Community Ecology of Deinococcus in Irradiated Soil

  • Matthew Chidozie Ogwu
  • Sathiyaraj Srinivasan
  • Ke Dong
  • Dhamodharan Ramasamy
  • Bruce WaldmanEmail author
  • Jonathan M. AdamsEmail author
Environmental Microbiology


Deinococcus is a genus of soil bacteria known for radiation resistance. However, the effects of radiation exposure on its community structure are unknown. We exposed soil to three levels of gamma radiation, 0.1 kGy/h (low), 1 kGy/h (medium), and 3 kGy/h (high), once a week for 6 weeks and then extracted soil DNA for 16S rRNA amplicon sequencing. We found the following: (1) Increasing radiation dose produced a major increase in relative abundance of Deinococcus, reaching ~ 80% of reads at the highest doses. Differing abundances of the various Deinococcus species in relation to exposure levels indicate distinct “radiation niches.” At 3 kGy/h, a single OTU identified as D. ficus overwhelmingly dominated the mesocosms. (2) Corresponding published genome data show that the dominant species at 3 kGy/h, D. ficus, has a larger and more complex genome than other Deinococcus species with a greater proportion of genes related to DNA and nucleotide metabolism, cell wall, membrane, and envelope biogenesis as well as more cell cycle control, cell division, and chromosome partitioning-related genes. Deinococcus ficus also has a higher guanine–cytosine ratio than most other Deinococcus. These features may be linked to genome stability and may explain its greater abundance in this apparently competitive system, under high-radiation exposures. (3) Genomic analysis suggests that Deinococcus, including D. ficus, are capable of utilizing diverse carbon sources derived from both microbial cells killed by the radiation (including C5–C12-containing compounds, like arabinose, lactose, N-acetyl-d-glucosamine) and plant-derived organic matter in the soil (e.g., cellulose and hemicellulose). (4) Overall, based on its metagenome, even the most highly irradiated (3 kGy/h) soil possesses a wide range of the activities necessary for a functional soil system. Future studies may consider the resilience and sustainability of such soils in a high-radiation environment.


Bacterial community Deinococcus–Thermus Gamma irradiation 16S rRNA sequencing Legacy effects Radiation-resistant 


Authors’ Contributions

JA and SS conceived the research questions and prepared the project strategy. KD did the field sampling and supervised the irradiation treatments, laboratory work, and 16S sequencing. MCO carried out the bioinformatics analysis of the 16s amplicon datasets, devised the data analysis methods, and carried out the analysis with contributions from SS and DR. MCO and JA interpreted the results, prepared all the draft versions, and co-wrote the main manuscript text. BW advised on the project at all stages. All the authors improved, reviewed, and approved the revisions and accepted the final manuscript.

Funding Information

This work was supported by the Basic Science Research Program of the National Research Foundation of Korea funded by the Ministry of Education (2016E1D1A1B03930385 and 2017R1D1A1B03035583). Matthew Chidozie Ogwu received the research support of BK-21 and the National Institute for International Education, Republic of Korea. Dhamodharan Ramasamy is a recipient of BK-21 Plus Postdoctoral Fellowship, Republic of Korea.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no competing interests.

Supplementary material

248_2019_1343_MOESM1_ESM.docx (1.6 mb)
ESM 1 (DOCX 1666 kb)


