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Title: Microbial cells can cooperate to resist high-level chronic ionizing radiation

Abstract

Understanding chronic ionizing radiation (CIR) effects is of utmost importance to protecting human health and the environment. Diverse bacteria and fungi inhabiting extremely radioactive waste and disaster sites (e.g. Hanford, Chernobyl, Fukushima) represent new targets of CIR research. We show that many microorganisms can grow under intense gamma-CIR dose rates of 13–126 Gy/h, with fungi identified as a particularly CIR-resistant group of eukaryotes: among 145 phylogenetically diverse strains tested, 78 grew under 36 Gy/h. Importantly, we demonstrate that CIR resistance can depend on cell concentration and that certain resistant microbial cells protect their neighbors (not only conspecifics, but even radiosensitive species from a different phylum), from high-level CIR. We apply a mechanistically-motivated mathematical model of CIR effects, based on accumulation/removal kinetics of reactive oxygen species (ROS) and antioxidants, in bacteria (3 Escherichia coli strains and Deinococcus radiodurans) and in fungi (Candida parapsilosis, Kazachstania exigua, Pichia kudriavzevii, Rhodotorula lysinophila, Saccharomyces cerevisiae, and Trichosporon mucoides). We also show that correlations between responses to CIR and acute ionizing radiation (AIR) among studied microorganisms are weak. For example, in D. radiodurans, the best molecular correlate for CIR resistance is the antioxidant enzyme catalase, which is dispensable for AIR resistance; and numerous CIR-resistant fungi aremore » not AIR-resistant. Our experimental findings and quantitative modeling thus demonstrate the importance of investigating CIR responses directly, rather than extrapolating from AIR. Protection of radiosensitive cell-types by radioresistant ones under high-level CIR is a potentially important new tool for bioremediation of radioactive sites and development of CIR-resistant microbiota as radioprotectors.« less

Authors:
ORCiD logo [1];  [2];  [2];  [2];  [2];  [2];  [2];  [3];  [4]
  1. Columbia Univ., New York, NY (United States)
  2. Uniformed Services University of the Health Sciences, Bethesda, MD (United States); Henry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, MD (United States)
  3. Uniformed Services University of the Health Sciences, Bethesda, MD (United States)
  4. Univ. of Arkansas, Fayetteville, AR (United States)
Publication Date:
Research Org.:
Uniformed Services University of the Health Sciences, Bethesda, MD (United States)
Sponsoring Org.:
USDOE National Nuclear Security Administration (NNSA)
OSTI Identifier:
1541922
Grant/Contract Number:  
NA0002322
Resource Type:
Accepted Manuscript
Journal Name:
PLoS ONE
Additional Journal Information:
Journal Volume: 12; Journal Issue: 12; Journal ID: ISSN 1932-6203
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
63 RADIATION, THERMAL, AND OTHER ENVIRON. POLLUTANT EFFECTS ON LIVING ORGS. AND BIOL. MAT.

