LasR variant cystic fibrosis isolates reveal an adaptable quorum-sensing hierarchy in Pseudomonas aeruginosa

mBio

Volumn 7, Issue 5, 2016, Pages

  Feltner, John B ^a   Wolter, Daniel J ^a,b,c   Pope, Christopher E ^a,b   Groleau, Marie Christine ^d   Smalley, Nicole E ^a   Greenberg, E Peter ^a   Mayer Hamblett, Nicole ^b,c   Burns, Jane ^b,c   Déziel, Eric ^d   Hoffman, Lucas R ^a,b,c   Dandekar, Ajai A ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^c SEATTLE CHILDREN S HOSPITAL   (United States)

^d INRS INSTITUT ARMAND FRAPPIER   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR LASR; TRANSCRIPTION FACTOR RHLR; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; LASR PROTEIN, PSEUDOMONAS AERUGINOSA; STOP CODON; TRANSACTIVATOR PROTEIN;

ARTICLE; BACTERIAL STRAIN; BACTERIUM ISOLATE; CHILD; CONTROLLED STUDY; CYSTIC FIBROSIS; GENE; GENE ACTIVATION; GENE CONTROL; GENE EXPRESSION; GENE IDENTIFICATION; GENETIC CODE; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; HUMAN; LASR GENE; LUNG INFECTION; MISSENSE MUTATION; NONHUMAN; NONSENSE MUTATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PSEUDOMONAS AERUGINOSA; QUORUM SENSING; SEQUENCE ANALYSIS; COMPLICATION; DNA SEQUENCE; GENE EXPRESSION REGULATION; GENETIC VARIATION; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; PSEUDOMONAS INFECTION; STOP CODON;

BACTERIAL PROTEINS; CODON, NONSENSE; CYSTIC FIBROSIS; GENE EXPRESSION REGULATION, BACTERIAL; GENETIC VARIATION; HUMANS; MUTATION, MISSENSE; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; QUORUM SENSING; SEQUENCE ANALYSIS, DNA; TRANS-ACTIVATORS;

EID: 84994474996     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.01513-16     Document Type: Article

References (61)

