IDEAS home Printed from https://ideas.repec.org/a/plo/pcbi00/1005269.html
   My bibliography  Save this article

Stability of Cross-Feeding Polymorphisms in Microbial Communities

Author

Listed:
  • Ivana Gudelj
  • Margie Kinnersley
  • Peter Rashkov
  • Karen Schmidt
  • Frank Rosenzweig

Abstract

Cross-feeding, a relationship wherein one organism consumes metabolites excreted by another, is a ubiquitous feature of natural and clinically-relevant microbial communities and could be a key factor promoting diversity in extreme and/or nutrient-poor environments. However, it remains unclear how readily cross-feeding interactions form, and therefore our ability to predict their emergence is limited. In this paper we developed a mathematical model parameterized using data from the biochemistry and ecology of an E. coli cross-feeding laboratory system. The model accurately captures short-term dynamics of the two competitors that have been observed empirically and we use it to systematically explore the stability of cross-feeding interactions for a range of environmental conditions. We find that our simple system can display complex dynamics including multi-stable behavior separated by a critical point. Therefore whether cross-feeding interactions form depends on the complex interplay between density and frequency of the competitors as well as on the concentration of resources in the environment. Moreover, we find that subtly different environmental conditions can lead to dramatically different results regarding the establishment of cross-feeding, which could explain the apparently unpredictable between-population differences in experimental outcomes. We argue that mathematical models are essential tools for disentangling the complexities of cross-feeding interactions.Author Summary: Simple environments, even those used in laboratory experimental evolution, have proven vastly richer than originally thought, capable of generating and supporting genetic and phenotypic diversity. This was not foreseen by Gause’s seminal competitive exclusion theory, which predicted that simple single niche environments cannot support diversity. We now know that cross-feeding interactions can be a major driver of diversity maintenance in simple environments. Cross-feeding, a relationship wherein one organism consumes metabolites excreted by another, is a ubiquitous feature of natural and clinically-relevant microbial communities and even tumour cell populations. However, it remains unclear how readily such relationships form, and therefore our ability to predict their emergence is limited. Here we developed a mathematical model of cross-feeding and find that this system can display complex dynamics including multi-stable behaviour separated by a critical point. Therefore, the emergence of cross-feeding depends on complex interplay between density and frequency of competitors. Moreover we predict that small changes in environmental conditions can cause abrupt and irreversible shifts from cross-feeding permissive to cross-feeding prohibitive states. We argue that mathematical models are essential tools for disentangling the complexities of cross-feeding interactions.

Suggested Citation

  • Ivana Gudelj & Margie Kinnersley & Peter Rashkov & Karen Schmidt & Frank Rosenzweig, 2016. "Stability of Cross-Feeding Polymorphisms in Microbial Communities," PLOS Computational Biology, Public Library of Science, vol. 12(12), pages 1-17, December.
  • Handle: RePEc:plo:pcbi00:1005269
    DOI: 10.1371/journal.pcbi.1005269
    as

    Download full text from publisher

    File URL: https://journals.plos.org/ploscompbiol/article?id=10.1371/journal.pcbi.1005269
    Download Restriction: no

    File URL: https://journals.plos.org/ploscompbiol/article/file?id=10.1371/journal.pcbi.1005269&type=printable
    Download Restriction: no

