F10 and D10 values for 90 % reduction of selected radioresistant prokaryotes (RP)
The extremely radioresistant eubacterium Deinococcus radiodurans and the phenotypically related prokaryotes, whose genomes have been completely sequenced, are presently used as model species in several laboratories to study the lethal effects of DNA-damaging and protein-oxidizing agents, particularly the effects of ionizing radiation (IR). Unfortunately, providing relevant information about radioresistant prokaryotes (RP) in a neatly centralized and organized manner still remains a need. In this study, we designed RadioP1 Web resource (www.radiop.org.tn) to gather information about RP defined by the published literature with specific emphasis on (i) predicted genes that produce and protect against oxidative stress, (ii) predicted proteins involved in DNA repair mechanisms and (iii) potential uses of RP in biotechnology. RadioP1 allows the complete RP proteogenomes to be queried using various patterns in a user-friendly and interactive manner. The output data can be saved in plain text, Excel or HyperText Markup Language (HTML) formats for subsequent analyses. Moreover, RadioP1 provides for users a tool “START ANALYSIS”, including the previously described R-packages “drc” and “lethal”, to generate exponential or sigmoid survival curves with D10 and D50 values. Furthermore, when accessible, links to external databases are provided. Supplementary data will be included in the future when the sequences of other RP genomes will become available.
- Web resource
To be considered as an RP, a microorganism should have a D10—the ionizing-radiation (IR) dose necessary to effect a 90 % reduction in colony-forming units (CFU)—threshold that is greater than 1 kilogray (kGy), corresponding to efficient physiological, genetic and proteic protection and repair mechanisms ([1, 2] and references therein). In this context, to our knowledge, even when prokaryotic members belonging to a radioresistant-species-harbouring genus have contrasted optimum temperatures—for example, ranging from 10 to 47 ºC—the least IR-resistant ones do not have D10 values inferior to 1 kGy . Furthermore, as suggested from D10 and F10—the ultraviolet (UV) dose necessary to effect a 90 % reduction in CFU—reported in literature [4-6], an RP is tolerant to both IR (e.g. α and β particles, γ- and x-rays, neutrons) and non-IR (UV light); and correlations were suggested . In this context, it is important to note that UV may cause effects similar to those stimulated by IR .
The first RP to be described, designated
As a complicated multifaceted phenotype, prokaryotic radioresistance is an important subject in radiation microbiology. A focus on just one contributing mechanism is unlikely to yield a complete understanding of the phenomenon . The radioresistance of prokaryotes depends on their ability to protect enzymes including those needed to repair and replicate DNA from inactivation by oxidative protein damage (protein-centric view) and to fully amend their DNA—double-strand breaks (DSBs)—(DNA-centric view). Obviously, much is yet to be discovered from the mesmerizing radioresistance strategies posed by RP. There is an increasing need to compile the entire data about RP in a centralized and organized manner and to mine it regarding prokaryotic radioresistance. RadioP1 is addressing these requests by providing pertinent information as well as diverse analytical tools. This first version of RadioP is a preliminary step towards the establishment of a comprehensive RP database. The increase of the number of side aspects of radioresistance make us keen to collect and to make available for the scientific community the most up-to-date and relevant information.
||7,000–11,000||n.d.||[37, 42, 43]|
||6,700–16,000||660–2000||[3, 37-39, 47-50]|
2. Source of data
Used information was obtained by searching the NCBI database . Clusters of Orthologous Group (COG)  were used to classify orthologous gene records in RadioP1. Orthology was calculated with Basic Local Alignment Search Tool (BLAST), the best reciprocal hit approach and InParanoid program.
3. Database construction
The database schema (Figure 2) consists of 13 tables, allowing to search and to retrieve any stored biological data. Among the main tables is the species table (primary information: organism name and taxon ID), which is connected to the taxonomy and chromosome tables. from NCBI, and is linked to the taxonomy and chromosome tables. This later is connected to seqfile tables detailing the different file formats and paths related to each chromosome. The gene table, related to the chromosome table, stores information such as gene name, gene ID, symbol, first position, last position and strand. The gene table is linked to the orthology table.
