Caenorhabditis elegans semi-automated liquid screen reveals a specialized role for the chemotaxis gene cheB2 in Pseudomonas aeruginosa virulence

PLoS Pathogens

Volumn 5, Issue 8, 2009, Pages

  Garvis, Steven ^a   Munder, Antje ^b   Ball, Geneviève ^a   De Bentzmann, Sophie ^a   Wiehlmann, Lutz ^b   Ewbank, Jonathan J ^a,c,d   Tümmler, Burkhard ^b   Filloux, Alain ^a,e  

^a CNRS   (France)

^b HANNOVER MEDICAL SCHOOL   (Germany)

^c CENTRE D IMMUNOLOGIE DE MARSEILLE LUMINY   (France)

^d INSERM   (France)

^e IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARAC PROTEIN; PROTEIN HISTIDINE KINASE; BACTERIAL PROTEIN; CHEB PROTEIN, BACTERIA;

ANIMAL TISSUE; ARTICLE; BACTERIAL GENE; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; BACTERIUM ISOLATE; BACTERIUM MUTANT; CAENORHABDITIS ELEGANS; CHEB2 GENE; CHEMOTAXIS; CONTROLLED STUDY; GENE CLUSTER; GENE INSERTION; LUNG FIBROSIS; LUNG INFECTION; MOUSE; NONHUMAN; PARASITE VIRULENCE; PATHOGENESIS; PHENOTYPE; PSEUDOMONAS AERUGINOSA; REGULATOR GENE; TRANSPOSON; ANIMAL; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MICROBIOLOGICAL EXAMINATION; MICROBIOLOGY; PATHOGENICITY; PATHOLOGY; PSEUDOMONAS INFECTION; VIRULENCE;

ANIMALIA; BACTERIA (MICROORGANISMS); CAENORHABDITIS ELEGANS; MURINAE; PSEUDOMONAS AERUGINOSA;

ANIMALS; BACTERIAL PROTEINS; BACTERIOLOGICAL TECHNIQUES; CAENORHABDITIS ELEGANS; CHEMOTAXIS; GENE EXPRESSION REGULATION, BACTERIAL; MICE; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; VIRULENCE;

EID: 70049104688     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000540     Document Type: Article

References (69)

