1. Physics of Living Systems

Surface-to-volume scaling and aspect ratio preservation in rod-shaped bacteria

  1. Nikola Ojkic
  2. Diana Serbanescu
  3. Shiladitya Banerjee  Is a corresponding author
  1. University College London, United Kingdom
https://doi.org/10.7554/eLife.47033
Share this article
Cite this article
  1. Nikola Ojkic
  2. Diana Serbanescu
  3. Shiladitya Banerjee
(2019)
Surface-to-volume scaling and aspect ratio preservation in rod-shaped bacteria
eLife 8:e47033.
https://doi.org/10.7554/eLife.47033
  2. Download BibTeX
  3. Download .RIS

Abstract

Rod-shaped bacterial cells can readily adapt their lengths and widths in response to environmental changes. While many recent studies have focused on the mechanisms underlying bacterial cell size control, it remains largely unknown how the coupling between cell length and width results in robust control of rod-like bacterial shapes. In this study we uncover a conserved surface-to-volume scaling relation in Escherichia coli and other rod-shaped bacteria, resulting from the preservation of cell aspect ratio. To explain the mechanistic origin of aspect-ratio control, we propose a quantitative model for the coupling between bacterial cell elongation and the accumulation of an essential division protein, FtsZ. This model reveals a mechanism for why bacterial aspect ratio is independent of cell size and growth conditions, and predicts cell morphological changes in response to nutrient perturbations, antibiotics, MreB or FtsZ depletion, in quantitative agreement with experimental data.

Data availability

All data generated or analysed during this study are referenced in the manuscript and supporting files.

The following previously published data sets were used

Article and author information

Author details

  1. Nikola Ojkic

    Department of Physics and Astronomy, University College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.

  2. Diana Serbanescu

    Department of Physics and Astronomy, University College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.

  3. Shiladitya Banerjee

    Department of Physics and Astronomy, University College London, London, United Kingdom
    For correspondence
    shiladitya.banerjee@ucl.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8000-2556

Funding

Royal Society (URF/R1/180187)

  • Shiladitya Banerjee

Royal Society (RGF/EA/181044)

  • Shiladitya Banerjee

Engineering and Physical Sciences Research Council (EP/R029822/1)

  • Shiladitya Banerjee

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

Reviewing Editor

  1. Raymond E Goldstein, University of Cambridge, United Kingdom

Version history

  1. Received: March 20, 2019
  2. Accepted: August 28, 2019
  3. Accepted Manuscript published: August 28, 2019 (version 1)
  4. Version of Record published: September 12, 2019 (version 2)

Copyright

© 2019, Ojkic 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

  • 9,297
    views
  • 648
    downloads
  • 43
    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. Nikola Ojkic
  2. Diana Serbanescu
  3. Shiladitya Banerjee
(2019)
Surface-to-volume scaling and aspect ratio preservation in rod-shaped bacteria
eLife 8:e47033.
https://doi.org/10.7554/eLife.47033

Share this article

https://doi.org/10.7554/eLife.47033

Categories and tags

Research organisms

Further reading

    1. Physics of Living Systems

    Substrate evaporation drives collective construction in termites

    Giulio Facchini, Alann Rathery ... Andrea Perna
    Research Article

    Termites build complex nests which are an impressive example of self-organization. We know that the coordinated actions involved in the construction of these nests by multiple individuals are primarily mediated by signals and cues embedded in the structure of the nest itself. However, to date there is still no scientific consensus about the nature of the stimuli that guide termite construction, and how they are sensed by termites. In order to address these questions, we studied the early building behavior of Coptotermes gestroi termites in artificial arenas, decorated with topographic cues to stimulate construction. Pellet collections were evenly distributed across the experimental setup, compatible with a collection mechanism that is not affected by local topography, but only by the distribution of termite occupancy (termites pick pellets at the positions where they are). Conversely, pellet depositions were concentrated at locations of high surface curvature and at the boundaries between different types of substrate. The single feature shared by all pellet deposition regions was that they correspond to local maxima in the evaporation flux. We can show analytically and we confirm experimentally that evaporation flux is directly proportional to the local curvature of nest surfaces. Taken together, our results indicate that surface curvature is sufficient to organize termite building activity and that termites likely sense curvature indirectly through substrate evaporation. Our findings reconcile the apparently discordant results of previous studies.

    1. Microbiology and Infectious Disease
    2. Physics of Living Systems

    Yeast cell responses and survival during periodic osmotic stress are controlled by glucose availability

    Fabien Duveau, Céline Cordier ... Pascal Hersen
    Research Article

    Natural environments of living organisms are often dynamic and multifactorial, with multiple parameters fluctuating over time. To better understand how cells respond to dynamically interacting factors, we quantified the effects of dual fluctuations of osmotic stress and glucose deprivation on yeast cells using microfluidics and time-lapse microscopy. Strikingly, we observed that cell proliferation, survival, and signaling depend on the phasing of the two periodic stresses. Cells divided faster, survived longer, and showed decreased transcriptional response when fluctuations of hyperosmotic stress and glucose deprivation occurred in phase than when the two stresses occurred alternatively. Therefore, glucose availability regulates yeast responses to dynamic osmotic stress, showcasing the key role of metabolic fluctuations in cellular responses to dynamic stress. We also found that mutants with impaired osmotic stress response were better adapted to alternating stresses than wild-type cells, showing that genetic mechanisms of adaptation to a persistent stress factor can be detrimental under dynamically interacting conditions.

    1. Physics of Living Systems

    Hydrodynamics and multiscale order in confluent epithelia

    Josep-Maria Armengol-Collado, Livio Nicola Carenza, Luca Giomi
    Research Article Updated

    We formulate a hydrodynamic theory of confluent epithelia: i.e. monolayers of epithelial cells adhering to each other without gaps. Taking advantage of recent progresses toward establishing a general hydrodynamic theory of p-atic liquid crystals, we demonstrate that collectively migrating epithelia feature both nematic (i.e. p = 2) and hexatic (i.e. p = 6) orders, with the former being dominant at large and the latter at small length scales. Such a remarkable multiscale liquid crystal order leaves a distinct signature in the system’s structure factor, which exhibits two different power-law scaling regimes, reflecting both the hexagonal geometry of small cells clusters and the uniaxial structure of the global cellular flow. We support these analytical predictions with two different cell-resolved models of epithelia – i.e. the self-propelled Voronoi model and the multiphase field model – and highlight how momentum dissipation and noise influence the range of fluctuations at small length scales, thereby affecting the degree of cooperativity between cells. Our construction provides a theoretical framework to conceptualize the recent observation of multiscale order in layers of Madin–Darby canine kidney cells and pave the way for further theoretical developments.