  1. 1.
    Stroes-Gascoyne S, Lucht LM, Borsa J, Delaney TL, Haveman SA, Hamon CJ (1994) Radiation resistance of the natural microbial population in buffer materials. MRS Online Proc Libr 353.
  2. 2.
    Lucht LM, Stroes-Gascoyne S (1996) Characterization of the radiation and heat resistance of the natural microbial population in buffer materials and selected pure cultures. Atomic Energy of Canada Limited, technical record. TR-744/COG-96–171. Atomic Energy of Canada, Ltd., Chalk RiverGoogle Scholar
  3. 3.
    Shuryak I, Matrosova VY, Gaidamakova EK, Tkavc R, Grichenko O, Klimenkova P, Volpe RP, Daly MJ (2017) Microbial cells can cooperate to resist high-level chronic ionizing radiation. PLoS One 12:e0189261. CrossRefGoogle Scholar
  4. 4.
    Wright SJL, Hill EC (1968) The development of radiation-resistant cultures of Escherichia coli I by a process of ‘growth-irradiation cycles’. J Gen Microbiol 51:97–106CrossRefGoogle Scholar
  5. 5.
    Jeon SH, Kang M-S, Joo ES, Kim EB, Lim S, Jeong S-W, Jung H-Y, Srinivasan S, Kim MK (2016) Deinococcus persicinus sp. nov., a radiation resistant bacterium from soil. Int J Syst Evol Microbiol 66:5077–5082. CrossRefGoogle Scholar
  6. 6.
    Popenoe H, Eno CF (1962) The effect of gamma radiation on the microbial population of the soil. Soil Sci Soc Am J 26:164–167CrossRefGoogle Scholar
  7. 7.
    Rainey FA, Ray K, Ferreira M, Gatz BZ, Nobre MF, Bagaley D, Rash BA, Park M-J, Earl AM, Shank NC, Small AL, Henk MC, Battista JR, Kampfer P, da Costa MS (2005) Extensive diversity of ionizing-radiation-resistant bacteria recovered from Sonoran desert soil and description of nine new species of the genus Deinococcus obtained from a single soil sample. Appl Environ Microbiol 71:5225–5235. CrossRefGoogle Scholar
  8. 8.
    McNamara NP, Griffiths RI, Tabouret A, Beresford NA, Bailey MJ, Whiteley AS (2007) The sensitivity of a forest soil microbial community to acute gamma-irradiation. Appl Soil Ecol 37:1–9CrossRefGoogle Scholar
  9. 9.
    Brown AR, Boothman C, Pimblott SM, Lloyd JR (2015) The impact of gamma radiation on sediment microbial processes. Appl Environ Microbiol 81:4014–4025. CrossRefGoogle Scholar
  10. 10.
    El-Sayed WS, Ghanem S (2009) Bacterial community structure change induced by gamma irradiation in hydrocarbon contaminated and uncontaminated soils revealed by PCR-denaturing gradient gel electrophoresis. Biotechnology 8:78–85. CrossRefGoogle Scholar
  11. 11.
    Monib M, Zayed MN (1963) The effect of gamma radiation on some of the organisms of soil. J Appl Bacteriol 26:35–42CrossRefGoogle Scholar
  12. 12.
    McLaren AD (1969) Radiation as a technique in soil biology and biochemistry. Soil Biol Biochem 1:63–73CrossRefGoogle Scholar
  13. 13.
    Romanovskaia VA, Rokitko PV, Mikheev AN, Gushcha NI, Malashenko I-UR, Chernaia NA (2002) The effect of gamma-radiation and desiccation on the viability of the soil bacteria isolated from the alienated zone around the Chernobyl nuclear power plant. Mikrobiologiia 71:705–712Google Scholar
  14. 14.
    Brown AR (2013) The impact of ionizing radiation on microbial cells pertinent to the storage, disposal and remediation of radioactive waste. A thesis submitted to the University of Manchester for the degree of Doctor of Philosophy in the Faculty of Engineering and Physical Sciences. 236 p. Accessed 12 June 2018
  15. 15.
