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The bacterial thiopurine methyltransferase tellurite resistance process is highly dependent upon aggregation properties and oxidative stress response

Authors

  • Claire Prigent-Combaret,

    1. Research group on «Bacterial Opportunistic Pathogens and Environment»
    2. Research group on «Rhizosphere»
    3. UMR5557 Ecologie Microbienne, Université de Lyon, Université Lyon 1, CNRS, VetAgro Sup, Villeurbanne, F-69622, France.
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  • Hervé Sanguin,

    1. Research group on «Rhizosphere»
    2. UMR5557 Ecologie Microbienne, Université de Lyon, Université Lyon 1, CNRS, VetAgro Sup, Villeurbanne, F-69622, France.
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    • Present address: CIRAD, UMR LSTM, F34398 Montpellier, France.

  • Ludovic Champier,

    1. Research group on «Bacterial Opportunistic Pathogens and Environment»
    2. UMR5557 Ecologie Microbienne, Université de Lyon, Université Lyon 1, CNRS, VetAgro Sup, Villeurbanne, F-69622, France.
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  • Cédric Bertrand,

    1. UMR5557 Ecologie Microbienne, Université de Lyon, Université Lyon 1, CNRS, VetAgro Sup, Villeurbanne, F-69622, France.
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  • Claire Monnez,

    1. Research group on «Bacterial Opportunistic Pathogens and Environment»
    2. UMR5557 Ecologie Microbienne, Université de Lyon, Université Lyon 1, CNRS, VetAgro Sup, Villeurbanne, F-69622, France.
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  • Céline Colinon,

    1. Research group on «Bacterial Opportunistic Pathogens and Environment»
    2. UMR5557 Ecologie Microbienne, Université de Lyon, Université Lyon 1, CNRS, VetAgro Sup, Villeurbanne, F-69622, France.
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  • Didier Blaha,

    1. Research group on «Bacterial Opportunistic Pathogens and Environment»
    2. UMR5557 Ecologie Microbienne, Université de Lyon, Université Lyon 1, CNRS, VetAgro Sup, Villeurbanne, F-69622, France.
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  • Jean-Marc Ghigo,

    1. Institut Pasteur, Unité de Génétique des Biofilms, Département de Microbiologie F-75015 Paris, France.
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  • Benoit Cournoyer

    Corresponding author
    1. Research group on «Bacterial Opportunistic Pathogens and Environment»
    2. UMR5557 Ecologie Microbienne, Université de Lyon, Université Lyon 1, CNRS, VetAgro Sup, Villeurbanne, F-69622, France.
      E-mail benoit.cournoyer@univ-lyon1.fr; Tel. (+33) 4 72 43 13 49; Fax (+33) 4 72 43 12 23.
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E-mail benoit.cournoyer@univ-lyon1.fr; Tel. (+33) 4 72 43 13 49; Fax (+33) 4 72 43 12 23.

Summary

Bacterial thiopurine methyltransferases (bTPMTs) can favour resistance towards toxic tellurite oxyanions through a pathway leading to the emission of a garlic-like smell. Gene expression profiling completed by genetic, physiological and electron microscopy analyses was performed to identify key bacterial activities contributing to this resistance process. Escherichia coli strain MG1655 expressing the bTPMT was used as a cell model in these experiments. This strain produced a garlic-like smell which was found to be due to dimethyl telluride, and cell aggregates in culture media supplemented with tellurite. Properties involved in aggregation were correlated with cell attachment to polystyrene, which increased with tellurite concentrations. Gene expression profiling supported a role of adhesins in the resistance process with 14% of the tellurite-regulated genes involved in cell envelope, flagella and fimbriae biogenesis. Other tellurite-regulated genes were, at 27%, involved in energy, carbohydrate and amino acid metabolism including the synthesis of antioxidant proteins, and at 12% in the synthesis of transcriptional regulators and signal transduction systems. Escherichia coli mutants impaired in tellurite-regulated genes showed ubiquinone and adhesins synthesis, oxidative stress response, and efflux to be essential in the bTPMT resistance process. High tellurite resistance required a synergistic expression of these functions and an efficient tellurium volatilization by the bTPMT.

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