Interactions of Aspergillus fumigatus and Stenotrophomonas maltophilia in an in vitro Mixed Biofilm Model: Does the Strain Matter?

Melloul, Emmanuel; Roisin, Lolita; Durieux, Marie‐Fleur; Woerther, Paul‐Louis; Jenot, Delphine; Risco, Veronica; Guillot, Jacques; Dannaoui, Éric; Decousser, Jean‐Winoc; Botterel, Françoise

doi:10.3389/fmicb.2018.02850

Cited by 19 publications

(24 citation statements)

References 45 publications

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“…S2). Similar phenotypes have been observed with other compounds of bacterial origin (Garbeva et al, 2014;Aunsbjerg et al, 2015;Torres et al, 2016;Melloul et al, 2018).…”

Section: Dose-inhibition Curve and Stability Of The Active Metabolitesupporting

confidence: 84%

7‐hydroxytropolone is the main metabolite responsible for the fungal antagonism of Pseudomonas donghuensis strain SVBP6

Muzio

Agaras

Masi

et al. 2020

Environmental Microbiology

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Summary Pseudomonas donghuensis strain SVBP6, an isolate from an agricultural plot in Argentina, displays a broad‐spectrum and diffusible antifungal activity, which requires a functional gacS gene but could not be ascribed yet to known secondary metabolites typical of Pseudomonas biocontrol species. Here, we report that Tn5 mutagenesis allowed the identification of a gene cluster involved in both the fungal antagonism and the production of a soluble tropolonoid compound. The ethyl acetate extract from culture supernatant showed a dose‐dependent inhibitory effect against the phytopathogenic fungus Macrophomina phaseolina. The main compound present in the organic extract was identified by spectroscopic and X‐ray analyses as 7‐hydroxytropolone (7HT). Its structure and tautomerism was confirmed by preparing the two key derivatives 2,3‐dimethoxy‐ and 2,7‐dimethoxy‐tropone. 7HT, but not 2,3‐ or 2,7‐dimethoxy‐tropone, mimicked the fungal inhibitory activity of the ethyl acetate extract from culture supernatant. The activity of 7HT, as well as its production, was barely affected by the presence of up to 50 μM added iron (Fe+2). To summarize, P. donghuensis SVBP6 produces 7HT under the positive control of the Gac‐Rsm cascade and is the main active metabolite responsible for the broad‐spectrum inhibition of different phytopathogenic fungi.

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“…S2). Similar phenotypes have been observed with other compounds of bacterial origin (Garbeva et al, 2014;Aunsbjerg et al, 2015;Torres et al, 2016;Melloul et al, 2018).…”

Section: Dose-inhibition Curve and Stability Of The Active Metabolitesupporting

confidence: 84%

7‐hydroxytropolone is the main metabolite responsible for the fungal antagonism of Pseudomonas donghuensis strain SVBP6

Muzio

Agaras

Masi

et al. 2020

Environmental Microbiology

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“…A possible explanation is the modification of fungal phenotype due to the presence of bacteria. In our model, the modification of A. fumigatus cell wall by S. maltophilia (Melloul et al, 2018 ) resembles the one induced by caspofungin or dirhamnolipids (diRhls) secreted by P. aeruginosa which specifically inhibit the fungal 1,3-glucan synthase activity (Briard et al, 2017 ). We suppose that some diRhls-like molecules secreted by S. maltophilia would modify A. fumigatus phenotype similarly to echinocandins.…”

Section: Discussionmentioning

confidence: 94%

“…The higher fitness of SM_CF, in comparison with SM_REF, could account for the larger antibiosis effect of the CF bacterial strain on the CF fungal growth in polymicrobial biofilm. Alike, in our latest study, we showed that S. maltophilia antibiosis on A. fumigatus was dependent on the bacterial fitness (Melloul et al, 2018 ). The fungal biomass of AF_CF + SM_CF biofilm was insufficient to protect the bacteria from levofloxacin, but upon increasing the fungal biomass (using a larger initial inoculum), the polymicrobial biofilm provided SM_CF with a better protection from levofloxacin ( Figure 6 ).…”

Section: Discussionmentioning

confidence: 94%

“…For such, this approach becomes unsuitable against polymicrobial biofilm with sessile cells embedded in ECM. We previously showed A. fumigatus - S. maltophilia interactions in polymicrobial biofilm (Melloul et al, 2016 , 2018 ), and from there we sought to determine whether the antimicrobial response of both pathogens would be modified in their polymicrobial biofilm.…”

Section: Discussionmentioning

confidence: 99%

“…We previously showed that S. maltophilia inhibited A. fumigatus growth and modified hyphae development in a polymicrobial biofilm (Melloul et al, 2016 ), with strain-dependent manner (Melloul et al, 2018 ). The aim of the present study was to investigate the in vitro antimicrobial response of A. fumigatus and S. maltophilia in our polymicrobial biofilm in comparison with monomicrobial biofilm.…”

Section: Introductionmentioning

confidence: 99%

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Modulated Response of Aspergillus fumigatus and Stenotrophomonas maltophilia to Antimicrobial Agents in Polymicrobial Biofilm

Roisin

Melloul

Woerther

et al. 2020

Front. Cell. Infect. Microbiol.