4. RadioP1 database user guide
RadioP1 is freely accessible through a Web browser at http://www.radiop.org.tn. There are at least three ways to use the database: browse, search and generate data.
5. Browse in the database
In the main page of RadioP1, a clickable list of currently available groups of IRRP—ionizing-radiation-resistant prokaryotes—is organized at the top-left side, allowing users to browse pages for each of the groups, IR-resistant archaea (IRRA) and IR-resistant bacteria (IRRB).
6. Search the database
RadioP1 provides a search engine that is able to extract information from the database through: (i) text search, (ii) BLAST search and (iii) function category search..
The text and homology search contains three categories:
“SEARCH GENES”: This search category allows extracting annotation information—gene symbol, chromosome name, strand, predicted orthologous genes, etc.—using querying gene locus tags.. The querying results are displayed in a table with each hit represented by a row containing a corresponding gene ID and a summary of characteristics—gene name, symbol, strand and product. In addition, each listed row in the output table provides a link to the individual gene pages, which highlight the querying genes found in the page of NCBI . Users can get results in HTML, plain text or Excel formats for further analyses.
“RETRIEVE SEQUENCES”: This search category enables extracting nucleic or proteic sequences using querying gene locus tags.
“HOMOLOGY DATA”: This search category enables extracting predicted orthologous gene clusters using querying gene locus tags.
The function category search contains four subclasses:
“OXIDATIVE STRESS PRODUCTION”:
When the generation of reactive oxygen species (ROS; superoxide (O2⋅⋅−), hydrogen peroxide (H2O2) and hydroxyl (HO⋅) radicals) produced by metabolism or irradiation exceeds the capacity of endogenous scavengers to neutralize them, cells become vulnerable to damage, a condition referred to as oxidative stress [56, 57]. Typically, during irradiation, ~80 % of DNA damage is caused indirectly by irradiation-induced ROS and the remaining ~20 % by direct interaction between c-photons and DNA . HO⋅ radicals are the primary product of the radiolysis of water and in the presence of oxygen, can also generate some O2⋅⋅− and H2O2 by dismutation of O2⋅⋅− . In contrast, the primary ROS generated by metabolism are O2⋅⋅− and H2O2 . The total intracellular titer of cytochromes and flavins might serve as a marker for the proclivity of cells to survive radiation and other oxidizing conditions [58, 59]. For instance, the total number of c-type cytochromes in
“OXIDATIVE STRESS PROTECTION”:
Unlike DNA DSB lesion yields ( and references therein), in IR-sensitive cells, yields of IR-induced protein oxidation can be ~100 times greater than in IR-resistant cells [60, 61]. Indeed, presently, it is demonstrated that proteins are major targets of IR damage and that shield against protein oxidation is an important mechanism for survival from IR exposure. IR resistance in some prokaryotes was highly correlated to the accumulation of high intracellular concentration of Mn2+, supporting the idea of a common model of Mn2+-dependent ROS scavenging in the aerobes ([6, 62] and references therein). For example, the aerobic archaeon
“DNA REPAIR GENES”:
During irradiation, DNA double-strand breaks (DSBs) are considered as the most lethal damage, although they are the least frequent form of cellular DNA damage—compared to single-strand breaks and DNA base damages . For example, in
“USE IN BIOTECHNOLOGY”:
RP provide inestimable opportunities in therapeutics for multiple diseases , biotechnology , pharmaceuticals  and bioengineering—bioremediation—of toxic and radioactive compounds [75-81]. The function “USE IN BIOTECHNOLOGY” in RadioP1 was designed to present the diversity of IRRP genomes in terms of genes with potential applications in biotechnology.
7. Generate survival plots and Dx (D10 and D50) values
Cell survival models aim to describe the relationship between the absorbed dose and the fraction of surviving cells—cell survival curve. Distinct cell survival models were described [82-86]: the linear—single-hit single-target, the linear-quadratic (LQ) and the repairable-conditionally repairable damage (RCR) models. Other models include those based on target theory first described by Lea  and those described by Tobias , Curtis  and Sontag .
