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

. 2021 Jun 22 ; 7 (7) : . [epub] 20210622

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid34206595

Grantová podpora
21-17044S Grantová Agentura České Republiky
IGA_PrF_2021_021 Palacky University

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.

Erratum v

PubMed

Zobrazit více v PubMed

Dobiáš R., Havlíček V. Microbial siderophores: Markers of infectious diseases. In: Das S., Das H.R., editors. Microbial and Natural Macromolecules: Synthesis and Applications. Elsevier Academic Press; London, UK: 2021.

Rutsaert L., Steinfort N., Van Hunsel T., Bomans P., Naesens R., Mertes H., Dits H., Van Regenmortel N. COVID-19-associated invasive pulmonary aspergillosis. Ann. Intensive Care. 2020;10:71. doi: 10.1186/s13613-020-00686-4. PubMed DOI PMC

Kotta-Loizou I., Coutts R.H.A. Mycoviruses in aspergilli: A comprehensive review. Front. Microbiol. 2017;8 doi: 10.3389/fmicb.2017.01699. PubMed DOI PMC

Chatterjee P., Sass G., Swietnicki W., Stevens D.A. Review of potential Pseudomonas weaponry, relevant to the Pseudomonas–Aspergillus interplay, for the mycology community. J. Fungi. 2020;6:81. doi: 10.3390/jof6020081. PubMed DOI PMC

Kanhayuwa L., Kotta-Loizou I., Özkan S., Gunning A.P., Coutts R.H.A. A novel mycovirus from Aspergillus fumigatus contains four unique dsRNAs as its genome and is infectious as dsRNA. Proc. Natl. Acad. Sci. USA. 2015;112:9100–9105. doi: 10.1073/pnas.1419225112. PubMed DOI PMC

Nazik H., Kotta-Loizou I., Sass G., Coutts R.H.H., Stevens D.A. Virus infection of Aspergillus fumigatus compromises the fungus in intermicrobial competition. Viruses. 2021;13:686. doi: 10.3390/v13040686. PubMed DOI PMC

Nazik H., Sass G., Deziel E., Stevens D.A. Aspergillus is inhibited by Pseudomonas aeruginosa volatiles. J. Fungi. 2020;6:118. doi: 10.3390/jof6030118. PubMed DOI PMC

Wallner A., Blatzer M., Schrettl M., Sarg B., Lindner H., Haas H. Ferricrocin, a siderophore involved in intra- and transcellular iron distribution in Aspergillus fumigatus. Appl. Environ. Microb. 2009;75:4194–4196. doi: 10.1128/AEM.00479-09. PubMed DOI PMC

Oide S., Berthiller F., Wiesenberger G., Adam G., Turgeon B.G. Individual and combined roles of malonichrome, ferricrocin, and TafC siderophores in Fusarium graminearum pathogenic and sexual development. Front. Microbiol. 2015;5 doi: 10.3389/fmicb.2014.00759. PubMed DOI PMC

Blatzer M., Schrettl M., Sarg B., Lindner H.H., Pfaller K., Haas H. SidL, an Aspergillus fumigatus transacetylase involved in biosynthesis of the siderophores ferricrocin and hydroxyferricrocin. Appl. Environ. Microbiol. 2011;77:4959–4966. doi: 10.1128/AEM.00182-11. PubMed DOI PMC

Kotta-Loizou I. Mycoviruses and their role in fungal pathogenesis. Curr. Opin. Microbiol. 2021 doi: 10.1016/j.mib.2021.05.007. in press. PubMed DOI

Filippou C., Diss R.M., Daudu J.O., Coutts R.H.A., Kotta-Loizou I. The polymycovirus-mediated growth enhancement of the entomopathogenic fungus Beauveria bassiana is dependent on carbon and nitrogen metabolism. Front. Microbiol. 2021;12 doi: 10.3389/fmicb.2021.606366. PubMed DOI PMC

Özkan S., Coutts R.H.A. Aspergillus fumigatus mycovirus causes mild hypervirulent effect on pathogenicity when tested on Galleria mellonella. Fungal Genet. Biol. 2015;76:20–26. doi: 10.1016/j.fgb.2015.01.003. PubMed DOI

