1. Microbiology and Infectious Disease

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
https://doi.org/10.7554/eLife.45084
Share this article
Cite this article
  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
  2. Download BibTeX
  3. Download .RIS

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.

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.

Metrics

  • 5,750
    views
  • 895
    downloads
  • 112
    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. 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

Share this article

https://doi.org/10.7554/eLife.45084

Categories and tags

Further reading

    1. Immunology and Inflammation
    2. Microbiology and Infectious Disease

    The relationship between gut and nasopharyngeal microbiome composition can predict the severity of COVID-19

    Benita Martin-Castaño, Patricia Diez-Echave ... Julio Galvez
    Research Article

    Coronavirus disease 2019 (COVID-19) is a respiratory illness caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) that displays great variability in clinical phenotype. Many factors have been described to be correlated with its severity, and microbiota could play a key role in the infection, progression, and outcome of the disease. SARS-CoV-2 infection has been associated with nasopharyngeal and gut dysbiosis and higher abundance of opportunistic pathogens. To identify new prognostic markers for the disease, a multicentre prospective observational cohort study was carried out in COVID-19 patients divided into three cohorts based on symptomatology: mild (n = 24), moderate (n = 51), and severe/critical (n = 31). Faecal and nasopharyngeal samples were taken, and the microbiota was analysed. Linear discriminant analysis identified Mycoplasma salivarium, Prevotella dentalis, and Haemophilus parainfluenzae as biomarkers of severe COVID-19 in nasopharyngeal microbiota, while Prevotella bivia and Prevotella timonensis were defined in faecal microbiota. Additionally, a connection between faecal and nasopharyngeal microbiota was identified, with a significant ratio between P. timonensis (faeces) and P. dentalis and M. salivarium (nasopharyngeal) abundances found in critically ill patients. This ratio could serve as a novel prognostic tool for identifying severe COVID-19 cases.

    1. Microbiology and Infectious Disease

    Maintenance of cell wall remodeling and vesicle production are connected in Mycobacterium tuberculosis

    Vivian C Salgueiro-Toledo, Jorge Bertol ... Rafael Prados-Rosales
    Research Article

    Pathogenic and nonpathogenic mycobacteria secrete extracellular vesicles (EVs) under various conditions. EVs produced by Mycobacterium tuberculosis (Mtb) have raised significant interest for their potential in cell communication, nutrient acquisition, and immune evasion. However, the relevance of vesicle secretion during tuberculosis infection remains unknown due to the limited understanding of mycobacterial vesicle biogenesis. We have previously shown that a transposon mutant in the LCP-related gene virR (virRmut) manifested a strong attenuated phenotype during experimental macrophage and murine infections, concomitant to enhanced vesicle release. In this study, we aimed to understand the role of VirR in the vesicle production process in Mtb. We employ genetic, transcriptional, proteomics, ultrastructural, and biochemical methods to investigate the underlying processes explaining the enhanced vesiculogenesis phenomenon observed in the virRmut. Our results establish that VirR is critical to sustain proper cell permeability via regulation of cell envelope remodeling possibly through the interaction with similar cell envelope proteins, which control the link between peptidoglycan and arabinogalactan. These findings advance our understanding of mycobacterial extracellular vesicle biogenesis and suggest that these set of proteins could be attractive targets for therapeutic intervention.