Below-Background Ionizing Radiation as an Environmental Cue for Bacteria
Abstract
All organisms on earth grow under the influence of a natural and relatively constant dose of ionizing radiation referred to as background radiation, and so cells have different mechanisms to prevent the accumulation of damage caused by its different components. However, current knowledge of the deleterious effects of radiation on cells is based on the exposure to acute and high or to chronic, above background doses of radiation and therefore is not appropriate to explain the cellular and biochemical mechanisms that cells employ to sense and respond to chronic below-background levels. Studies at below-background radiation doses can provide insight into the biological role of radiation, as suggested by several examples of what appears to be a stress response in cells grown at doses that range from 10 to 79 times lower than background. Here, we discuss some of the technical constraints to shield cells from radiation to below-background levels, as well as different approaches used to detect and measure responses to such unusual environmental conditions. Then, we present data from Shewanella oneidensis and Deinococcus radiodurans experiments that show how two taxonomically distant bacterial species sense and respond to unnaturally low levels of radiation. Finally, in brief, we grew S. oneidensismore »
- Authors:
-
- New Mexico State Univ., Las Cruces, NM (United States). Dept. of Biology
- Publication Date:
- Research Org.:
- New Mexico State Univ., Las Cruces, NM (United States)
- Sponsoring Org.:
- USDOE Office of Environmental Management (EM)
- OSTI Identifier:
- 1358357
- Grant/Contract Number:
- EM0002423
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Frontiers in Microbiology
- Additional Journal Information:
- Journal Volume: 8; Journal ID: ISSN 1664-302X
- Publisher:
- Frontiers Research Foundation
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 63 RADIATION, THERMAL, AND OTHER ENVIRON. POLLUTANT EFFECTS ON LIVING ORGS. AND BIOL. MAT.; below-background radiation; stress response; relative gene expression; radiation biology; Shewanella oneidensis; Deinococcus radiodurans
Citation Formats
Castillo, Hugo, and Smith, Geoffrey B. Below-Background Ionizing Radiation as an Environmental Cue for Bacteria. United States: N. p., 2017.
Web. doi:10.3389/fmicb.2017.00177.
Castillo, Hugo, & Smith, Geoffrey B. Below-Background Ionizing Radiation as an Environmental Cue for Bacteria. United States. https://doi.org/10.3389/fmicb.2017.00177
Castillo, Hugo, and Smith, Geoffrey B. Tue .
"Below-Background Ionizing Radiation as an Environmental Cue for Bacteria". United States. https://doi.org/10.3389/fmicb.2017.00177. https://www.osti.gov/servlets/purl/1358357.
@article{osti_1358357,
title = {Below-Background Ionizing Radiation as an Environmental Cue for Bacteria},
author = {Castillo, Hugo and Smith, Geoffrey B.},
abstractNote = {All organisms on earth grow under the influence of a natural and relatively constant dose of ionizing radiation referred to as background radiation, and so cells have different mechanisms to prevent the accumulation of damage caused by its different components. However, current knowledge of the deleterious effects of radiation on cells is based on the exposure to acute and high or to chronic, above background doses of radiation and therefore is not appropriate to explain the cellular and biochemical mechanisms that cells employ to sense and respond to chronic below-background levels. Studies at below-background radiation doses can provide insight into the biological role of radiation, as suggested by several examples of what appears to be a stress response in cells grown at doses that range from 10 to 79 times lower than background. Here, we discuss some of the technical constraints to shield cells from radiation to below-background levels, as well as different approaches used to detect and measure responses to such unusual environmental conditions. Then, we present data from Shewanella oneidensis and Deinococcus radiodurans experiments that show how two taxonomically distant bacterial species sense and respond to unnaturally low levels of radiation. Finally, in brief, we grew S. oneidensis and D. radiodurans in liquid culture at dose rates of 72.05 (control) and 0.91 (treatment) nGy hr-1 (including radon) for up to 72 h and measured cell density and the expression of stress-related genes. Our results suggest that a stress response is triggered in the absence of normal levels of radiation.},
doi = {10.3389/fmicb.2017.00177},
journal = {Frontiers in Microbiology},
number = ,
volume = 8,
place = {United States},
year = {Tue Feb 14 00:00:00 EST 2017},
month = {Tue Feb 14 00:00:00 EST 2017}
}
Web of Science
Works referenced in this record:
RBE-LET Relationship for the Survival of V79 Cells Irradiated with Low Energy Protons
journal, January 1989
- Belli, M.; Cherubini, R.; Finotto, S.
- International Journal of Radiation Biology, Vol. 55, Issue 1
SOS induction by γ-radiation in Escherichia coli strains defective in repair and/or recombination mechanisms
journal, January 1998
- Breña-Valle, Matilde; Serment-Guerrero, Jorge
- Mutagenesis, Vol. 13, Issue 6
Molecular Dynamics of the Shewanella oneidensis Response to Chromate Stress
journal, March 2006
- Brown, Steven D.; Thompson, Melissa R.; VerBerkmoes, Nathan C.
