Abstract
Pseudomonas aeruginosa and Aspergillus fumigatus infections frequently co-localize in lungs of immunocompromised patients and individuals with cystic fibrosis (CF). The antifungal activity of P. aeruginosa has been described for its filtrates. Pyoverdine and pyocyanin are the principal antifungal P. aeruginosa molecules active against A. fumigatus biofilm metabolism present in iron-limited or iron-replete planktonic P. aeruginosa culture filtrates, respectively. Using various P. aeruginosa laboratory wild-type strains (PA14, PAO1, PAK), we found antifungal activity against Aspergillus colonies on agar. Comparing 36 PA14 and 7 PAO1 mutants, we found that mutants lacking both major siderophores, pyoverdine and pyochelin, display higher antifungal activity on agar than their wild types, while quorum sensing mutants lost antifungal activity. Addition of ferric iron, but not calcium or magnesium, reduced the antifungal effects of P. aeruginosa on agar, whereas iron-poor agar enhanced antifungal effects. Antifungal activity on agar was mediated by PQS and HHQ, via MvfR. Among the MvfR downstream factors, rhamnolipids and elastase were produced in larger quantities by pyoverdine–pyochelin double mutants and showed antifungal activity on agar. In summary, antifungal factors produced by P. aeruginosa on agar differ from those produced by bacteria grown in liquid cultures, are dependent on quorum sensing, and are downregulated by the availability of ferric iron. Rhamnolipids and elastase seem to be major mediators of Pseudomonas’ antifungal activity on a solid surface.
Highlights
IntroductionP. aeruginosa and A. fumigatus are frequently co-inhabiting airways of cystic fibrosis (CF) individuals and lungs of immune-compromised persons (Smyth and Hurley, 2010; de Bentzmann and Plésiat, 2011; Walsh and Stevens, 2011; Folkesson et al, 2012; Williams and Davies, 2012; Sabino et al, 2015) and have been associated with deterioration of lung function in CF (Schønheyder et al, 1985; Forsyth et al, 1988; Nicolai et al, 1990; Shoseyov et al, 2006; Amin et al, 2010; de Boer et al, 2011; Coughlan et al, 2012; Fillaux et al, 2012; Speirs et al, 2012; Williams and Davies, 2012; Baxter et al, 2013; Ramsey et al, 2014; Mirković et al, 2016).Pseudomonas Antifungal Activity on AgarP. aeruginosa and A. fumigatus have developed strategies to compete
Under iron-limiting conditions, planktonic filtrates of P. aeruginosa mutants defective in production of the major siderophore pyoverdine inhibit
Increased effects of coculture with PA14pvdD-/pchE- compared to wild type on A. fumigatus growth were visible morphologically
Summary
P. aeruginosa and A. fumigatus are frequently co-inhabiting airways of cystic fibrosis (CF) individuals and lungs of immune-compromised persons (Smyth and Hurley, 2010; de Bentzmann and Plésiat, 2011; Walsh and Stevens, 2011; Folkesson et al, 2012; Williams and Davies, 2012; Sabino et al, 2015) and have been associated with deterioration of lung function in CF (Schønheyder et al, 1985; Forsyth et al, 1988; Nicolai et al, 1990; Shoseyov et al, 2006; Amin et al, 2010; de Boer et al, 2011; Coughlan et al, 2012; Fillaux et al, 2012; Speirs et al, 2012; Williams and Davies, 2012; Baxter et al, 2013; Ramsey et al, 2014; Mirković et al, 2016).Pseudomonas Antifungal Activity on AgarP. aeruginosa and A. fumigatus have developed strategies to compete. The most prominent antifungal P. aeruginosa molecule is pyoverdine (Sass et al, 2017), a siderophore whose main role is to compete for Fe+3 in more stringent iron-limiting conditions. Pyochelin (Cornelis and Dingemans, 2013) is the secondary main siderophore, which has 100-fold less binding affinity for Fe+3 compared to pyoverdine; it acquires Fe+3 when iron is less limited and has reactive oxygen species-generating capabilities, which can be useful in intermicrobial competition. These Fe+3 uptake mechanisms rely on the Fe+3 uptake regulator protein, Fur (Pasqua et al, 2017)
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