1. Burns JL, Gibson RL, McNamara S, Yim D, Emerson J, Rosenfeld M, Hiatt P, McCoy K, Castile R, Smith AL, Ramsey BW. 2001. Longitudinal assessment of Pseudomonas aeruginosa in young children with cystic fibrosis. J Infect Dis 183:444-452. http://dx.doi.org/10.1086/318075
2. Costerton JW, Stewart PS, Greenberg EP. 1999. Bacterial biofilms: a common cause of persistent infections. Science 284:1318-1322. http://dx.doi.org/10.1126/science.284.5418.1318
3. Smith EE, Buckley DG, Wu Z, Saenphimmachak C, Hoffman LR, D’Argenio DA, Miller SI, Ramsey BW, Speert DP, Moskowitz SM, Burns JL, Kaul R, Olson MV. 2006. Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients. Proc Natl Acad Sci USA 103:8487-8492. http://dx.doi.org/10.1073/pnas.0602138103
4. D’Argenio DA, Wu M, Hoffman LR, Kulasekara HD, Déziel E, Smith EE, Nguyen H, Ernst RK, Larson Freeman TJ, Spencer DH, Brittnacher M, Hayden HS, Selgrade S, Klausen M, Goodlett DR, Burns JL, Ramsey BW, Miller SI. 2007. Growth phenotypes of Pseudomonas aeruginosa lasR mutants adapted to the airways of cystic fibrosis patients. Mol Microbiol 64:512-533. http://dx.doi.org/10.1111/j.1365-2958.2007.05678.x
5. Fuqua WC, Winans SC, Greenberg EP. 1994. Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators. J Bacteriol 176:269-275
6. Schuster M, Lostroh CP, Ogi T, Greenberg EP. 2003. Identification, timing, and signal specificity of Pseudomonas aeruginosa quorumcontrolled genes: a transcriptome analysis. J Bacteriol 185:2066-2079. http://dx.doi.org/10.1128/JB.185.7.2066-2079.2003
7. Wagner VE, Bushnell D, Passador L, Brooks AI, Iglewski BH. 2003. Microarray analysis of Pseudomonas aeruginosa quorumsensing regulons: effects of growth phase and environment. J Bacteriol 185: 2080-2095. http://dx.doi.org/10.1128/JB.185.7.2080-2095.2003
8. Pearson JP, Passador L, Iglewski BH, Greenberg EP. 1995. A second N-acylhomoserine lactone signal produced by Pseudomonas aeruginosa. Proc Natl Acad Sc i U S A 92:1490-1494. http://dx.doi.org/10.1073/pnas.92.5.1490
9. Pesci EC, Pearson JP, Seed PC, Iglewski BH. 1997. Regulation of las and rhl quorum sensing in Pseudomonas aeruginosa. J Bacteriol 179: 3127-3132
10. Passador L, Cook JM, Gambello MJ, Rust L, Iglewski BH. 1993. Expression of Pseudomonas aeruginosa virulence genes requires cell-to-cell communication. Science 260:1127-1130. http://dx.doi.org/10.1126/science.8493556
11. Rumbaugh KP, Griswold JA, Iglewski BH, Hamood AN. 1999. Contribution of quorum sensing to the virulence of Pseudomonas aeruginosa in burn wound infections. Infect Immun 67:5854-5862
12. Tang HB, DiMango E, Bryan R, Gambello M, Iglewski BH, Goldberg JB, Prince A. 1996. Contribution of specific Pseudomonas aeruginosa virulence factors to pathogenesis of pneumonia in a neonatal mouse model of infection. Infect Immun 64:37-43
13. 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 177:7155-7163
14. Déziel E, Lépine F, Milot S, He J, Mindrinos MN, Tompkins RG, Rahme LG. 2004. 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 U S A 101:1339-1344. http://dx.doi.org/10.1073/pnas.0307694100
15. Pesci EC, Milbank JB, Pearson JP, McKnight S, Kende AS, Greenberg EP, Iglewski BH. 1999. Quinolone signaling in the cell-to-cell communi-cation system of Pseudomonas aeruginosa. Proc Natl Acad Sci USA 96: 11229-11234
16. Wade DS, Calfee MW, Rocha ER, Ling EA, Engstrom E, Coleman JP, Pesci EC. 2005. Regulation of Pseudomonas quinolone signal synthesis in Pseudomonas aeruginosa. J Bacteriol 187:4372-4380. http://dx.doi.org/10.1128/JB.187.13.4372-4380.2005