1. Lyczak JB, Cannon CL, Pier GB (2000) Establishment of Pseudomonas aeruginosa infection: lessons from a versatile opportunist. Microbes Infect 2: 1051-1060.
2. O'Toole GA, Kolter R (1998) Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol Microbiol 30: 295-304.
3. Vallet I, Olson JW, Lory S, Lazdunski A, Filloux A (2001) The chaperone/usher pathways of Pseudomonas aeruginosa: identification of fimbrial gene clusters (cup) and their involvement in biofilm formation. Proc Natl Acad Sci U S A 98: 6911-6916. (Pubitemid 32538316)
4. Filloux A, Hachani A, Bleves S (2008) The bacterial type VI secretion machine: yet another player for protein transport across membranes. Microbiology 154: 1570-1583.
5. Pradel E, Ewbank JJ (2004) Genetic models in pathogenesis. Annu Rev Genet 38: 347-363.
6. Sifri CD, Begun J, Ausubel FM (2005) The worm has turned-microbial virulence modeled in Caenorhabditis elegans. Trends Microbiol 13: 119-127. (Pubitemid 40311894)
7. Tan MW, Mahajan-Miklos S, Ausubel FM (1999) Killing of Caenorhabditis elegans by Pseudomonas aeruginosa used to model mammalian bacterial pathogenesis. Proc Natl Acad Sci U S A 96: 715-720. (Pubitemid 29061274)
8. Tan MW, Rahme LG, Sternberg JA, Tompkins RG, Ausubel FM (1999) Pseudomonas aeruginosa killing of Caenorhabditis elegans used to identify P. aeruginosa virulence factors. Proc Natl Acad Sci U S A 96: 2408-2413. (Pubitemid 29117928)
9. Gallagher LA, Manoil C (2001) Pseudomonas aeruginosa PAO1 kills Caenorhabditis elegans by cyanide poisoning. J Bacteriol 183: 6207-6214.
10. Zaborin A, Romanowski K, Gerdes S, Holbrook C, Lepine F, et al. (2009) Red death in Caenorhabditis elegans caused by Pseudomonas aeruginosa PAO1. Proc Natl Acad Sci U S A 106: 6327-6332.
11. Choi JY, Sifri CD, Goumnerov BC, Rahme LG, Ausubel FM, et al. (2002) Identification of virulence genes in a pathogenic strain of Pseudomonas aeruginosa by representational difference analysis. J Bacteriol 184: 952-961.
12. Heurlier K, Denervaud V, Haenni M, Guy L, Krishnapillai V, et al. (2005) Quorum-sensing-negative (lasR) mutants of Pseudomonas aeruginosa avoid cell lysis and death. J Bacteriol 187: 4875-4883. (Pubitemid 40962204)
13. Liang X, Pham XQ, Olson MV, Lory S (2001) Identification of a genomic island present in the majority of pathogenic isolates of Pseudomonas aeruginosa. J Bacteriol 183: 843-853. (Pubitemid 32095293)
14. Tümmler B, Koopmann U, Grothues D, Weissbrodt H, Steinkamp G, et al. (1991) Nosocomial acquisition of Pseudomonas aeruginosa by cystic fibrosis patients. J Clin Microbiol 29: 1265-1267.
15. Wiehlmann L, Wagner G, Cramer N, Siebert B, Gudowius P, et al. (2007) Population structure of Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 104: 8101-8106.
16. Hagelueken G, Adams TM, Wiehlmann L, Widow U, Kolmar H, et al. (2006) The crystal structure of SdsA1, an alkylsulfatase from Pseudomonas aeruginosa, defines a third class of sulfatases. Proc Natl Acad Sci USA 103: 7631-7636. (Pubitemid 43752832)
17. Hagelueken G, Wiehlmann L, Adams TM, Kolmar H, Heinz DW, et al. (2007) Crystal structure of the electron transfer complex rubredoxin rubredoxin reductase of Pseudomonas aeruginosa. Proc Natl Acad Sci USA 104: 12276-12281. (Pubitemid 47206128)
18. Tümmler B (1987) Unusual mechanism of pathogenicity of Pseudomonas aeruginosa isolates from patients with cystic fibrosis. Infection 15: 311-312.
19. Rakhimova E, Munder A, Wiehlmann L, Bredenbruch F, Tümmler B (2008) Fitness of isogenic colony morphology variants of Pseudomonas aeruginosa in murine airway infection. PLoS ONE 3: 1685. doi:10.1371/journal.pone.0001685. (Pubitemid 351891073)
20. Wiehlmann L, Larbig K, Ritzka M, Tümmler B (2002) Signature tagged mutagenesis of Pseudomonas aeruginosa. Genome Lett 1: 131-139.
21. Ferrandez A, Hawkins AC, Summerfield DT, Harwood CS (2002) Cluster II che genes from Pseudomonas aeruginosa are required for an optimal chemotactic response. J Bacteriol 184: 4374-4383. (Pubitemid 34832565)
22. Stover CK, Pham XQ, Erwin AL, Mizoguchi SD, Warrener P, et al. (2000) Complete genome sequence of Pseudomonas aeruginosa PA01, an opportunistic pathogen. Nature 406: 959-964. (Pubitemid 30690454)
23. Kato J, Nakamura T, Kuroda A, Ohtake H (1999) Cloning and characterization of chemotaxis genes in Pseudomonas aeruginosa. Biosci Biotechnol Biochem 63: 155-161. (Pubitemid 129555252)
