Integrated whole-genome screening for Pseudomonas aeruginosa virulence genes using multiple disease models reveals that pathogenicity is host specific

Environmental Microbiology

Volumn 17, Issue 11, 2015, Pages 4379-4393

  Dubern, Jean Frédéric ^a   Cigana, Cristina ^b   De Simone, Maura ^b   Lazenby, James ^a   Juhas, Mario ^c   Schwager, Stephan ^c   Bianconi, Irene ^b   Döring, Gerd ^d   Eberl, Leo ^c   Williams, Paul ^a   Bragonzi, Alessandra ^b   Cámara, Miguel ^a  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^b SAN RAFFAELE HOSPITAL   (Italy)

^c UNIVERSITY OF ZURICH   (Switzerland)

^d UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIINFECTIVE AGENT; VIRULENCE FACTOR;

ANIMAL; C57BL MOUSE; CAENORHABDITIS ELEGANS; CELL LINE; DISEASE MODEL; DROSOPHILA MELANOGASTER; GENE LIBRARY; GENETICS; GENOMICS; HOST RANGE; HUMAN; MALE; METABOLISM; MICROBIOLOGY; MOUSE; PATHOGENICITY; PATHOLOGY; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTION; VIRULENCE;

ANIMALS; ANTI-BACTERIAL AGENTS; CAENORHABDITIS ELEGANS; CELL LINE; DISEASE MODELS, ANIMAL; DROSOPHILA MELANOGASTER; GENE LIBRARY; GENOMICS; HOST SPECIFICITY; HUMANS; MALE; MICE; MICE, INBRED C57BL; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; VIRULENCE; VIRULENCE FACTORS;

EID: 84949314449     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/1462-2920.12863     Document Type: Article

References (41)