- Molecular & Cellular Proteomics, Vol. 5, Issue 6
The Cosmic Silence experiment: on the putative adaptive role of environmental ionizing radiation
journal, January 2009
- Carbone, M. C.; Pinto, M.; Antonelli, F.
- Radiation and Environmental Biophysics, Vol. 48, Issue 2
Expression of recA in Deinococcus radiodurans.
journal, January 1996
- Carroll, J. D.; Daly, M. J.; Minton, K. W.
- Journal of bacteriology, Vol. 178, Issue 1
Stress induction in the bacteria Shewanella oneidensis and Deinococcus radiodurans in response to below-background ionizing radiation
journal, July 2015
- Castillo, Hugo; Schoderbek, Donald; Dulal, Santosh
- International Journal of Radiation Biology, Vol. 91, Issue 9
A Novel OxyR Sensor and Regulator of Hydrogen Peroxide Stress with One Cysteine Residue in Deinococcus radiodurans
journal, February 2008
- Chen, Huan; Xu, Guangzhi; Zhao, Ye
- PLoS ONE, Vol. 3, Issue 2
The multifaceted capacity of Dps proteins to combat bacterial stress conditions: Detoxification of iron and hydrogen peroxide and DNA binding
journal, August 2010
- Chiancone, Emilia; Ceci, Pierpaolo
- Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 1800, Issue 8
Creating a baseline radiological standard for the waste isolation pilot plant underground
journal, September 2004
- Chiou, Hung-Cheng; Hayes, Robert
- Isotopes in Environmental and Health Studies, Vol. 40, Issue 3
A new perspective on radiation resistance based on Deinococcus radiodurans
journal, January 2009
- Daly, Michael J.
- Nature Reviews Microbiology, Vol. 7, Issue 3
Low-radiation environment affects the development of protection mechanisms in V79 cells
journal, January 2015
- Fratini, E.; Carbone, C.; Capece, D.
- Radiation and Environmental Biophysics, Vol. 54, Issue 2
How radiation kills cells: Survival of Deinococcus radiodurans and Shewanella oneidensis under oxidative stress
journal, April 2005
- Ghosal, Debabrota; Omelchenko, Marina V.; Gaidamakova, Elena K.
- FEMS Microbiology Reviews, Vol. 29, Issue 2
Direct Comparison between Protons and Alpha-particles of the Same LET: I. Irradiation Methods and Inactivation of Asynchronous V79, HeLa and C3H 10T½ Cells
journal, January 1992
- Goodhead, D. T.; Belli, M.; Mill, A. J.
- International Journal of Radiation Biology, Vol. 61, Issue 5
Mechanislns for the Biological Effectiveness of High-LET Radiations.
journal, January 1999
- Goodhead, Dudley T.
- Journal of Radiation Research, Vol. 40, Issue Suppl.
Protection from Oxidative Stress Relies Mainly on Derepression of OxyR-Dependent KatB and Dps in Shewanella oneidensis
journal, November 2013
- Jiang, Y.; Dong, Y.; Luo, Q.
- Journal of Bacteriology, Vol. 196, Issue 2
Chronic Irradiation of Scots pine Trees (Pinus Sylvestris) in the Chernobyl Exclusion Zone: Dosimetry and Radiobiological Effects
journal, January 2011
- Yoschenko, Vasyl I.; Kashparov, Valery A.; Melnychuk, Maxim D.
- Health Physics, Vol. 101, Issue 4
Growth Retardation of Paramecium and Mouse Cells by Shielding Them from Background Radiation
journal, January 2012
- Kawanishi, Masanobu; Okuyama, Katsuyuki; Shiraishi, Kazunori
- Journal of Radiation Research, Vol. 53, Issue 3
Molecular and Evolutionary Basis of the Cellular Stress Response
journal, March 2005
- Kültz, Dietmar
- Annual Review of Physiology, Vol. 67, Issue 1
An Auto-regulatory Loop between Stress Sensors INrf2 and Nrf2 Controls Their Cellular Abundance
journal, October 2007
- Lee, Ok-Hee; Jain, Abhinav K.; Papusha, Victor
- Journal of Biological Chemistry, Vol. 282, Issue 50
Relative expression software tool (REST(C)) for group-wise comparison and statistical analysis of relative expression results in real-time PCR
journal, May 2002
- Pfaffl, M. W.
- Nucleic Acids Research, Vol. 30, Issue 9
Influence on Cell Proliferation of Background Radiation Or Exposure to Very Low, Chronic Gamma Radiation
journal, January 1987
- Planel, H.; Soleilhavoup, J. P.; Tixador, R.
- Health Physics, Vol. 52, Issue 5
Transcriptome Analysis Applied to Survival of Shewanella oneidensis MR-1 Exposed to Ionizing Radiation
journal, January 2006
- Qiu, X.; Daly, M. J.; Vasilenko, A.
- Journal of Bacteriology, Vol. 188, Issue 3
Comparative Analysis of Differentially Expressed Genes in Shewanella oneidensis MR-1 following Exposure to UVC, UVB, and UVA Radiation
journal, May 2005
- Qiu, X.; Sundin, G. W.; Wu, L.
