G, Leoni L, Williams P, The art of antibacterial warfare: deception through interference with quorum sensing-mediated communication. Bioorg Chem. 2014;55:60–8. doi: 10.1016/j.bioorg.2014.04.00524823895
9. Heeb S, Fletcher MP, Chhabra SR, Diggle SP, Williams P, Cámara M, Quinolones: from antibiotics to autoinducers. FEMS Microbiol Rev. 2010;35:247–74.
10. Déziel E, Gopalan S, Tampakaki AP, Lépine F, Padfield KE, Saucier M, et al. The contribution of MvfR to Pseudomonas aeruginosa pathogenesis and quorum sensing circuitry regulation: multiple quorum sensing-regulated genes are modulated without affecting lasRI, rhlRI or the production of N-acyl-L-homoserine lactones. Mol Microbiol. 2005;55:998–1014. doi: 10.1111/j.1365-2958.2004.04448.x15686549
11. Rampioni G, Pustelny C, Fletcher MP, Wright VJ, Bruce M, Rumbaugh KP, et al. Transcriptomic analysis reveals a global alkyl-quinolone-independent regulatory role for PqsE in facilitating the environmental adaptation of Pseudomonas aeruginosa to plant and animal hosts. Environ Microbiol. 2010;12:1659–73. doi: 10.1111/j.1462-2920.2010.02214.x20406282
12. Barr HL, Halliday N, Cámara M, Barrett DA, Williams P, Forrester DL, et al. Pseudomonas aeruginosa quorum sensing molecules correlate with clinical status in cystic fibrosis. Eur Respir J. 2015;46:1046–54. doi: 10.1183/09031936.0022521426022946
13. Winsor GL, Lam DK, Fleming L, Lo R, Whiteside MD, Yu NY, et al. Pseudomonas Genome Database: improved comparative analysis and population genomics capability for Pseudomonas genomes. Nucleic Acids Res. 2011;39:596–600.
14. Déziel E, Lépine F, Milot S, He J, Mindrinos MN, Tompkins RG, et al. Analysis of Pseudomonas aeruginosa 4-hydroxy-2-alkylquinolines (HAQs) reveals a role for 4-hydroxy-2-heptylquinoline in cell-to-cell communication. Proc Natl Acad Sci USA. 2004;101:1339–44. doi: 10.1073/pnas.030769410014739337
15. Coleman JP, Hudson LL, McKnight SL, Farrow JM, 3rdCalfee MW, Lindsey CA, et al. Pseudomonas aeruginosa PqsA is an anthranilate-coenzyme A ligase. J Bacteriol. 2008;190:1247–55. doi: 10.1128/JB.01140-0718083812
16. Zhang YM, Frank MW, Zhu K, Mayasundari A, Rock CO, PqsD is responsible for the synthesis of 2,4-dihydroxyquinoline, an extracellular metabolite produced by Pseudomonas aeruginosa. J Biol Chem. 2008;283:28788–94. doi: 10.1074/jbc.M80455520018728009
17. Drees SL, Fetzner S, PqsE of Pseudomonas aeruginosa acts as pathway-specific thioesterase in the biosynthesis of alkylquinolone signaling molecules. Chem Biol. 2015;22:611–8. doi: 10.1016/j.chembiol.2015.04.01225960261
18. Dulcey CE, Dekimpe V, Fauvelle DA, Milot S, Groleau MC, Doucet N, et al. The end of an old hypothesis: the Pseudomonas signalling molecules 4-hydroxy-2-alkylquinolines derive from fatty acids, not 3-ketofatty acids. Chem Biol. 2013;20:1481–91. doi: 10.1016/j.chembiol.2013.09.02124239007
19. Drees SL, Li C, Prasetya F, Saleem M, Dreveny I, Williams P, et al. PqsBC, a condensing enzyme in the biosynthesis of the Pseudomonas aeruginosa Quinolone Signal: crystal structure, inhibition, and reaction mechanism. J Biol Chem. 2016;291:6610–24. doi: 10.1074/jbc.M115.70845326811339
20. Schertzer JW, Brown SA, Whiteley M, Oxygen levels rapidly modulate Pseudomonas aeruginosa social behaviors via substrate limitation of PqsH. Mol Microbiol. 2010;77:1527–38. doi: 10.1111/j.1365-2958.2010.07303.x20662781
21. Lépine F, Milot S, Déziel E, He J, Rahme LG, Electrospray/mass spectrometric identification and analysis of 4-hydroxy-2-alkylquinolines (HAQs) produced by Pseudomonas aeruginosa. J Am Soc Mass Spectrom. 2004;15:862–9. doi: 10.1016/j.jasms.2004.02.01215144975
22. Wade DS, Calfee MW, Rocha ER, Ling EA, Engstrom E, Coleman JP, et al. Regulation of Pseudomonas quinolone signal synthesis in Pseudomonas aeruginosa. J Bacteriol. 2005;187:4372–80. doi: 10.1128/JB.187.13.4372-4380.200515968046
23. Xiao G, Déziel E, He J, Lépine F, Lesic B, Castonguay MH, et al. MvfR, a key Pseudomonas aeruginosa pathogenicity LTTR-class regulatory protein, has dual ligands. Mol Microbiol. 2006;262:1689–99.