1. Alibaud, L., Köhler, T., Coudray, A., Prigent-Combaret, C., Bergeret, E., Perrin, J., etal. (2008) Pseudomonas aeruginosa virulence genes identified in a Dictyostelium host model. Cell Microbiol 10: 729-740.
2. Apidianakis, Y., and Rahme, L.G. (2009) Drosophila melanogaster as a model host for studying Pseudomonas aeruginosa infection. Nat Protoc 4: 1285-1294.
3. Bianconi, I., Milani, A., Paroni, M., Cigana, C., Levesque, R.C., Bertoni, G., and Bragonzi, A. (2011) Positive signature-tagged mutagenesis in Pseudomonas aeruginosa: tracking patho-adaptive mutations promoting long-term airways chronic infection. PLoS Pathog 7: e1001270.
4. Boucher, H.W., Talbot, G.H., Bradley, J.S., Edwards, J.E., Gilbert, D., Rice, L.B., etal. (2009) Bad bugs, no drugs: no ESKAPE! An update from the Infectious Diseases Society of America. Clin Infect Dis 48: 1-12.
5. Chapman, S.J., and Hill, A.V. (2012) Human genetic susceptibility to infectious disease. Nat Rev Genet 13: 175-188.
6. Chen, L., Yang, J., Yu, J., Yao, Z., Sun, L., Shen, Y., and Jin, Q. (2005) VFDB: a reference database for bacterial virulence factors. Nucleic Acids Res 33: D325-D328.
7. Chieda, Y., Iiyama, K., Yasunaga-Aoki, C., Lee, J.M., Kusakabe, T., and Shimizu, S. (2005) Pathogenicity of gacA mutant of Pseudomonas aeruginosa PA01 in the silkworm, Bombyx mori. FEMS Microbiol Lett 244: 181-186.
8. Cosson, P., Zulianello, L., Join-Lambert, O., Faurisson, F., Gebbie, L., Benghezal, M., etal. (2002) Pseudomonas aeruginosa virulence analyzed in a Dictyostelium discoideum host system. J Bacteriol 184: 3027-3033.
9. Engelmann, I., and Pujol, N. (2010) Innate immunity in C.elegans. Adv Exp Med Biol 708: 105-121.
10. Essar, D., Eberly, L., Hadero, A., and Crawford, I.P. (1990) Identification and characterization of genes for a second anthranilate synthase in Pseudomonas aeruginosa: interchangeability of the two anthranilate synthases and evolutionary implications. J Bacteriol 172: 884-900.
11. Feinbaum, R., Urbach, J.M., Liberati, N.T., Djonovic, S., Adonizio, A., Carvunis, A.R., and Ausubel, F.M. (2012) Genome-wide identification of Pseudomonas aeruginosa virulence-related genes using a Caenorhabditis elegans infection model. PLoS Pathog 8: e1002813.
12. Fernebro, J. (2011) Fighting bacterial infections-future treatment options. Drug Resist Updat 14: 125-139.
13. Ferrandon, D., Imler, J.L., Hetru, C., and Hoffmann, J.A. (2007) The Drosophila systemic immune response: sensing and signalling during bacterial and fungal infections. Nat Rev Immunol 11: 862-874.
14. Finlay, B. (1999) Bacterial disease in diverse hosts. Cell 96: 315-318.
15. Gellatly, S., and Hancock, R.E. (2013) Pseudomonas aeruginosa: new insights into pathogenesis and host defenses. Pathog Dis 67: 159-173.
16. Heurlier, K., Denervaud, V., Pessi, G., Reimmann, C., and Haas, D. (2003) Negative control of quorum sensing by RpoN (sigma54) in Pseudomonas aeruginosa PAO1. J Bacteriol 185: 2227-2235.
17. Hilker, R., Munder, A., Klockgether, J., Losada, P.M., Chouvarine, P., Cramer, N., etal. (2015) Interclonal gradient of virulence in the Pseudomonas aeruginosa pangenome from disease and environment. Environ Microbiol 17: 29-46.
18. Jander, G., Rahme, L.G., and Ausubel, F.M. (2000) Positive correlation between virulence of Pseudomonas aeruginosa mutants in mice and insects. J Bacteriol 182: 3843-3845.
19. Kim, S., Park, S.Y., Heo, Y.J., and Cho, Y.H. (2008) Drosophila melanogaster-based screening for multihost virulence factors of Pseudomonas aeruginosa PA14 and identification of a virulence-attenuating factor, HudA. Infect Immun 76: 4152-4162.
20. Kung, V., Ozer, E.A., and Hauser, A.R. (2010) The accessory genome of Pseudomonas aeruginosa. Microbiol Mol Biol Rev 74: 621-641.
21. Larsen, R.A., Wilson, M.M., Guss, A.M., and Metcalf, W.W. (2002) Genetic analysis of pigment biosynthesis in Xanthobacter autotrophicus Py2 using a new, highly efficient transposon mutagenesis system that is functional in a wide variety of bacteria. Arch Microbiol 178: 193-201.