Lagashetti A.C., Dufossé L., Singh S.K., Singh P.N. Fungal pigments and their prospects in different industries. Microorganisms. 2019;7:604. doi: 10.3390/microorganisms7120604. PubMed DOI PMC

Heinekamp T., Thywissen A., Macheleidt J., Keller S., Valiante V., Brakhage A. Aspergillus fumigatus melanins: Interference with the host endocytosis pathway and impact on virulence. Front. Microbiol. 2013;3 doi: 10.3389/fmicb.2012.00440. PubMed DOI PMC

Fuller K.K., Cramer R.A., Zegans M.E., Dunlap J.C., Loros J.J. Aspergillus fumigatus photobiology illuminates the marked heterogeneity between isolates. MBio. 2016;7:e01517. doi: 10.1128/mBio.01517-16. PubMed DOI PMC

Takahashi-Nakaguchi A., Shishido E., Yahara M., Urayama S.-I., Ninomiya A., Chiba Y., Sakai K., Hagiwara D., Chibana H., Moriyama H., et al. Phenotypic and molecular biological analysis of polymycovirus AfuPmv-1M from Aspergillus fumigatus: Reduced fungal virulence in a mouse infection model. Front. Microbiol. 2020;11 doi: 10.3389/fmicb.2020.607795. PubMed DOI PMC

Liu G.-L., Chi Z., Wang G.-Y., Wang Z.-P., Li Y., Chi Z.-M. Yeast killer toxins, molecular mechanisms of their action and their applications. Crit. Rev. Biotechnol. 2015;35:222–234. doi: 10.3109/07388551.2013.833582. PubMed DOI

Van de Sande W.W.J., Vonk A.G. Mycovirus therapy for invasive pulmonary aspergillosis? Med. Mycol. 2019;57:S179–S188. doi: 10.1093/mmy/myy073. PubMed DOI

Schmidt F., Lemke P., Esser K. Viral influences on aflatoxin formation by Aspergillus flavus. Appl. Microbiol. Biotechnol. 1986;24:248–252. doi: 10.1007/BF00261546. DOI

Silva V.N., Durigon E.L., Pires M.d.F.C., Lourenço A., Faria M.J.d., Corrêa B. Time course of virus-like particles (VLPs) double-stranded RNA accumulation in toxigenic and non-toxigenic strains of Aspergillus flavus. Braz. J. Microbiol. 2001;32:56–60. doi: 10.1590/S1517-83822001000100013. DOI

Nerva L., Chitarra W., Siciliano I., Gaiotti F., Ciuffo M., Forgia M., Varese G.C., Turina M. Mycoviruses mediate mycotoxin regulation in Aspergillus ochraceus. Environ. Microbiol. 2019;21:1957–1968. doi: 10.1111/1462-2920.14436. PubMed DOI

Takahashi-Nakaguchi A., Shishido E., Yahara M., Urayama S.I., Sakai K., Chibana H., Kamei K., Moriyama H., Gonoi T. Analysis of an intrinsic mycovirus associated with reduced virulence of the human pathogenic fungus Aspergillus fumigatus. Front. Microbiol. 2019;10:3045. doi: 10.3389/fmicb.2019.03045. PubMed DOI PMC

Özkan S., Mohorianu I., Xu P., Dalmay T., Coutts R.H.A. Profile and functional analysis of small RNAs derived from Aspergillus fumigatus infected with double-stranded RNA mycoviruses. BMC Genom. 2017;18:416. doi: 10.1186/s12864-017-3773-8. PubMed DOI PMC

Matthaiou E.I., Sass G., Stevens D.A., Hsu J.L. Iron: An essential nutrient for Aspergillus fumigatus and a fulcrum for pathogenesis. Curr. Opin. Infect. Dis. 2018;31:506–511. doi: 10.1097/QCO.0000000000000487. PubMed DOI PMC

Houšť J., Spížek J., Havlíček V. Antifungal Drugs. Metabolites. 2020;10:106. doi: 10.3390/metabo10030106. PubMed DOI PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

    Možnosti archivace