For instance, for UV-C-irradiated prokaryotes, as summarized previously , the mathematical dose-response models which describe the probability of a specific biological response at a given dose can be represented as follows (Figure 3):
RadioP1 provides a tool “START ANALYSIS” for users to generate exponential survival curves [92, 93]. In addition, it integrated the previously described R-packages “drc”  for sigmoid curves and “lethal”  that computes lethal doses (LD) with confidence intervals . All curves are supplied with D10 and D50 values.
8. Future directions
RadioP1 is a specialized database aimed at making a comprehensive repository of identified RP with experimentally determined D10. It is complemented by data extraction and analysis tools to help further analysis of RP. Researchers are kindly requested and encouraged to invigorate RadioP1 by depositing their new results—D10—of RP at RadioP1. Submission might either be performed through the “Submit new RP with a D10” form accessible under the IRRP main page or by e-mail to corresponding authors. In the future, we intend to include more detailed information about RP in the area of evolutionary biology, biotechnology and theranostics. Additional data sources like Kyoto Encyclopedia of Genes and Genomes (KEGG) and COGs will be integrated to extract further information about gene functions, clusters and pathways, helping users to categorise genes of interest into functional units and perform more efficient analysis on RP genomes.
This work was supported by the Tunisian National Center for Nuclear Sciences and Technology (CNSTN), the Pasteur Institute (Tunis) and a bilateral cooperation project coordinated by Dr Haïtham Sghaier from Tunisia and Dr Houria Ouled-Haddar from Algeria.
Authors would like to thank colleagues who gave their feedbacks after testing the database. Particularly, authors thank Prof. Issay NARUMI from the Radiation Microbiology Laboratory, in Toyo University, Japan, for many helpful comments concerning the content of RadioP1; and InTech team for excellent editorial assistance.
Sghaier H: DNA Repair: Lessons from the Evolution of Ionizing- Radiation-Resistant Prokaryotes – Fact and Theory. In: Selected Topics in DNA Repair.Edited by Clark CC, University of California. San Diego: InTech; 2011: 145–156.
Sghaier H, Ghedira K, Benkahla A, Barkallah I: Basal DNA repair machinery is subject to positive selection in ionizing-radiation-resistant bacteria. BMC Genomics2008, 9:297.
Callegan RP, Nobre MF, McTernan PM, Battista JR, Navarro-Gonzalez R, McKay CP, da Costa MS, Rainey FA: Description of four novel psychrophilic, ionizing radiation-sensitive Deinococcusspecies from alpine environments. Int J Syst Evol Microbiol2008, 58(Pt 5):1252–1258.
Beblo K, Douki T, Schmalz G, Rachel R, Wirth R, Huber H, Reitz G, Rettberg P: Survival of thermophilic and hyperthermophilic microorganisms after exposure to UV-C, ionizing radiation and desiccation. Arch Microbiol2011, 193(11):797–809.
Daly MJ: Modulating radiation resistance: insights based on defenses against reactive oxygen species in the radioresistant bacterium Deinococcus radiodurans. Clin Lab Med2006, 26(2):491–504.
Daly MJ: Death by protein damage in irradiated cells. DNA Repair (Amst)2011, 11(1):12–21.
Arrange AA, Phelps TJ, Benoit RE, Palumbo AV, White DC: Bacterial sensitivity to UV light as a model for ionizing radiation resistance. J Microbiol Methods1993, 18(2):127–136.
Nikogosyan DN: Two-quantum UV photochemistry of nucleic acids: comparison with conventional low-intensity UV photochemistry and radiation chemistry. Int J Radiat Biol1990, 57(2):233–299.
Anderson AW, Nordan HC, Cain RF, Parrish G, Duggan D: Studies on a radio-resistant Micrococcus. I. Isolation, morphology, cultural characteristics, and resistance to gamma radiation. Food Technol1956, 10:575–577.