Citation Formats

Shuryak, Igor, Matrosova, Vera Y., Gaidamakova, Elena K., Tkavc, Rok, Grichenko, Olga, Klimenkova, Polina, Volpe, Robert P., Daly, Michael J., and Aykin-Burns, Nukhet. Microbial cells can cooperate to resist high-level chronic ionizing radiation. United States: N. p., 2017. Web. doi:10.1371/journal.pone.0189261.
Shuryak, Igor, Matrosova, Vera Y., Gaidamakova, Elena K., Tkavc, Rok, Grichenko, Olga, Klimenkova, Polina, Volpe, Robert P., Daly, Michael J., & Aykin-Burns, Nukhet. Microbial cells can cooperate to resist high-level chronic ionizing radiation. United States. doi:10.1371/journal.pone.0189261.
Shuryak, Igor, Matrosova, Vera Y., Gaidamakova, Elena K., Tkavc, Rok, Grichenko, Olga, Klimenkova, Polina, Volpe, Robert P., Daly, Michael J., and Aykin-Burns, Nukhet. Wed . "Microbial cells can cooperate to resist high-level chronic ionizing radiation". United States. doi:10.1371/journal.pone.0189261. https://www.osti.gov/servlets/purl/1541922.
@article{osti_1541922,
title = {Microbial cells can cooperate to resist high-level chronic ionizing radiation},
author = {Shuryak, Igor and Matrosova, Vera Y. and Gaidamakova, Elena K. and Tkavc, Rok and Grichenko, Olga and Klimenkova, Polina and Volpe, Robert P. and Daly, Michael J. and Aykin-Burns, Nukhet},
abstractNote = {Understanding chronic ionizing radiation (CIR) effects is of utmost importance to protecting human health and the environment. Diverse bacteria and fungi inhabiting extremely radioactive waste and disaster sites (e.g. Hanford, Chernobyl, Fukushima) represent new targets of CIR research. We show that many microorganisms can grow under intense gamma-CIR dose rates of 13–126 Gy/h, with fungi identified as a particularly CIR-resistant group of eukaryotes: among 145 phylogenetically diverse strains tested, 78 grew under 36 Gy/h. Importantly, we demonstrate that CIR resistance can depend on cell concentration and that certain resistant microbial cells protect their neighbors (not only conspecifics, but even radiosensitive species from a different phylum), from high-level CIR. We apply a mechanistically-motivated mathematical model of CIR effects, based on accumulation/removal kinetics of reactive oxygen species (ROS) and antioxidants, in bacteria (3 Escherichia coli strains and Deinococcus radiodurans) and in fungi (Candida parapsilosis, Kazachstania exigua, Pichia kudriavzevii, Rhodotorula lysinophila, Saccharomyces cerevisiae, and Trichosporon mucoides). We also show that correlations between responses to CIR and acute ionizing radiation (AIR) among studied microorganisms are weak. For example, in D. radiodurans, the best molecular correlate for CIR resistance is the antioxidant enzyme catalase, which is dispensable for AIR resistance; and numerous CIR-resistant fungi are not AIR-resistant. Our experimental findings and quantitative modeling thus demonstrate the importance of investigating CIR responses directly, rather than extrapolating from AIR. Protection of radiosensitive cell-types by radioresistant ones under high-level CIR is a potentially important new tool for bioremediation of radioactive sites and development of CIR-resistant microbiota as radioprotectors.},
doi = {10.1371/journal.pone.0189261},
journal = {PLoS ONE},
number = 12,
volume = 12,
place = {United States},
year = {2017},
month = {12}
}

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Works referenced in this record:

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Quantifying Particulate and Colloidal Release of Radionuclides in Waste-Weathered Hanford Sediments
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Effects of radiation quality on interactions between oxidative stress, protein and DNA damage in Deinococcus radiodurans
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Fungi and ionizing radiation from radionuclides: Fungi and ionizing radiation
journal, April 2008


Radiation Induced Non-targeted Response: Mechanism and Potential Clinical Implications
journal, June 2011


The three catalases in Deinococcus radiodurans: Only two show catalase activity
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Effects of acute γ-irradiation on community structure of the aquatic microbial microcosm
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Accumulation of Mn(II) in Deinococcus radiodurans Facilitates Gamma-Radiation Resistance
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Quorum sensing enhancement of the stress response promotes resistance to quorum quenching and prevents social cheating
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Death by protein damage in irradiated cells
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Extending Applicability of the Oxygen Radical Absorbance Capacity (ORAC−Fluorescein) Assay
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Modelling study on the protective role of OH radical scavengers and DNA higher‐order structures in induction of single‐ and double‐strand break by gamma‐radiation
journal, August 2003


A model of interactions between radiation-induced oxidative stress, protein and DNA damage in Deinococcus radiodurans
journal, November 2009


A Comparison of DNA Damages Produced under Conditions of Direct and Indirect Action of Radiation
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Long-Term Consequences of Radiation-Induced Bystander Effects Depend on Radiation Quality and Dose and Correlate with Oxidative Stress
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Responses of Mn2+ speciation in Deinococcus radiodurans and Escherichia coli to  -radiation by advanced paramagnetic resonance methods
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Chk2 is required for optimal mitotic delay in response to irradiation-induced DNA damage incurred in G2 phase
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High-quality genome sequence of the radioresistant bacterium Deinococcus ficus KS 0460
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Intraspecific Variation in Gamma-Radiation Resistance and Genomic Structure in the Filamentous Fungus Alternaria alternata: A Case Study of Strains Inhabiting Chernobyl Reactor No. 4
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Survival, DNA Integrity, and Ultrastructural Damage in Antarctic Cryptoendolithic Eukaryotic Microorganisms Exposed to Ionizing Radiation
journal, February 2017

  • Pacelli, Claudia; Selbmann, Laura; Zucconi, Laura
  • Astrobiology, Vol. 17, Issue 2
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Biologically relevant mechanism for catalytic superoxide removal by simple manganese compounds
journal, April 2012

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Ionizing radiation: how fungi cope, adapt, and exploit with the help of melanin
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Mechanistic Analysis of the Contributions of DNA and Protein Damage to Radiation-Induced Cell Death
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journal, June 2000


    Works referencing / citing this record:

    Relationship between Mitotic Delay and the Minimum Dose Rate of X Irradiation Required to Stop Cell Proliferation
    journal, February 1993

    • Yi, Pon Nyong; Stanley, Wayne S.; Lee, Wah
    • Radiation Research, Vol. 133, Issue 2
    • DOI: 10.2307/3578352

    Effects of acute γ-irradiation on community structure of the aquatic microbial microcosm
    journal, November 2010


    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
    • DOI: 10.1126/science.1103185

    A model of interactions between radiation-induced oxidative stress, protein and DNA damage in Deinococcus radiodurans
    journal, November 2009


    Chk2 is required for optimal mitotic delay in response to irradiation-induced DNA damage incurred in G2 phase
    journal, August 2007


    Hydrogen peroxide induced cell death: One or two modes of action?
    journal, December 2015


    Hypofractionation Results in Reduced Tumor Cell Kill Compared to Conventional Fractionation for Tumors With Regions of Hypoxia
    journal, March 2011

    • Carlson, David J.; Keall, Paul J.; Loo, Billy W.
    • International Journal of Radiation Oncology*Biology*Physics, Vol. 79, Issue 4
    • DOI: 10.1016/j.ijrobp.2010.10.007

    Quorum sensing enhancement of the stress response promotes resistance to quorum quenching and prevents social cheating
    journal, June 2014

    • García-Contreras, Rodolfo; Nuñez-López, Leslie; Jasso-Chávez, Ricardo
    • The ISME Journal, Vol. 9, Issue 1
    • DOI: 10.1038/ismej.2014.98

    Extending Applicability of the Oxygen Radical Absorbance Capacity (ORAC−Fluorescein) Assay
    journal, January 2004

    • Dávalos, Alberto; Gómez-Cordovés, Carmen; Bartolomé, Begoña
    • Journal of Agricultural and Food Chemistry, Vol. 52, Issue 1
    • DOI: 10.1021/jf0305231

    Radiation Chemical Mechanisms of Single- and Double-Strand Break Formation in Irradiated SV40 DNA
    journal, May 1991

    • Krisch, Robert E.; Flick, Maryann B.; Trumbore, Conrad N.
    • Radiation Research, Vol. 126, Issue 2
    • DOI: 10.2307/3577826

    Ionizing radiation: how fungi cope, adapt, and exploit with the help of melanin
    journal, December 2008


    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
    • DOI: 10.1371/journal.pbio.0050092

    Cellular Defenses against Superoxide and Hydrogen Peroxide
    journal, June 2008


    Engineering Deinococcus radiodurans for metal remediation in radioactive mixed waste environments
    journal, January 2000

    • Brim, Hassan; McFarlan, Sara C.; Fredrickson, James K.
    • Nature Biotechnology, Vol. 18, Issue 1
    • DOI: 10.1038/71986

    Death by protein damage in irradiated cells
    journal, January 2012


    Effects of radiation quality on interactions between oxidative stress, protein and DNA damage in Deinococcus radiodurans
    journal, June 2010


    Modelling study on the protective role of OH radical scavengers and DNA higher‐order structures in induction of single‐ and double‐strand break by gamma‐radiation
    journal, August 2003


    Survival, DNA Integrity, and Ultrastructural Damage in Antarctic Cryptoendolithic Eukaryotic Microorganisms Exposed to Ionizing Radiation
    journal, February 2017

    • Pacelli, Claudia; Selbmann, Laura; Zucconi, Laura
    • Astrobiology, Vol. 17, Issue 2
    • DOI: 10.1089/ast.2015.1456

    Biologically relevant mechanism for catalytic superoxide removal by simple manganese compounds
    journal, April 2012

    • Barnese, K.; Gralla, E. B.; Valentine, J. S.
    • Proceedings of the National Academy of Sciences, Vol. 109, Issue 18
    • DOI: 10.1073/pnas.1203051109

    Intraspecific Variation in Gamma-Radiation Resistance and Genomic Structure in the Filamentous Fungus Alternaria alternata: A Case Study of Strains Inhabiting Chernobyl Reactor No. 4
    journal, February 2000

    • Mironenko, Nina V.; Alekhina, Irina A.; Zhdanova, Nelli N.
    • Ecotoxicology and Environmental Safety, Vol. 45, Issue 2
    • DOI: 10.1006/eesa.1999.1848

    Fungi and ionizing radiation from radionuclides: Fungi and ionizing radiation
    journal, April 2008


    Repair of oxidative DNA damage by amino acids
    journal, November 2003


    Quantifying Particulate and Colloidal Release of Radionuclides in Waste-Weathered Hanford Sediments
    journal, January 2015

    • Perdrial, Nicolas; Thompson, Aaron; LaSharr, Kelsie
    • Journal of Environment Quality, Vol. 44, Issue 3
    • DOI: 10.2134/jeq2014.09.0388

    Radiation Induced Non-targeted Response: Mechanism and Potential Clinical Implications
    journal, June 2011


    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
    • DOI: 10.1186/s40793-017-0258-y

    Effects of chronic γ-irradiation on the aquatic microbial microcosm: equi-dosimetric comparison with effects of heavy metals
    journal, February 2012


    The three catalases in Deinococcus radiodurans: Only two show catalase activity
    journal, January 2016

    • Jeong, Sun-Wook; Jung, Jong-Hyun; Kim, Min-Kyu
    • Biochemical and Biophysical Research Communications, Vol. 469, Issue 3
    • DOI: 10.1016/j.bbrc.2015.12.017

    Role of the Quorum Sensing Mechanism in the Response of Pseudomonas aeruginosa to Lethal and Sublethal UVA Irradiation: Photochemistry and Photobiology
    journal, September 2010


    Radiation countermeasure agents: an update (2011 – 2014)
    journal, October 2014

    • Singh, Vijay K.; Newman, Victoria L.; Romaine, Patricia LP
    • Expert Opinion on Therapeutic Patents, Vol. 24, Issue 11
    • DOI: 10.1517/13543776.2014.964684

    Non-Targeted Effects Models Predict Significantly Higher Mars Mission Cancer Risk than Targeted Effects Models
    journal, May 2017


    Responses of Mn2+ speciation in Deinococcus radiodurans and Escherichia coli to  -radiation by advanced paramagnetic resonance methods
    journal, March 2013

    • Sharma, A.; Gaidamakova, E. K.; Matrosova, V. Y.
    • Proceedings of the National Academy of Sciences, Vol. 110, Issue 15
    • DOI: 10.1073/pnas.1303376110

    Interplasmidic recombination following irradiation of the radioresistant bacterium Deinococcus radiodurans.
    journal, December 1994


    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
    • DOI: 10.1371/journal.pone.0012570

    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
    • DOI: 10.1089/ars.2012.5093

    A Comparison of DNA Damages Produced under Conditions of Direct and Indirect Action of Radiation
    journal, January 1994

    • Jones, G. D. D.; Boswell, T. V.; Lee, J.
    • International Journal of Radiation Biology, Vol. 66, Issue 5
    • DOI: 10.1080/09553009414551431