17. Xiao G, Déziel E, He J, Lépine F, Lesic B, Castonguay MH, Milot S, Tampakaki AP, Stachel SE, Rahme LG. 2006. MvfR, a key Pseudomonas aeruginosa pathogenicity LTTR-class regulatory protein, has dual ligands. Mol Microbiol 62:1689-1699. http://dx.doi.org/10.1111/j.1365-2958.2006.05462.x
18. Hoffman LR, Kulasekara HD, Emerson J, Houston LS, Burns JL, Ramsey BW, Miller SI. 2009. Pseudomonas aeruginosa lasR mutants are associated with cystic fibrosis lung disease progression. J Cyst Fibros 8:66-70. http://dx.doi.org/10.1016/j.jcf.2008.09.006
19. Wilder CN, Allada G, Schuster M. 2009. Instantaneous withinpatient diversity of Pseudomonas aeruginosa quorumsensing populations from cystic fibrosis lung infections. Infect Immun 77:5631-5639. http://dx.doi.org/10.1128/IAI.00755-09
20. Hoffman LR, Richardson AR, Houston LS, Kulasekara HD, Martens-Habbena W, Klausen M, Burns JL, Stahl DA, Hassett DJ, Fang FC, Miller SI. 2010. Nutrient availability as a mechanism for selection of antibiotic tolerant Pseudomonas aeruginosa within the CF airway. PLoS Pathog 6:e1000712. http://dx.doi.org/10.1371/journal.ppat.1000712
21. Mellbye B, Schuster M. 2011. The sociomicrobiology of antivirulence drug resistance: a proof of concept. mBio 2(5):e00131-11. http://dx.doi.org/10.1128/mBio.00131-11
22. Barth AL, Pitt TL. 1996. The high aminoacid content of sputum from cystic fibrosis patients promotes growth of auxotrophic Pseudomonas aeruginosa. J Med Microbiol 45:110-119. http://dx.doi.org/10.1099/00222615-45-2-110
23. Sandoz KM, Mitzimberg SM, Schuster M. 2007. Social cheating in Pseudomonas aeruginosa quorum sensing. Proc Natl Acad Sci U S A 104: 15876-15881. http://dx.doi.org/10.1073/pnas.0705653104
24. West SA, Griffin AS, Gardner A, Diggle SP. 2006. Social evolution theory for microorganisms. Nat Rev Microbiol 4:597-607. http://dx.doi.org/10.1038/nrmicro1461
25. Harrison F, Muruli A, Higgins S, Diggle SP. 2014. Development of an ex vivo porcine lung model for studying growth, virulence, and signaling of Pseudomonas aeruginosa. Infect Immun 82:3312-3323. http://dx.doi.org/10.1128/IAI.01554-14
26. Köhler T, Buckling A, van Delden C. 2009. Cooperation and virulence of clinical Pseudomonas aeruginosa populations. Proc Natl Acad Sc i U S A 106:6339-6344. http://dx.doi.org/10.1073/pnas.0811741106
27. Rosenfeld M, Emerson J, McNamara S, Joubran K, Retsch-Bogart G, Graff GR, Gutierrez HH, Kanga JF, Lahiri T, Noyes B, Ramsey B, Ren CL, Schechter M, Morgan W, Gibson RL, EPIC Study Group Partici-pating Clinical Sites. 2010. Baseline characteristics and factors associated with nutritional and pulmonary status at enrollment in the cystic fibrosis EPIC observational cohort. Pediatr Pulmonol 45:934-944. http://dx.doi.org/10.1002/ppul.21279
28. Bottomley MJ, Muraglia E, Bazzo R, Carfì A. 2007. Molecular insights into quorum sensing in the human pathogen Pseudomonas aeruginosa from the structure of the virulence regulator LasR bound to its autoinducer. J Biol Chem 282:13592-13600. http://dx.doi.org/10.1074/jbc.M700556200
29. Zhang RG, Pappas KM, Pappas T, Brace JL, Miller PC, Oulmassov T, Molyneaux JM, Anderson JC, Bashkin JK, Winans SC, Joachimiak A. 2002. Structure of a bacterial quorum-sensing transcription factor complexed with pheromone and DNA. Nature 417:971-974. http://dx.doi.org/10.1038/nature00833
30. Egland KA, Greenberg EP. 2001. Quorum sensing in Vibrio fischeri: analysis of the LuxR DNA binding region by alanine-scanning mutagenesis. J Bacteriol 183:382-386. http://dx.doi.org/10.1128/JB.183.1.382-386.2001
31. Trott AE, Stevens AM. 2001. Amino acid residues in LuxR critical for its mechanism of transcriptional activation during quorum sensing in Vibrio fischeri. J Bacteriol 183:387-392. http://dx.doi.org/10.1128/JB.183.1.387-392.2001
