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

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

Publication 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

  • 6,814
    Page views
  • 488
    Downloads
  • 26
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, Scopus, PubMed Central.

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

Further reading

    1. Physics of Living Systems
    Patrick Bakenecker et al.
    Research Article

    Little is known about how muscle length affects residual force enhancement (rFE) in humans. We therefore investigated rFE at short, long, and very long muscle lengths within the human quadriceps and patellar tendon (PT) using conventional dynamometry with motion capture (rFETQ) and a new, non-invasive shear-wave tensiometry technique (rFEWS). Eleven healthy male participants performed submaximal (50% max.) EMG-matched fixed-end reference and stretch-hold contractions across these muscle lengths while muscle fascicle length changes of the vastus lateralis (VL) were captured using B-mode ultrasound. We found significant rFETQ at long (7±5%) and very long (12±8%), but not short (2±5%) muscle lengths, whereas rFEWS was only significant at the very long (38±27%), but not short (8±12%) or long (6±10%) muscle lengths. We also found significant relationships between VL fascicle length and rFETQ (r=0.63, p=.001) and rFEWS (r=0.52, p=.017), but relationships were not significant between VL fascicle stretch amplitude and rFETQ (r=0.33, p=.126) or rFEWS (r=0.29, p=.201). PT shear-wave speed-angle relationships did not agree with estimated PT force-angle relationships, which indicates that estimating PT loads from shear-wave tensiometry might be inaccurate. We conclude that increasing muscle length rather than stretch amplitude contributes more to rFE during submaximal voluntary contractions of the human quadriceps.

    1. Cell Biology
    2. Physics of Living Systems
    Sohyeon Park et al.
    Research Article Updated

    In addition to diffusive signals, cells in tissue also communicate via long, thin cellular protrusions, such as airinemes in zebrafish. Before establishing communication, cellular protrusions must find their target cell. Here, we demonstrate that the shapes of airinemes in zebrafish are consistent with a finite persistent random walk model. The probability of contacting the target cell is maximized for a balance between ballistic search (straight) and diffusive search (highly curved, random). We find that the curvature of airinemes in zebrafish, extracted from live-cell microscopy, is approximately the same value as the optimum in the simple persistent random walk model. We also explore the ability of the target cell to infer direction of the airineme’s source, finding that there is a theoretical trade-off between search optimality and directional information. This provides a framework to characterize the shape, and performance objectives, of non-canonical cellular protrusions in general.