24. Masduki A, Nakamura J, Ohga T, Umezaki R, Kato J, et al. (1995) Isolation and characterization of chemotaxis mutants and genes of Pseudomonas aeruginosa. J Bacteriol 177: 948-952.
25. Hickman JW, Tifrea DF, Harwood CS (2005) A chemosensory system that regulates biofilm formation through modulation of cyclic diguanylate levels. Proc Natl Acad Sci U S A 102: 14422-14427.
26. Darzins A (1994) Characterization of a Pseudomonas aeruginosa gene cluster involved in pilus biosynthesis and twitching motility: sequence similarity to the chemotaxis proteins of enterics and the gliding bacterium Myxococcus xanthus. Mol Microbiol 11: 137-153. (Pubitemid 24985835)
27. Kearns DB, Robinson J, Shimkets LJ (2001) Pseudomonas aeruginosa exhibits directed twitching motility up phosphatidylethanolamine gradients. J Bacteriol 183: 763-767. (Pubitemid 32048137)
28. Li M, Hazelbauer GL (2005) Adaptational assistance in clusters of bacterial chemoreceptors. Mol Microbiol 56: 1617-1626. (Pubitemid 40780655)
29. Baker MD, Wolanin PM, Stock JB (2006) Signal transduction in bacterial chemotaxis. Bioessays 28: 9-22.
30. Yonekawa H, Hayashi H, Parkinson JS (1983) Requirement of the CheB function for sensory adaptation in Escherichia coli. J Bacteriol 156: 1228-1235. (Pubitemid 14216350)
31. Jones BD, Lee CA, Falkow S (1992) Invasion by Salmonella typhimurium is affected by the direction of flagellar rotation. Infect Immun 60: 2475-2480.
32. Begun J, Sifri CD, Goldman S, Calderwood SB, Ausubel FM (2005) Staphylococcus aureus virulence factors identified by using a high-throughput Caenorhabditis elegans-killing model. Infect Immun 73: 872-877. (Pubitemid 40165745)
33. Kurz CL, Chauvet S, Andres E, Aurouze M, Vallet I, et al. (2003) Virulence factors of the human opportunistic pathogen Serratia marcescens identified by in vivo screening. EMBO J 22: 1451-1460. (Pubitemid 36417394)
34. Liberati NT, Urbach JM, Miyata S, Lee DG, Drenkard E, et al. (2006) An ordered, nonredundant library of Pseudomonas aeruginosa strain PA14 transposon insertion mutants. Proc Natl Acad Sci U S A 103: 2833-2838. (Pubitemid 43306635)
35. Dennis JJ, Zylstra GJ (1998) Plasposons: modular self-cloning minitransposon derivatives for rapid genetic analysis of gram-negative bacterial genomes. Appl Environ Microbiol 64: 2710-2715.
36. Hebert MD, Houghton JE (1997) Regulation of ornithine utilization in Pseudomonas aeruginosa (PAO1) is mediated by a transcriptional regulator, OruR. J Bacteriol 179: 7834-7842.
37. Dekkers LC, Bloemendaal CJ, de Weger LA, Wijffelman CA, Spaink HP, et al. (1998) A two-component system plays an important role in the root-colonizing ability of Pseudomonas fluorescens strain WCS365. Mol Plant Microbe Interact 11: 45-56.
38. de Weert S, Dekkers LC, Bitter W, Tuinman S, Wijfjes AH, et al. (2006) The two-component ColR/S system of Pseudomonas fluorescens WCS365 plays a role in rhizosphere competence through maintaining the structure and function of the outer membrane. FEMS Microbiol Ecol 58: 205-213. (Pubitemid 44583804)
39. Hu N, Zhao B (2007) Key genes involved in heavy-metal resistance in Pseudomonas putida CD2. FEMS Microbiol Lett 267: 17-22. (Pubitemid 46066534)
40. Horak R, Ilves H, Pruunsild P, Kuljus M, Kivisaar M (2004) The ColR-ColS two-component signal transduction system is involved in regulation of Tn4652 transposition in Pseudomonas putida under starvation conditions. Mol Microbiol 54: 795-807. (Pubitemid 39457299)
41. Alm RA, Hallinan JP, Watson AA, Mattick JS (1996) Fimbrial biogenesis genes of Pseudomonas aeruginosa: pilW and pilX increase the similarity of type 4 fimbriae to the GSP protein-secretion systems and pilY1 encodes a gonococcal PilC homologue. Mol Microbiol 22: 161-173.
42. Doyle TB, Hawkins AC, McCarter LL (2004) The complex flagellar torque generator of Pseudomonas aeruginosa. J Bacteriol 186: 6341-6350.
43. Toutain CM, Zegans ME, O'Toole GA (2005) Evidence for two flagellar stators and their role in the motility of Pseudomonas aeruginosa. J Bacteriol 187: 771-777.
44. Stewart RC, Russell CB, Roth AF, Dahlquist FW (1988) Interaction of CheB with chemotaxis signal transduction components in Escherichia coli: modulation of the methylesterase activity and effects on cell swimming behavior. Cold Spring Harb Symp Quant Biol 53 Pt 1: 27-40.
45. Comolli JC, Waite LL, Mostov KE, Engel JN (1999) Pili binding to asialo-GM1 on epithelial cells can mediate cytotoxicity or bacterial internalization by Pseudomonas aeruginosa. Infect Immun 67: 3207-3214.
