Chronic gamma radiation resistance in fungi correlates with resistance to chromium and elevated temperatures, but not with resistance to acute irradiation
Abstract
Abstract Exposure to chronic ionizing radiation (CIR) from nuclear power plant accidents, acts of terrorism, and space exploration poses serious threats to humans. Fungi are a group of highly radiation-resistant eukaryotes, and an understanding of fungal CIR resistance mechanisms holds the prospect of protecting humans. We compared the abilities of 95 wild-type yeast and dimorphic fungal isolates, representing diverse Ascomycota and Basidiomycota , to resist exposure to five environmentally-relevant stressors: CIR (long-duration growth under 36 Gy/h) and acute (10 kGy/h) ionizing radiation (IR), heavy metals (chromium, mercury), elevated temperature (up to 50 °C), and low pH (2.3). To quantify associations between resistances to CIR and these other stressors, we used correlation analysis, logistic regression with multi-model inference, and customized machine learning. The results suggest that resistance to acute IR in fungi is not strongly correlated with the ability of a given fungal isolate to grow under CIR. Instead, the strongest predictors of CIR resistance in fungi were resistance to chromium (III) and to elevated temperature. These results suggest fundamental differences between the mechanisms of resistance to chronic and acute radiation. Convergent evolution towards radioresistance among genetically distinct groups of organisms is considered here.
- Publication Date:
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1619547
- Resource Type:
- Published Article
- Journal Name:
- Scientific Reports
- Additional Journal Information:
- Journal Name: Scientific Reports Journal Volume: 9 Journal Issue: 1; Journal ID: ISSN 2045-2322
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United Kingdom
- Language:
- English
Citation Formats
Shuryak, Igor, Tkavc, Rok, Matrosova, Vera Y., Volpe, Robert P., Grichenko, Olga, Klimenkova, Polina, Conze, Isabel H., Balygina, Irina A., Gaidamakova, Elena K., and Daly, Michael J. Chronic gamma radiation resistance in fungi correlates with resistance to chromium and elevated temperatures, but not with resistance to acute irradiation. United Kingdom: N. p., 2019.
Web. doi:10.1038/s41598-019-47007-9.
Shuryak, Igor, Tkavc, Rok, Matrosova, Vera Y., Volpe, Robert P., Grichenko, Olga, Klimenkova, Polina, Conze, Isabel H., Balygina, Irina A., Gaidamakova, Elena K., & Daly, Michael J. Chronic gamma radiation resistance in fungi correlates with resistance to chromium and elevated temperatures, but not with resistance to acute irradiation. United Kingdom. https://doi.org/10.1038/s41598-019-47007-9
Shuryak, Igor, Tkavc, Rok, Matrosova, Vera Y., Volpe, Robert P., Grichenko, Olga, Klimenkova, Polina, Conze, Isabel H., Balygina, Irina A., Gaidamakova, Elena K., and Daly, Michael J. Tue .
"Chronic gamma radiation resistance in fungi correlates with resistance to chromium and elevated temperatures, but not with resistance to acute irradiation". United Kingdom. https://doi.org/10.1038/s41598-019-47007-9.
