Radioadapted Wangiella dermatitidis senses radiation in its environment in a melanin-dependent fashion
Graphical abstract
Introduction
Fungi grow and thrive in some of the most extreme environments, both on earth and in space, and experience exposure to varied stresses. The presence of the pigment melanin in black fungi imparts an apparent selective advantage in these extreme locations, as a higher incidence of melanized fungi are observed in the Chernobyl atomic energy station (ChAES), can survive the Antarctic desserts, and are resistant to simulated space conditions (Onofri et al., 2008, Selbmann et al., 2015, Dighton et al., 2008). The advantage melanin imparts is through 1) its ability to provide physical and chemical protection from ionizing radiation, through Compton scattering and free-radical scavenging (Revskaya et al., 2012, Malo and Dadachova, 2019, Schweitzer et al., 2009), 2) the structural integrity it provides improving the ability to withstand sparsely and densely ionizing radiation (Malo et al., 2017), and 3) its radiation sensitive electronic properties positioning it for a role in a yet undefined signaling mechanism (Dadachova et al., 2007, Turick et al., 2011, Kim et al., 2017). These advantages manifest in a biological response in the form of increased growth, metabolism, and tropism in response to radiation (Robertson et al., 2012, Dadachova et al., 2007, Zhdanova et al., 2003, Zhdanova et al., 2004, Tugay et al., 2006).
The goal of this study was to develop radioadapted fungal strains in the laboratory through a protracted exposure to Actinium-225 (225Ac) which is a mixed alpha (α)-, beta (β)-, and gamma (γ)-emitter. Such strains would be more sensitive to low levels of radiation, and would possibly develop the ability to discern between qualitatively different forms of radiation. An additional goal was to separate the ability to sense radiation from the response to direct irradiation which would provide a mechanistic explanation of the tropic nature observed in isolates from the ChAES (Zhdanova et al., 2004).
We completed our study with the constitutively melanized pathogenic fungus Wangiella dermatitidis as a model (Szaniszlo, 2002). Previous studies have established that this strain shows stimulation of growth in response to radiation (Dadachova et al., 2007), both by increasing cell number and size, but also by altering DNA synthesis and response to reactive oxygen species (Robertson et al., 2012).
Section snippets
Growth conditions
The wild type (WT) strain of W. dermatitidis 8656 (ATCC34100, Exophiala dermatitidis CBS 525.76) and mutant strain, wdpks1 (Feng et al., 2001) used in this study were kind gifts from Dr. P. Szaniszlo (The University of Texas, Austin TX). Both strains were cultured in a modified Sabouraud Emmons Broth (SAB; 2 % dextrose, 1 % peptone) at 34 °C with shaking at 200 rpm until they reached an approximate concentration of 106 cells/ml. Cells were then transferred into minimal media (MM; 2 g/L KH2PO4,
Results and discussion
In this study we used a naturally pigmented wild type (WT) strain of W. dermatitidis that produces 1,8-dihydroxynaphthalene (1,8-DHN) melanin under normal growth conditions and deposits it in the cell wall (Geis et al., 1984). We used wdpks1as a non-melanized control, a strain with a disruption of the polyketide synthase 1 gene (Feng et al., 2001). While this mutant is still capable of producing melanin, the amounts of melanin produced are severely reduced and the dark pigmentation observed in
Conclusion
The results generated in this study have helped to elucidate the radio-stimulatory response in previously exposed fungus to indirect interaction with ionizing radiation. It has been demonstrated that fungal cultures isolated from sites contaminated with radioisotopes present radiotropic properties (Tugay et al., 2006) (Zhdanova et al., 2003, Zhdanova et al., 2004). These strains grow towards a radiation source while not being directly exposed to the radiation. In these studies the ionizing
Acknowledgements
This research was funded by the Defense Threat Reduction Agency grant HDTRA1-17-1-0020. This article is part of the Fungal Adaptation to Hostile Challenges special issue for the third International Symposium on Fungal Stress (ISFUS), which is supported by the Fundação de Amparo à Pesquisa do Estado de São Paulo grant 2018/20571-6 and the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior grant 88881.289327/2018-01.
