Heterogeneity in surface sensing suggests a division of labor in Pseudomonas aeruginosa populations

  1. Catherine R Armbruster
  2. Calvin K Lee
  3. Jessica Parker-Gilham
  4. Jaime de Anda
  5. Aiguo Xia
  6. Kun Zhao
  7. Boo Shan Tseng
  8. Lucas R Hoffman
  9. Fan Jin
  10. Caroline S Harwood
  11. Gerard C L Wong
  12. Matthew R Parsek  Is a corresponding author
  1. University of Washington, United States
  2. University of California, Los Angeles, United States
  3. University of Science and Technology of China, China
  4. Tianjin University, China
  5. University of Nevada, Las Vegas, United States

Abstract

The second messenger signaling molecule cyclic diguanylate monophosphate (c-di-GMP) drives the transition from planktonic to biofilm growth in many bacterial species. Pseudomonas aeruginosa has two surface sensing systems that produce c-di-GMP in response to surface adherence. The current thinking in the field is that once cells attach to a surface, they uniformly respond with elevated c-di-GMP. Here, we describe how the Wsp system generates heterogeneity in surface sensing, resulting in two physiologically distinct subpopulations of cells. One subpopulation has elevated c-di-GMP and produces biofilm matrix, serving as the founders of initial microcolonies. The other subpopulation has low c-di-GMP and engages in surface motility, allowing for exploration of the surface. We also show that this heterogeneity strongly correlates to surface behavior for descendent cells. Together, our results suggest that after surface attachment, P. aeruginosa engages in a division of labor that persists across generations, accelerating early biofilm formation and surface exploration.

Data availability

Source data files and/or MATLAB code have been provided for Figures 3, 4, and 5.

Article and author information

Author details

  1. Catherine R Armbruster

    Department of Microbiology, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0795-802X
  2. Calvin K Lee

    Department of Bioengineering, University of California, Los Angeles, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Jessica Parker-Gilham

    Department of Microbiology, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Jaime de Anda

    Department of Bioengineering, University of California, Los Angeles, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Aiguo Xia

    Hefei National Laboratory for Physical Sciences at the Microscale, University of Science and Technology of China, Hefei, China
    Competing interests
    The authors declare that no competing interests exist.
  6. Kun Zhao

    Key Laboratory of Systems Bioengineering (Ministry of Education), School of Chemical Engineering and Technology, Tianjin University, Tianjin, China
    Competing interests
    The authors declare that no competing interests exist.
  7. Boo Shan Tseng

    School of Life Sciences, University of Nevada, Las Vegas, Las Vegas, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7563-0232
  8. Lucas R Hoffman

    Department of Microbiology, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Fan Jin

    Hefei National Laboratory for Physical Sciences at the Microscale, University of Science and Technology of China, Hefei, China
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2313-0388
  10. Caroline S Harwood

    Deptartment of Microbiology, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  11. Gerard C L Wong

    Department of Bioengineering, University of California, Los Angeles, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.
  12. Matthew R Parsek

    Department of Microbiology, University of Washington, Seattle, United States
    For correspondence
    parsem@uw.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2932-7966

Funding

National Institutes of Health (T32GM007270)

  • Catherine R Armbruster

National Natural Science Foundation of China (21774117)

  • Fan Jin

National Natural Science Foundation of China (21522406)

  • Fan Jin

Fundamental Research Funds for the Central Universities (WK3450000003)

  • Fan Jin

Charlie Moore Endowed Fellowship

  • Catherine R Armbruster

Army Research Office (W911NF1810254)

  • Matthew R Parsek

National Institutes of Health (K22AI121097)

  • Boo Shan Tseng

National Institute of General Medical Sciences (GM56665)

  • Caroline S Harwood

National Natural Science Foundation of China (21474098)

  • Fan Jin

Fundamental Research Funds for the Central Universities (WK2340000066)

  • Fan Jin

National Institutes of Health (K24HL141669)

  • Lucas R Hoffman

National Institutes of Health (5R01AI077628)

  • Matthew R Parsek

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

Reviewing Editor

  1. Alexandre Persat, EPFL, Switzerland

Publication history

  1. Received: January 11, 2019
  2. Accepted: June 8, 2019
  3. Accepted Manuscript published: June 10, 2019 (version 1)
  4. Version of Record published: July 9, 2019 (version 2)
  5. Version of Record updated: May 26, 2020 (version 3)

Copyright

© 2019, Armbruster 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. Catherine R Armbruster
  2. Calvin K Lee
  3. Jessica Parker-Gilham
  4. Jaime de Anda
  5. Aiguo Xia
  6. Kun Zhao
  7. Boo Shan Tseng
  8. Lucas R Hoffman
  9. Fan Jin
  10. Caroline S Harwood
  11. Gerard C L Wong
  12. Matthew R Parsek
(2019)
Heterogeneity in surface sensing suggests a division of labor in Pseudomonas aeruginosa populations
eLife 8:e45084.
https://doi.org/10.7554/eLife.45084

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