@article{osti_1619547,
title = {Chronic gamma radiation resistance in fungi correlates with resistance to chromium and elevated temperatures, but not with resistance to acute irradiation},
author = {Shuryak, Igor and Tkavc, Rok and Matrosova, Vera Y. and Volpe, Robert P. and Grichenko, Olga and Klimenkova, Polina and Conze, Isabel H. and Balygina, Irina A. and Gaidamakova, Elena K. and Daly, Michael J.},
abstractNote = {Abstract Exposure to chronic ionizing radiation (CIR) from nuclear power plant accidents, acts of terrorism, and space exploration poses serious threats to humans. Fungi are a group of highly radiation-resistant eukaryotes, and an understanding of fungal CIR resistance mechanisms holds the prospect of protecting humans. We compared the abilities of 95 wild-type yeast and dimorphic fungal isolates, representing diverse Ascomycota and Basidiomycota , to resist exposure to five environmentally-relevant stressors: CIR (long-duration growth under 36 Gy/h) and acute (10 kGy/h) ionizing radiation (IR), heavy metals (chromium, mercury), elevated temperature (up to 50 °C), and low pH (2.3). To quantify associations between resistances to CIR and these other stressors, we used correlation analysis, logistic regression with multi-model inference, and customized machine learning. The results suggest that resistance to acute IR in fungi is not strongly correlated with the ability of a given fungal isolate to grow under CIR. Instead, the strongest predictors of CIR resistance in fungi were resistance to chromium (III) and to elevated temperature. These results suggest fundamental differences between the mechanisms of resistance to chronic and acute radiation. Convergent evolution towards radioresistance among genetically distinct groups of organisms is considered here.},
doi = {10.1038/s41598-019-47007-9},
journal = {Scientific Reports},
number = 1,
volume = 9,
place = {United Kingdom},
year = {2019},
month = {8}
}
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Works referenced in this record:
Modeling species richness and abundance of phytoplankton and zooplankton in radioactively contaminated water bodies
journal, December 2018
- Shuryak, Igor
- Journal of Environmental Radioactivity, Vol. 192
Modulation of oxidative responses by a virulent isolate of Colletotrichum fructicola in apple leaves
journal, October 2016
- Velho, Aline Cristina; Rockenbach, Mathias F.; Mondino, Pedro
- Fungal Biology, Vol. 120, Issue 10
Microbial cells can cooperate to resist high-level chronic ionizing radiation
journal, December 2017
- Shuryak, Igor; Matrosova, Vera Y.; Gaidamakova, Elena K.
- PLOS ONE, Vol. 12, Issue 12
Advantages of Synthetic Noise and Machine Learning for Analyzing Radioecological Data Sets
journal, January 2017
- Shuryak, Igor
- PLOS ONE, Vol. 12, Issue 1
A Major Role for Nonenzymatic Antioxidant Processes in the Radioresistance of Halobacterium salinarum
journal, January 2011
- Robinson, C. K.; Webb, K.; Kaur, A.
- Journal of Bacteriology, Vol. 193, Issue 7
Protein Oxidation Implicated as the Primary Determinant of Bacterial Radioresistance
journal, March 2007
- Daly, Michael J.; Gaidamakova, Elena K.; Matrosova, Vera Y.
- PLoS Biology, Vol. 5, Issue 4, Article No. e92
Across the tree of life, radiation resistance is governed by antioxidant Mn 2+ , gauged by paramagnetic resonance
journal, October 2017
- Sharma, Ajay; Gaidamakova, Elena K.; Grichenko, Olga
- Proceedings of the National Academy of Sciences, Vol. 114, Issue 44
Multiple-Stress Tolerance of Ionizing Radiation-Resistant Bacterial Isolates Obtained from Various Habitats: Correlation Between Stresses
journal, December 2006
- Shukla, Manish; Chaturvedi, Ruchi; Tamhane, Dhruti
- Current Microbiology, Vol. 54, Issue 2
Extreme resistance of bdelloid rotifers to ionizing radiation
journal, March 2008
- Gladyshev, Eugene; Meselson, Matthew
- Proceedings of the National Academy of Sciences, Vol. 105, Issue 13
Small-Molecule Antioxidant Proteome-Shields in Deinococcus radiodurans
journal, September 2010
- Daly, Michael J.; Gaidamakova, Elena K.; Matrosova, Vera Y.
- PLoS ONE, Vol. 5, Issue 9, Article No. e12570
Chromium enhances insulin responsiveness via AMPK
journal, May 2014
- Hoffman, Nolan J.; Penque, Brent A.; Habegger, Kirk M.
- The Journal of Nutritional Biochemistry, Vol. 25, Issue 5
Transcription Factors That Defend Bacteria Against Reactive Oxygen Species
journal, October 2015
- Imlay, James A.
