Context-dependent siderophore exploitability shapes microbial community structure

The ISME Journal, vol. 20

Abstract

Siderophores are classically viewed as shared iron-scavenging public goods, yet their ecological roles in multispecies communities remain incompletely understood. Here, we establish a synthetic microbial community to dissect how different siderophores, their uptake compatibility and spatial structure shape iron competition. Using Corynebacterium glutamicum as a model, we show that this siderophore non-producer accesses diverse xenosiderophores, including enterobactin secreted by Escherichia coli. However, exploitation was constrained and co-cultures converged to stable compositions. Dose-response experiments combined with mathematical modelling indicated that the producer retains more effective access to enterobactin than the exploiter. The presence of Pseudomonas putida altered this interaction, as it exploited enterobactin while producing pyoverdine, a siderophore inaccessible to the other community members that restricted their iron access. Across different cultivation scales, community dynamics was strongly influenced by spatial organization and initial composition. These findings identify siderophores as context-dependent iron-allocation agents that can promote microbial coexistence or exclusion.

Authors 19

1. A. Krüger

   Forschungszentrum Jülich · Heinrich Heine University Düsseldorf

   Affiliation as printed

   Institute of Bio- and Geosciences 1 , IBG-1: Biotechnology, Forschungszentrum Jülich, Wilhelm-Johnen-Straße, 52428 Jülich ,

   Institute of Microbial Interactions, Faculty of Mathematics and Natural Sciences, Heinrich-Heine-University Düsseldorf , Universitätsstraße 1, 40225 Düsseldorf ,

2. Sanga Paik

   Forschungszentrum Jülich · Heinrich Heine University Düsseldorf

   Affiliation as printed

   Institute of Molecular Enzyme Technology, IMET, Faculty of Mathematics and Natural Sciences, Heinrich Heine University Düsseldorf , Forschungszentrum Jülich, Wilhelm-Johnen-Straße, 52428 Jülich ,

3. Michelle Bund

   Forschungszentrum Jülich

   Affiliation as printed

   Institute of Bio- and Geosciences 1 , IBG-1: Biotechnology, Forschungszentrum Jülich, Wilhelm-Johnen-Straße, 52428 Jülich ,

4. Matthias Pesch

   Forschungszentrum Jülich

   Affiliation as printed

   Institute of Bio- and Geosciences 1 , IBG-1: Biotechnology, Forschungszentrum Jülich, Wilhelm-Johnen-Straße, 52428 Jülich ,

5. Stephan Krueger

   Cluster of Excellence on Plant Sciences · Heinrich Heine University Düsseldorf

   Affiliation as printed

   CEPLAS Metabolism and Metabolomics Laboratory, Cluster of Excellence on Plant Sciences (CEPLAS), Faculty of Mathematics and Natural Sciences, Heinrich Heine University Düsseldorf , Universitätsstraße 1, 40225 Düsseldorf ,

6. Benita Lückel

   Forschungszentrum Jülich

   Affiliation as printed

   Institute of Bio- and Geosciences 1 , IBG-1: Biotechnology, Forschungszentrum Jülich, Wilhelm-Johnen-Straße, 52428 Jülich ,

7. Athanasios Papadopoulos

   Heinrich Heine University Düsseldorf

   Affiliation as printed

   Center for Structural Studies, Faculty of Mathematics and Natural Sciences, Heinrich Heine University Düsseldorf, Universitätsstraße 1 , 40225 Düsseldorf ,

8. Johanna Wiechert

   Forschungszentrum Jülich

   Affiliation as printed

   Institute of Bio- and Geosciences 1 , IBG-1: Biotechnology, Forschungszentrum Jülich, Wilhelm-Johnen-Straße, 52428 Jülich ,

9. Tanvir Hassan Aachen Computational Life Science Department of Biology

   RWTH Aachen University

   Affiliation as printed

   Computational Life Science, Department of Biology, RWTH Aachen University , 52074 Worringerweg 3, Aachen ,

10. Ulrike Weber

    Forschungszentrum Jülich · Heinrich Heine University Düsseldorf

    Affiliation as printed

    Institute of Bio- and Geosciences 1 , IBG-1: Biotechnology, Forschungszentrum Jülich, Wilhelm-Johnen-Straße, 52428 Jülich ,

    Institute of Microbial Interactions, Faculty of Mathematics and Natural Sciences, Heinrich-Heine-University Düsseldorf , Universitätsstraße 1, 40225 Düsseldorf ,

11. Romain Avellan Aachen Institute of Biology, Leiden University

    Leiden University

    Affiliation as printed

    Institute of Biology, Leiden University , Sylviusweg 72, 2333 Leiden ,

12. Sander H. J. Smits

    Heinrich Heine University Düsseldorf

    Affiliation as printed

    Center for Structural Studies, Faculty of Mathematics and Natural Sciences, Heinrich Heine University Düsseldorf, Universitätsstraße 1 , 40225 Düsseldorf ,

13. Michael H. Bott

    Forschungszentrum Jülich

    Affiliation as printed

    Institute of Bio- and Geosciences 1 , IBG-1: Biotechnology, Forschungszentrum Jülich, Wilhelm-Johnen-Straße, 52428 Jülich ,

14. Ákos T. Kovács Aachen Institute of Biology, Leiden University

    Leiden University

    Affiliation as printed

    Institute of Biology, Leiden University , Sylviusweg 72, 2333 Leiden ,

15. Philipp Westhoff

    Cluster of Excellence on Plant Sciences · Heinrich Heine University Düsseldorf

    Affiliation as printed

    CEPLAS Metabolism and Metabolomics Laboratory, Cluster of Excellence on Plant Sciences (CEPLAS), Faculty of Mathematics and Natural Sciences, Heinrich Heine University Düsseldorf , Universitätsstraße 1, 40225 Düsseldorf ,

16. Anna Matuszyńska Aachen Computational Life Science Department of Biology

    RWTH Aachen University

    Affiliation as printed

    Computational Life Science, Department of Biology, RWTH Aachen University , 52074 Worringerweg 3, Aachen ,

17. Dietrich Kohlheyer corresponding

    Forschungszentrum Jülich

    Affiliation as printed

    Institute of Bio- and Geosciences 1 , IBG-1: Biotechnology, Forschungszentrum Jülich, Wilhelm-Johnen-Straße, 52428 Jülich ,

18. Thomas Drepper corresponding

    Forschungszentrum Jülich · Heinrich Heine University Düsseldorf

    Affiliation as printed

    Institute of Molecular Enzyme Technology, IMET, Faculty of Mathematics and Natural Sciences, Heinrich Heine University Düsseldorf , Forschungszentrum Jülich, Wilhelm-Johnen-Straße, 52428 Jülich ,

19. Julia Frunzke corresponding

    Forschungszentrum Jülich · Heinrich Heine University Düsseldorf

    Affiliation as printed

    Institute of Bio- and Geosciences 1 , IBG-1: Biotechnology, Forschungszentrum Jülich, Wilhelm-Johnen-Straße, 52428 Jülich ,

    Institute of Microbial Interactions, Faculty of Mathematics and Natural Sciences, Heinrich-Heine-University Düsseldorf , Universitätsstraße 1, 40225 Düsseldorf ,