Transcriptomic and genomic changes associated with radioadaptation in Exophiala dermatitidis

Graphical abstract
Highlights • Exophiala dermatitidis is a constitutively melanized yeast that is highly resistant to ionizing radiation. • We analyzed the genome and transcriptomes of E. dermatitidis strains adapted to chronic ionizing radiation exposure. • Radioadaptation induces transcriptomic but few genomic changes in E. dermatitidis. • Radioadaptation also results in an altered transcriptomic response to subsequent ionizing radiation exposure. • This regulation involves downregulation of basal metabolic processes and upregulation of translation and DNA repair.
Melanized fungi have been isolated from some of the harshest radioactive environments, and their ability to thrive in these locations is in part due to the pigment melanin. Melanin imparts a selective advantage to fungi by providing a physical shield, a chemical shield, and possibly a signaling mechanism. In previous work we demonstrated that protracted exposure of the melanized yeast Exophiala dermatitidis to mixed alpha-, beta-, and gamma-emitting radiation resulted in an adapted strain able to mount a unique response to ionizing radiation in the environment in a melanin-dependent fashion. By exploring the genome and transcriptome of this adapted melanized strain relative to a non-irradiated control we determined the altered response was transcriptomic in nature, as whole genome sequencing revealed limited variation. Transcriptomic analysis indicated that of the adapted isolates analyzed, two lineages existed: one like the naïve, non-adapted strain, and one with a unique transcriptomic signature that exhibited downregulation of metabolic processes, and upregulation of translation-associated genes. Analysis of differential gene expression in the adapted strain showed an overlap in response between the control conditions and reactive oxygen species conditions, whereas exposure to an alpha particle source resulted in a robust downregulation of metabolic processes and upregulation of DNA replication and repair genes, and RNA metabolic processes. This suggest previous exposure to radiation primes the fungus to respond to subsequent exposures in a unique way. By exploring this unique response, we have expanded our knowledge of how melanized fungi interact with and respond to ionizing radiation in their environment.