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.
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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.
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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- Genetics and Genomics
- Microbiology and Infectious Disease
Polyamines are biologically ubiquitous cations that bind to nucleic acids, ribosomes, and phospholipids and, thereby, modulate numerous processes, including surface motility in Escherichia coli. We characterized the metabolic pathways that contribute to polyamine-dependent control of surface motility in the commonly used strain W3110 and the transcriptome of a mutant lacking a putrescine synthetic pathway that was required for surface motility. Genetic analysis showed that surface motility required type 1 pili, the simultaneous presence of two independent putrescine anabolic pathways, and modulation by putrescine transport and catabolism. An immunological assay for FimA—the major pili subunit, reverse transcription quantitative PCR of fimA, and transmission electron microscopy confirmed that pili synthesis required putrescine. Comparative RNAseq analysis of a wild type and ΔspeB mutant which exhibits impaired pili synthesis showed that the latter had fewer transcripts for pili structural genes and for fimB which codes for the phase variation recombinase that orients the fim operon promoter in the ON phase, although loss of speB did not affect the promoter orientation. Results from the RNAseq analysis also suggested (a) changes in transcripts for several transcription factor genes that affect fim operon expression, (b) compensatory mechanisms for low putrescine which implies a putrescine homeostatic network, and (c) decreased transcripts of genes for oxidative energy metabolism and iron transport which a previous genetic analysis suggests may be sufficient to account for the pili defect in putrescine synthesis mutants. We conclude that pili synthesis requires putrescine and putrescine concentration is controlled by a complex homeostatic network that includes the genes of oxidative energy metabolism.