- Annual Review of Microbiology, Vol. 69, Issue 1
A new perspective on radiation resistance based on Deinococcus radiodurans
journal, January 2009
- Daly, Michael J.
- Nature Reviews Microbiology, Vol. 7, Issue 3
Manganese Complexes: Diverse Metabolic Routes to Oxidative Stress Resistance in Prokaryotes and Yeast
journal, September 2013
- Culotta, Valeria C.; Daly, Michael J.
- Antioxidants & Redox Signaling, Vol. 19, Issue 9
Probing in vivo Mn2+ speciation and oxidative stress resistance in yeast cells with electron-nuclear double resonance spectroscopy
journal, August 2010
- McNaughton, R. L.; Reddi, A. R.; Clement, M. H. S.
- Proceedings of the National Academy of Sciences, Vol. 107, Issue 35
Collinearity: a review of methods to deal with it and a simulation study evaluating their performance
journal, May 2012
- Dormann, Carsten F.; Elith, Jane; Bacher, Sven
- Ecography, Vol. 36, Issue 1
Unusual radioresistance of nitrogen-fixing cultures of Anabaena strains
journal, August 2010
- Singh, Harinder; Fernandes, Tonina; Apte, Shree Kumar
- Journal of Biosciences, Vol. 35, Issue 3
Experimental Evolution of Extreme Resistance to Ionizing Radiation in Escherichia coli after 50 Cycles of Selection
journal, January 2019
- Bruckbauer, Steven T.; Trimarco, Joseph D.; Martin, Joel
- Journal of Bacteriology, Vol. 201, Issue 8
Radioresistance of Deinococcus radiodurans: functions necessary to survive ionizing radiation are also necessary to survive prolonged desiccation.
journal, January 1996
- Mattimore, V.; Battista, J. R.
- Journal of bacteriology, Vol. 178, Issue 3
A Novel ATM/TP53/p21-Mediated Checkpoint Only Activated by Chronic γ-Irradiation
journal, August 2014
- Cao, Lili; Kawai, Hidehiko; Sasatani, Megumi
- PLoS ONE, Vol. 9, Issue 8
Review of microbial resistance to chronic ionizing radiation exposure under environmental conditions
journal, January 2019
- Shuryak, Igor
- Journal of Environmental Radioactivity, Vol. 196
Ionizing radiation attracts soil fungi
journal, September 2004
- Zhdanova, Nelli N.; Tugay, Tatyana; Dighton, John
- Mycological Research, Vol. 108, Issue 9
A model for repair of radiation-induced DNA double-strand breaks in the extreme radiophileDeinococcus radiodurans
journal, May 1995
- Minton, Kenneth W.; Daly, Michael J.
- BioEssays, Vol. 17, Issue 5
The role of Chromium III in the organism and its possible use in diabetes and obesity treatment
journal, January 2014
- Lewicki, Sławomir; Zdanowski, Robert; Krzyżowska, Małgorzata
- Annals of Agricultural and Environmental Medicine, Vol. 21, Issue 2
Effects of intracellular Mn on the radiation resistance of the halophilic archaeon Halobacterium salinarum
journal, March 2013
- Webb, Kimberly M.; Yu, Jerry; Robinson, Courtney K.
- Extremophiles, Vol. 17, Issue 3
P values are only an index to evidence: 20th- vs. 21st-century statistical science
journal, March 2014
- Burnham, K. P.; Anderson, D. R.
- Ecology, Vol. 95, Issue 3
Stress adaptation in a pathogenic fungus
journal, December 2013
- Brown, A. J. P.; Budge, S.; Kaloriti, D.
- Journal of Experimental Biology, Vol. 217, Issue 1
Prospects for Fungal Bioremediation of Acidic Radioactive Waste Sites: Characterization and Genome Sequence of Rhodotorula taiwanensis MD1149
journal, January 2018
- Tkavc, Rok; Matrosova, Vera Y.; Grichenko, Olga E.
