Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Privatization of public goods can cause population decline

Nature Ecology & Evolution volume 3, pages 1206–1216 (2019)Cite this article

Subjects

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.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

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.

Similar content being viewed by others

Data availability

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

References

  1. Richards, T. A. & Talbot, N. J. Horizontal gene transfer in osmotrophs: playing with public goods. Nat. Rev. Microbiol. 11, 720–727 (2013).

    CAS  PubMed  Google Scholar 

  2. Drescher, K., Nadell, C. D., Stone, H. A., Wingreen, N. S. & Bassler, B. L. Solutions to the public goods dilemma in bacterial biofilms. Curr. Biol. 24, 50–55 (2014).

    CAS  PubMed  Google Scholar 

  3. Lindsay, R. J., Kershaw, M. J., Pawlowska, B. J., Talbot, N. J. & Gudelj, I. Harbouring public good mutants within a pathogen population can increase both fitness and virulence. eLife 5, e18678 (2016).

    PubMed  PubMed Central  Google Scholar 

  4. Bachmann, H., Molenaar, D., Kleerebezem, M. & van Hylckama Vlieg, J. E. High local substrate availability stabilizes a cooperative trait. ISME J. 5, 929–932 (2010).

    PubMed  PubMed Central  Google Scholar 

  5. Griffin, A. S., West, S. A. & Buckling, A. Cooperation and competition in pathogenic bacteria. Nature 430, 1024–1027 (2004).

    CAS  PubMed  Google Scholar 

  6. Chang, Q. et al. A unique invertase is important for sugar absorption of an obligate biotrophic pathogen during infection. New Phytol. 215, 1548–1561 (2017).

    CAS  PubMed  Google Scholar 

  7. Lincoln, L. & More, S. S. Bacterial invertases: occurrence, production, biochemical characterization, and significance of transfructosylation. J. Basic Microbiol. 57, 803–813 (2017).

    CAS  PubMed  Google Scholar 

  8. Parrent, J. L., James, T. Y., Vasaitis, R. & Taylor, A. F. Friend or foe? Evolutionary history of glycoside hydrolase family 32 genes encoding for sucrolytic activity in fungi and its implications for plant–fungal symbioses. BMC Evol. Biol. 9, 148 (2009).

    PubMed  PubMed Central  Google Scholar 

  9. Voegele, R. T., Wirsel, S., Möll, U., Lechner, M. & Mendgen, K. Cloning and characterization of a novel invertase from the obligate biotroph Uromyces fabae and analysis of expression patterns of host and pathogen invertases in the course of infection. Mol. Plant Microbe Interact. 19, 625–634 (2006).

    CAS  PubMed  Google Scholar 

  10. Koschwanez, J. H., Foster, K. R. & Murray, A. W. Improved use of a public good selects for the evolution of undifferentiated multicellularity. eLife 2, e00367 (2013).

    PubMed  PubMed Central  Google Scholar 

  11. Dai, L., Vorselen, D., Korolev, K. S. & Gore, J. Generic indicators for loss of resilience before a tipping point leading to population collapse. Science 336, 1175–1177 (2012).

    CAS  PubMed  Google Scholar 

  12. Völker, C. & Wolf-Gladrow, D. A. Physical limits on iron uptake mediated by siderophores or surface reductases. Mar. Chem. 65, 227–244 (1999).

    Google Scholar 

  13. Greig, D. & Travisano, M. The Prisoner’s Dilemma and polymorphism in yeast SUC genes. Proc. Biol. Sci. 271(Suppl. 3), S25–S26 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Gore, J., Youk, H. & van Oudenaarden, A. Snowdrift game dynamics and facultative cheating in yeast. Nature 459, 253–256 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Harrison, F., Browning, L. E., Vos, M. & Buckling, A. Cooperation and virulence in acute Pseudomonas aeruginosa infections. BMC Biol. 4, 21 (2006).