    File URL: https://libkey.io/10.1371/journal.pcbi.1005269?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Robert E. Beardmore & Ivana Gudelj & David A. Lipson & Laurence D. Hurst, 2011. "Metabolic trade-offs and the maintenance of the fittest and the flattest," Nature, Nature, vol. 472(7343), pages 342-346, April.
    2. Hauert, Christoph & Wakano, Joe Yuichiro & Doebeli, Michael, 2008. "Ecological public goods games: Cooperation and bifurcation," Theoretical Population Biology, Elsevier, vol. 73(2), pages 257-263.
    3. Lei Dai & Kirill S. Korolev & Jeff Gore, 2013. "Slower recovery in space before collapse of connected populations," Nature, Nature, vol. 496(7445), pages 355-358, April.
    4. Andrew Chen & Alvaro Sanchez & Lei Dai & Jeff Gore, 2014. "Dynamics of a producer-freeloader ecosystem on the brink of collapse," Nature Communications, Nature, vol. 5(1), pages 1-6, September.
    5. R. Craig MacLean & Ivana Gudelj, 2006. "Resource competition and social conflict in experimental populations of yeast," Nature, Nature, vol. 441(7092), pages 498-501, May.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Olga A Nev & Richard J Lindsay & Alys Jepson & Lisa Butt & Robert E Beardmore & Ivana Gudelj, 2021. "Predicting microbial growth dynamics in response to nutrient availability," PLOS Computational Biology, Public Library of Science, vol. 17(3), pages 1-20, March.
    2. Elhanati, Yuval & Schuster, Stefan & Brenner, Naama, 2011. "Dynamic modeling of cooperative protein secretion in microorganism populations," Theoretical Population Biology, Elsevier, vol. 80(1), pages 49-63.
    3. Felix Funk & Christoph Hauert, 2019. "Directed migration shapes cooperation in spatial ecological public goods games," PLOS Computational Biology, Public Library of Science, vol. 15(8), pages 1-14, August.
    4. Borofsky, Talia & Feldman, Marcus W. & Ram, Yoav, 2024. "Cultural transmission, competition for prey, and the evolution of cooperative hunting," Theoretical Population Biology, Elsevier, vol. 156(C), pages 12-21.
    5. Wakano, Joe Y. & Kawasaki, Kohkichi & Shigesada, Nanako & Aoki, Kenichi, 2011. "Coexistence of individual and social learners during range expansion," Theoretical Population Biology, Elsevier, vol. 80(2), pages 132-140.
    6. Feng Zhang & Cang Hui, 2011. "Eco-Evolutionary Feedback and the Invasion of Cooperation in Prisoner's Dilemma Games," PLOS ONE, Public Library of Science, vol. 6(11), pages 1-7, November.
    7. Kazufumi Hosoda & Shingo Suzuki & Yoshinori Yamauchi & Yasunori Shiroguchi & Akiko Kashiwagi & Naoaki Ono & Kotaro Mori & Tetsuya Yomo, 2011. "Cooperative Adaptation to Establishment of a Synthetic Bacterial Mutualism," PLOS ONE, Public Library of Science, vol. 6(2), pages 1-9, February.
    8. Soomi Lee & Shu Wang, 2023. "Impacts of political fragmentation on inclusive economic resilience: Examining American metropolitan areas after the Great Recession," Urban Studies, Urban Studies Journal Limited, vol. 60(1), pages 26-45, January.
    9. De Jaegher, Kris, 2017. "Harsh environments and the evolution of multi-player cooperation," Theoretical Population Biology, Elsevier, vol. 113(C), pages 1-12.
    10. Wei Fan & Jingchao Yuan & Jinggui Wu & Hongguang Cai, 2023. "Effects of Straw Maize on the Bacterial Community and Carbon Stability at Different Soil Depths," Agriculture, MDPI, vol. 13(7), pages 1-15, June.
    11. Wildemeersch, Matthias & Franklin, Oskar & Seidl, Rupert & Rogelj, Joeri & Moorthy, Inian & Thurner, Stefan, 2019. "Modelling the multi-scaled nature of pest outbreaks," Ecological Modelling, Elsevier, vol. 409(C), pages 1-1.
    12. Rafael Muñoz-Tamayo & Milka Popova & Maxence Tillier & Diego P Morgavi & Jean-Pierre Morel & Gérard Fonty & Nicole Morel-Desrosiers, 2019. "Hydrogenotrophic methanogens of the mammalian gut: Functionally similar, thermodynamically different—A modelling approach," PLOS ONE, Public Library of Science, vol. 14(12), pages 1-20, December.
    13. Tetsushi Ohdaira & Takao Terano, 2009. "Cooperation in the Prisoner's Dilemma Game Based on the Second-Best Decision," Journal of Artificial Societies and Social Simulation, Journal of Artificial Societies and Social Simulation, vol. 12(4), pages 1-7.
    14. Mohammad Salahshour, 2021. "Freedom to choose between public resources promotes cooperation," PLOS Computational Biology, Public Library of Science, vol. 17(2), pages 1-15, February.
    15. Liu, Yuan & Cao, Lixuan & Wu, Bin, 2022. "General non-linear imitation leads to limit cycles in eco-evolutionary dynamics," Chaos, Solitons & Fractals, Elsevier, vol. 165(P2).
    16. Wang, Ching-Hao & Matin, Sakib & George, Ashish B. & Korolev, Kirill S., 2019. "Pinned, locked, pushed, and pulled traveling waves in structured environments," Theoretical Population Biology, Elsevier, vol. 127(C), pages 102-119.
    17. González Casanova, Adrián & Miró Pina, Verónica & Pardo, Juan Carlos, 2020. "The Wright–Fisher model with efficiency," Theoretical Population Biology, Elsevier, vol. 132(C), pages 33-46.
    18. de Oliveira, Viviane M. & Amado, André & Campos, Paulo R.A., 2018. "The interplay of tradeoffs within the framework of a resource-based modelling," Ecological Modelling, Elsevier, vol. 384(C), pages 249-260.
    19. Behar, Hilla & Brenner, Naama & Louzoun, Yoram, 2014. "Coexistence of productive and non-productive populations by fluctuation-driven spatio-temporal patterns," Theoretical Population Biology, Elsevier, vol. 96(C), pages 20-29.
    20. Tran, Huy T. & Balchanos, Michael & Domerçant, Jean Charles & Mavris, Dimitri N., 2017. "A framework for the quantitative assessment of performance-based system resilience," Reliability Engineering and System Safety, Elsevier, vol. 158(C), pages 73-84.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:plo:pcbi00:1005269. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: ploscompbiol (email available below). General contact details of provider: https://journals.plos.org/ploscompbiol/ .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.