Biophysics: Common concepts for bacterial collectives

The expansion of bacterial swarms and the spreading of biofilms can be described by a unified biophysical theory that involves both active and passive processes.
  1. Hannah Jeckel
  2. Noémie Matthey
  3. Knut Drescher  Is a corresponding author
  1. Max Planck Institute for Terrestrial Microbiology, Germany
  2. Philipps-Universität Marburg, Germany
  3. Swiss Federal Institute of Technology Lausanne, Switzerland

A long-held paradigm in microbiology has been that bacteria are unicellular creatures, and that the effect of a large population of bacteria is the sum of the effects of all the individual cells. However, this view of bacterial life has changed fundamentally over the last few decades (Parsek and Greenberg, 2005), and it is now clear that bacteria can communicate with each other via small molecules and coordinate their behavior. Bacteria can, for example, form swarms as they move across a surface to explore their surroundings and search for nutrients, and they can also grow into multicellular structured communities termed biofilms, which provide various benefits to the cells, such as an improved tolerance to antibiotics. The study of behaviors that only occur in groups of bacterial cells now represents an exciting frontier in microbiology research. It has also caught the attention of physicists and mathematicians who are interested in identifying the quantitative principles that underpin multicellular organization.

Bacterial swarms and biofilms are typically viewed as two fundamentally different phenotypes because they are regulated by different genes, are caused by different cellular processes, and display obvious differences at the microscopic scale: swarms involve highly motile cells that move collectively (Darnton et al., 2010; Kearns, 2010; Zhang et al., 2010), whereas biofilms consist primarily of non-motile cells that are held together by an extracellular matrix (Flemming et al., 2016). However, at a more macroscopic level of description, there are also some similarities: swarms and biofilms both involve the spreading of bacterial communities with low height-to-width ratios over an agar substrate, and both consist of multiple different components (cells, matrix and fluid).

Biofilms and swarms are similar in many ways.

Illustration showing a biofilm (right) made of bacteria (green shapes) and extracellular matrix (gray) looking at itself in a mirror and seeing a swarm of bacteria, where different colors indicate groups of cells that are moving together in the same direction. Srinivasan et al. have shown that the spreading dynamics of swarms and biofilms at the macroscopic level can be described by a single biophysical theory. Illustration by Noémie Matthey.

Now, in eLife, inspired by these similarities, Siddarth Srinivasan, Nadir Kaplan and L Mahadevan of Harvard University report that they have developed a unifying theory that can describe the expansion of both swarms and biofilms (Srinivasan et al., 2019). Srinivasan et al. realized that the spread of both systems can be viewed as involving just two phases of matter: an active, growing phase of bacteria and/or matrix components, and a passive phase of fluid which can move from the substrate to the system and back. Based on this insight, Srinivasan et al. formulated a two-phase model which establishes a general set of coupled equations that include the effects of growth, fluid fluxes, nutrients and diffusion, with the specific components of the equations being adapted for swarms and biofilms. They found that despite the differences between swarms and biofilms, their model could quantitatively predict the dynamics of how they expand.

The model neglects biological details such as gene regulation and the actual mechanisms of cell-cell interactions. Instead, it relies only on growth and physical effects. A remarkable conclusion of the fact that such a theory quantitatively reproduces the bacterial spreading dynamics is that, on the macroscopic scale, physical interactions between the two phases and the agar substrate together with cellular growth are the driving factors of colony expansion.

Similarly, studies focusing on the microscopic dynamics of swarms and biofilms have identified a unifying concept for cell-cell interactions: physical interactions (such as collisions between cells) determine both the architecture of a biofilm and the collective movement of a swarm (Hartmann et al., 2019; Jeckel et al., 2019; Trejo et al., 2013; Wensink et al., 2012). This suggests that while biological mechanisms determine the physiological state of cells and the type of community they build, physical interactions can in certain conditions predict the structure of this community and the dynamics of the cells within the community both microscopically and macroscopically.

