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The PprA–PprB two-component system activates CupE, the first non-archetypal Pseudomonas aeruginosa chaperone–usher pathway system assembling fimbriae

Authors

  • Caroline Giraud,

    1. Laboratoire d'Ingénierie des Systèmes Macromoléculaires, CNRS – Aix Marseille Université, 31 Chemin Joseph Aiguier, 13402 Marseille, France.
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  • Christophe S. Bernard,

    1. Laboratoire d'Ingénierie des Systèmes Macromoléculaires, CNRS – Aix Marseille Université, 31 Chemin Joseph Aiguier, 13402 Marseille, France.
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  • Virginie Calderon,

    1. Université de Toulouse; UPS; Laboratoire de Microbiologie et Génétique Moléculaire; F31000 Toulouse, France.
    2. CNRS; LMGM; F31000 Toulouse, France.
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  • Liang Yang,

    1. Infection Microbiology Group, DTU-System Biology, Technical University of Denmark, DK 2800, Lyngby, Denmark.
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  • Alain Filloux,

    1. Laboratoire d'Ingénierie des Systèmes Macromoléculaires, CNRS – Aix Marseille Université, 31 Chemin Joseph Aiguier, 13402 Marseille, France.
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    • Present address: Imperial College London, Division of Cell and Molecular Biology, Centre for Molecular Microbiology and Infection, South Kensington Campus, Flowers Building, London SW7 2AZ, UK.

  • Søren Molin,

    1. Infection Microbiology Group, DTU-System Biology, Technical University of Denmark, DK 2800, Lyngby, Denmark.
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  • Gwennaele Fichant,

    1. Université de Toulouse; UPS; Laboratoire de Microbiologie et Génétique Moléculaire; F31000 Toulouse, France.
    2. CNRS; LMGM; F31000 Toulouse, France.
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  • Christophe Bordi,

    1. Laboratoire d'Ingénierie des Systèmes Macromoléculaires, CNRS – Aix Marseille Université, 31 Chemin Joseph Aiguier, 13402 Marseille, France.
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  • Sophie de Bentzmann

    Corresponding author
    1. Laboratoire d'Ingénierie des Systèmes Macromoléculaires, CNRS – Aix Marseille Université, 31 Chemin Joseph Aiguier, 13402 Marseille, France.
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E-mail bentzman@ifr88.cnrs-mrs.fr; Tel. (+33) 491164117; Fax (+33) 491712124.

Summary

The opportunistic pathogen Pseudomonas aeruginosa has redundant molecular systems that contribute to its pathogenicity. Those assembling fimbrial structures promote complex organized community lifestyle. We characterized a new 5.8 kb genetic locus, cupE, that includes the conserved usher- and chaperone-encoding genes. This locus, widely conserved in different bacterial species, contains four additional genes encoding non-archetypal fimbrial subunits. We first evidenced that the cupE gene cluster was specifically expressed in biofilm conditions and was responsible for fibre assembly containing at least CupE1 protein, at the bacterial cell surface. These fimbriae not only played a significant role in the early stages (microcolony and macrocolony formation) but also in shaping 3D mushrooms during P. aeruginosa biofilm development. Using wide-genome transposon mutagenesis, we identified the PprAB two-component system (TCS) as a regulator of cupE expression, and further demonstrated the involvement of the PprAB TCS in direct CupE fimbrial assembly activation. Thus, this TCS represents a new regulatory element controlling the transition between planktonic and community lifestyles in P. aeruginosa.

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