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Growth of bacteria in 3-d colonies

Author

Listed:
  • Xinxian Shao
  • Andrew Mugler
  • Justin Kim
  • Ha Jun Jeong
  • Bruce R Levin
  • Ilya Nemenman

Abstract

The dynamics of growth of bacterial populations has been extensively studied for planktonic cells in well-agitated liquid culture, in which all cells have equal access to nutrients. In the real world, bacteria are more likely to live in physically structured habitats as colonies, within which individual cells vary in their access to nutrients. The dynamics of bacterial growth in such conditions is poorly understood, and, unlike that for liquid culture, there is not a standard broadly used mathematical model for bacterial populations growing in colonies in three dimensions (3-d). By extending the classic Monod model of resource-limited population growth to allow for spatial heterogeneity in the bacterial access to nutrients, we develop a 3-d model of colonies, in which bacteria consume diffusing nutrients in their vicinity. By following the changes in density of E. coli in liquid and embedded in glucose-limited soft agar, we evaluate the fit of this model to experimental data. The model accounts for the experimentally observed presence of a sub-exponential, diffusion-limited growth regime in colonies, which is absent in liquid cultures. The model predicts and our experiments confirm that, as a consequence of inter-colony competition for the diffusing nutrients and of cell death, there is a non-monotonic relationship between total number of colonies within the habitat and the total number of individual cells in all of these colonies. This combined theoretical-experimental study reveals that, within 3-d colonies, E. coli cells are loosely packed, and colonies produce about 2.5 times as many cells as the liquid culture from the same amount of nutrients. We verify that this is because cells in liquid culture are larger than in colonies. Our model provides a baseline description of bacterial growth in 3-d, deviations from which can be used to identify phenotypic heterogeneities and inter-cellular interactions that further contribute to the structure of bacterial communities.Author summary: The vast majority of theoretical and experimental studies assume that bacteria exist as planktonic cells in well-mixed liquid cultures, all with equal access to nutrients, wastes, toxins, antibiotics, bacterial viruses, and each other. However, in the real world, bacteria are more often found in physically structured, spatially heterogeneous habitats as colonies and micro-colonies. While one can experimentally explore the population and evolutionary dynamics of bacteria in such physically structured habitats, there is dearth of mathematical models to generate hypotheses for and to interpret results of these experiments. As a step towards the construction of a theory of the population dynamics of bacteria in physically structured habitats, we develop and experientially explore the simplest such model of the dynamics of bacterial growth in 3-d structured colonies.

Suggested Citation

  • Xinxian Shao & Andrew Mugler & Justin Kim & Ha Jun Jeong & Bruce R Levin & Ilya Nemenman, 2017. "Growth of bacteria in 3-d colonies," PLOS Computational Biology, Public Library of Science, vol. 13(7), pages 1-19, July.
  • Handle: RePEc:plo:pcbi00:1005679
    DOI: 10.1371/journal.pcbi.1005679
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    References listed on IDEAS

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    1. Ryan N Gutenkunst & Joshua J Waterfall & Fergal P Casey & Kevin S Brown & Christopher R Myers & James P Sethna, 2007. "Universally Sloppy Parameter Sensitivities in Systems Biology Models," PLOS Computational Biology, Public Library of Science, vol. 3(10), pages 1-8, October.
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    1. Matthieu Haudiquet & Julie Bris & Amandine Nucci & Rémy A. Bonnin & Pilar Domingo-Calap & Eduardo P. C. Rocha & Olaya Rendueles, 2024. "Capsules and their traits shape phage susceptibility and plasmid conjugation efficiency," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    2. M Sreepadmanabh & Meenakshi Ganesh & Pratibha Sanjenbam & Christina Kurzthaler & Deepa Agashe & Tapomoy Bhattacharjee, 2024. "Cell shape affects bacterial colony growth under physical confinement," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    3. 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.

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