    PubMed  PubMed Central  Google Scholar 

  16. Kümmerli, R., Schiessl, K. T., Waldvogel, T., McNeill, K. & Ackermann, M. Habitat structure and the evolution of diffusible siderophores in bacteria. Ecol. Lett. 17, 1536–1544 (2014).

    PubMed  Google Scholar 

  17. Niehus, R., Picot, A., Oliveira, N. M., Mitri, S. & Foster, K. R. The evolution of siderophore production as a competitive trait. Evolution 71, 1443–1455 (2017).

    CAS  PubMed  Google Scholar 

  18. Lee, W., Van Baalen, M. & Jansen, V. A. An evolutionary mechanism for diversity in siderophore‐producing bacteria. Ecol. Lett. 15, 119–125 (2012).

    PubMed  Google Scholar 

  19. Riley, M. A. & Wertz, J. E. Bacteriocins: evolution, ecology, and application. Annu Rev. Microbiol. 56, 117–137 (2002).

    CAS  PubMed  Google Scholar 

  20. Celiker, H. & Gore, J. Competition between species can stabilize public-goods cooperation within a species. Mol. Syst. Biol. 8, 621 (2012).

    PubMed  PubMed Central  Google Scholar 

  21. Verstrepen, K. J. et al. Glucose and sucrose: hazardous fast-food for industrial yeast? Trends Biotechnol. 22, 531–537 (2004).

    CAS  PubMed  Google Scholar 

  22. Lindsay, R. J., Pawlowska, B. J. & Gudelj, I. When increasing population density can promote the evolution of metabolic cooperation. ISME J. 12, 849–859 (2018).

    PubMed  PubMed Central  Google Scholar 

  23. Ross-Gillespie, A., Gardner, A., West, S. A. & Griffin, A. S. Frequency dependence and cooperation: theory and a test with bacteria. Am. Nat. 170, 331–342 (2007).

    PubMed  Google Scholar 

  24. Ross-Gillespie, A., Gardner, A., Buckling, A., West, S. A. & Griffin, A. S. Density dependence and cooperation: theory and a test with bacteria. Evolution 63, 2315–2325 (2009).

    PubMed  Google Scholar 

  25. Kümmerli, R., Griffin, A. S., West, S. A., Buckling, A. & Harrison, F. Viscous medium promotes cooperation in the pathogenic bacterium Pseudomonas aeruginosa. Proc. Biol. Sci. 276, 3531–3538 (2009).

    PubMed  PubMed Central  Google Scholar 

  26. Allison, S. D. Cheaters, diffusion and nutrients constrain decomposition by microbial enzymes in spatially structured environments. Ecol. Lett. 8, 626–635 (2005).

    Google Scholar 

  27. Julou, T. et al. Cell–cell contacts confine public goods diffusion inside Pseudomonas aeruginosa clonal microcolonies. Proc. Natl Acad. Sci. USA 110, 12577–12582 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  28. MacLean, R. C., Fuentes-Hernandez, A., Greig, D., Hurst, L. D. & Gudelj, I. A mixture of ‘cheats’ and ‘co-operators’ can enable maximal group benefit. PLoS Biol. 8, e1000486 (2010).

    PubMed  PubMed Central  Google Scholar 

  29. Driscoll, W. W., Pepper, J. W., Pierson, L. S. & Pierson, E. A. Spontaneous Gac mutants of Pseudomonas biological control strains: cheaters or mutualists? Appl. Environ. Microbiol. 77, 7227–7235 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Rainey, P. B. & Rainey, K. Evolution of cooperation and conflict in experimental bacterial populations. Nature 425, 72 (2003).

