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Pulcherriminic acid modulates iron availability and protects against oxidative stress during microbial interactions

Author

Listed:
  • Vincent Charron-Lamoureux

    (Université de Sherbrooke)

  • Lounès Haroune

    (Université de Sherbrooke
    Faculté de médecine, Université de Sherbrooke)

  • Maude Pomerleau

    (Université de Sherbrooke)

  • Léo Hall

    (Université de Sherbrooke)

  • Frédéric Orban

    (Université de Sherbrooke)

  • Julie Leroux

    (Université de Sherbrooke)

  • Adrien Rizzi

    (Université de Sherbrooke)

  • Jean-Sébastien Bourassa

    (Université de Sherbrooke)

  • Nicolas Fontaine

    (Université de Sherbrooke)

  • Élodie V. d’Astous

    (Université de Sherbrooke)

  • Philippe Dauphin-Ducharme

    (Université de Sherbrooke)

  • Claude Y. Legault

    (Université de Sherbrooke)

  • Jean-Philippe Bellenger

    (Université de Sherbrooke)

  • Pascale B. Beauregard

    (Université de Sherbrooke)

Abstract

Siderophores are soluble or membrane-embedded molecules that bind the oxidized form of iron, Fe(III), and play roles in iron acquisition by microorganisms. Fe(III)-bound siderophores bind to specific receptors that allow microbes to acquire iron. However, certain soil microbes release a compound (pulcherriminic acid, PA) that, upon binding to Fe(III), forms a precipitate (pulcherrimin) that apparently functions by reducing iron availability rather than contributing to iron acquisition. Here, we use Bacillus subtilis (PA producer) and Pseudomonas protegens as a competition model to show that PA is involved in a peculiar iron-managing system. The presence of the competitor induces PA production, leading to precipitation of Fe(III) as pulcherrimin, which prevents oxidative stress in B. subtilis by restricting the Fenton reaction and deleterious ROS formation. In addition, B. subtilis uses its known siderophore bacillibactin to retrieve Fe(III) from pulcherrimin. Our findings indicate that PA plays multiple roles by modulating iron availability and conferring protection against oxidative stress during inter-species competition.

Suggested Citation

  • Vincent Charron-Lamoureux & Lounès Haroune & Maude Pomerleau & Léo Hall & Frédéric Orban & Julie Leroux & Adrien Rizzi & Jean-Sébastien Bourassa & Nicolas Fontaine & Élodie V. d’Astous & Philippe Daup, 2023. "Pulcherriminic acid modulates iron availability and protects against oxidative stress during microbial interactions," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-38222-0
    DOI: 10.1038/s41467-023-38222-0
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    References listed on IDEAS

    as
    1. Yuxuan Qin & Yinghao He & Qianxuan She & Philip Larese-Casanova & Pinglan Li & Yunrong Chai, 2019. "Heterogeneity in respiratory electron transfer and adaptive iron utilization in a bacterial biofilm," Nature Communications, Nature, vol. 10(1), pages 1-12, December.
    2. Elena Butaitė & Michael Baumgartner & Stefan Wyder & Rolf Kümmerli, 2017. "Siderophore cheating and cheating resistance shape competition for iron in soil and freshwater Pseudomonas communities," Nature Communications, Nature, vol. 8(1), pages 1-12, December.
    3. Kevin Rychel & Anand V. Sastry & Bernhard O. Palsson, 2020. "Machine learning uncovers independently regulated modules in the Bacillus subtilis transcriptome," Nature Communications, Nature, vol. 11(1), pages 1-10, December.
    4. Jintao Liu & Arthur Prindle & Jacqueline Humphries & Marçal Gabalda-Sagarra & Munehiro Asally & Dong-yeon D. Lee & San Ly & Jordi Garcia-Ojalvo & Gürol M. Süel, 2015. "Metabolic co-dependence gives rise to collective oscillations within biofilms," Nature, Nature, vol. 523(7562), pages 550-554, July.
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