Microbial cells can cooperate to resist high-level chronic ionizing radiation.
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...
Main Authors: | , , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
Public Library of Science (PLoS)
2017-01-01
|
Series: | PLoS ONE |
Online Access: | http://europepmc.org/articles/PMC5738026?pdf=render |
id |
doaj-1c8baa4bb2c84d9fa6484dd6504368fe |
---|---|
record_format |
Article |
spelling |
doaj-1c8baa4bb2c84d9fa6484dd6504368fe2020-11-25T01:52:39ZengPublic Library of Science (PLoS)PLoS ONE1932-62032017-01-011212e018926110.1371/journal.pone.0189261Microbial cells can cooperate to resist high-level chronic ionizing radiation.Igor ShuryakVera Y MatrosovaElena K GaidamakovaRok TkavcOlga GrichenkoPolina KlimenkovaRobert P VolpeMichael J DalyUnderstanding 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.http://europepmc.org/articles/PMC5738026?pdf=render |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Igor Shuryak Vera Y Matrosova Elena K Gaidamakova Rok Tkavc Olga Grichenko Polina Klimenkova Robert P Volpe Michael J Daly |
spellingShingle |
Igor Shuryak Vera Y Matrosova Elena K Gaidamakova Rok Tkavc Olga Grichenko Polina Klimenkova Robert P Volpe Michael J Daly Microbial cells can cooperate to resist high-level chronic ionizing radiation. PLoS ONE |
author_facet |
Igor Shuryak Vera Y Matrosova Elena K Gaidamakova Rok Tkavc Olga Grichenko Polina Klimenkova Robert P Volpe Michael J Daly |
author_sort |
Igor Shuryak |
title |
Microbial cells can cooperate to resist high-level chronic ionizing radiation. |
title_short |
Microbial cells can cooperate to resist high-level chronic ionizing radiation. |
title_full |
Microbial cells can cooperate to resist high-level chronic ionizing radiation. |
title_fullStr |
Microbial cells can cooperate to resist high-level chronic ionizing radiation. |
title_full_unstemmed |
Microbial cells can cooperate to resist high-level chronic ionizing radiation. |
title_sort |
microbial cells can cooperate to resist high-level chronic ionizing radiation. |
publisher |
Public Library of Science (PLoS) |
series |
PLoS ONE |
issn |
1932-6203 |
publishDate |
2017-01-01 |
description |
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. |
url |
http://europepmc.org/articles/PMC5738026?pdf=render |
work_keys_str_mv |
AT igorshuryak microbialcellscancooperatetoresisthighlevelchronicionizingradiation AT veraymatrosova microbialcellscancooperatetoresisthighlevelchronicionizingradiation AT elenakgaidamakova microbialcellscancooperatetoresisthighlevelchronicionizingradiation AT roktkavc microbialcellscancooperatetoresisthighlevelchronicionizingradiation AT olgagrichenko microbialcellscancooperatetoresisthighlevelchronicionizingradiation AT polinaklimenkova microbialcellscancooperatetoresisthighlevelchronicionizingradiation AT robertpvolpe microbialcellscancooperatetoresisthighlevelchronicionizingradiation AT michaeljdaly microbialcellscancooperatetoresisthighlevelchronicionizingradiation |
_version_ |
1724993914495041536 |