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The Neurotropic Black Yeast Exophiala dermatitidis Induces Neurocytotoxicity in Neuroblastoma Cells and Progressive Cell Death.

ABSTRACT: The neurotropic and extremophilic black yeast Exophiala dermatitidis (Herpotrichellaceae) inhabits diverse indoor environments, in particular bathrooms, steam baths, and dishwashers. Here, we show that the selected strain, EXF-10123, is polymorphic, can grow at 37 °C, is able to assimilate aromatic hydrocarbons (toluene, mineral oil, n-hexadecane), and shows abundant growth with selected neurotransmitters (acetylcholine, gamma-aminobutyric acid, glycine, glutamate, and dopamine) as sole carbon sources. We have for the first time demonstrated the effect of E. dermatitidis on neuroblastoma cell model SH-SY5Y. Aqueous and organic extracts of E. dermatitidis biomass reduced SH-SY5Y viability by 51% and 37%, respectively. Melanized extracellular vesicles (EVs) prepared from this strain reduced viability of the SH-SY5Y to 21%, while non-melanized EVs were considerably less neurotoxic (79% viability). We also demonstrated direct interactions of E. dermatitidis with SH-SY5Y by scanning electron and confocal fluorescence microscopy. The observed invasion and penetration of neuroblastoma cells by E. dermatitidis hyphae presumably causes the degradation of most neuroblastoma cells in only three days. This may represent a so far unknown indirect or direct cause for the development of some neurodegenerative diseases such as Alzheimer's.

SUBMITTER: Lavrin T

PROVIDER: S-EPMC7226985 | biostudies-literature | 2020 Apr

REPOSITORIES: biostudies-literature

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The Neurotropic Black Yeast Exophiala dermatitidis Induces Neurocytotoxicity in Neuroblastoma Cells and Progressive Cell Death.

Lavrin Teja T Konte Tilen T Kostanjšek Rok R Sitar Simona S Sepčič Kristina K Prpar Mihevc Sonja S Žagar Ema E Župunski Vera V Lenassi Metka M Rogelj Boris B Gunde Cimerman Nina N

Cells 20200414 4

The neurotropic and extremophilic black yeast Exophiala dermatitidis (Herpotrichellaceae) inhabits diverse indoor environments, in particular bathrooms, steam baths, and dishwashers. Here, we show that the selected strain, EXF-10123, is polymorphic, can grow at 37 °C, is able to assimilate aromatic hydrocarbons (toluene, mineral oil, n-hexadecane), and shows abundant growth with selected neurotransmitters (acetylcholine, gamma-aminobutyric acid, glycine, glutamate, and dopamine) as ...[more]

PMID: 32295162

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Project description:We investigated the diversity and distribution of fungi in nine different sites inside 30 residential dishwashers. In total, 503 fungal strains were isolated, which belong to 10 genera and 84 species. Irrespective of the sampled site, 83% of the dishwashers were positive for fungi. The most frequent opportunistic pathogenic species were Exophiala dermatitidis, Candida parapsilosis sensu stricto, Exophiala phaeomuriformis, Fusarium dimerum, and the Saprochaete/Magnusiomyces clade. The black yeast E. dermatitidis was detected in 47% of the dishwashers, primarily at the dishwasher rubber seals, at up to 106 CFU/cm2; the other fungi detected were in the range of 102 to 105 CFU/cm2. The other most heavily contaminated dishwasher sites were side nozzles, doors and drains. Only F. dimerum was isolated from washed dishes, while dishwasher waste water contained E. dermatitidis, Exophiala oligosperma and Sarocladium killiense. Plumbing systems supplying water to household appliances represent the most probable route for contamination of dishwashers, as the fungi that represented the core dishwasher mycobiota were also detected in the tap water. Hot aerosols from dishwashers contained the human opportunistic yeast C. parapsilosis, Rhodotorula mucilaginosa and E. dermatitidis (as well as common air-borne genera such as Aspergillus, Penicillium, Trichoderma and Cladosporium). Comparison of fungal contamination of kitchens without and with dishwashers revealed that virtually all were contaminated with fungi. In both cases, the most contaminated sites were the kitchen drain and the dish drying rack. The most important difference was higher prevalence of black yeasts (E. dermatitidis in particular) in kitchens with dishwashers. In kitchens without dishwashers, C. parapsilosis strongly prevailed with negligible occurrence of E. dermatitidis. F. dimerum was isolated only from kitchens with dishwashers, while Saprochaete/Magnusiomyces isolates were only found within dishwashers. We conclude that dishwashers represent a reservoir of enriched opportunistic pathogenic species that can spread from the dishwasher into the indoor biome.

Project description:Melanized fungi thrive in extreme environments, including those with high levels of ionizing radiation. To understand the role that melanin may play in ionizing radiation resistance, we previously performed an adaptive laboratory evolution experiment in which we used melanized and non-melanized strains of the yeast Exophiala dermatitidis to develop evolved lines that exhibit increased ionizing radiation resistance. In this study, we further characterized these evolved lines by analyzing their response to ionizing radiation at the transcriptomic and genomic levels. RNA sequencing showed that the response to gamma irradiation in both unevolved and evolved strains involved the induction of DNA repair genes. However, in the melanized lines evolved to exhibit increased ionizing radiation resistance, DNA-associated genes were constitutively expressed, compared to their expression levels in wild type. Non-melanized lines that were evolved to be resistant to ionizing radiation, on the other hand, exhibited upregulation of genes involved in redox homeostasis, even under non-irradiated conditions. Additionally, we characterized genome-wide mutations induced by a single high dose of gamma radiation in these evolved lines and observed that while melanin did not directly affect survival after gamma radiation exposure, melanized lines that evolved to exhibit higher ionizing radiation resistance experienced fewer mutations, whereas similarly evolved, non-melanized lines accumulated more mutations, similar to the parent, non-melanized strain. These results underscore the complex yet measurable role of melanin in the response to ionizing radiation in E. dermatitidis. Furthermore, this study enhances our understanding of the mechanisms underlying the recovery after ionizing radiation exposure in melanized fungi and offers insights into the potential therapeutic applications of melanin and other redox molecules for protecting against ionizing radiation-induced damage. IMPORTANCE Ionizing radiation poses a significant threat to living organisms and human health, given its destructive nature and widespread use in fields such as medicine and the potential for nuclear disasters. Melanized fungi exhibit remarkable survival capabilities, enduring doses up to 1,000-fold higher than mammals. Through adaptive laboratory evolution, we validated the protective role of constitutive upregulation of DNA repair genes in the black yeast Exophiala dermatitidis, enhancing survival after radiation exposure. Surprisingly, we found that evolved strains lacking melanin still achieved high levels of radioresistance. Our study unveiled the significance of robust activation and enhancement of redox homeostasis, as evidenced by the profound transcriptional changes and increased accumulation of mutations, in substantially improving ionizing radiation resistance in the absence of melanin. These findings underscore the delicate balance between DNA repair and redox homeostasis for an organism's ability to endure and recover from radiation exposure.

Dataset Information

The Neurotropic Black Yeast Exophiala dermatitidis Induces Neurocytotoxicity in Neuroblastoma Cells and Progressive Cell Death.

Publications

The Neurotropic Black Yeast <i>Exophiala dermatitidis</i> Induces Neurocytotoxicity in Neuroblastoma Cells and Progressive Cell Death.

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