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MOLECULAR BIOLOGY OF PATHOGENS

Pseudomonas aeruginosa Virulence Analyzed in a Dictyostelium discoideum Host System

Pierre Cosson, Laurence Zulianello, Olivier Join-Lambert, François Faurisson, Leigh Gebbie, Mohammed Benghezal, Christian van Delden, Lasta Kocjancic Curty, Thilo Köhler
Pierre Cosson
Département de Morphologie
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Laurence Zulianello
Département de Morphologie
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Olivier Join-Lambert
INSERM-EMI-U 9933, Hôpital Bichat-Claude Bernard, Paris, France
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François Faurisson
INSERM-EMI-U 9933, Hôpital Bichat-Claude Bernard, Paris, France
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Leigh Gebbie
Département de Morphologie
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Mohammed Benghezal
Département de Morphologie
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Christian van Delden
Département de Génétique et Microbiologie, Université de Genève, Centre Médical Universitaire, CH-1211 Geneva 4, Switzerland
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Lasta Kocjancic Curty
Département de Génétique et Microbiologie, Université de Genève, Centre Médical Universitaire, CH-1211 Geneva 4, Switzerland
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Thilo Köhler
Département de Génétique et Microbiologie, Université de Genève, Centre Médical Universitaire, CH-1211 Geneva 4, Switzerland
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  • For correspondence: Thilo.Kohler@medecine.unige.ch
DOI: 10.1128/JB.184.11.3027-3033.2002
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  • FIG. 1.
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    FIG. 1.

    Quorum sensing in P. aeruginosa. In P. aeruginosa, secreted components such as proteases (LasB elastase), rhamnolipids, and pyocyanin are under the transcriptional control of two quorum-sensing systems, las and rhl. Both systems involve a transcriptional regulator (LasR and RhlR, respectively) and an autoinducer synthase (LasI and RhlI, respectively). When the bacterial density reaches a threshold, the accumulation in the medium of signaling autoinducer molecules (• and ▪) induces the las and rhl pathways, leading to transcription of virulence genes. The las quorum-sensing system can also induce, to some extent, the rhl quorum-sensing system. SOD, superoxide dismutase.

  • FIG. 2.
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    FIG. 2.

    Growth of D. discoideum clones in the presence of Klebsiella and P. aeruginosa. Approximately 200 D. discoideum cells were plated with a lawn of K. pneumoniae bacteria alone (A) or supplemented with P. aeruginosa strain PT5 (wild type [wt]) (B), PT462 (rhlR [C]), PT498 (lasR [D]), PT531 (lasR-rhlR [E]), or PT712 (rhlA [F]). Growth of D. discoideum created plaques in the bacterial lawn after 5 days of incubation at 25°C.

  • FIG. 3.
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    FIG. 3.

    Quantitative assessment of D. discoideum growth in the presence of P. aeruginosa. Dictyostelium cells were applied as droplets onto a lawn of pure P. aeruginosa bacteria, as represented in the upper left panel. The numbers of Dictyostelium cells applied were 50,000 in drop number 1, 10,000 in 2, 2000 in 3, etc., as described in Materials and Methods. After 5 days at 25°C, the ability of Dictyostelium cells to create plaques in the bacterial lawn was recorded. The bacteria used here were PT5 (wild type [wt]), PT498 (lasR), PT462 (rhlR), and PT531 (lasR-rhlR). In a scale measuring growth of Dictyostelium cells, the results obtained were scored 0 for wild-type PT5, 1 for PT498, 5 for PT462, and 8 for PT531.

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    FIG. 4.

    Lysis of Dictyostelium cells exposed to Pseudomonas supernatants. Dictyostelium cells were exposed to culture supernatants of wild-type (wt) strain PT5 (A, upper panels) and the double mutant PT531 (A, lower panels) and observed with a phase-contrast microscope. Arrows indicate individual Dictyostelium cells being lysed by wild-type supernatant during the indicated time frame. The kinetics of cell lysis induced by supernatants of the wild type (PT5), the lasR-rhlR double mutant (PT531) and the rhlA mutant (PT712) was determined by counting Dictoystelium cells under the microscope in a field containing approximately 100 cells at time zero (B).