22. Lee, D., Urbach, J.M., Wu, G., Liberati, N.T., Feinbaum, R.L., Miyata, S., etal. (2006) Genomic analysis reveals that Pseudomonas aeruginosa virulence is combinatorial. Genome Biol 7: R90.
23. Liberati, N., Urbach, J.M., Miyata, S., Lee, D.G., Drenkard, E., Wu, G., etal. (2006) An ordered, nonredundant library of Pseudomonas aeruginosa strain PA14 transposon insertion mutants. Proc Natl Acad Sci USA 103: 2833-2838.
24. Lorè, N., Cigana, C., De Fino, I., Riva, C., Juhas, M., Schwager, S., etal. (2012) Cystic fibrosis-niche adaptation of Pseudomonas aeruginosa reduces virulence in multiple infection hosts. PLoS One 7: e35648.
25. de Lorenzo, V. (2015) Pseudomonas aeruginosa: the making of a pathogen. Environ Microbiol 17: 1-3.
26. Lyczak, J.B., Cannon, C.L., and Pier, G.B. (2000) Establishment of Pseudomonas aeruginosa infection: lessons from a versatile opportunist. Microbes Infect 2: 1051-1060.
27. Mayer-Hamblett, N., Rosenfeld, M., Gibson, R.L., Ramsey, B.W., Kulasekara, H.D., Retsch-Bogart, G.Z., etal. (2014) Pseudomonas aeruginosa in vitro phenotypes distinguish cystic fibrosis infection stages and outcomes. Am J Respir Crit Care Med 190: 289-297.
28. Page, M.G.P., and Heim, J. (2009) Prospects for the next anti-Pseudomonas drug. Curr Opin Pharmacol 9: 558-565.
29. Phennicie, R., Sullivan, M.J., Singer, J.T., Yoder, J.A., and Kim, C.H. (2010) Specific resistance to Pseudomonas aeruginosa infection in zebrafish is mediated by the cystic fibrosis transmembrane conductance regulator. Infect Immun 78: 4542-4550.
30. Pirone, L., Bragonzi, A., Farcomeni, A., Paroni, M., Auriche, C., Conese, M., etal. (2008) Burkholderia cenocepacia strains isolated from cystic fibrosis patients are apparently more invasive and more virulent than rhizosphere strains. Environ Microbiol 10: 2773-2784.
31. Poole, K. (2011) Pseudomonas aeruginosa: resistance to the max. Front Microbiol 2: 65.
32. Potvin, E., Lehoux, D.E., Kukavica-Ibrulj, I., Richard, K.L., Sanschagrin, F., Lau, G.W., and Levesque, R.C. (2003) In vivo functional genomics of Pseudomonas aeruginosa for high-throughput screening of new virulence factors and antibacterial targets. Environ Microbiol 5: 1294-1308.
33. Rahme, L., Stevens, E.J., Wolfort, S.F., Shao, J., Tompkins, R.G., and Ausubel, F.M. (1995) Common virulence factors for bacterial pathogenicity in plants and animals. Science 268: 1899-1902.
34. Rampioni, G., Pustelny, C., Fletcher, M.P., Wright, V.J., Bruce, M., Rumbaugh, K.P., etal. (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.
35. Sambrook, J., and Russel, D.W. (2001) Molecular Cloning: A Laboratory Manual, Vol. 1, 2, 3. New York, USA: Cold Spring Harbor Laboratory Press.
36. Stover, C.K., Pham, X.Q., Erwin, A.L., Mizoguchi, S.D., Warrener, P., Hickey, M.J., etal. (2000) Complete genome sequence of Pseudomonas aeruginosa PA01, an opportunistic pathogen. Nature 406: 959-964.
37. Tan, M., Mahajan-Miklos, S., and Ausubel, F.M. (1999) Killing of Caenorhabditis elegans by Pseudomonas aeruginosa used to model mammalian bacterial pathogenesis. Proc Natl Acad Sci USA 96: 715-720.
38. Thomas, S., Ray, A., Hodson, M., and Pitt, T. (2000) Increased sputum amino acid concentrations and auxotrophy of Pseudomonas aeruginosa in severe cystic fibrosis lung disease. Thorax 55: 795-797.
39. Tielen, P., Narten, M., Rosin, N., Biegler, I., Haddad, I., Hogardt, M., etal. (2011) Genotypic and phenotypic characterization of Pseudomonas aeruginosa isolates from urinary tract infections. Int J Med Microbiol 301: 282-292.
40. Vale, P., Fenton, A., and Brown, S.P. (2014) Limiting damage during infection: lessons from infection tolerance for novel therapeutics. PLoS Biol 12: e1001769.
41. Winstanley, C., Langille, M.G., Fothergill, J.L., Kukavica-Ibrulj, I., Paradis-Bleau, C., Sanschagrin, F., etal. (2009) Newly introduced genomic prophage islands are critical determinants of in vivo competitiveness in the Liverpool Epidemic Strain of Pseudomonas aeruginosa. Genome Res 19: 12-23.