- Journal of Bacteriology, Vol. 187, Issue 10
Escherichia coli under Ionic Silver Stress: An Integrative Approach to Explore Transcriptional, Physiological and Biochemical Responses
journal, December 2015
- Saulou-Bérion, Claire; Gonzalez, Ignacio; Enjalbert, Brice
- PLOS ONE, Vol. 10, Issue 12
Dps from Deinococcus radiodurans : oligomeric forms of Dps1 with distinct cellular functions and Dps2 involved in metal storage
journal, September 2015
- Santos, Sandra P.; Mitchell, Edward P.; Franquelim, Henri G.
- FEBS Journal, Vol. 282, Issue 22
Influence of a low background radiation environment on biochemical and biological responses in V79 cells
journal, September 2002
- Satta, L.; Antonelli, F.; Belli, M.
- Radiation and Environmental Biophysics, Vol. 41, Issue 3
Low environmental radiation background impairs biological defence of the yeast Saccharomyces cerevisiae to chemical radiomimetic agents
journal, August 1995
- Satta, L.; Augusti-Tocco, G.; Ceccarelli, R.
- Mutation Research Letters, Vol. 347, Issue 3-4
Exploring Biological Effects of low Level Radiation from the Other side of Background
journal, January 2011
- Smith, Geoffrey Battle; Grof, Yair; Navarrette, Adrianne
- Health Physics, Vol. 100, Issue 3
Background radiation: natural and man-made
journal, March 2003
- Thorne, M. C.
- Journal of Radiological Protection, Vol. 23, Issue 1
Early effects of gamma rays and protons on human melanoma cell viability and morphology
journal, December 2008
- TodoroviĆ, D.; PetroviĆ, I.; TodoroviĆ, M.
- Journal of Microscopy, Vol. 232, Issue 3
Influence of a low background radiation environment on biochemical and biological responses in V79 cells
journal, September 2002
- Satta, L.; Antonelli, F.; Belli, M.
- Radiation and Environmental Biophysics, Vol. 41, Issue 3
The Cosmic Silence experiment: on the putative adaptive role of environmental ionizing radiation
journal, January 2009
- Carbone, M. C.; Pinto, M.; Antonelli, F.
- Radiation and Environmental Biophysics, Vol. 48, Issue 2
The multifaceted capacity of Dps proteins to combat bacterial stress conditions: Detoxification of iron and hydrogen peroxide and DNA binding
journal, August 2010
- Chiancone, Emilia; Ceci, Pierpaolo
- Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 1800, Issue 8
How radiation kills cells: Survival of Deinococcus radiodurans and Shewanella oneidensis under oxidative stress
journal, April 2005
- Ghosal, Debabrota; Omelchenko, Marina V.; Gaidamakova, Elena K.
- FEMS Microbiology Reviews, Vol. 29, Issue 2
A new perspective on radiation resistance based on Deinococcus radiodurans
journal, January 2009
- Daly, Michael J.
- Nature Reviews Microbiology, Vol. 7, Issue 3
RBE-LET Relationship for the Survival of V79 Cells Irradiated with Low Energy Protons
journal, January 1989
- Belli, M.; Cherubini, R.; Finotto, S.
- International Journal of Radiation Biology, Vol. 55, Issue 1
Creating a baseline radiological standard for the waste isolation pilot plant underground
journal, September 2004
- Chiou, Hung-Cheng; Hayes, Robert
- Isotopes in Environmental and Health Studies, Vol. 40, Issue 3
SOS induction by γ-radiation in Escherichia coli strains defective in repair and/or recombination mechanisms
journal, January 1998
- Breña-Valle, Matilde; Serment-Guerrero, Jorge
- Mutagenesis, Vol. 13, Issue 6
Expression of recA in Deinococcus radiodurans.
journal, January 1996
- Carroll, J. D.; Daly, M. J.; Minton, K. W.
- Journal of bacteriology, Vol. 178, Issue 1
Molecular and Evolutionary Basis of the Cellular Stress Response
journal, March 2005
- Kültz, Dietmar
- Annual Review of Physiology, Vol. 67, Issue 1
Growth Retardation of Paramecium and Mouse Cells by Shielding Them from Background Radiation
journal, January 2012
- Kawanishi, Masanobu; Okuyama, Katsuyuki; Shiraishi, Kazunori
- Journal of Radiation Research, Vol. 53, Issue 3
Escherichia coli under Ionic Silver Stress: An Integrative Approach to Explore Transcriptional, Physiological and Biochemical Responses
journal, December 2015
- Saulou-Bérion, Claire; Gonzalez, Ignacio; Enjalbert, Brice
- PLOS ONE, Vol. 10, Issue 12
Works referencing / citing this record:
Low-dose radiation from A-bombs elongated lifespan and reduced cancer mortality relative to un-irradiated individuals
journal, December 2018
- Sutou, Shizuyo
- Genes and Environment, Vol. 40, Issue 1
Transcriptome analysis reveals a stress response of Shewanella oneidensis deprived of background levels of ionizing radiation
journal, May 2018
- Castillo, Hugo; Li, Xiaoping; Schilkey, Faye
- PLOS ONE, Vol. 13, Issue 5