    CAS  PubMed  Google Scholar 

  31. Sanchez, A. & Gore, J. Feedback between population and evolutionary dynamics determines the fate of social microbial populations. PLoS Biol. 11, e1001547 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Rakoff-Nahoum, S., Foster, K. R. & Comstock, L. E. The evolution of cooperation within the gut microbiota. Nature 533, 255–259 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  33. Galeote, V. et al. FSY1, a horizontally transferred gene in the Saccharomyces cerevisiae EC1118 wine yeast strain, encodes a high-affinity fructose/H+ symporter. Microbiology 156, 3754–3761 (2010).

    CAS  PubMed  Google Scholar 

  34. Brown, C. J., Todd, K. M. & Rosenzweig, R. F. Multiple duplications of yeast hexose transport genes in response to selection in a glucose-limited environment. Mol. Biol. Evol. 15, 931–942 (1998).

    CAS  PubMed  Google Scholar 

  35. Wahl, R., Wippel, K., Goos, S., Kämper, J. & Sauer, N. A novel high-affinity sucrose transporter is required for virulence of the plant pathogen Ustilago maydis. PLoS Biol. 8, e1000303 (2010).

    PubMed  PubMed Central  Google Scholar 

  36. Cuskin, F. et al. Human gut Bacteroidetes can utilize yeast mannan through a selfish mechanism. Nature 517, 165–169 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Martens, E. C., Koropatkin, N. M., Smith, T. J. & Gordon, J. I. Complex glycan catabolism by the human gut microbiota: the Bacteroidetes Sus-like paradigm. J. Biol. Chem. 284, 24673–24677 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Reintjes, G., Arnosti, C., Fuchs, B. M. & Amann, R. An alternative polysaccharide uptake mechanism of marine bacteria. ISME J. 11, 1640 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  39. Dandekar, A. A., Chugani, S. & Greenberg, E. P. Bacterial quorum sensing and metabolic incentives to cooperate. Science 338, 264–266 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  40. Jin, Z. et al. Conditional privatization of a public siderophore enables Pseudomonas aeruginosa to resist cheater invasion. Nat. Commun. 9, 1383 (2018).

    PubMed  PubMed Central  Google Scholar 

  41. Zhang, X. X. & Rainey, P. B. Exploring the sociobiology of pyoverdin‐producing Pseudomonas. Evolution 67, 3161–3174 (2013).

    PubMed  Google Scholar 

  42. Pande, S. et al. Privatization of cooperative benefits stabilizes mutualistic cross-feeding interactions in spatially structured environments. ISME J. 10, 1413 (2016).

    PubMed  Google Scholar 

  43. Inglis, R. F., Biernaskie, J. M., Gardner, A. & Kümmerli, R. Presence of a loner strain maintains cooperation and diversity in well-mixed bacterial communities. Proc. Biol. Sci. 283, https://doi.org/10.1098/rspb.2015.2682 (2016).

    PubMed  PubMed Central  Google Scholar 

  44. Schweizer, M. & Dickinson, J. R. The Metabolism and Molecular Physiology of Saccharomyces cerevisiae (CRC Press, 2004).

  45. Zhou, L., Slamti, L., Nielsen-LeRoux, C., Lereclus, D. & Raymond, B. The social biology of quorum sensing in a naturalistic host pathogen system. Curr. Biol. 24, 2417–2422 (2014).

    CAS  PubMed  Google Scholar 

  46. Travisano, M. & Velicer, G. J. Strategies of microbial cheater control. Trends Microbiol. 12, 72–78 (2004).

    CAS  PubMed  Google Scholar 

  47. Brockhurst, M. A., Buckling, A. & Gardner, A. Cooperation peaks at intermediate disturbance. Curr. Biol. 17, 761–765 (2007).

    CAS  PubMed  Google Scholar 

  48. Rouwenhorst, R. J., Van Der Baan, A. A., Scheffers, W. A. & Van Dijken, J. Production and localization of beta-fructosidase in asynchronous and synchronous chemostat cultures of yeasts. Appl. Environ. Microbiol. 57, 557–562 (1991).

