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Phenotypic Characterization and Comparative Genomics of the Melanin-Producing Yeast Exophiala lecanii-corni Reveals a Distinct Stress Tolerance Profile and Reduced Ribosomal Genetic Content.

ABSTRACT: The black yeast Exophiala lecanii-corni of the order Chaetothyriales is notable for its ability to produce abundant quantities of DHN-melanin. While many other Exophiala species are frequent causal agents of human infection, E. lecanii-corni CBS 102400 lacks the thermotolerance requirements that enable pathogenicity, making it appealing for use in targeted functional studies and biotechnological applications. Here, we report the stress tolerance characteristics of E. lecanii-corni, with an emphasis on the influence of melanin on its resistance to various forms of stress. We find that E. lecanii-corni has a distinct stress tolerance profile that includes variation in resistance to temperature, osmotic, and oxidative stress relative to the extremophilic and pathogenic black yeast Exophiala dermatitidis. Notably, the presence of melanin substantially impacts stress resistance in E. lecanii-corni, while this was not found to be the case in E. dermatitidis. The cellular context, therefore, influences the role of melanin in stress protection. In addition, we present a detailed analysis of the E. lecanii-corni genome, revealing key differences in functional genetic content relative to other ascomycetous species, including a significant decrease in abundance of genes encoding ribosomal proteins. In all, this study provides insight into how genetics and physiology may underlie stress tolerance and enhances understanding of the genetic diversity of black yeasts.

SUBMITTER: Romsdahl J

PROVIDER: S-EPMC8709033 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Fungi can tolerate extremely high doses of ionizing radiation compared with most other eukaryotes, a phenomenon encompassing both the recovery from acute exposure and the growth of melanized fungi in chronically contaminated environments such as nuclear disaster sites. This observation has led to the use of fungi in radiobiology studies, with the goal of finding novel resistance mechanisms. However, it is still not entirely clear what underlies this phenomenon, as genetic studies have not pinpointed unique responses to ionizing radiation in the most resistant fungi. Additionally, little work has been done examining how fungi (other than budding yeast) respond to irradiation by ionizing particles (e.g., protons, α-particles), although particle irradiation may cause distinct cellular damage, and is more relevant for human risks. To address this paucity of data, in this study we have characterized the phenotypic and transcriptomic response of the highly radioresistant yeast Exophiala dermatitidis to irradiation by three separate ionizing radiation sources: protons, deuterons, and α-particles. The experiment was performed with both melanized and non-melanized strains of E. dermatitidis, to determine the effect of this pigment on the response. No significant difference in survival was observed between these strains under any condition, suggesting that melanin does not impart protection to acute irradiation to these particles. The transcriptomic response during recovery to particle exposure was similar to that observed after γ-irradiation, with DNA repair and replication genes upregulated, and genes involved in translation and ribosomal biogenesis being heavily repressed, indicating an attenuation of cell growth. However, a comparison of global gene expression showed clear clustering of particle and γ-radiation groups. The response elicited by particle irradiation was, in total, more complex. Compared to the γ-associated response, particle irradiation resulted in greater changes in gene expression, a more diverse set of differentially expressed genes, and a significant induction of gene categories such as autophagy and protein catabolism. Additionally, analysis of individual particle responses resulted in identification of the first unique expression signatures and individual genes for each particle type that could be used as radionuclide discrimination markers.

Dataset Information

Phenotypic Characterization and Comparative Genomics of the Melanin-Producing Yeast Exophiala lecanii-corni Reveals a Distinct Stress Tolerance Profile and Reduced Ribosomal Genetic Content.

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