46. Prince A (1992) Adhesins and receptors of Pseudomonas aeruginosa associated with infection of the respiratory tract. Microb Pathog 13: 251-260.
47. Hoang TT, Kutchma AJ, Becher A, Schweizer HP (2000) Integration- proficient plasmids for Pseudomonas aeruginosa: site-specific integration and use for engineering of reporter and expression strains. Plasmid 43: 59-72. (Pubitemid 30049004)
48. Munder A, Zelmer A, Schmiedl A, Dittmar KE, Rohde M, et al. (2005) Murine pulmonary infection with Listeria monocytogenes: differential susceptibility of BALB/c, C57BL/6 and DBA/2 mice. Microbes Infect 7: 600-611. (Pubitemid 40720413)
49. Kurz CL, Ewbank JJ (2003) Caenorhabditis elegans: an emerging genetic model for the study of innate immunity. Nat Rev Genet 4: 380-390.
50. Ewbank JJ (2002) Tackling both sides of the host-pathogen equation with Caenorhabditis elegans. Microbes Infect 4: 247-256.
51. Mahajan-Miklos S, Rahme LG, Ausubel FM (2000) Elucidating the molecular mechanisms of bacterial virulence using non-mammalian hosts. Mol Microbiol 37: 981-988. (Pubitemid 30701227)
52. Rodrigue A, Quentin Y, Lazdunski A, Méjean V, Foglino M (2000) Two-component systems in Pseudomonas aeruginosa: why so many? Trends Microbiol 8: 498-504.
53. Goodman AL, Kulasekara B, Rietsch A, Boyd D, Smith RS, et al. (2004) A signaling network reciprocally regulates genes associated with acute infection and chronic persistence in Pseudomonas aeruginosa. Dev Cell 7: 745-754. (Pubitemid 39462694)
54. Schuster M, Greenberg EP (2006) A network of networks: quorum-sensing gene regulation in Pseudomonas aeruginosa. Int J Med Microbiol 296: 73-81. (Pubitemid 43375989)
55. 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. Proc Natl Acad Sci U S A 103: 171-176. (Pubitemid 43076123)
56. Kato J, Kim HE, Takiguchi N, Kuroda A, Ohtake H (2008) Pseudomonas aeruginosa as a model microorganism for investigation of chemotactic behaviors in ecosystem. J Biosci Bioeng 106: 1-7.
57. Schuster M, Hawkins AC, Harwood CS, Greenberg EP (2004) The Pseudomonas aeruginosa RpoS regulon and its relationship to quorum sensing. Mol Microbiol 51: 973-985. (Pubitemid 38270793)
58. 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. (Pubitemid 36363167)
59. Burrowes E, Baysse C, Adams C, O'Gara F (2006) Influence of the regulatory protein RsmA on cellular functions in Pseudomonas aeruginosa PAO1, as revealed by transcriptome analysis. Microbiology 152: 405-418. (Pubitemid 43210672)
60. Pessi G, Williams F, Hindle Z, Heurlier K, Holden MT, et al. (2001) The global posttranscriptional regulator RsmA modulates production of virulence determinants and N-acylhomoserine lactones in Pseudomonas aeruginosa. J Bacteriol 183: 6676-6683. (Pubitemid 33026760)
61. Guvener ZT, Tifrea DF, Harwood CS (2006) Two different Pseudomonas aeruginosa chemosensory signal transduction complexes localize to cell poles and form and remould in stationary phase. Mol Microbiol 61: 106-118.
62. Terry K, Williams SM, Connolly L, Ottemann KM (2005) Chemotaxis plays multiple roles during Helicobacter pylori animal infection. Infect Immun 73: 803-811. (Pubitemid 40165736)
63. Lewis JA, Fleming JT (1995) Basic culture methods. Methods Cell Biol 48: 3-29.
64. Couillault C, Pujol N, Reboul J, Sabatier L, Guichou JF, et al. (2004) TLR-independent control of innate immunity in Caenorhabditis elegans by the TIR domain adaptor protein TIR-1, an ortholog of human SARM. Nat Immunol 5: 488-494. (Pubitemid 38660460)
65. Head NE, Yu H (2004) Cross-sectional analysis of clinical and environmental isolates of Pseudomonas aeruginosa: biofilm formation, virulence, and genome diversity. Infect Immun 72: 133-144.
66. Kohler T, Curty LK, Barja F, van Delden C, Pechere JC (2000) Swarming of Pseudomonas aeruginosa is dependent on cell-to-cell signaling and requires flagella and pili. J Bacteriol 182: 5990-5996. (Pubitemid 30823755)
67. Mazumder R, Phelps TJ, Krieg NR, Benoit RE (1999) Determining chemotactic responses by two subsurface microaerophiles using a simplified capillary assay method. J Microbiol Methods 37: 255-263. (Pubitemid 29342293)
68. Moulton RC, Montie TC (1979) Chemotaxis by Pseudomonas aeruginosa. J Bacteriol 137: 274-280.
69. Sambrook J, Fritsch E, Maniatis T (1989) Molecular Cloning: A Laboratory Manual Cold Spring Harbor Laboratory Press.