Adaptation of the black yeast Wangiella dermatitidis to ionizing radiation: molecular and cellular mechanisms

• Published in: PloS one 2012-11, Vol.7 (11), p.e48674-e48674
• Main Authors: Robertson, Kelly L, Mostaghim, Anahita, Cuomo, Christina A, Soto, Carissa M, Lebedev, Nikolai, Bailey, Robert F, Wang, Zheng
• Format: Article
• Language: English
• Subjects: Adaptation, Physiological - genetics; Adaptation, Physiological - radiation effects; Amino acids; Analysis; Antioxidants; Antioxidants - metabolism; Baking yeast; Biological activity; Biological Transport - genetics; Biological Transport - radiation effects; Biology; Biosynthesis; Carbohydrate metabolism; Carbohydrates; Carotenoids - biosynthesis; Cell cycle; Cell Cycle - genetics; Cell Cycle - radiation effects; Cell division; Cell size; Deoxyribonucleic acid; DNA; DNA biosynthesis; DNA Repair - genetics; DNA Repair - radiation effects; DNA synthesis; Dose-Response Relationship, Radiation; Exophiala - cytology; Exophiala - genetics; Exophiala - physiology; Exophiala - radiation effects; Exposure; Fluidity; Free radicals; Functional analysis; Fungi; Gene expression; Gene Expression Profiling; Gene Expression Regulation, Fungal - radiation effects; Genes; Genes, Fungal - genetics; Genetic engineering; Genomes; Genomics; Ionizing radiation; Irradiation; Laboratories; Melanin; Melanins - metabolism; Membrane fluidity; Membrane Fluidity - genetics; Membrane Fluidity - radiation effects; Metabolism; Microbial Viability - genetics; Microbial Viability - radiation effects; Mutation; Nuclear energy; Nuclear facilities; Nuclear reactors; Oxygen; Radiation; Radiation damage; Radiation dosage; Radiation, Ionizing; Reactive oxygen species; Reactive Oxygen Species - metabolism; Reproducibility of Results; Reverse Transcriptase Polymerase Chain Reaction; Ribonucleic acid; Ribosomes - genetics; Ribosomes - radiation effects; RNA; RNA, Messenger - genetics; RNA, Messenger - metabolism; Saccharomyces cerevisiae; Science; Signal transduction; Studies; Survivability; Transcriptome - genetics; Transcriptome - radiation effects; Up-Regulation - genetics; Up-Regulation - radiation effects; Water - metabolism; Yeast; Yeasts
• ISSN: 1932-6203; 1932-6203
• DOI: 10.1371/journal.pone.0048674

Observations of enhanced growth of melanized fungi under low-dose ionizing radiation in the laboratory and in the damaged Chernobyl nuclear reactor suggest they have adapted the ability to survive or even benefit from exposure to ionizing radiation. However, the cellular and molecular mechanism of fungal responses to such radiation remains poorly understood. Using the black yeast Wangiella dermatitidis as a model, we confirmed that ionizing radiation enhanced cell growth by increasing cell division and cell size. Using RNA-seq technology, we compared the transcriptomic profiles of the wild type and the melanin-deficient wdpks1 mutant under irradiation and non-irradiation conditions. It was found that more than 3000 genes were differentially expressed when these two strains were constantly exposed to a low dose of ionizing radiation and that half were regulated at least two fold in either direction. Functional analysis indicated that many genes for amino acid and carbohydrate metabolism and cell cycle progression were down-regulated and that a number of antioxidant genes and genes affecting membrane fluidity were up-regulated in both irradiated strains. However, the expression of ribosomal biogenesis genes was significantly up-regulated in the irradiated wild-type strain but not in the irradiated wdpks1 mutant, implying that melanin might help to contribute radiation energy for protein translation. Furthermore, we demonstrated that long-term exposure to low doses of radiation significantly increased survivability of both the wild-type and the wdpks1 mutant, which was correlated with reduced levels of reactive oxygen species (ROS), increased production of carotenoid and induced expression of genes encoding translesion DNA synthesis. Our results represent the first functional genomic study of how melanized fungal cells respond to low dose ionizing radiation and provide clues for the identification of biological processes, molecular pathways and individual genes regulated by radiation.