    Brown AR, Small JS, Pimblott SM, Goodacre R, Lloyd JR (2017) The impact of ionizing radiation on microbial cells pertinent to the geological disposal of radioactive waste. Radioactive Waste Management Limited, UK. 43pGoogle Scholar
  16. 16.
    Venkateswaran A, McFarlan SC, Ghosal D, Minton KW, Vasilenko A, Makarova K, Wackett LP, Daly MJ (2000) Physiologic determinants of radiation resistance in Deinococcus radiodurans. Appl Environ Microbiol 66:2620–2626CrossRefGoogle Scholar
  17. 17.
    Sukhi SS, Shashidhar R, Kumar SA, Bandekar JR (2009) Radiation resistance of Deinococcus radiodurans R1 with respect to growth phase. FEMS Microbiol Lett 297:49–53CrossRefGoogle Scholar
  18. 18.
    Bornot J, Molina-Jouve C, Uribelarrea J-L, Gorret N (2015) Quantitative characterization of the growth of Deinococcus geothermalis DSM-11302: effect of inoculum size, growth medium and culture conditions. Microorganisms 3:441–463. CrossRefGoogle Scholar
  19. 19.
    Ragon M, Restoux G, Moreira D, Møller AP, López-García P (2011) Sunlight-exposed biofilm microbial communities are naturally resistant to Chernobyl ionizing-radiation levels. PLoS One 6:e21764. CrossRefGoogle Scholar
  20. 20.
    Ruiz-González MX, Czirják GA, Genevaux P, Møller AP, Mousseau TA, Heeb P (2016) Resistance of feather-associated bacteria to intermediate levels of ionizing radiation near Chernobyl. Sci Rep 6:22969CrossRefGoogle Scholar
  21. 21.
    Castillo H, Smith GB (2017) Below-background ionizing radiation as an environmental cue for bacteria. Front Microbiol 8:177. Google Scholar
  22. 22.
    Repar J, Supek F, Klanjscek T, Warnecke T, Zahradka K, Zahradka D (2017) Elevated rate of genome rearrangements in radiation-resistant bacteria. Genetics 205:1677–1689. CrossRefGoogle Scholar
  23. 23.
    Mattimore V, Battista JR (1996) Radioresistance of Deinococcus radiodurans: functions necessary to survive ionizing radiation are also necessary to survive prolonged desiccation. J Bacteriol 178:633–637CrossRefGoogle Scholar
  24. 24.
    Saito T, Terato H, Yamamoto O (1994) Pigments of Rubrobacter radiotolerans. Arch Microbiol 162:414–421CrossRefGoogle Scholar
  25. 25.
    Asgarani E, Terato H, Asagoshi K, Shahmohammadi HR, Ohyama Y, Saito T, Yamamoto O, Ide H (2000) Purification and characterization of a novel DNA repair enzyme from the extremely radioresistant bacterium Rubrobacter radiotolerans. J Radiat Res (Tokyo) 41:19–34CrossRefGoogle Scholar
  26. 26.
    Liu Y, Zhou J, Omelchenko MV, Beliaev AS, Venkateswaran A, Stair J, Wu L, Thompson DK, Xu D, Rogozin IB, Gaiadamakova EK, Zhai M, Makarova KS, Koonin EV, Daly MJ (2003) Transcriptome dynamics of Deinococcus radiodurans recovering from ionizing radiation. Proc Natl Acad Sci USA 100:4191–4196. CrossRefGoogle Scholar
  27. 27.
    de la Torre JR, Goebel BM, Friedmann EI, Pace NR (2003) Microbial diversity of cryptoendolithic communities from the McMurdo Dry Valleys, Antarctica. Appl Environ Microbiol 69:3858–3867CrossRefGoogle Scholar
  28. 28.
    Zhdanova NN, Redchits TI, Zheltonozhsky VA, Sadovnikov LV, Gerzabek MH, Olsson S, Strebl F, Muck K (2003) Accumulation of radionuclides from radioactive substrata by some micromycetes. J Environ Radioact 67:119–130. CrossRefGoogle Scholar
  29. 29.
