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Under nonlimiting iron conditions pyocyanin is a major antifungal molecule, and differences between prototypic
Gabriele Sass1, Hasan Nazik1, Paulami Chatterjee1
1California Institute for Medical Research, San Jose, California, USA.
Abstract:
Airways of immunocompromised patients, or individuals with cystic fibrosis (CF), are common ground for Pseudomonas aeruginosa and Aspergillus fumigatus infections. Hence, in such a microenvironment both pathogens compete for resources. While under limiting iron conditions the siderophore pyoverdine is the most effective antifungal P. aeruginosa product, we now provide evidence that under nonlimiting iron conditions P. aeruginosa supernatants lack pyoverdine but still possess considerable antifungal activity. Spectrometric analyses of P. aeruginosa supernatants revealed the presence of phenazines, such as pyocyanin, only under nonlimiting iron conditions. Supernatants of quorum sensing mutants of strain PA14, defective in phenazine production, as well as supernatants of the P. aeruginosa strain PAO1, lacked pyocyanin, and were less inhibitory toward A. fumigatus biofilms under nonlimiting iron conditions. When blood as a natural source of iron was present during P. aeruginosa supernatant production, pyoverdine was absent, and phenazines, including pyocyanin, appeared, resulting in an antifungal effect on A. fumigatus biofilms. Pure pyocyanin reduced A. fumigatus biofilm metabolism. In summary, P. aeruginosa has mechanisms to compete with A. fumigatus under limiting and non-limiting iron conditions, and can switch from iron-denial-based to toxin-based antifungal activity. This has implications for the evolution of the microbiome in clinical settings where the two pathogens co-exist. Important differences in the iron response of P. aeruginosa laboratory strains PA14 and PAO1 were also uncovered.
Insights
Pseudomonas aeruginosa switches from iron competition to toxin production, like pyocyanin, to fight Aspergillus fumigatus infections in immunocompromised patients. This pathogen competition impacts the clinical microbiome.
Area of Science:
- Medical Microbiology
- Pathogen Interaction
- Antimicrobial Resistance
Background:
- Immunocompromised patients and those with cystic fibrosis (CF) are susceptible to co-infections by Pseudomonas aeruginosa and Aspergillus fumigatus.
- These pathogens compete for resources within the host airways, influencing disease progression.
- Pseudomonas aeruginosa employs various strategies to outcompete other microbes.
Purpose of the Study:
- To investigate the antifungal mechanisms of Pseudomonas aeruginosa against Aspergillus fumigatus under varying iron conditions.
- To identify the specific molecules responsible for antifungal activity.
- To understand the implications for microbial competition in clinical settings.
Main Methods:
- Spectrometric analysis of Pseudomonas aeruginosa supernatants.
- Assays evaluating antifungal activity against Aspergillus fumigatus biofilms.
- Comparison of wild-type strains with quorum sensing mutants and different laboratory strains (PA14, PAO1).
- Inclusion of blood to simulate natural iron availability.
Main Results:
- Under iron-limiting conditions, pyoverdine is the primary antifungal product.
- Under non-limiting iron conditions, pyoverdine is absent, but phenazines, such as pyocyanin, are produced and exhibit antifungal activity.
- Phenazine-deficient mutants and strain PAO1 showed reduced antifungal activity.
- The presence of blood (a source of iron) induced phenazine production and antifungal effects.
- Pure pyocyanin demonstrated direct inhibition of Aspergillus fumigatus biofilm metabolism.
Conclusions:
- Pseudomonas aeruginosa utilizes distinct antifungal strategies based on iron availability, switching from iron sequestration to toxin production.
- Phenazines, particularly pyocyanin, are key mediators of antifungal activity under non-limiting iron conditions.
- These findings highlight the dynamic nature of pathogen competition and have implications for understanding airway microbiome evolution in co-infected individuals.
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