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Introduction: The complexity of biofilms constitutes a therapeutic challenge and the antimicrobial susceptibility of fungal-bacterial biofilms remains poorly studied. The filamentous fungus Aspergillus fumigatus (Af) and the Gram-negative bacillus Stenotrophomonas maltophilia (Sm) can form biofilms and can be co-isolated from the airways of cystic fibrosis (CF) patients. We previously developed an in vitro biofilm model which highlighted the antibiosis effect of Sm on Af, which was dependent on the bacterial fitness. The aim of the present study was to investigate the in vitro susceptibility of Af and Sm in mono- or polymicrobial biofilms to five antimicrobial agents alone and in two-drug combinations. Methods: Af and Sm clinical reference strains and two strains from CF sputa were tested through a planktonic and biofilm approaches. Af, Sm, or Af-Sm susceptibilities to amphotericin B (AMB), itraconazole (ITC), voriconazole (VRC), levofloxacin (LVX), and rifampicin (RFN) were evaluated by conventional planktonic techniques, crystal violet, XTT, qPCR, and viable plate count. Results: Af planktonic cells and biofilms in formation were more susceptible to AMB, ITC, and VRC than Af mature biofilms. Af mature biofilms were susceptible to AMB, but not to ITC and VRC. Based on viable plate count, a lower concentration of LVX and RFN was required to reduce Sm cell numbers on biofilms in formation compared with mature biofilms. The antibiosis effect of Sm on Af growth was more pronounced for the association of CF strains that exhibited a higher fitness than the reference strains. In Af-Sm biofilms, the fungal susceptibility to AMB was increased compared with Af biofilms. In contrast, the bacterial susceptibility to LVX decreased in Af-Sm biofilms and was fungal biomass-dependent. The combination of AMB (64 μg/mL) with LVX or RFN (4 μg/mL) was efficient to impair Af and Sm growth in the polymicrobial biofilm. Conclusion: Sm increased the Af susceptibility to AMB, whereas Af protected Sm from LVX. Interactions between Af and Sm within biofilms modulate susceptibility to antimicrobial agents, opening the way to new antimicrobial strategies in CF patients.

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Clinical characteristics of people with cystic fibrosis and frequent fungal infection

Poore

Meier

Towler

et al. 2021

Pediatric Pulmonology

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Background: Individuals with cystic fibrosis (CF) and fungal airway infection may present with fungal bronchitis, allergic bronchopulmonary aspergillosis (ABPA) or may appear unaffected despite fungal detection. We sought to characterize people with CF with frequent detection of fungi from airway samples and determine clinical outcomes.Methods: This retrospective study included individuals with CF with ≥4 lower airway cultures over a 2-year baseline period and ≥2 years of follow-up. We defined two groups: ≤1 positive fungus culture (rare) or ≥2 positive cultures during baseline (frequent). Clinical characteristics and outcomes were determined.Results: Between 2004 and 2016, 294 individuals met inclusion with 62% classified as rare and 38% as frequent fungi during baseline. Median follow-up was 6 years (range: 2-9 years). Aspergillus fumigatus was the most common fungal species detected. Individuals with frequent fungi were older (13.7 vs. 11.7 years, p = .02) and more likely to have Stenotrophomonas maltophilia (35% vs. 17%, p < .001) at baseline, but did not differ in lung function or ABPA diagnosis. During follow-up, those with frequent fungi were more likely to have chronic Pseudomonas aeruginosa and S. maltophilia. Individuals with ABPA and frequent fungi had the highest rates of co-infection and co-morbidities, and a trend towards more rapid lung function decline.Discussion: Fungal infection in CF was associated with frequent P. aeruginosa and S. maltophilia co-infection even in those without ABPA. Individuals with frequent fungi and ABPA had worse outcomes, highlighting the potential contribution of fungi to CF pulmonary disease.

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Interactions of Aspergillus fumigatus and Stenotrophomonas maltophilia in an in vitro Mixed Biofilm Model: Does the Strain Matter?

Cited by 19 publications

References 45 publications

7‐hydroxytropolone is the main metabolite responsible for the fungal antagonism of Pseudomonas donghuensis strain SVBP6

7‐hydroxytropolone is the main metabolite responsible for the fungal antagonism of Pseudomonas donghuensis strain SVBP6

Modulated Response of Aspergillus fumigatus and Stenotrophomonas maltophilia to Antimicrobial Agents in Polymicrobial Biofilm

Clinical characteristics of people with cystic fibrosis and frequent fungal infection

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