    Robinson CK, Webb K, Kaur A, Jaruga P, Dizdaroglu M, Baliga NS, Place A, DiRuggiero J (2011) A major role for nonenzymatic antioxidant processes in the radioresistance of Halobacterium salinarum. J Bacteriol 193:1653–1662. CrossRefGoogle Scholar
  30. 30.
    Rowell MJ, Florence ZA (1993) Characteristics associated with differences between undisturbed and industrially-disturbed soil. Soil Biol Biochem 25:1499–1151CrossRefGoogle Scholar
  31. 31.
    Rowell MJ (2000) Measurement of soil organic matter: a compromise between efficacy and environmental friendliness. Agricola 2000:66–69Google Scholar
  32. 32.
    Rowell DL (2014) Soil science: methods and applications. Routledge, New YorkCrossRefGoogle Scholar
  33. 33.
    Kalra YP (1995) Determination of pH of soils by different methods: collaborative study. J AOAC Int 78:310–324Google Scholar
  34. 34.
    Thomas GW (1982) Exchangeable cations. In: Page AL, Miller RH, Kenny DR (eds) Method of soil analysis part-2. American Society of Agronomy, Madison, pp 159–165Google Scholar
  35. 35.
    Bray RH, Kurtz LT (1945) Determination of total, organic, and available forms of phosphorus in soils. Soil Sci 59:39–45CrossRefGoogle Scholar
  36. 36.
    Dong K, Moroenyane I, Tripathi B, Kerfahi D, Takahashi K, Yamamoto N, An C, Cho H, Adams J (2017) Soil nematode show a mid-elevation diversity maximum and elevation zonation on Mt. Norikura, Japan. Sci Rep 7:3028Google Scholar
  37. 37.
    Nadkarni MA, Martin FE, Jacques NA, Hunter N (2002) Determination of bacterial load by real-time PCR using a broad-range (universal) probe and primers set. Microbiology 148:257–266CrossRefGoogle Scholar
  38. 38.
    Hospodsky D, Yamamoto N, Peccia J (2010) Accuracy, precision, and method detection limits of quantitative PCR for airborne bacteria and fungi. Appl Environ Microbiol 76:7004–7012CrossRefGoogle Scholar
  39. 39.
    Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541. CrossRefGoogle Scholar
  40. 40.
    Chun J, Lee JH, Jung Y, Kim M, Kim S, Kim BK, Lim YW (2007) EzTaxon: a web-based tool for the identification of prokaryotes based on 16S ribosomal RNA gene sequences. Int J Syst Evol Microbiol 57:2259–2261CrossRefGoogle Scholar
  41. 41.
    Huse SM, Welch DM, Morrison HG, Sogin ML (2008) Ironing out the wrinkles in the rare biosphere through improved OTU clustering. Environ Microbiol 12:1889–1898. CrossRefGoogle Scholar
  42. 42.
    Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200. CrossRefGoogle Scholar
  43. 43.
    R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna Google Scholar
  44. 44.
    Oksanen J, Blanchet F, Kindt R, Legendre P, O’Hara R, Simpson G, Solymos P, Stevens M, Wagner H (2013) Vegan: community ecology package. R package version 2:3–2 Available at
  45. 45.
    Tao T (2010) Standalone BLAST setup for Unix. In: BLAST® Help [internet]. Bethesda: National Center for Biotechnology Information (US). Available from: Accessed 19 Aug 2018
  46. 46.
    Meyer F, Paarmann D, D’Souza M, Olson R, Glass EM, Kubal M, Paczian T, Rodriguez A, Stevens R, Wilke A (2008) The metagenomics RAST server—a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinformatics 9:386CrossRefGoogle Scholar
  47. 47.
    Krogh A, Larsson B, von Heijne G, Sonnhammer EL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305:567–580. CrossRefGoogle Scholar
  48. 48.
