Heterogeneity in surface sensing suggests a division of labor in Pseudomonas aeruginosa populations
- University of Washington, United States
- University of California, Los Angeles, United States
- University of Science and Technology of China, China
- Tianjin University, China
- 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
Catherine R Armbruster
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
- Alexandre Persat, EPFL, Switzerland
Version history
- Received: January 11, 2019
- Accepted: June 8, 2019
- Accepted Manuscript published: June 10, 2019 (version 1)
- Version of Record published: July 9, 2019 (version 2)
- 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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Heterogeneity in surface sensing suggests a division of labor in Pseudomonas aeruginosa populations
eLife 8:e45084.
https://doi.org/10.7554/eLife.45084
Further reading
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- Microbiology and Infectious Disease
- Structural Biology and Molecular Biophysics
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