Biology Faculty Articles

Document Type

Article

Publication Date

9-28-2021

Publication Title

mSystems

Keywords

Pseudomonas aeruginosa, pyoverdine, biofilms, disturbance, mathematical modeling, virulence factors

ISSN

2379-5077

Volume

6

Issue/No.

5

First Page

e00961-21

Abstract

Understanding the environmental factors that affect the production of virulence factors has major implications in evolution and medicine. While spatial structure is important in virulence factor production, observations of this relationship have occurred in undisturbed or continuously disturbed environments. However, natural environments are subject to periodic fluctuations, including changes in physical forces, which could alter the spatial structure of bacterial populations and impact virulence factor production. Using Pseudomonas aeruginosa PA14, we periodically applied a physical force to biofilms and examined production of pyoverdine. Intermediate frequencies of disturbance reduced the amount of pyoverdine produced compared to undisturbed or frequently disturbed conditions. To explore the generality of this finding, we examined how an intermediate disturbance frequency affected pyoverdine production in 21 different strains of P. aeruginosa. Periodic disturbance increased, decreased, or did not change the amount of pyoverdine produced relative to undisturbed populations. Mathematical modeling predicts that interactions between pyoverdine synthesis rate and biofilm density determine the amount of pyoverdine synthesized. When the pyoverdine synthesis rates are high, depletion of the biofilm due to disturbance reduces the accumulation of pyoverdine. At intermediate synthesis rates, production of pyoverdine increases during disturbance as bacteria dispersed into the planktonic state enjoy increased growth and pyoverdine production rates. At low synthesis rates, disturbance does not alter the amount of pyoverdine produced since disturbance-driven access to nutrients does not augment pyoverdine synthesis. Our results suggest that environmental conditions shape robustness in the production of virulence factors and may lead to novel approaches to treat infections.

Comments

Research was sponsored by the Army Research Office and was accomplished under grant W911NF-18-1-0443. The views and conclusions contained in this document are those of the authors and should not be interpreted as representing the official policies, either expressed or implied, of the Army Research Office or the U.S. Government. The U.S. Government is authorized to reproduce and distribute reprints for Government purposes notwithstanding any copyright notation here.

Additional Comments

© 2021 Quinn et al.

Creative Commons License

Creative Commons Attribution 4.0 International License
This work is licensed under a Creative Commons Attribution 4.0 International License.

Supplemental_Fig.S1.jpg (534 kB)
Supplemental Figure 1

Supplemental_Fig.S2.jpg (632 kB)
Supplemental Figure 2

Supplemental_Fig.S3.jpg (743 kB)
Supplemental Figure 3

Supplemental_Fig.S4.jpg (376 kB)
Supplemental Figure 4

Supplemental_Fig.S5.jpg (547 kB)
Supplemental Figure 5

Supplemental_Fig.S6.jpg (491 kB)
Supplemental Figure 6

Supplemental_Fig.S7.jpg (531 kB)
Supplemental Figure 7

msystems.00961-21-st002.docx (14 kB)
Supplementary Data

msystems.00961-21-st002.docx (14 kB)
Supplementary Data

msystems.00961-21-st003.docx (21 kB)
Supplementary Data

ORCID ID

0000-0001-7405-427X, 0000-0003-2744-7390, 0000-0002-4807-4979

DOI

10.1128/mSystems.00961-21

Peer Reviewed

Included in

Biology Commons

Share

COinS
 
 

To view the content in your browser, please download Adobe Reader or, alternately,
you may Download the file to your hard drive.

NOTE: The latest versions of Adobe Reader do not support viewing PDF files within Firefox on Mac OS and if you are using a modern (Intel) Mac, there is no official plugin for viewing PDF files within the browser window.