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Metabolic co-dependence gives rise to collective oscillations within biofilms

Author

Listed:
  • Jintao Liu

    (University of California San Diego)

  • Arthur Prindle

    (University of California San Diego)

  • Jacqueline Humphries

    (University of California San Diego)

  • Marçal Gabalda-Sagarra

    (Universitat Pompeu Fabra)

  • Munehiro Asally

    (Warwick Integrative Synthetic Biology Centre, School of Life Sciences, University of Warwick)

  • Dong-yeon D. Lee

    (University of California San Diego)

  • San Ly

    (University of California San Diego)

  • Jordi Garcia-Ojalvo

    (Universitat Pompeu Fabra)

  • Gürol M. Süel

    (University of California San Diego)

Abstract

Cells that reside within a community can cooperate and also compete with each other for resources. It remains unclear how these opposing interactions are resolved at the population level. Here we investigate such an internal conflict within a microbial (Bacillus subtilis) biofilm community: cells in the biofilm periphery not only protect interior cells from external attack but also starve them through nutrient consumption. We discover that this conflict between protection and starvation is resolved through emergence of long-range metabolic co-dependence between peripheral and interior cells. As a result, biofilm growth halts periodically, increasing nutrient availability for the sheltered interior cells. We show that this collective oscillation in biofilm growth benefits the community in the event of a chemical attack. These findings indicate that oscillations support population-level conflict resolution by coordinating competing metabolic demands in space and time, suggesting new strategies to control biofilm growth.

Suggested Citation

  • Jintao Liu & Arthur Prindle & Jacqueline Humphries & Marçal Gabalda-Sagarra & Munehiro Asally & Dong-yeon D. Lee & San Ly & Jordi Garcia-Ojalvo & Gürol M. Süel, 2015. "Metabolic co-dependence gives rise to collective oscillations within biofilms," Nature, Nature, vol. 523(7562), pages 550-554, July.
    • Handle: RePEc:nat:nature:v:523:y:2015:i:7562:d:10.1038_nature14660
    DOI: 10.1038/nature14660
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    Cited by:

    1. Yuzhen Zhang & Yukmi Cai & Bing Zhang & Yi-Heng P. Job Zhang, 2024. "Spatially structured exchange of metabolites enhances bacterial survival and resilience in biofilms," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    2. John C. Boik, 2016. "Optimality of Social Choice Systems: Complexity, Wisdom, and Wellbeing Centrality," Working Paper 0005, Principled Societies Project, revised Mar 2017.
    3. Vincent Charron-Lamoureux & Lounès Haroune & Maude Pomerleau & Léo Hall & Frédéric Orban & Julie Leroux & Adrien Rizzi & Jean-Sébastien Bourassa & Nicolas Fontaine & Élodie V. d’Astous & Philippe Daup, 2023. "Pulcherriminic acid modulates iron availability and protects against oxidative stress during microbial interactions," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    4. Matthias Bec & Sylvain Pouzet & Céline Cordier & Simon Barral & Vittore Scolari & Benoit Sorre & Alvaro Banderas & Pascal Hersen, 2024. "Optogenetic spatial patterning of cooperation in yeast populations," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    5. Fondi, Marco & Di Patti, Francesca, 2019. "A synthetic ecosystem for the multi-level modelling of heterotroph-phototroph metabolic interactions," Ecological Modelling, Elsevier, vol. 399(C), pages 13-22.
    6. Jung Hun Park & Gábor Holló & Yolanda Schaerli, 2024. "From resonance to chaos by modulating spatiotemporal patterns through a synthetic optogenetic oscillator," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    7. Xiaoling Zhai & Joseph W Larkin & Kaito Kikuchi & Samuel E Redford & Ushasi Roy & Gürol M Süel & Andrew Mugler, 2019. "Statistics of correlated percolation in a bacterial community," PLOS Computational Biology, Public Library of Science, vol. 15(12), pages 1-19, December.
    8. Yan, Xuejun & Lee, Hyung-Sool & Li, Nan & Wang, Xin, 2020. "The micro-niche of exoelectrogens influences bioelectricity generation in bioelectrochemical systems," Renewable and Sustainable Energy Reviews, Elsevier, vol. 134(C).

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