Brooks BW, Murray RGE: Nomenclature for “ Micrococcus radiodurans” and other radiation-resistant cocci: Deinococcaceaefam. nov. and Deinococcusgen. nov., including five species. Int J Syst Bacteriol1981, 31:353–360.
Kopylov VM, Bonch-Osmolovskaya EA, Svetlichnyi VA, Miroshnicheko ML, Skobin VS: Gamma-irradiation resistance and UV sensitivity of extremely thermophilic archaebacteria and eubacteria. Mikrobiologiya1993(62):90–95.
Kottemann M, Kish A, Iloanusi C, Bjork S, DiRuggiero J: Physiological responses of the halophilic archaeon Halobacteriumsp. strain NRC1 to desiccation and gamma irradiation. Extremophiles2005, 9(3):219–227.
DiRuggiero J, Santangelo N, Nackerdien Z, Ravel J, Robb FT: Repair of extensive ionizing-radiation DNA damage at 95 degrees C in the hyperthermophilic archaeon Pyrococcus furiosus. J Bacteriol1997, 179(14):4643–4645.
Jolivet E, Matsunaga F, Ishino Y, Forterre P, Prieur D, Myllykallio H: Physiological responses of the hyperthermophilic archaeon " Pyrococcus abyssi" to DNA damage caused by ionizing radiation. J Bacteriol2003, 185(13):3958–3961.
Jolivet E, Corre E, L'Haridon S, Forterre P, Prieur D: Thermococcus marinussp. nov. and Thermococcus radiotoleranssp. nov., two hyperthermophilic archaea from deep-sea hydrothermal vents that resist ionizing radiation. Extremophiles2004, 8(3):219–227.
Jolivet E, L'Haridon S, Corre E, Forterre P, Prieur D: Thermococcus gammatoleranssp. nov., a hyperthermophilic archaeon from a deep-sea hydrothermal vent that resists ionizing radiation. Int J Syst Evol Microbiol2003, 53(Pt 3):847–851.
Yoshinaka T, Yano K, Yamaguchi H: Isolation of highly radioresistant bacterium, Arthrobacter radiotoleransnov. sp. Agr Biol Chem1973, 37(10):2269–2275.
Ferreira AC, Nobre MF, Moore E, Rainey FA, Battista JR, da Costa MS: Characterization and radiation resistance of new isolates of Rubrobacter radiotoleransand Rubrobacter xylanophilus. Extremophiles1999, 3(4):235–238.
Chen MY, Wu SH, Lin GH, Lu CP, Lin YT, Chang WC, Tsay SS: Rubrobacter taiwanensissp. nov., a novel thermophilic, radiation-resistant species isolated from hot springs. Int J Syst Evol Microbiol2004, 54(Pt 5):1849–1855.
Phillips RW, Wiegel J, Berry CJ, Fliermans C, Peacock AD, White DC, Shimkets LJ: Kineococcus radiotoleranssp. nov., a radiation-resistant, gram-positive bacterium. Int J Syst Evol Microbiol2002, 52(Pt 3):933–938.
Gtari M, Essoussi I, Maaoui R, Sghaier H, Boujmil R, Gury J, Pujic P, Brusetti L, Chouaia B, Crotti E et al: Contrasted resistance of stone-dwelling Geodermatophilaceaespecies to stresses known to give rise to reactive oxygen species. FEMS Microbiol Ecol2012, 80(3):566–577.
Montero-Calasanz MC, Hofner B, Göker M, Rohde M, Spröer C, Hezbri K, Gtari M, Schumann P, Klenk HP: Geodermatophilus poikilotrophisp. nov.: a multitolerant actinomycete isolated from dolomitic marble. Biomed Res Int2014, 2014:11.
Montero-Calasanz MC, Hezbri K, Göker M, Sghaier H, Rohde M, Spröer C, Schumann P, Klenk HP: Description of gamma radiation-resistant Geodermatophilus dictyosporussp. nov. to accommodate the not validly named Geodermatophilus obscurussubsp. dictyosporus(Luedemann, 1968). Extremophiles2015, 19(1):77–85.