    CAS  PubMed  PubMed Central  Google Scholar 

  49. Tammi, M., Ballou, L., Taylor, A. & Ballou, C. Effect of glycosylation on yeast invertase oligomer stability. J. Biol. Chem. 262, 4395–4401 (1987).

    CAS  PubMed  Google Scholar 

  50. Carlson, M. & Botstein, D. Two differentially regulated mRNAs with different 5′ ends encode secreted and intracellular forms of yeast invertase. Cell 28, 145–154 (1982).

    CAS  PubMed  Google Scholar 

  51. Williams, R. S., Trumbly, R. J., MacColl, R., Trimble, R. B. & Maley, F. Comparative properties of amplified external and internal invertase from the yeast SUC2 gene. J. Biol. Chem. 260, 13334–13341 (1985).

    CAS  PubMed  Google Scholar 

  52. Gascón, S., Neumann, N. P. & Lampen, J. O. Comparative study of the properties of the purified internal and external invertases from yeast. J. Biol. Chem. 243, 1573–1577 (1968).

    PubMed  Google Scholar 

  53. Kaiser, C. A. & Botstein, D. Secretion-defective mutations in the signal sequence for Saccharomyces cerevisiae invertase. Mol. Cell. Biol. 6, 2382–2391 (1986).

    CAS  PubMed  PubMed Central  Google Scholar 

  54. Stambuk, B. U., Batista, A. S. & De Araujo, P. S. Kinetics of active sucrose transport in Saccharomyces cerevisiae. J. Biosci. Bioeng. 89, 212–214 (2000).

    CAS  PubMed  Google Scholar 

  55. Stambuk, B. U., da Silva, M. A., Panek, A. D. & de Araujo, P. S. Active α-glucoside transport in Saccharomyces cerevisiae. FEMS Microbiol. Lett. 170, 105–110 (1999).

    CAS  PubMed  Google Scholar 

  56. Vidgren, V., Ruohonen, L. & Londesborough, J. Characterization and functional analysis of the MAL and MPH loci for maltose utilization in some ale and lager yeast strains. Appl. Environ. Microbiol. 71, 7846–7857 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  57. Lion, S. Theoretical approaches in evolutionary ecology: environmental feedback as a unifying perspective. Am. Nat. 191, 21–44 (2017).

    PubMed  Google Scholar 

  58. McPeek, M. A. The ecological dynamics of natural selection: traits and the coevolution of community structure. Am. Nat. 189, E91–E117 (2017).

    PubMed  Google Scholar 

  59. Otterstedt, K. et al. Switching the mode of metabolism in the yeast Saccharomyces cerevisiae. EMBO Rep. 5, 532–537 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  60. Sauer, N. & Stolz, J. SUC1 and SUC2: two sucrose transporters from Arabidopsis thaliana; expression and characterization in baker’s yeast and identification of the histidine‐tagged protein. Plant J. 6, 67–77 (1994).

    CAS  PubMed  Google Scholar 

  61. Weise, A. et al. A new subfamily of sucrose transporters, SUT4, with low affinity/high capacity localized in enucleate sieve elements of plants. Plant Cell 12, 1345–1355 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  62. Reinders, A. & Ward, J. M. Functional characterization of the α‐glucoside transporter Sut1p from Schizosaccharomyces pombe, the first fungal homologue of plant sucrose transporters. Mol. Microbiol. 39, 445–455 (2001).

    CAS  PubMed  Google Scholar 

  63. Elbing, K. et al. Role of hexose transport in control of glycolytic flux in Saccharomyces cerevisiae. Appl. Environ. Microbiol. 70, 5323–5330 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  64. Bisson, L. F., Coons, D. M., Kruckeberg, A. L. & Lewis, D. A. Yeast sugar transporters. Crit. Rev. Biochem. Mol. Biol. 28, 259–308 (1993).

    CAS  PubMed  Google Scholar 

  65. Özcan, S. & Johnston, M. Function and regulation of yeast hexose transporters. Microbiol. Mol. Biol. Rev. 63, 554–569 (1999).