Taken together with previous work on the similarities between swarms and biofilms at microscopic length scales (Hartmann et al., 2019; Jeckel et al., 2019), the results of Srinivasan et al. are another step forward in efforts to identify general principles that are able to explain the behavior of bacterial communities across a range of length scales and across species.


Article and author information

Author details

  1. Hannah Jeckel

    Hannah Jeckel is in the Max Planck Institute for Terrestrial Microbiology, and the Department of Physics, Philipps-Universität Marburg, Marburg, Germany

    Competing interests
    No competing interests declared
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7080-4907
  2. Noémie Matthey

    Noémie Matthey is in the School of Life Sciences, Swiss Federal Institute of Technology Lausanne, Lausanne, Switzerland

    Competing interests
    No competing interests declared
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6056-2756
  3. Knut Drescher

    Knut Drescher is in the Max Planck Institute for Terrestrial Microbiology, and the Department of Physics, Philipps-Universität Marburg, Marburg, Germany

    For correspondence
    Competing interests
    No competing interests declared
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7340-2444

Publication history

  1. Version of Record published: April 30, 2019 (version 1)


© 2019, Jeckel et al.

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


  • 2,220
    Page views
  • 273
  • 2

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

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. Hannah Jeckel
  2. Noémie Matthey
  3. Knut Drescher
Biophysics: Common concepts for bacterial collectives
eLife 8:e47019.

Further reading

    1. Physics of Living Systems
    Steffen Geisel et al.
    Research Article

    Biofilms, bacterial communities of cells encased by a self-produced matrix, exhibit a variety of three-dimensional structures. Specifically, channel networks formed within the bulk of the biofilm have been identified to play an important role in the colonies' viability by promoting the transport of nutrients and chemicals. Here, we study channel formation and focus on the role of the adhesion of the biofilm matrix to the substrate in Pseudomonas aeruginosa biofilms grown under constant flow in microfluidic channels. We perform phase contrast and confocal laser scanning microscopy to examine the development of the biofilm structure as a function of the substrates' surface energy. The formation of the wrinkles and folds is triggered by a mechanical buckling instability, controlled by biofilm growth rate and the film’s adhesion to the substrate. The three-dimensional folding gives rise to hollow channels that rapidly increase the effective volume occupied by the biofilm and facilitate bacterial movement inside them. The experiments and analysis on mechanical instabilities for the relevant case of a bacterial biofilm grown during flow enable us to predict and control the biofilm morphology.

    1. Microbiology and Infectious Disease
    2. Physics of Living Systems
    Urszula Łapińska et al.
    Research Article

    Phenotypic variations between individual microbial cells play a key role in the resistance of microbial pathogens to pharmacotherapies. Nevertheless, little is known about cell individuality in antibiotic accumulation. Here, we hypothesise that phenotypic diversification can be driven by fundamental cell-to-cell differences in drug transport rates. To test this hypothesis, we employed microfluidics-based single-cell microscopy, libraries of fluorescent antibiotic probes and mathematical modelling. This approach allowed us to rapidly identify phenotypic variants that avoid antibiotic accumulation within populations of Escherichia coli, Pseudomonas aeruginosa, Burkholderia cenocepacia, and Staphylococcus aureus. Crucially, we found that fast growing phenotypic variants avoid macrolide accumulation and survive treatment without genetic mutations. These findings are in contrast with the current consensus that cellular dormancy and slow metabolism underlie bacterial survival to antibiotics. Our results also show that fast growing variants display significantly higher expression of ribosomal promoters before drug treatment compared to slow growing variants. Drug-free active ribosomes facilitate essential cellular processes in these fast-growing variants, including efflux that can reduce macrolide accumulation. We used this new knowledge to eradicate variants that displayed low antibiotic accumulation through the chemical manipulation of their outer membrane inspiring new avenues to overcome current antibiotic treatment failures.