24. Ilangovan A, Fletcher M, Rampioni G, Pustelny C, Rumbaugh K, Heeb S, et al. Structural basis for native agonist and synthetic inhibitor recognition by the Pseudomonas aeruginosa quorum sensing regulator PqsR (MvfR). PLoS Pathog. 2013;9(7):e1003508. doi: 10.1371/journal.ppat.100350823935486
25. Mashburn-Warren L, Howe J, Garidel P, Richter W, Steiniger F, Roessle M, et al. Interaction of quorum signals with outer membrane lipids: insights into prokaryotic membrane vesicle formation. Mol Microbiol. 2008;69:491–502. doi: 10.1111/j.1365-2958.2008.06302.x18630345
26. Macdonald IA, Kuehn MJ, Stress-induced outer membrane vesicle production by Pseudomonas aeruginosa. J Bacteriol. 2013;195:2971–81. doi: 10.1128/JB.02267-1223625841
27. Diggle SP, Matthijs S, Wright VJ, Fletcher MP, Chhabra SR, Lamont IL, et al. The Pseudomonas aeruginosa 4-quinolone signal molecules HHQ and PQS play multifunctional roles in quorum sensing and iron entrapment. Chem Biol. 2007;14:87–96. doi: 10.1016/j.chembiol.2006.11.01417254955
28. Bredenbruch F, Geffers R, Nimtz M, Buer J, Häussler S, The Pseudomonas aeruginosa quinolone signal (PQS) has an iron-chelating activity. Environ Microbiol. 2006;8:1318–29. doi: 10.1111/j.1462-2920.2006.01025.x16872396
29. Nguyen AT, Jones JW, Ruge MA, Kane MA, Oglesby-Sherrouse AG, Iron depletion enhances production of antimicrobials by Pseudomonas aeruginosa. J Bacteriol. 2015;197:2265–75. doi: 10.1128/JB.00072-1525917911
30. Voggu L, Schlag S, Biswas R, Rosenstein R, Rausch C, Götz F, Microevolution of cytochrome bd oxidase in Staphylococci and its implication in resistance to respiratory toxins released by Pseudomonas. J Bacteriol. 2006;188:8079–86. doi: 10.1128/JB.00858-0617108291
31. Gallagher LA, McKnight SL, Kuznetsova MS, Pesci EC, Manoil C, Functions required for extracellular quinolone signaling by Pseudomonas aeruginosa. J Bacteriol. 2002;184:6472–80. doi: 10.1128/JB.184.23.6472-6480.200212426334
32. Farrow JM, 3rdSund ZM, Ellison ML, Wade DS, Coleman JP, Pesci EC, PqsE functions independently of PqsR-Pseudomonas quinolone signal and enhances the rhl quorum-sensing system. J Bacteriol. 2008;190:7043–51. doi: 10.1128/JB.00753-0818776012
33. Folch B, Déziel E, Doucet N, Systematic mutational analysis of the putative hydrolase PqsE: toward a deeper molecular understanding of virulence acquisition in Pseudomonas aeruginosa. PLoS One. 2013;8(9):e73727. doi: 10.1371/journal.pone.007372724040042
34. Storey JD, Tibshirani R, Statistical significance for genome-wide studies. Proc Natl Acad Sci USA. 2003;100:9440–5. doi: 10.1073/pnas.153050910012883005
35. Aendekerk S, Diggle SP, Song Z, Høiby N, Cornelis P, Williams P, et al. The MexGHI-OpmD multidrug efflux pump controls growth, antibiotic susceptibility and virulence in Pseudomonas aeruginosa via 4-quinolone-dependent cell-to-cell communication. Microbiology. 2005;151:1113–25. doi: 10.1099/mic.0.27631-015817779
36. Dietrich LE, Price-Whelan A, Petersen A, Whiteley M, Newman DK, The phenazine pyocyanin is a terminal signalling factor in the quorum sensing network of Pseudomonas aeruginosa. Mol Microbiol. 2006;61:1308–21. doi: 10.1111/j.1365-2958.2006.05306.x16879411
37. Yu S, Jensen V, Seeliger J, Feldmann I, Weber S, Schleicher E, et al. Structure elucidation and preliminary assessment of hydrolase activity of PqsE, the Pseudomonas quinolone signal (PQS) response protein. Biochemistry. 2009;48:10298–307. doi: 10.1021/bi900123j19788310
38. Knoten CA, Wells G, Coleman JP, Pesci EC, A conserved suppressor mutation in a tryptophan auxotroph results in dysregulation of Pseudomonas quinolone signal synthesis. J Bacteriol. 2014;196:2413–22. doi: 10.1128/JB.01635-1424748618
