Freeing Aspergillus fumigatus of Polymycovirus Infection Renders It More Resistant to Competition with Pseudomonas aeruginosa Due to Altered Iron-Acquiring Tactics

Abstract

A virus-free (VF) A. fumigatus isolate has been shown to be resistant in competition with Pseudomonas as compared to the isogenic line infected with Aspergillus fumigatus polymycovirus 1 (AfuPmV-1), and this phenotype was apparently related to alterations in iron metabolism. Here we investigated further the mechanisms underpinning this phenotype. The extracellular siderophore profiles of five isogenic VF and virus-infected (VI) strains were sampled at 24, 31, 48, 54, and 72 h in submerged cultures and quantitatively examined by liquid chromatography and mass spectrometry. Intracellular profiles of conidia and cultures at the stationary growth phase were defined. VF A. fumigatus demonstrated the best fitness represented by the fastest onset of its exponential growth when grown on an iron-limited mineral medium. The exponential phase and transitional production phase of the extracellular triacetylfusarinine C (TafC) were achieved at 24 and 31 h, respectively, contrary to VI strains, which acted more slowly. As a result, the TafC reservoir was consumed sooner in the VF strain. Additionally, the VF strain had lower ferricrocin and higher hydroxyferricrocin content in the pellet during the stationary phase. All of these differences were significant (Kruskal–Wallis, p < 0.01). In our study, the siderophore reservoir of a VF strain was consumed sooner, improving the fitness of the VF strain in competition with P. aeruginosa.

ICTV Virus Taxonomy Profile: Polymycoviridae 2022

“…Infection has also been reported to increase sensitivity to antifungals [3] and to the bacterium Pseudomonas aeruginosa [6]. Although the molecular mechanisms underpinning the above phenotypes have not been elucidated, there is evidence that polymycoviruses modulate host carbon, nitrogen and iron metabolism [5, 7]. Finally, polymycoviruses are targeted by the host RNA silencing machinery [8].…”

Molecular characterization and transcriptomic analysis of a novel polymycovirus in the fungus Talaromyces amestolkiae

“…Polymycovirus infections are associated with various alterations in hosts, including changes in pigmentation, sectoring, and decreased host growth and host virulence, as well as increased sporulation, host growth, host virulence, and improved sensitivity to antifungals ( Kanhayuwa et al, 2015 ; Zhai et al, 2016 ; Kotta-Loizou and Coutts, 2017 ; Niu et al, 2018 ; Takahashi-Nakaguchi et al, 2020 ; Filippou et al, 2021 ; Patil et al, 2021 ). In this study, we therefore compared the colony morphology, growth rate, and biomass production of the virus-infected strain LSH3 with those of the virus-cured strain LSH3VF.…”

“…The measurement of mRNA expression patterns at the transcriptome level following infection with polymycoviruses in fungi is vital for understanding the mechanism underlying mycovirus-mediated alterations in pathogenic fungi. Previous studies have demonstrated that polymycovirus infections alter the phenotypes of virus-infected and isogenic virus-free strains ( Kanhayuwa et al, 2015 ; Zhai et al, 2016 ; Kotta-Loizou and Coutts, 2017 ; Niu et al, 2018 ; Takahashi-Nakaguchi et al, 2020 ; Filippou et al, 2021 ; Patil et al, 2021 ). However, there are no reports on the alterations in transcript accumulation in polymycovirus-infected fungi.…”

“…Previous studies have demonstrated the majority of mycoviruses have no obvious effects on their hosts. However, previous studies have demonstrated that infection with polymycoviruses alters various features of hosts ( Kanhayuwa et al, 2015 ; Zhai et al, 2016 ; Jia et al, 2017 ; Kotta-Loizou and Coutts, 2017 ; Niu et al, 2018 ; Takahashi-Nakaguchi et al, 2020 ; Filippou et al, 2021 ; Patil et al, 2021 ). For instance, it has been reported that infection with Aspergillus fumigatus polymycovirus 1 (AfuPmV-1) and Botryoshaeria dothidea polymycovirus 1(BdRV1) alters host virulence ( Kanhayuwa et al, 2015 ; Zhai et al, 2016 ; Takahashi-Nakaguchi et al, 2020 ), which indicates that polymycoviruses can be exploited as potential biocontrol agents of disease-causing fungi.…”

Siderophores: a potential role as a diagnostic for invasive fungal disease

“…Siderophore mobilization was slowed in virus-infected strains, and the consequent drop in Aspergillus fitness impaired its competition for iron with P. aeruginosa . In contrast, due to shifts in iron-acquiring tactics, the reservoir of the siderophore TAFC was consumed more rapidly by the virus-free A. fumigatus strain, which better withstood competition for iron with P. aeruginosa [60]. Third, both small and large molecular weight mammalian siderophores representatives warrant attention due to their involvement in iron scavenging.…”