- Frontiers in Microbiology, Vol. 8
Accumulation of Mn(II) in Deinococcus radiodurans Facilitates Gamma-Radiation Resistance
journal, November 2004
- Daly, M. J.; Gaidamakova, E. K.; Matrosova, V. Y.
- Science, Vol. 306, Issue 5698, p. 1025-1028
Protein oxidation: key to bacterial desiccation resistance?
journal, February 2008
- Fredrickson, James K.; Li, Shu-mei W.; Gaidamakova, Elena K.
- The ISME Journal, Vol. 2, Issue 4
Preserving Immunogenicity of Lethally Irradiated Viral and Bacterial Vaccine Epitopes Using a Radio- Protective Mn2+-Peptide Complex from Deinococcus
journal, July 2012
- Gaidamakova, Elena K.; Myles, Ian A.; McDaniel, Dennis P.
- Cell Host & Microbe, Vol. 12, Issue 1, p. 117-124
High-quality genome sequence of the radioresistant bacterium Deinococcus ficus KS 0460
journal, July 2017
- Matrosova, Vera Y.; Gaidamakova, Elena K.; Makarova, Kira S.
- Standards in Genomic Sciences, Vol. 12, Issue 1
MDP: A Deinococcus Mn2+-Decapeptide Complex Protects Mice from Ionizing Radiation
journal, August 2016
- Gupta, Paridhi; Gayen, Manoshi; Smith, Joan T.
- PLOS ONE, Vol. 11, Issue 8
Microbial response to environmental stresses: from fundamental mechanisms to practical applications
journal, April 2017
- Guan, Ningzi; Li, Jianghua; Shin, Hyun-dong
- Applied Microbiology and Biotechnology, Vol. 101, Issue 10
The biology of habitat dominance; can microbes behave as weeds?: The biology of habitat dominance
journal, January 2013
- Cray, Jonathan A.; Bell, Andrew N. W.; Bhaganna, Prashanth
- Microbial Biotechnology, Vol. 6, Issue 5
Dose-Rate Effects in Mammalian Cells in Culture: III. Comparison of Cell Killing and Cell Proliferation during Continuous Irradiation for Six Different Cell Lines
journal, September 1979
- Mitchell, J. B.; Bedford, J. S.; Bailey, S. M.
- Radiation Research, Vol. 79, Issue 3
Fungal invasion of the rhizosphere microbiome
journal, May 2015
- Chapelle, Emilie; Mendes, Rodrigo; Bakker, Peter A. HM
- The ISME Journal, Vol. 10, Issue 1
Deinococcus geothermalis: The Pool of Extreme Radiation Resistance Genes Shrinks
journal, September 2007
- Makarova, Kira S.; Omelchenko, Marina V.; Gaidamakova, Elena K.
- PLoS ONE, Vol. 2, Issue 9
Ionizing radiation: how fungi cope, adapt, and exploit with the help of melanin
journal, December 2008
- Dadachova, Ekaterina; Casadevall, Arturo
- Current Opinion in Microbiology, Vol. 11, Issue 6
Where in the world do bacteria experience oxidative stress?: Oxidative stress in natural environments
journal, November 2018
- Imlay, James A.
- Environmental Microbiology, Vol. 21, Issue 2
Oxidative Stress Resistance in Deinococcus radiodurans
journal, March 2011
- Slade, D.; Radman, M.
- Microbiology and Molecular Biology Reviews, Vol. 75, Issue 1
Deinococcus radiodurans engineered for complete toluene degradation facilitates Cr(VI) reduction
journal, August 2006
- Brim, H.
- Microbiology, Vol. 152, Issue 8
Advances in mechanisms and modifications for rendering yeast thermotolerance
journal, June 2016
- Gao, Liman; Liu, Yueqin; Sun, Hun
- Journal of Bioscience and Bioengineering, Vol. 121, Issue 6
Deinococcus Mn 2+ -peptide complex: A novel approach to alphavirus vaccine development
journal, June 2017
- Gayen, Manoshi; Gupta, Paridhi; Morazzani, Elaine M.
- Vaccine, Vol. 35, Issue 29