The effects of gamma radiation, UV and visible light on ATP levels in yeast cells depend on cellular melanization

Bryan, Ruth; Jiang, Zewei; Friedman, Matthew; Dadachova, Ekaterina

doi:10.1016/j.funbio.2011.04.003

Cited by 38 publications

(28 citation statements)

References 21 publications

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“…This second possibility seems to support the intriguing hypothesis proposed by Dadachova et al [6] that melanin is able to harness ionizing radiation for metabolic energy. This hypothesis was further confirmed by the recent observation that three forms of radiation (visible light, UV light and gamma radiation) led to a reduction in the ATP levels only in melanized C. neoformans cells [39], which reflected that melanized cells might consume more energy when they were irradiated. The effect of melanin on energy conversion, however, is so subtle that further detailed investigations, such as the quantification of cellular protein and metabolic energy in single cells, are needed to prove this hypothesis.…”

Section: Discussionsupporting

confidence: 58%

Adaptation of the Black Yeast Wangiella dermatitidis to Ionizing Radiation: Molecular and Cellular Mechanisms

et al. 2012

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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.

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Section: Discussionsupporting

confidence: 58%

Adaptation of the Black Yeast Wangiella dermatitidis to Ionizing Radiation: Molecular and Cellular Mechanisms

et al. 2012

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“…Gamma radiation-induced oxidation of melanin resulted in electric current production, especially in the presence of a reducing agent (Turick et al, 2011). The biological significance of this phenomenon is still unclear and some experiments yield contradicting results: gamma radiation, UV, and visible light seem to cause a reduction of ATP levels in melanized cells of the fungus Cryptococcus neoformans (Bryan et al, 2011). …”

Section: Melanin As a Versatile Polymer Of Oligotrophic Fungimentioning

confidence: 99%

Polyextremotolerant black fungi: oligotrophism, adaptive potential, and a link to lichen symbioses

Gostinčar¹,

Muggia²,

Grube³

2012

Front. Microbio.

103

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Black meristematic fungi can survive high doses of radiation and are resistant to desiccation. These adaptations help them to colonize harsh oligotrophic habitats, e.g., on the surface and subsurface of rocks. One of their most characteristic stress-resistance mechanisms is the accumulation of melanin in the cell walls. This, production of other protective molecules and a plastic morphology further contribute to ecological flexibility of black fungi. Increased growth rates of some species after exposure to ionizing radiation even suggest yet unknown mechanisms of energy production. Other unusual metabolic strategies may include harvesting UV or visible light or gaining energy by forming facultative lichen-like associations with algae or cyanobacteria. The latter is not entirely surprising, since certain black fungal lineages are phylogenetically related to clades of lichen-forming fungi. Similar to black fungi, lichen-forming fungi are adapted to growth on exposed surfaces with low availability of nutrients. They also efficiently use protective molecules to tolerate frequent periods of extreme stress. Traits shared by both groups of fungi may have been important in facilitating the evolution and radiation of lichen-symbioses.

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“…The mechanisms for this energy dependence are as yet unknown. Prior reports have shown that ionizing radiation alters the oxidation-reduction behavior of melanin [15], and that melanin affects ATP levels in irradiated cells [12]. Perhaps these interactions between melanin and ionizing photons are photon energy dependent, and we intend to investigate this in future studies.…”

Section: Discussionmentioning

confidence: 91%

“…These findings suggest that the biological effects of ionizing radiation are not limited to cell death, mutagenesis and carcinogenesis [11], but can include growth stimulation of certain life forms. Interactions of ionizing photons with fungal melanin represent an important candidate mechanism for pro-proliferative effects of radiation on melanized fungi [9], [12]–[15].…”

Section: Introductionmentioning

confidence: 99%

Mathematical Modeling Predicts Enhanced Growth of X-Ray Irradiated Pigmented Fungi

et al. 2014

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Ionizing radiation is known for its cytotoxic and mutagenic properties. However, recent evidence suggests that chronic sub-lethal irradiation stimulates the growth of melanin-pigmented (melanized) fungi, supporting the hypothesis that interactions between melanin and ionizing photons generate energy useful for fungal growth, and/or regulate growth-promoting genes. There are no quantitative models of how fungal proliferation is affected by ionizing photon energy, dose rate, and presence versus absence of melanin on the same genetic background. Here we present such a model, which we test using experimental data on melanin-modulated radiation-induced proliferation enhancement in the fungus Cryptococcus neoformans, exposed to two different peak energies (150 and 320 kVp) over a wide range of X-ray dose rates. Our analysis demonstrates that radiation-induced proliferation enhancement in C. neoformans behaves as a binary “on/off” phenomenon, which is triggered by dose rates <0.002 mGy/h, and stays in the “on” position. A competing dose rate-dependent growth inhibition becomes apparent at dose rates >5000 mGy/h. Proliferation enhancement of irradiated cells compared with unirradiated controls occurs at both X-ray peak energies, but its magnitude is modulated by X-ray peak energy and cell melanization. At dose rates <5000 mGy/h, both melanized and non-melanized cells exposed to 150 kVp X-rays, and non-melanized cells exposed to 320 kVp X-rays, all exhibit the same proliferation enhancement: on average, chronic irradiation stimulates each founder cell to produce 100 (95% CI: 83, 116) extra descendants over 48 hours. Interactions between melanin and 320 kVp X-rays result in a significant (2-tailed p-value = 4.8×10−5) additional increase in the number of radiation-induced descendants per founder cell: by 55 (95% CI: 29, 81). These results show that both melanin-dependent and melanin-independent mechanisms are involved in radiation-induced fungal growth enhancement, and implicate direct and/or indirect interactions of melanin with high energy ionizing photons as an important pro-proliferative factor.

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The effects of gamma radiation, UV and visible light on ATP levels in yeast cells depend on cellular melanization

Cited by 38 publications

References 21 publications

Adaptation of the Black Yeast Wangiella dermatitidis to Ionizing Radiation: Molecular and Cellular Mechanisms

Adaptation of the Black Yeast Wangiella dermatitidis to Ionizing Radiation: Molecular and Cellular Mechanisms

Polyextremotolerant black fungi: oligotrophism, adaptive potential, and a link to lichen symbioses

Mathematical Modeling Predicts Enhanced Growth of X-Ray Irradiated Pigmented Fungi

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