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Spatiotemporal development of expanding bacterial colonies driven by emergent mechanical constraints and nutrient gradients

Author

Listed:
  • Harish Kannan

    (San Diego)

  • Hui Sun

    (California State University)

  • Mya Warren

    (San Diego)

  • Tolga Çağlar

    (San Diego
    San Diego)

  • Pantong Yao

    (San Diego)

  • Brian R. Taylor

    (San Diego
    Sandia National Laboratories)

  • Kinshuk Sahu

    (San Diego
    Duke University)

  • Daotong Ge

    (San Diego)

  • Matteo Mori

    (San Diego)

  • David Kleinfeld

    (San Diego
    San Diego)

  • JiaJia Dong

    (Bucknell University)

  • Bo Li

    (San Diego)

  • Terence Hwa

    (San Diego)

Abstract

Bacterial colonies growing on solid surfaces can exhibit robust expansion kinetics, with constant radial growth and saturating vertical expansion, suggesting a common developmental program. Here, we study this process for Escherichia coli cells using a combination of modeling and experiments. We show that linear radial colony expansion is set by the verticalization of interior cells due to mechanical constraints rather than radial nutrient gradients as commonly assumed. In contrast, vertical expansion slows down from an initial linear regime even while radial expansion continues linearly. This vertical slowdown is due to limitation of cell growth caused by vertical nutrient gradients, exacerbated by concurrent oxygen depletion. Starvation in the colony interior results in a distinct death zone which sets in as vertical expansion slows down, with the death zone increasing in size along with the expanding colony. Thus, our study reveals complex heterogeneity within simple monoclonal bacterial colonies, especially along the vertical dimension. The intricate dynamics of such emergent behavior can be understood quantitatively from an interplay of mechanical constraints and nutrient gradients arising from obligatory metabolic processes.

Suggested Citation

  • Harish Kannan & Hui Sun & Mya Warren & Tolga Çağlar & Pantong Yao & Brian R. Taylor & Kinshuk Sahu & Daotong Ge & Matteo Mori & David Kleinfeld & JiaJia Dong & Bo Li & Terence Hwa, 2025. "Spatiotemporal development of expanding bacterial colonies driven by emergent mechanical constraints and nutrient gradients," Nature Communications, Nature, vol. 16(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:16:y:2025:i:1:d:10.1038_s41467-025-60004-z
    DOI: 10.1038/s41467-025-60004-z
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    References listed on IDEAS

    as
    1. Kapil Amarnath & Avaneesh V. Narla & Sammy Pontrelli & Jiajia Dong & Jack Reddan & Brian R. Taylor & Tolga Caglar & Julia Schwartzman & Uwe Sauer & Otto X. Cordero & Terence Hwa, 2023. "Stress-induced metabolic exchanges between complementary bacterial types underly a dynamic mechanism of inter-species stress resistance," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    2. Charles R. Harris & K. Jarrod Millman & Stéfan J. Walt & Ralf Gommers & Pauli Virtanen & David Cournapeau & Eric Wieser & Julian Taylor & Sebastian Berg & Nathaniel J. Smith & Robert Kern & Matti Picu, 2020. "Array programming with NumPy," Nature, Nature, vol. 585(7825), pages 357-362, September.
    3. 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.
    4. Japinder Nijjer & Changhao Li & Qiuting Zhang & Haoran Lu & Sulin Zhang & Jing Yan, 2021. "Mechanical forces drive a reorientation cascade leading to biofilm self-patterning," Nature Communications, Nature, vol. 12(1), pages 1-9, December.
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