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Gluconic acid-producing Pseudomonas sp. prevent γ-actinorhodin biosynthesis by Streptomyces coelicolor A3(2)

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Abstract

Streptomyces are ubiquitous soil bacteria well known for their ability to produce a wide range of secondary metabolites including antibiotics. In their natural environments, they co-exist and interact with complex microbial communities and their natural products are assumed to play a major role in mediating these interactions. Reciprocally, their secondary metabolism can be influenced by the surrounding microbial communities. Little is known about these complex interactions and the underlying molecular mechanisms. During pairwise co-culture experiments, a fluorescent Pseudomonas, Pseudomonas fluorescens BBc6R8, was shown to prevent the production of the diffusible blue pigment antibiotic γ-actinorhodin by Streptomyces coelicolor A3(2) M145 without altering the biosynthesis of the intracellular actinorhodin. A mutant of the BBc6R8 strain defective in the production of gluconic acid from glucose and consequently unable to acidify the culture medium did not show any effect on the γ-actinorhodin biosynthesis in contrast to the wild-type strain and the mutant complemented with the wild-type allele. In addition, when glucose was substituted by mannitol in the culture medium, P. fluorescens BBc6R8 was unable to acidify the medium and to prevent the biosynthesis of the antibiotic. All together, the results show that P. fluorescens BBc6R8 impairs the biosynthesis of the lactone form of actinorhodin in S. coelicolor by acidifying the medium through the production of gluconic acid. Other fluorescent Pseudomonas and the opportunistic pathogen Pseudomonas aeruginosa PAO1 also prevented the γ-actinorhodin production in a similar way. We propose some hypotheses on the ecological significance of such interaction.

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Acknowledgments

This work was founded by the French National Research Agency through the Laboratory of Excellence ARBRE (ANR-11-LABX-0002-01), by the French National Institute for Agricultural Research (INRA) and Région Lorraine. JG was supported by a CJS (Contrat Jeune Scientifique) Grant from INRA. We thank Jean-Selim Medot for his help in this work.

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Authors and Affiliations

  1. Dynamique des Génomes et Adaptation Microbienne, UMR 1128, Université de Lorraine, 54506, Vandœuvre-lès-Nancy, France

    Justine Galet, Laurence Hôtel, Pierre Leblond & Bertrand Aigle

  2. Dynamique des Génomes et Adaptation Microbienne, UMR 1128, INRA, 54506, Vandœuvre-lès-Nancy, France

    Justine Galet, Laurence Hôtel, Pierre Leblond & Bertrand Aigle

  3. Interactions Arbres-Microorganismes, UMR 1136, INRA, 54280, Champenoux, France

    Aurélie Deveau & Pascale Frey-Klett

  4. Interactions Arbres-Microorganismes, UMR 1136, Université de Lorraine, 54506, Vandœuvre-lès-Nancy, France

    Aurélie Deveau & Pascale Frey-Klett

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  1. Justine Galet
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  2. Aurélie Deveau
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Correspondence to Bertrand Aigle.

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Communicated by Matthias Boll.

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Galet, J., Deveau, A., Hôtel, L. et al. Gluconic acid-producing Pseudomonas sp. prevent γ-actinorhodin biosynthesis by Streptomyces coelicolor A3(2). Arch Microbiol 196, 619–627 (2014). https://doi.org/10.1007/s00203-014-1000-4

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