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  4. The loss of the pyoverdine secondary receptor in Pseudomonas aeruginosa results in a fitter strain suitable for population invasion
 
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The loss of the pyoverdine secondary receptor in Pseudomonas aeruginosa results in a fitter strain suitable for population invasion
File(s)
Pyo-Supp info_201111.pdf (3.65 MB)
Supporting information
Pyo-Dyn_201111_symplectic.pdf (2.71 MB)
Accepted version
Author(s)
González, Jaime
Salvador, Manuel
Özkaya, Özhan
Spick, Matt
Reid, Kate
more
Type
Journal Article
Abstract
The rapid emergence of antibiotic resistant bacterial pathogens constitutes a critical problem in healthcare and requires the development of novel treatments. Potential strategies include the exploitation of microbial social interactions based on public goods, which are produced at a fitness cost by cooperative microorganisms, but can be exploited by cheaters that do not produce these goods. Cheater invasion has been proposed as a ‘Trojan horse’ approach to infiltrate pathogen populations with strains deploying built-in weaknesses (e.g., sensitiveness to antibiotics). However, previous attempts have been often unsuccessful because population invasion by cheaters was prevented by various mechanisms including the presence of spatial structure (e.g., growth in biofilms), which limits the diffusion and exploitation of public goods. Here we followed an alternative approach and examined whether the manipulation of public good uptake and not its production could result in potential ‘Trojan horses’ suitable for population invasion. We focused on the siderophore pyoverdine produced by the human pathogen Pseudomonas aeruginosa MPAO1 and manipulated its uptake by deleting and/or overexpressing the pyoverdine primary (FpvA) and secondary (FpvB) receptors. We found that receptor synthesis feeds back on pyoverdine production and uptake rates, which led to strains with altered pyoverdine-associated costs and benefits. Moreover, we found that the receptor FpvB was advantageous under iron-limited conditions but revealed hidden costs in the presence of an antibiotic stressor (gentamicin). As a consequence, FpvB mutants became the fittest strain under gentamicin exposure, displacing the wildtype in liquid cultures, and in biofilms and during infections of the wax moth larvae Galleria mellonella, which both represent structured environments. Our findings reveal that an evolutionary trade-off associated with the costs and benefits of a versatile pyoverdine uptake strategy can be harnessed for devising a Trojan-horse candidate for medical interventions.
Date Issued
2020-12-15
Date Acceptance
2020-11-20
Citation
The ISME Journal: multidisciplinary journal of microbial ecology, 2020, 15, pp.1330-1343
URI
http://hdl.handle.net/10044/1/83877
URL
https://www.nature.com/articles/s41396-020-00853-2
DOI
https://www.dx.doi.org/10.1038/s41396-020-00853-2
ISSN
1751-7362
Publisher
Springer Nature [academic journals on nature.com]
Start Page
1330
End Page
1343
Journal / Book Title
The ISME Journal: multidisciplinary journal of microbial ecology
Volume
15
Copyright Statement
© The Author(s), under exclusive licence to International Society for Microbial Ecology 2020. The final publication is available at Springer via https://doi.org/10.1038/s41396-020-00853-2
Sponsor
Biotechnology and Biological Sciences Research Council
Identifier
https://www.nature.com/articles/s41396-020-00853-2
Grant Number
BB/T011289/1
Subjects
Science & Technology
Life Sciences & Biomedicine
Ecology
Microbiology
Environmental Sciences & Ecology
FERRIPYOVERDINE RECEPTOR
SIGMA-FACTOR
COOPERATION
VIRULENCE
EVOLUTION
FPVA
05 Environmental Sciences
06 Biological Sciences
10 Technology
Microbiology
Publication Status
Published
Date Publish Online
2020-12-15
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