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Experimental evolution of yeast shows that public-goods upregulation can evolve despite challenges from exploitative non-producers

Author

Listed:
  • Richard J. Lindsay

    (University of Exeter)

  • Philippa J. Holder

    (University of Exeter)

  • Mark Hewlett

    (University of Exeter)

  • Ivana Gudelj

    (University of Exeter)

Abstract

Microbial secretions, such as metabolic enzymes, are often considered to be cooperative public goods as they are costly to produce but can be exploited by others. They create incentives for the evolution of non-producers, which can drive producer and population productivity declines. In response, producers can adjust production levels. Past studies suggest that while producers lower production to reduce costs and exploitation opportunities when under strong selection pressure from non-producers, they overproduce secretions when these pressures are weak. We challenge the universality of this trend with the production of a metabolic enzyme, invertase, by Saccharomyces cerevisiae, which catalyses sucrose hydrolysis into two hexose molecules. Contrary to past studies, overproducers evolve during evolutionary experiments even when under strong selection pressure from non-producers. Phenotypic and competition assays with a collection of synthetic strains - engineered to have modified metabolic attributes - identify two mechanisms for suppressing the benefits of invertase to those who exploit it. Invertase overproduction increases extracellular hexose concentrations that suppresses the metabolic efficiency of competitors, due to the rate-efficiency trade-off, and also enhances overproducers’ hexose capture rate by inducing transporter expression. Thus, overproducers are maintained in the environment originally thought to not support public goods production.

Suggested Citation

  • Richard J. Lindsay & Philippa J. Holder & Mark Hewlett & Ivana Gudelj, 2024. "Experimental evolution of yeast shows that public-goods upregulation can evolve despite challenges from exploitative non-producers," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-52043-9
    DOI: 10.1038/s41467-024-52043-9
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    References listed on IDEAS

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    3. Justin R. Meyer & Ivana Gudelj & Robert Beardmore, 2015. "Biophysical mechanisms that maintain biodiversity through trade-offs," Nature Communications, Nature, vol. 6(1), pages 1-7, May.
    4. Zhenyu Jin & Jiahong Li & Lei Ni & Rongrong Zhang & Aiguo Xia & Fan Jin, 2018. "Conditional privatization of a public siderophore enables Pseudomonas aeruginosa to resist cheater invasion," Nature Communications, Nature, vol. 9(1), pages 1-11, December.
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