32. Pearson JP, Pesci EC, Iglewski BH. 1997. Roles of Pseudomonas aeruginosa las and rhl quorumsensing systems in control of elastase and rhamnolipid biosynthesis genes. J Bacteriol 179:5756-5767
33. Mayer-Hamblett N, Rosenfeld M, Gibson RL, Ramsey BW, Kulasekara HD, Retsch-Bogart GZ, Morgan W, Wolter DJ, Pope CE, Houston LS, Kulasekara BR, Khan U, Burns JL, Miller SI, Hoffman LR. 2014. Pseudomonas aeruginosa in vitro phenotypes distinguish cystic fibrosis infection stages and outcomes. Am J Respir Crit Care Med 190:289-297. http://dx.doi.org/10.1164/rccm.201404-0681OC
34. Mayer-Hamblett N, Ramsey BW, Kulasekara HD, Wolter DJ, Houston LS, Pope CE, Kulasekara BR, Armbruster CR, Burns JL, Retsch-Bogart G, Rosenfeld M, Gibson RL, Miller SI, Khan U, Hoffman LR. 2014. Pseudomonas aeruginosa phenotypes associated with eradication failure in children with cystic fibrosis. Clin Infect Dis 59:624-631. http://dx.doi.org/10.1093/cid/ciu385
35. Cabeen MT. 2014. Stationary phasespecific virulence factor overproduc-tion by a lasR mutant of Pseudomonas aeruginosa. PLoS One 9:e88743. http://dx.doi.org/10.1371/journal.pone.0088743
36. Dekimpe V, Déziel E. 2009. Revisiting the quorumsensing hierarchy in Pseudomonas aeruginosa: the transcriptional regulator RhlR regulates LasR-specific factors. Microbiology 155:712-723. http://dx.doi.org/10.1099/mic.0.022764-0
37. Déziel E, Gopalan S, Tampakaki AP, Lépine F, Padfield KE, Saucier M, Xiao G, Rahme LG. 2005. The contribution of MvfR to Pseudomonas aeruginosa pathogenesis and quorum sensing circuitry regulation: multiple quorum sensing-regulated genes are modulated without af-fecting lasRI, rhlRI or the production of N-acyl-L-homoserine lactones. Mol Microbiol 55:998-1014. http://dx.doi.org/10.1111/j.1365-2958.2004.04448.x
38. 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 rhldependent genes at the onset of stationary phase and can be produced in the absence of LasR. Mol Microbiol 50:29-43. http://dx.doi.org/10.1046/j.1365-2958.2003.03672.x
39. Müh U, Schuster M, Heim R, Singh A, Olson ER, Greenberg EP. 2006. Novel Pseudomonas aeruginosa quorum-sensing inhibitors identified in an ultra-high-throughput screen. Antimicrob Agents Chemother 50: 3674-3679. http://dx.doi.org/10.1128/AAC.00665-06
40. Farrow JM III, Sund ZM, Ellison ML, Wade DS, Coleman JP, Pesci EC. 2008. PqsE functions independently of PqsR-Pseudomonas quinolone signal and enhances the rhl quorum-sensing system. J Bacteriol 190: 7043-7051. http://dx.doi.org/10.1128/JB.00753-08
41. Rampioni G, Pustelny C, Fletcher MP, Wright VJ, Bruce M, Rumbaugh KP, Heeb S, Cámara M, Williams P. 2010. 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 12:1659-1673. http://dx.doi.org/10.1111/j.1462-2920.2010.02214.x
42. Dong YH, Xu JL, Li XZ, Zhang LH. 2000. AiiA, an enzyme that inacti-vates the acylhomoserine lactone quorum-sensing signal and attenuates the virulence of Erwinia carotovora. Proc Natl Acad Sci U S A 97: 3526-3531. http://dx.doi.org/10.1073/pnas.060023897
43. Van Delden C, Pesci EC, Pearson JP, Iglewski BH. 1998. Starvation selection restores elastase and rhamnolipid production in a Pseudomonas aeruginosa quorum-sensing mutant. Infect Immun 66:4499-4502
44. Bjarnsholt T, Jensen PØ, Jakobsen TH, Phipps R, Nielsen AK, Rybtke MT, Tolker-Nielsen T, Givskov M, Høiby N, Ciofu O, Scandinavian Cystic Fibrosis Study Consortium. 2010. Quorum sensing and virulence of Pseudomonas aeruginosa during lung infection of cystic fibrosis patients. PLoS One 5:e10115. http://dx.doi.org/10.1371/journal.pone.0010115