Billi D, Friedmann EI, Hofer KG, Caiola MG, Ocampo-Friedmann R: Ionizing-radiation resistance in the desiccation-tolerant cyanobacterium Chroococcidiopsis. Appl Environ Microbiol2000, 66(4):1489–1492.
Badri H, Monsieurs P, Coninx I, Wattiez R, Leys N: Molecular investigation of the radiation resistance of edible cyanobacterium Arthrospirasp. PCC 8005. Microbiologyopen2015:doi: 10.1002/mbo1003.1229.
Albuquerque L, Simoes C, Nobre MF, Pino NM, Battista JR, Silva MT, Rainey FA, da Costa MS: Truepera radiovictrixgen. nov., sp. nov., a new radiation resistant species and the proposal of Trueperaceaefam. nov. FEMS Microbiol Lett2005, 247(2):161–169.
Dong N, Li HR, Yuan M, Zhang XH, Yu Y: Deinococcus antarcticussp. nov., isolated from soil. Int J Syst Evol Microbiol2015, 65(Pt 2):331–335.
Srinivasan S, Lee JJ, Lim SY, Joe MH, Im SH, Kim MK: Deinococcus radioresistenssp. nov., a UV and gamma radiation-resistant bacterium isolated from mountain soil. Antonie Van Leeuwenhoek2015, 107(2):539–545.
Ito H, Iizuka H: Taxonomic studies on a radio-resistant Pseudomonas. Part XII. Studies on the microorganisms of cereal grain. Agric Biol Chem1971, 35(10):1566–1571.
Nishimura Y, Uchida K, Tanaka K, Ino T, Ito H: Radiation sensitivities of Acinetobacterstrains isolated from clinical sources. J Basic Microbiol1994, 34(5):357–360.
Collins MD, Hutson RA, Grant IR, Patterson MF: Phylogenetic characterization of a novel radiation-resistant bacterium from irradiated pork: description of Hymenobacter actinosclerussp. nov. Int J Syst Evol Microbiol2000, 50(Pt 2):731–734.
Yu LZ, Luo XS, Liu M, Huang Q: Diversity of ionizing radiation-resistant bacteria obtained from the Taklimakan Desert. J Basic Microbiol2015, 55(1):135–140.
Shahmohammadi HR, Asgarani E, Terato H, Saito T, Ohyama Y, Gekko K, Yamamoto O, Ide H: Protective roles of bacterioruberin and intracellular KCl in the resistance of Halobacterium salinariumagainst DNA-damaging agents. J Radiat Res1998, 39(4):251–262.
Yang Y, Itoh T, Yokobori S, Itahashi S, Shimada H, Satoh K, Ohba H, Narumi I, Yamagishi A: Deinococcus aeriussp. nov., isolated from the high atmosphere. Int J Syst Evol Microbiol2009, 59(Pt 8):1862–1866.
Yang Y, Itoh T, Yokobori S, Shimada H, Itahashi S, Satoh K, Ohba H, Narumi I, Yamagishi A: Deinococcus aetheriussp. nov., isolated from the stratosphere. Int J Syst Evol Microbiol2010, 60(Pt 4):776–779.
de Groot A, Chapon V, Servant P, Christen R, Saux MF, Sommer S, Heulin T: Deinococcus desertisp. nov., a gamma-radiation-tolerant bacterium isolated from the Sahara Desert. Int J Syst Evol Microbiol2005, 55(Pt 6):2441–2446.
Shashidhar R, Kumar SA, Misra HS, Bandekar JR: Evaluation of the role of enzymatic and nonenzymatic antioxidant systems in the radiation resistance of Deinococcus. Can J Microbiol2010, 56(3):195–201.
Daly MJ, Gaidamakova EK, Matrosova VY, Vasilenko A, Zhai M, Venkateswaran A, Hess M, Omelchenko MV, Kostandarithes HM, Makarova KS et al: Accumulation of Mn(II) in Deinococcus radioduransfacilitates gamma-radiation resistance. Science2004, 306(5698):1025–1028.