References (24)
- et al.
Spectroelectrochemical reverse engineering DemonstratesThat melanin’s redox and radical scavenging activities are linked
Biomacromolecules
(2017) - et al.
Resistance of Antarctic black fungi and cryptoendolithic communities to simulated space and Martian conditions
Stud. Mycol.
(2008) Molecular genetic studies of the model dematiaceous pathogen Wangiella dermatitidis
Int. J. Med. Microbiol.
(2002)- et al.
Gamma radiation interacts with melanin to alter its oxidation-reduction potential and results in electric current production
Bioelectrochemistry
(2011) - et al.
Accumulation of radionuclides from radioactive substrata by some micromycetes
J. Environ. Radioact.
(2003) - et al.
Ionizing radiation attracts soil fungi
Mycol. Res.
(2004) Natural background radiation
- et al.
Ionizing radiation changes the electronic properties of melanin and enhances the growth of melanized fungi
PLoS One
(2007) - et al.
Fungi and ionizing radiation from radionuclides
FEMS Microbiol. Lett.
(2008) - et al.
Molecular cloning and characterization of WdPKS1, a gene involved in dihydroxynaphthalene melanin biosynthesis and virulence in Wangiella (Exophiala) dermatitidis
Infect. Immun.
Pentaketide metabolites of melanin synthesis in the dematiaceous fungus Wangiella dermatitidis
Arch. Microbiol.
Cited by (6)
Transcriptomic and genomic changes associated with radioadaptation in Exophiala dermatitidis
2021, Computational and Structural Biotechnology JournalCitation Excerpt :Another notable variant was an intergenic SNP, identified in 2 WTA and both pksA radioadapted strains, that was approximately 1.4 kbps away from HMPREF1120_07545, which encodes a protein with similarity to redox-sensitive bicupin YhaK. We previously demonstrated that radioadaptation resulted in the increased colony growth in radioadapted strains in comparison with naïve strains when both strains were exposed to ionizing radiation from an α particle emitting Polonium-210 source, as well as increased electron transfer capacity, and improved resistance to the toxic effects of ROS [30]. To understand what was occurring to produce this altered biological response, we set out to characterize the transcriptome of the adapted, melanized strain (WTA) relative to the naïve, melanized strain (WT).
The Third International Symposium on Fungal Stress – ISFUS
2020, Fungal BiologyCitation Excerpt :A special issue has been published after each ISFUS that featured articles related to fungal stress primarily from researchers who presented at that ISFUS: for ISFUS-2014 in Current Genetics (Rangel et al., 2015a, 2015b), and for ISFUS-2017 in Fungal Biology, by Elsevier on behalf of the British Mycological Society (Alder-Rangel et al., 2018). After the success of that special issue, Fungal Biology agreed to publish this special issue arising from ISFUS-2019, which is titled “Fungal Adaptation to Hostile Challenges” focused on cellular biology, ecology, photobiology, environment, agricultural, industrial, and medical mycology in the context of fungal stress (Acheampong et al., 2019; Antal et al., 2019; Araújo et al., 2019; Brown et al., 2020; Dias et al., 2018; Fomina et al., 2019; Harari et al., 2019; Kelliher et al., 2019; Király et al., 2019; Laz et al., 2019; Malo et al., 2019; Medina et al., 2020; Mendoza-Martínez et al., 2019; Rodrigues et al., 2019; Schumacher and Gorbushina, 2020; Sethiya et al., 2019; Tagua et al., 2019; Walker and Basso, 2019; Yu et al., 2020; Yuan et al., 2019), and several other manuscripts under review, for a total of 31 articles in this special edition. Although the Symposium started Monday, May 20, most international speakers arrived in Brazil on Saturday, May 18 to have time to recuperate from long flights.
Enlisting electrochemistry to reveal melanin's redox-related properties
2024, Materials AdvancesMitigating effects of sublethal and lethal whole-body gamma irradiation in a mouse model with soluble melanin
2022, Journal of Radiological Protection