45. LaFayette SL, Houle D, Beaudoin T, Wojewodka G, Radzioch D, Hoffman LR, Burns JL, Dandekar AA, Smalley NE, Chandler JR, Zlosnik JE, Speert DP, Bernier J, Matouk E, Brochiero E, Rousseau S, Nguyen D. 2015. Cystic fibrosisadapted Pseudomonas aeruginosa quo-rum sensing lasR mutants cause hyperinflammatory responses. Sci Adv 1:e1500199. http://dx.doi.org/10.1126/sciadv.1500199
46. Schuster M, Greenberg EP. 2006. A network of networks: quorum-sensing gene regulation in Pseudomonas aeruginosa. Int J Med Microbiol 296:73-81. http://dx.doi.org/10.1016/j.ijmm.2006.01.036
47. Asfahl KL, Walsh J, Gilbert K, Schuster M. 2015. Non-social adaptation defers a tragedy of the commons in Pseudomonas aeruginosa quorum sensing. ISME J 9:1734-1746. http://dx.doi.org/10.1038/ismej.2014.259
48. Hazan R, He J, Xiao G, Dekimpe V, Apidianakis Y, Lesic B, Astrakas C, Déziel E, Lépine F, Rahme LG. 2010. Homeostatic interplay between bacterial cell-cell signaling and iron in virulence. PLoS Pathog 6:e1000810. http://dx.doi.org/10.1371/journal.ppat.1000810
49. Drees SL, Fetzner S. 2015. PqsE of Pseudomonas aeruginosa acts as pathway-specific thioesterase in the biosynthesis of alkylquinolone signaling molecules. Chem Biol 22:611-618. http://dx.doi.org/10.1016/j.chembiol.2015.04.012
50. Rumbaugh KP, Griswold JA, Hamood AN. 1999. Pseudomonas aerugi-nosa strains obtained from patients with tracheal, urinary tract and wound infection: variations in virulence factors and virulence genes. J Hosp Infect 43:211-218. http://dx.doi.org/10.1053/jhin.1999.0252
51. Dandekar AA, Chugani S, Greenberg EP. 2012. Bacterial quorum sensing and metabolic incentives to cooperate. Science 338:264-266. http://dx.doi.org/10.1126/science.1227289
52. Sambrook J, Fritsch EF, Maniatis T. 1989. Molecular cloning: a labora-tory manual. Cold Spring Harbor Laboratory Press, Plainview, NY
53. Shaw PD, Ping G, Daly SL, Cha C, Cronan JE, Jr., Rinehart KL, Farrand SK. 1997. Detecting and characterizing N-acyl-homoserine lactone signal molecules by thin-layer chromatography. Proc Natl Acad Sci U S A 94: 6036-6041. http://dx.doi.org/10.1073/pnas.94.12.6036
54. 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 Sc i U S A 98: 2752-2757. http://dx.doi.org/10.1073/pnas.051624298
55. Lee JH, Lequette Y, Greenberg EP. 2006. Activity of purified QscR, a Pseudomonas aeruginosa orphan quorum-sensing transcription factor. Mol Microbiol 59:602-609. http://dx.doi.org/10.1111/j.1365-2958.2005.04960.x
56. Lépine F, Déziel E. 2011. Liquid chromatography/mass spectrometry for the detection and quantification of N-acyl-L-homoserine lactones and 4-hydroxy-2-alkylquinolines. Methods Mol Biol 692:61-69. http://dx.doi.org/10.1007/978-1-60761-971-0_5
57. Lépine F, Déziel E, Milot S, Rahme LG. 2003. A stable isotope dilution assay for the quantification of the Pseudomonas quinolone signal in Pseu-domonas aeruginosa cultures. Biochim Biophys Acta 1622:36-41. http://dx.doi.org/10.1016/S0304-4165(03)00103-X
58. Miller WG, Leveau JH, Lindow SE. 2000. Improved gfp and inaZ broad-host-range promoter-probe vectors. Mol Plant Microbe Interact 13: 1243-1250. http://dx.doi.org/10.1094/MPMI.2000.13.11.1243
59. Choi KH, Kumar A, Schweizer HP. 2006. A 10-min method for preparation of highly electrocompetent Pseudomonas aeruginosa cells: application for DNA fragment transfer between chromosomes and plasmid transformation. J Microbiol Methods 64:391-397. http://dx.doi.org/10.1016/j.mimet.2005.06.001
60. Kurachi M. 1958. Studies on the biosynthesis of pyocyanine. Isolation and determination of pyocyanine. Bull Inst Chem Res Kyoto Univ 36:163-173
61. King EO, Ward MK, Raney DE. 1954. Two simple media for the demonstration of pyocyanin and fluorescin. J Lab Clin Med 44: 301-307