Makarova KS, Omelchenko MV, Gaidamakova EK, Matrosova VY, Vasilenko A, Zhai M, Lapidus A, Copeland A, Kim E, Land M et al: Deinococcus geothermalis: the pool of extreme radiation resistance genes shrinks. PLoS One2007, 2(9):e955.
Ferreira AC, Nobre MF, Rainey FA, Silva MT, Wait R, Burghardt J, Chung AP, da Costa MS: Deinococcus geothermalissp. nov. and Deinococcus murrayisp. nov., two extremely radiation-resistant and slightly thermophilic species from hot springs. Int J Syst Bacteriol1997, 47(4):939–947.
Yuan M, Zhang W, Dai S, Wu J, Wang Y, Tao T, Chen M, Lin M: Deinococcus gobiensissp. nov., an extremely radiation-resistant bacterium. Int J Syst Evol Microbiol2009, 59(Pt 6):1513–1517.
Chanal A, Chapon V, Benzerara K, Barakat M, Christen R, Achouak W, Barras F, Heulin T: The desert of Tataouine: an extreme environment that hosts a wide diversity of microorganisms and radiotolerant bacteria. Environ Microbiol2006, 8(3):514–525.
Oyaizu H, Stackebrandt E, Schleifer KH, Ludwig W, Pohla H, Ito H, Hirata A, Oyaizu Y, Komagata K: A radiation-resistant rod-shaped bacterium, Deinobacter grandisgen. nov., sp. nov., with peptidoglycan containing ornithine. Int J Syst Bacteriol1987, 37:62–67.
Sun J, Shen P, Chao H, Wu B: Isolation and identification of a new radiation-resistant bacterium Deinococcus guangriensissp.nov. and analysis of its radioresistant character. Wei Sheng Wu Xue Bao2009, 49(7):918–924.
Shashidhar R, Bandekar JR: Deinococcus mumbaiensissp. nov., a radiation-resistant pleomorphic bacterium isolated from Mumbai, India. FEMS Microbiol Lett2006, 254(2):275–280.
Shashidhar R, Bandekar JR: Deinococcus piscissp. nov., a radiation-resistant bacterium isolated from a marine fish. Int J Syst Evol Microbiol2009, 59(Pt 11):2714–2717.
Battista JR, Earl AM, Park MJ: Why is Deinococcus radioduransso resistant to ionizing radiation? Trends Microbiol1999, 7(9):362–365.
Bauermeister A, Bentchikou E, Moeller R, Rettberg P: Roles of PprA, IrrE, and RecA in the resistance of Deinococcus radioduransto germicidal and environmentally relevant UV radiation. Arch Microbiol2009, 191(12):913–918.
Shukla M, Chaturvedi R, Tamhane D, Vyas P, Archana G, Apte S, Bandekar J, Desai A: Multiple-stress tolerance of ionizing radiation-resistant bacterial isolates obtained from various habitats: correlation between stresses. Curr Microbiol2007, 54(2):142–148.
Battista JR: Against all odds: the survival strategies of Deinococcus radiodurans. Annu Rev Microbiol1997, 51:203–224.
Lewis NF: Studies on a radio-resistant coccus isolated from Bombay duck (Harpodon nehereus). J Gen Microbiol1971, 66(1):29–35.
Davis NS, Silverman GJ, Keller WH: Combined effects of ultrahigh vacuum and temperature on the viability of some spores and soil organisms. Appl Microbiol1963, 11:202–210.
Harris DR, Pollock SV, Wood EA, Goiffon RJ, Klingele AJ, Cabot EL, Schackwitz W, Martin J, Eggington J, Durfee TJ et al: Directed evolution of ionizing radiation resistance in Escherichia coli. J Bacteriol2009, 191(16):5240–5252.
Wheeler DL, Chappey C, Lash AE, Leipe DD, Madden TL, Schuler GD, Tatusova TA, Rapp BA: Database resources of the National Center for Biotechnology Information. Nucleic Acids Res2000, 28(1):10–14.
Tatusov RL, Galperin MY, Natale DA, Koonin EV: The COG database: a tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Res2000, 28(1):33–36.
