Three-dimensional biofilm colony growth supports a mutualism involving matrix and nutrient sharing

  1. Heidi A Arjes
  2. Lisa Willis
  3. Haiwen Gui
  4. Yangbo Xiao
  5. Jason Peters
  6. Carol Gross
  7. Kerwyn Casey Huang  Is a corresponding author
  1. Stanford University, United States
  2. University of Michigan, United States
  3. University of Wisconsin, United States
  4. University of California, San Francisco, United States

Abstract

Life in a three-dimensional biofilm is typical for many bacteria, yet little is known about how strains interact in this context. Here, we created essential-gene CRISPRi knockdown libraries in biofilm-forming Bacillus subtilis and measured competitive fitness during colony co-culture with wild type. Partial knockdown of some translation-related genes reduced growth rates and led to out-competition. Media composition led some knockdowns to compete differentially as biofilm versus non-biofilm colonies. Cells depleted for the alanine racemase AlrA died in monoculture but survived in a biofilm-colony co-culture via nutrient sharing. Rescue was enhanced in biofilm-colony co-culture with a matrix-deficient parent, due to a mutualism involving nutrient and matrix sharing. We identified several examples of mutualism involving matrix sharing that occurred in three-dimensional biofilm colonies but not when cultured in two dimensions. Thus, growth in a three-dimensional colony can promote genetic diversity through sharing of secreted factors and may drive evolution of mutualistic behavior.

Data availability

Related scripts and data deposited in Dryad Digital Repository (doi:10.5061/dryad.79cnp5htm). Remaining data generated or analysed during this study is included in the manuscript and supporting files.

The following data sets were generated

Article and author information

Author details

  1. Heidi A Arjes

    Department of Bioengineering, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Lisa Willis

    Department of Bioengineering, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Haiwen Gui

    Department of Bioengineering, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0564-940X
  4. Yangbo Xiao

    Cell and Developmental Biology, University of Michigan, Ann Arbor, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Jason Peters

    Medical Microbiology and Immunology, University of Wisconsin, Madison, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Carol Gross

    Department of Cell and Tissue Biology, University of California, San Francisco, San Francisco, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5595-9732
  7. Kerwyn Casey Huang

    Department of Bioengineering, Stanford University, Stanford, United States
    For correspondence
    kchuang@stanford.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8043-8138

Funding

Paul G. Allen Foundation (Discovery Center at Stanford on Systems Modeling of Infection)

  • Heidi A Arjes
  • Kerwyn Casey Huang

National Institutes of Health (K22 Award AI137122)

  • Jason Peters

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

Reviewing Editor

  1. Babak Momeni, Boston College, United States

Publication history

  1. Received: October 19, 2020
  2. Accepted: February 15, 2021
  3. Accepted Manuscript published: February 17, 2021 (version 1)
  4. Version of Record published: March 2, 2021 (version 2)
  5. Version of Record updated: March 3, 2021 (version 3)

Copyright

© 2021, Arjes 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.

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  1. Heidi A Arjes
  2. Lisa Willis
  3. Haiwen Gui
  4. Yangbo Xiao
  5. Jason Peters
  6. Carol Gross
  7. Kerwyn Casey Huang
(2021)
Three-dimensional biofilm colony growth supports a mutualism involving matrix and nutrient sharing
eLife 10:e64145.
https://doi.org/10.7554/eLife.64145

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