Privatization of public goods can cause population decline

Abstract

Microbes commonly deploy a risky strategy to acquire nutrients from their environment, involving the production of costly public goods that can be exploited by neighbouring individuals. Why engage in such a strategy when an exploitation-free alternative is readily available whereby public goods are kept private? We address this by examining metabolism of Saccharomyces cerevisiae in its native form and by creating a new three-strain synthetic community deploying different strategies of sucrose metabolism. Public-metabolizers digest resources externally, private-metabolizers internalize resources before digestion, and cheats avoid the metabolic costs of digestion but exploit external products generated by competitors. A combination of mathematical modelling and ecological experiments reveal that private-metabolizers invade and take over an otherwise stable community of public-metabolizers and cheats. However, owing to the reduced growth rate of private-metabolizers and population bottlenecks that are frequently associated with microbial communities, privatizing public goods can become unsustainable, leading to population decline.

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Fig. 1: Growth rates on privately metabolized maltose or publicly metabolized sucrose with respect to cell and resource concentration.
Fig. 2: Single season growth and pairwise competitiveness of differing sucrose metabolic strategies.
Fig. 3: Competitiveness and long-term dynamics of sucrose-use polymorphisms.
Fig. 4: Initial strain frequencies determine the timing of population decline in this transfer regimen.
Fig. 5: Relative resilience of opposing metabolic strategies.

Data availability

The research data supporting this publication can be found at https://doi.org/10.24378/exe.1383.

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Acknowledgements

We thank R. Beardmore, A. Jepson and P. Holder for comments and helpful discussions. R.J.L. and I.G. are funded by European Research Council Consolidator Grant No. 647292 MathModExp awarded to I.G., and B.J.P. was funded by an EPSRC Doctoral training studentship.

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R.J.L. and I.G. conceived the idea. R.J.L. and I.G designed the experiments. R.J.L. carried out the experiments. B.J.P. and I.G. developed the mathematical model. B.J.P. carried out numerical simulations. R.J.L. and I.G. analysed the results and wrote the manuscript.

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Correspondence to Ivana Gudelj.

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Lindsay, R.J., Pawlowska, B.J. & Gudelj, I. Privatization of public goods can cause population decline. Nat Ecol Evol 3, 1206–1216 (2019). https://doi.org/10.1038/s41559-019-0944-9

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