Tables

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  • TABLE 1.

    P. aeruginosa strains used in this study

    StrainPhenotype or genotypeSource or reference
    35
    PT5PAO1 wild typeLaboratory collection
    PT149PT5NfxC (previously called PAO-7H)18
    PT454PT5ΔrhlI::Tn501 Hgr17
    PT462PT5ΔrhlR::Tn501 Hgr17
    PT466PT5ΔlasI Tcr17
    PT498PT5ΔlasR Tcr17
    PT502PT5ΔrhlI::Tn501 ΔlasI Hgr TcrThis study
    PT531PT5rhlR::Tn501 ΔlasR Hgr Tcr17
    PT625PT5NalC19
    PT637PT149mexE::ΩHg20
    PT648PT5nfxB19
    PT712PT5rhlA::Gm17
  • TABLE 2.

    Growth of D. discoideum in the presence of various P. aeruginosa mutants

    StrainD. discoideum growth on substrate(s)a
    K. pneumoniae + P. aeruginosaP. aeruginosab
    PT5 (wild type)−0
    PT462 (rhlR)+5
    PT498 (lasR)−1
    PT531 (rhlR-lasR)+8
    PT454 (rhlI)+4
    PT466 (lasI)−1
    PT502 (rhlI-lasI)+8
    PT712 (rhlA)+2
    PT149 (NfxC)+4
    PT637 (NfxC, mexE)−0
    PT625 (NalC)−0
    PT648 (nfxB)−1
    • ↵a Clonal growth of D. discoideum was tested on a mixture of K. pneumoniae and P. aeruginosa cells, as described in Fig. 2. +, growth of D. discoideum on the given substrate; −, no growth of D. discoideum.

    • ↵b The ability of D. discoideum cells to form plaques was tested on a lawn of pure P. aeruginosa cells as described in the legend to Fig. 3.

  • TABLE 3.

    Virulence of P. aeruginosa efflux mutants in a rat model of acute pneumonia

    StrainInoculum (106 CFU)n% MortalityaPTime to death (days)Lung wt (g)bBacterial counts in lungs (log CFU/g)
    PT5 (wild type)3.022721.6 ± 0.633.98 ± 0.508.30 ± 0.54
    PT625 (NalC)1.718500.192.1 ± 1.03.84 ± 0.98.53 ± 0.38
    PT648 (nfxB)2.111450.151.6 ± 0.894.83 ± 1.358.85 ± 0.28
    PT149 (NfxC)2.1180<0.001NRcNDdND
    PT637 (NfxC, mexE)0.912420.0062.8 ± 14 ± 1.218.44 ± 0.48
    • ↵a Statistical significance (P < 0.05) was evaluated with a Student's t test calculated versus PT5, except for PT637, which was calculated against PT149.

    • ↵b Lung weight of uninfected rat, 1.0 ± 0.2 g.

    • ↵c NR, not relevant.

    • ↵d ND, not determined.

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Pseudomonas aeruginosa Virulence Analyzed in a Dictyostelium discoideum Host System
Pierre Cosson, Laurence Zulianello, Olivier Join-Lambert, François Faurisson, Leigh Gebbie, Mohammed Benghezal, Christian van Delden, Lasta Kocjancic Curty, Thilo Köhler
Journal of Bacteriology Jun 2002, 184 (11) 3027-3033; DOI: 10.1128/JB.184.11.3027-3033.2002

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Pseudomonas aeruginosa Virulence Analyzed in a Dictyostelium discoideum Host System
Pierre Cosson, Laurence Zulianello, Olivier Join-Lambert, François Faurisson, Leigh Gebbie, Mohammed Benghezal, Christian van Delden, Lasta Kocjancic Curty, Thilo Köhler
Journal of Bacteriology Jun 2002, 184 (11) 3027-3033; DOI: 10.1128/JB.184.11.3027-3033.2002
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