Genetic architecture constrains exploitation of siderophore cooperation in the bacterium Burkholderia cenocepacia
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Abstract
Explaining how cooperation can persist in the presence of cheaters, exploiting the cooperative acts, is a challenge for evolutionary biology. Microbial systems have proved extremely useful to test evolutionary theory and identify mechanisms maintaining cooperation. One of the most widely studied system is the secretion and sharing of iron-scavenging siderophores by Pseudomonas bacteria, with many insights gained from this system now being considered as hallmarks of bacterial cooperation. Here, we introduce siderophore secretion by the bacterium Burkholderia cenocepacia H111 as a novel parallel study system, and show that this system behaves differently. For ornibactin, the main siderophore of this species, we discovered a novel mechanism of how cheating can be prevented. Particularly, we found that secreted ornibactin cannot be exploited by ornibactin-defective mutants because ornibactin receptor and synthesis genes are co-expressed from the same operon, such that disruptive mutations in synthesis genes compromise receptor availability required for siderophore uptake and cheating. For pyochelin, the secondary siderophore of this species, we found that cheating was possible, but the relative success of cheaters was positive frequency dependent, thus diametrically opposite to the Pseudomonas and other microbial systems. Altogether, our results highlight that expanding our repertoire of microbial study systems leads to new discoveries and suggest that there is an enormous diversity of social interactions out there in nature, and we might have only looked at the tip of the iceberg so far.
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- Authors
- Sathe, S., Mathew, A., Agnoli, K., Eberl, L., & Kümmerli, R.
- Affiliations
- University of Zurich (CH)
- Corresponding author
- Sathe, Santosh
- Kümmerli, Rolf
- Venue
- Evolution Letters
- Publisher
- Oxford University Press (OUP)
- Published
- 2019-12-01
- Volume
- 3
- Issue
- 6
- Pages
- 610-622
- ISSN
- 2056-3744 (ISSN-L)
- PMC
- PMC6906993
- OpenAlex
- W2979257221
- Cited by
- 23
- References
- 64
- Citations by year
- 2026: 3 · 2025: 4 · 2023: 2 · 2022: 5 · 2021: 5 · 2020: 3 · 2019: 1
- FWCI
- 7.04
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Evolution Letters (publishedVersion, cc-by)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Zurich Open Repository and Archive (University of Zurich) (acceptedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Zurich Open Repository and Archive (University of Zurich) (submittedVersion, cc-by)
- Zurich Open Repository and Archive (University of Zurich)
- Funders
- Swiss National Science Foundation (31003A_169307, PP00P3_165835)
- European Research Council (grant agreement n° 681295)
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (31003A_169307, PP00P3_165835)
- Topics
- Social Sciences › Sociology and Political Science › Evolutionary Game Theory and Cooperation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bacterial biofilms and quorum sensing
- Keywords
- bacterial cooperation, siderophores, iron acquisition, Burkholderia cenocepacia, pyochelin, cheaters, cheating prevention, siderophore receptors, genetic architecture
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