    PubMed  PubMed Central  Google Scholar 

  66. Leventhal, G. E., Ackermann, M. & Schiessl, K. T. Why microbes secrete molecules to modify their environment: the case of iron-chelating siderophores. J. R. Soc. Interface 16, 20180674 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  67. Andersen, S. B. et al. Privatisation rescues function following loss of cooperation. eLife 7, e38594 (2018).

    PubMed  PubMed Central  Google Scholar 

  68. Vetter, Y., Deming, J., Jumars, P. & Krieger-Brockett, B. A predictive model of bacterial foraging by means of freely released extracellular enzymes. Microb. Ecol. 36, 75–92 (1998).

    CAS  PubMed  Google Scholar 

  69. Dean, R. et al. The top 10 fungal pathogens in molecular plant pathology. Mol. Plant Pathol. 13, 414–430 (2012).

    PubMed  PubMed Central  Google Scholar 

  70. Kothary, M. H. & Babu, U. S. Infective dose of foodborne pathogens in volunteers: a review. J. Food Safety 21, 49–68 (2001).

    Google Scholar 

  71. Schmid-Hempel, P. & Frank, S. A. Pathogenesis, virulence, and infective dose. PLoS Pathog. 3, e147 (2007).

    PubMed Central  Google Scholar 

  72. Piskur, J., Rozpedowska, E., Polakova, S., Merico, A. & Compagno, C. How did Saccharomyces evolve to become a good brewer? Trends Genet. 22, 183–186 (2006).

    CAS  PubMed  Google Scholar 

  73. Sikorski, R. S. & Hieter, P. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122, 19–27 (1989).

    CAS  PubMed  PubMed Central  Google Scholar 

  74. Reding-Roman, C. et al. The unconstrained evolution of fast and efficient antibiotic-resistant bacterial genomes. Nat. Ecol. Evol. 1, 0050 (2017).

    Google Scholar 

  75. Lenski, R. E., Rose, M. R., Simpson, S. C. & Tadler, S. C. Long-term experimental evolution in Escherichia coli. I. Adaptation and divergence during 2,000 generations. Am. Nat. 138, 1315–1341 (1991).

    Google Scholar 

  76. Pfeiffer, T., Schuster, S. & Bonhoeffer, S. Cooperation and competition in the evolution of ATP-producing pathways. Science 292, 504 (2001).

    CAS  PubMed  Google Scholar 

  77. Bauchop, T. & Elsden, S. R. The growth of micro-organisms in relation to their energy supply. J. Gen. Microbiol. 23, 457–469 (1960).

    CAS  PubMed  Google Scholar 

  78. Postma, E., Verduyn, C., Scheffers, W. A. & Van Dijken, J. P. Enzymic analysis of the crabtree effect in glucose-limited chemostat cultures of Saccharomyces cerevisiae. Appl Environ. Microbiol 55, 468–477 (1989).

    CAS  PubMed  PubMed Central  Google Scholar 

  79. Weusthuis, R. A., Pronk, J. T., van den Broek, P. J. & van Dijken, J. P. Chemostat cultivation as a tool for studies on sugar transport in yeasts. Microbiol. Rev. 58, 616–630 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  80. Badotti, F. et al. Switching the mode of sucrose utilization by Saccharomyces cerevisiae. Microb. Cell Fact. 7, 4 (2008).

    PubMed  PubMed Central  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

  1. Biosciences, University of Exeter, Exeter, UK

    Richard J. Lindsay, Bogna J. Pawlowska & Ivana Gudelj

Authors
  1. Richard J. Lindsay
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bogna J. Pawlowska
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ivana Gudelj
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

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.

Corresponding author

Correspondence to Ivana Gudelj.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Figs. 1–14 and Table 1.

Reporting Summary

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41559-019-0944-9

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing