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

Journal Article · · PLoS ONE
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)

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.

Research Organization:
Uniformed Services University of the Health Sciences, Bethesda, MD (United States)
Sponsoring Organization:
USDOE National Nuclear Security Administration (NNSA)
Grant/Contract Number:
NA0002322
OSTI ID:
1541922
Journal Information:
PLoS ONE, Vol. 12, Issue 12; ISSN 1932-6203
Publisher:
Public Library of ScienceCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 27 works
Citation information provided by
Web of Science

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Chronic gamma radiation resistance in fungi correlates with resistance to chromium and elevated temperatures, but not with resistance to acute irradiation journal August 2019
Concomitant changes in radiation resistance and trehalose levels during life stages of Drosophila melanogaster suggest radio-protective function of trehalose journal April 2018
Helical and linear morphotypes of Arthrospira sp. PCC 8005 display genomic differences and respond differently to 60 Co gamma irradiation journal November 2019
Conservation and diversity of radiation and oxidative stress resistance mechanisms in Deinococcus species journal October 2018
Transcriptomic analysis reveals the relationship of melanization to growth and resistance to gamma radiation in Cryptococcus neoformans journal February 2019
Survival of Radioresistant Bacteria on Europa’s Surface after Pulse Ejection of Subsurface Ocean Water journal December 2018
Metataxonomics of Tunisian phosphogypsum based on five bioinformatics pipelines: Insights for bioremediation journal January 2020
Signal Recognition Particle RNA Contributes to Oxidative Stress Response in Deinococcus radiodurans by Modulating Catalase Localization journal December 2020