Imlay JA: Pathways of oxidative damage. Annu Rev Microbiol2003, 57:395–418.
Halliwell B, Gutteridge JMC: Free Radicals in Biology and Medicine, 4 edn. Oxford: Oxford University Press; 2007.
Ghosal D, Omelchenko MV, Gaidamakova EK, Matrosova VY, Vasilenko A, Venkateswaran A, Zhai M, Kostandarithes HM, Brim H, Makarova KS et al: How radiation kills cells: survival of Deinococcus radioduransand Shewanella oneidensisunder oxidative stress. FEMS Microbiol Rev2005, 29(2):361–375.
Messner KR, Imlay JA: Mechanism of superoxide and hydrogen peroxide formation by fumarate reductase, succinate dehydrogenase, and aspartate oxidase. J Biol Chem2002, 277(45):42563–42571.
Daly MJ: A new perspective on radiation resistance based on Deinococcus radiodurans. Nat Rev Microbiol2009, 7(3):237–245.
Daly MJ, Gaidamakova EK, Matrosova VY, Kiang JG, Fukumoto R, Lee DY, Wehr NB, Viteri GA, Berlett BS, Levine RL: Small-molecule antioxidant proteome-shields in Deinococcus radiodurans. PLoS One2010, 5(9):e12570.
Webb KM, DiRuggiero J: Role of Mn2+ and compatible solutes in the radiation resistance of thermophilic Bacteria and Archaea. Archaea2012, 2012:11.
Robinson CK, Webb K, Kaur A, Jaruga P, Dizdaroglu M, Baliga NS, Place A, Diruggiero J: A major role for nonenzymatic antioxidant processes in the radioresistance of Halobacterium salinarum. J Bacteriol2011, 193(7):1653–1662.
Narumi I, Satoh K, Cui S, Funayama T, Kitayama S, Watanabe H: PprA: a novel protein from Deinococcus radioduransthat stimulates DNA ligation. Mol Microbiol2004, 54(1):278–285.
Tanaka M, Earl AM, Howell HA, Park MJ, Eisen JA, Peterson SN, Battista JR: Analysis of Deinococcus radiodurans's transcriptional response to ionizing radiation and desiccation reveals novel proteins that contribute to extreme radioresistance. Genetics2004, 168(1):21–33.
Gutman PD, Fuchs P, Minton KW: Restoration of the DNA damage resistance of Deinococcus radioduransDNA polymerase mutants by Escherichia coliDNA polymerase I and Klenow fragment. Mutat Res1994, 314(1):87–97.
Huang L, Hua X, Lu H, Gao G, Tian B, Shen B, Hua Y: Three tandem HRDC domains have synergistic effect on the RecQ functions in Deinococcus radiodurans. DNA Repair (Amst)2007, 6(2):167–176.
Servinsky MD, Julin DA: Effect of a recDmutation on DNA damage resistance and transformation in Deinococcus radiodurans. J Bacteriol2007, 189(14):5101–5107.
Zhang L, Yang Q, Luo X, Fang C, Zhang Q, Tang Y: Knockout of crtBor crtIgene blocks the carotenoid biosynthetic pathway in Deinococcus radioduransR1 and influences its resistance to oxidative DNA-damaging agents due to change of free radicals scavenging ability. Arch Microbiol2007, 188(4):411–419.
Bentchikou E, Servant P, Coste G, Sommer S: Additive effects of SbcCD and PolX deficiencies in the in vivo repair of DNA double-strand breaks in Deinococcus radiodurans. J Bacteriol2007, 189(13):4784–4790.
Lecointe F, Shevelev IV, Bailone A, Sommer S, Hubscher U: Involvement of an X family DNA polymerase in double-stranded break repair in the radioresistant organism Deinococcus radiodurans. Mol Microbiol2004, 53(6):1721–1730.
Singh OV, Gabani P: Extremophiles: radiation resistance microbial reserves and therapeutic implications. J Appl Microbiol2011, 110(4):851–861.
Gabani P, Singh OV: Radiation-resistant extremophiles and their potential in biotechnology and therapeutics. Appl Microbiol Biotechnol2013, 97(3):993–1004.
