Large-scale orientational order in bacterial colonies during inward growth

  1. Mustafa Basaran
  2. Y Ilker Yaman
  3. Tevfik Can Yüce
  4. Roman Vetter
  5. Askin Kocabas  Is a corresponding author
  1. Koç University, Turkey
  2. ETH Zurich, Switzerland

Abstract

During colony growth, complex interactions regulate the bacterial orientation, leading to the formation of large-scale ordered structures, including topological defects, microdomains, and branches. These structures may benefit bacterial strains, providing invasive advantages during colonization. Active matter dynamics of growing colonies drives the emergence of these ordered structures. However, additional biomechanical factors also play a significant role during this process. Here we show that the velocity profile of growing colonies creates strong radial orientation during inward growth when crowded populations invade a closed area. During this process, growth geometry sets virtual confinement and dictates the velocity profile. Herein, flow-induced alignment and torque balance on the rod-shaped bacteria result in a new stable orientational equilibrium in the radial direction. Our analysis revealed that the dynamics of these radially oriented structures also known as aster defects, depend on bacterial length and can promote the survival of the longest bacteria around localized nutritional hot spots. The present results indicate a new mechanism underlying structural order and provide mechanistic insights into the dynamics of bacterial growth on complex surfaces.

Data availability

The critical experimental data generated or analyzed during this study are provided as supporting video files.Code Availability:The codes utilized previously published open-source software from https://depts.washington.edu/soslab/gro/ and are made available on GitHub (https://github.com/mustafa-basaran/Large_Scale_Orientation_Bacteria).

Article and author information

Author details

  1. Mustafa Basaran

    Department of Physics, Koç University, Istanbul, Turkey
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1895-254X
  2. Y Ilker Yaman

    Department of Physics, Koç University, Istanbul, Turkey
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4094-616X
  3. Tevfik Can Yüce

    Department of Physics, Koç University, Istanbul, Turkey
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6888-2690
  4. Roman Vetter

    Department of Biosystems Science and Engineering, ETH Zurich, Basel, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2901-7036
  5. Askin Kocabas

    Department of Physics, Koç University, Istanbul, Turkey
    For correspondence
    akocabas@ku.edu.tr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6930-1202

Funding

EMBO Installation Grant (IG 3275)

  • Askin Kocabas

BAGEP (young investigator award)

  • Askin Kocabas

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

© 2022, Basaran et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 1,790
    views
  • 317
    downloads
  • 22
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Mustafa Basaran
  2. Y Ilker Yaman
  3. Tevfik Can Yüce
  4. Roman Vetter
  5. Askin Kocabas
(2022)
Large-scale orientational order in bacterial colonies during inward growth
eLife 11:e72187.
https://doi.org/10.7554/eLife.72187

Share this article

https://doi.org/10.7554/eLife.72187

Further reading

    1. Neuroscience
    2. Physics of Living Systems
    Iksoo Chang, Taegon Chung, Sangyeol Kim
    Research Article

    Recent experimental studies showed that electrically coupled neural networks like in mammalian inferior olive nucleus generate synchronized rhythmic activity by the subthreshold sinusoidal-like oscillations of the membrane voltage. Understanding the basic mechanism and its implication of such phenomena in the nervous system bears fundamental importance and requires preemptively the connectome information of a given nervous system. Inspired by these necessities of developing a theoretical and computational model to this end and, however, in the absence of connectome information for the inferior olive nucleus, here we investigated interference phenomena of the subthreshold oscillations in the reference system Caenorhabditis elegans for which the structural anatomical connectome was completely known recently. We evaluated how strongly the sinusoidal wave was transmitted between arbitrary two cells in the model network. The region of cell-pairs that are good at transmitting waves changed according to the wavenumber of the wave, for which we named a wavenumber-dependent transmission map. Also, we unraveled that (1) the transmission of all cell-pairs disappeared beyond a threshold wavenumber, (2) long distance and regular patterned transmission existed in the body-wall muscles part of the model network, and (3) major hub cell-pairs of the transmission were identified for many wavenumber conditions. A theoretical and computational model presented in this study provided fundamental insight for understanding how the multi-path constructive/destructive interference of the subthreshold oscillations propagating on electrically coupled neural networks could generate wavenumber-dependent synchronized rhythmic activity.

    1. Developmental Biology
    2. Physics of Living Systems
    Fridtjof Brauns, Nikolas H Claussen ... Boris I Shraiman
    Research Article

    Shape changes of epithelia during animal development, such as convergent extension, are achieved through the concerted mechanical activity of individual cells. While much is known about the corresponding large-scale tissue flow and its genetic drivers, fundamental questions regarding local control of contractile activity on the cellular scale and its embryo-scale coordination remain open. To address these questions, we develop a quantitative, model-based analysis framework to relate cell geometry to local tension in recently obtained time-lapse imaging data of gastrulating Drosophila embryos. This analysis systematically decomposes cell shape changes and T1 rearrangements into internally driven, active, and externally driven, passive, contributions. Our analysis provides evidence that germ band extension is driven by active T1 processes that self-organize through positive feedback acting on tensions. More generally, our findings suggest that epithelial convergent extension results from the controlled transformation of internal force balance geometry which combines the effects of bottom-up local self-organization with the top-down, embryo-scale regulation by gene expression.