39. Recinos DA, Sekedat MD, Hernandez A, Cohen TS, Sakhtah H, Prince AS, Price-Whelan A, Dietrich LE, Redundant phenazine operons in Pseudomonas aeruginosa exhibit environment-dependent expression and differential roles in pathogenicity. Proc Natl Acad Sci USA. 2012; 109:19420–5. doi: 10.1073/pnas.121390110923129634
40. Ochsner UA, Wilderman PJ, Vasil AI, Vasil ML, GeneChip expression analysis of the iron starvation response in Pseudomonas aeruginosa: identification of novel pyoverdine biosynthesis genes. Mol Microbiol. 2002;45:1277–87. 12207696
41. Palma M, Worgall S, Quadri LE, Transcriptome analysis of the Pseudomonas aeruginosa response to iron. Arch Microbiol. 2003;180:374–9. doi: 10.1007/s00203-003-0602-z14513207
42. Singh G, Wu B, Baek MS, Camargo A, Nguyen A, Slusher NA, et al. Secretion of Pseudomonas aeruginosa type III cytotoxins is dependent on Pseudomonas quinolone signal concentration. Microb Pathog. 2010;49:196–203. doi: 10.1016/j.micpath.2010.05.01320570614
43. Hogardt M, Roeder M, Schreff AM, Eberl L, Heesemann J, Expression of Pseudomonas aeruginosa exoS is controlled by quorum sensing and RpoS. Microbiology. 2004;150:843–51. doi: 10.1099/mic.0.26703-015073294
44. Toyofuku M, Nomura N, Kuno E, Tashiro Y, Nakajima T, Uchiyama H, Influence of the Pseudomonas quinolone signal on denitrification in Pseudomonas aeruginosa. J Bacteriol. 2008;190:7947–56. doi: 10.1128/JB.00968-0818931133
45. Häussler S, Becker T, The Pseudomonas quinolone signal (PQS) balances life and death in Pseudomonas aeruginosa populations. PLoS Pathog. 2008;4(9):e1000166. doi: 10.1371/journal.ppat.100016618818733
46. Visca P, Ramos JL, Iron regulation and siderophore signaling in Pseudomonas aeruginosa virulence. In: Pseudomonas, vol. 2. New York: Kluwer Academic/Plenum Publishers; 2004. p. 69–124.
47. Bergh A, Offenhartz P, George P, Haight GP, Complexes of 2,2′, 2″, 2-quaterpyridine with ferrous and ferric ions. J Chem Soc. 1964;1:1533–8.
48. Boelaert JR, Van Cutsem J, de Locht M, Schneider YJ, Crichton RR, Deferoxamine augments growth and pathogenicity of Rhizopus, while hydroxypyridinone chelators have no effect. Kidney Int. 1994;45:667–71. 8196268
49. Liu Y, Yang L, Molin S, Synergistic activities of an efflux pump inhibitor and iron chelators against Pseudomonas aeruginosa growth and biofilm formation. Antimicrob Agents Chemother. 2010;54:3960–3. doi: 10.1128/AAC.00463-1020566773
50. Thompson MG, Corey BW, Si Y, Craft DW, Zurawski DV, Antibacterial activities of iron chelators against common nosocomial pathogens. Antimicrob Agents Chemother. 2012;56:5419–21. doi: 10.1128/AAC.01197-1222850524
51. Stojiljkovic I, Bäumler AJ, Hantke K, Fur regulon in Gram-negative bacteria. Identification and characterization of new iron-regulated Escherichia coli genes by a fur titration assay. J Mol Biol. 1994;236:531–45. doi: 10.1006/jmbi.1994.11638107138
52. Chugani S, Greenberg EP, LuxR homolog-independent gene regulation by acyl-homoserine lactones in Pseudomonas aeruginosa. Proc Natl Acad Sci USA. 2010;107:10673–8. doi: 10.1073/pnas.100590910720498077
53. Imperi F, Massai F, Facchini M, Frangipani E, Visaggio D, Leoni L, et al. Repurposing the antimycotic drug flucytosine for suppression of Pseudomonas aeruginosa pathogenicity. Proc Natl Acad Sci USA. 2013;110:7458–63. doi: 10.1073/pnas.122270611023569238
54. Ortori CA, Dubern JF, Chhabra SR, Cámara M, Hardie K, Williams P, et al. Simultaneous quantitative profiling of N-acyl-L-homoserine lactone and 2-alkyl-4(1H)-quinolone families of quorum-sensing signaling molecules using LC-MS/MS. Anal Bioanal Chem. 2011;399:839–50. doi: 10.1007/s00216-010-4341-021046079