Gaidamakova EK, Myles IA, McDaniel DP, Fowler CJ, Valdez PA, Naik S, Gayen M, Gupta P, Sharma A, Glass PJ et al: Preserving immunogenicity of lethally irradiated viral and bacterial vaccine epitopes using a radio- protective Mn2+-Peptide complex from Deinococcus. Cell Host Microbe2012, 12(1):117–124.
Daly MJ: Engineering radiation-resistant bacteria for environmental biotechnology. Curr Opin Biotechnol2000, 11(3):280–285.
Appukuttan D, Rao AS, Apte SK: Engineering of Deinococcus radioduransR1 for bioprecipitation of uranium from dilute nuclear waste. Appl Environ Microbiol2006, 72(12):7873–7878.
Appukuttan D, Seetharam C, Padma N, Rao AS, Apte SK: PhoN-expressing, lyophilized, recombinant Deinococcus radioduranscells for uranium bioprecipitation. J Biotechnol2011, 154(4):285–290.
Kulkarni S, Ballal A, Apte SK: Bioprecipitation of uranium from alkaline waste solutions using recombinant Deinococcus radiodurans. J Hazard Mater2013, 262:853–861.
Misra CS, Appukuttan D, Kantamreddi VS, Rao AS, Apte SK: Recombinant D. radioduranscells for bioremediation of heavy metals from acidic/neutral aqueous wastes. Bioeng Bugs2012, 3(1):44–48.
Misra CS, Mukhopadhyaya R, Apte SK: Harnessing a radiation inducible promoter of Deinococcus radioduransfor enhanced precipitation of uranium. J Biotechnol2014, 189:88–93.
Brim H, Venkateswaran A, Kostandarithes HM, Fredrickson JK, Daly MJ: Engineering Deinococcus geothermalisfor bioremediation of high-temperature radioactive waste environments. Appl Environ Microbiol2003, 69(8):4575–4582.
Lea D, Catcheside D: The mechanism of the induction by radiation of chromosome aberrations in tradesoantia. J Genet1942, 44:216–245.
Kellerer AM, Rossi HH: A generalized formulation of dual radiation action. Radiat Res1978, 75(3):471–488.
Chadwick KH, Leenhouts HP: A molecular theory of cell survival. Phys Med Biol1973, 18(1):78–87.
Brahme A: Accurate description of the cell survival and biological effect at low and high doses and LET's. J Radiat Res2011, 52(4):389–407.
Lind BK, Persson LM, Edgren MR, Hedlof I, Brahme A: Repairable-conditionally repairable damage model based on dual Poisson processes. Radiat Res2003, 160(3):366–375.
Lea D: Actions of radiations on living cells. Cambridge: University Press; 1946.
Tobias CA: The repair-misrepair model in radiobiology: comparison to other models. Radiat Res Suppl1985, 8:S77–95.
Curtis SB: Lethal and potentially lethal lesions induced by radiation--a unified repair model. Radiat Res1986, 106(2):252–270.
Sontag W: A discrete cell survival model including repair after high dose-rate of ionizing radiation. Int J Radiat Biol1997, 71(2):129–144.
Salata F, D’Orazio A, Fabiani M, D’Alessandro D: Effectiveness of UV radiation for reducing Aspergillus Nigerand Actynomicescontamination in air-conditioning systems. In: Proceedings of Clima 2007 WellBeing Indoors: 10 Jun 2007 – 14 Jun 2007; Helsinki (Finland): FINVAC; 2007: 8.
McCullagh P, Nelder JA: Generalized Linear Models. London: Chapman & Hall; 1989.
R Development Core Team: R: a language and environment for statistical computing. R Foundation for Statistical Computinghttp://www.R-project.org 2007.
Knezevic SZ, Streibig JC, Ritz C: Utilizing R software package for dose-response studies: the concept and data analysis. Weed Technol2007, 21:840–848.
Hofner B: Lethal: compute lethal doses (LD) with confidence intervals. R package, https://github.com/hofnerb/lethal 2014.