    Huang L, Zhang H, Wu P, Entwistle S, Li X, Yohe T, Yi H, Yang Z, Yin Y (2018) dbCAN-seq: a database of carbohydrate-active enzyme (CAZyme) sequence and annotation. Nucleic Acids Res 46:D516–D521. CrossRefGoogle Scholar
  49. 49.
    Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM, Kubal M, Meyer F, Olsen GJ, Olsen R, Osterman AL, Overbeek RA, McNeil LK, Paarmann D, Paczian T, Parrello B, Pusch GD, Reich C, Stevens R, Vassieva O, Vonstein V, Wilke A, Zagnitko O (2008) The RAST server: rapid annotations using subsystems technology. BMC Genomics 9:75. CrossRefGoogle Scholar
  50. 50.
    Pogoda VU, Rettberg P, Douki T, Cadet J, Horneck G (2005) Sensitivity to polychromatic UV-radiation of strains of Deinococccus radiodurans differing in their DNA repair capacity. Int J Radiat Biol 81(8):601–611. CrossRefGoogle Scholar
  51. 51.
    Romanovskaya VA, Sokolov IG, Rokitko PV, Chernaya NA (1998) Effect of radioactive contamination on soil bacteria in the 10-km zone around the Chernobyl Nuclear Power Plant. Microbiology 67:226–231Google Scholar
  52. 52.
    Ryan PC, Fernanda N, Patrick MM, John RB, Rafael NG, Christopher PM, Milton SC, Fred AR (2008) Description of four novel psychrophilic, ionizing radiation-sensitive Deinococcus species from alpine environments. Int J Syst Evol Microbiol 58:1252–1258CrossRefGoogle Scholar
  53. 53.
    Liu D, Keiblinger KM, Schindbacher A, Wegner U, Sun H, Fuchs S, Lassek C, Riedel K, Zechmeister-Bolternstern S (2017) Microbial functionality as affected by experimental warming of a temperate mountain forest soil—a metaproteomics survey. Appl Soil Ecol 117–118:196–202. CrossRefGoogle Scholar
  54. 54.
    Theodorakopoulos N, Bachar D, Christen R, Alain K, Chapon V (2013) Exploration of Deinococcus-Thermus molecular diversity by novel group-specific PCR primers. Microbiologyopen 2:862–872. Google Scholar
  55. 55.
    Pereira LB, Vicentini R, Ottoboni LMM (2014) Changes in the bacterial community of soil from a neutral mine drainage channel. PLoS One 9:e96605. CrossRefGoogle Scholar
  56. 56.
    Li C-H, Tang L-S, Jia Z-J, Li Y (2015) Profile changes in the soil microbial community when desert becomes oasis. PLoS One 10:e0139626. CrossRefGoogle Scholar
  57. 57.
    Musilova M, Wright G, Ward JM, Dartnell LR (2015) Isolation of radiation-resistant bacteria from Mars Analog Antarctic Dry Valleys by preselection, and the correlation between radiation and desiccation resistance. Astrobiology 15:1076–1090CrossRefGoogle Scholar
  58. 58.
    Beblo-Vranesevic K, Bohmeier M, Perras AK, Schwendner P, Rabbow E, Moissl-Eichinger C, Cockell CS, Vannier P, Marteinsson PT, Monaghan EP, Ehrenfreund P, Garcia-Descalzo L, Gómez F, Malki M, Amils R, Gaboyer F, Westall F, Cabezas P, Walter N, Rettberg P (2018) Lack of correlation of desiccation and radiation tolerance in microorganisms from diverse extreme environments tested under anoxic conditions. FEMS Microbiol Lett 365.
  59. 59.
    Cox MM, Battista JR (2005) Deinococcus radiodurans—the consummate survivor. Nat Rev Microbiol 3:882–892CrossRefGoogle Scholar
  60. 60.
    Makarova KS, Aravind L, Wolf YI, Tutosov RL, Minton KW, Koonin EV, Daly MJ (2001) Genome of the extremely radiation-resistant bacterium Deinococcus radiodurans viewed from the perspective of comparative genomics. Microbiol Mol Biol Rev 65:44–79CrossRefGoogle Scholar
  61. 61.
    Makarova KS, Omelchenko MV, Gaidamakova EK, Matrosova VY, Vasilenko A, Zhai M, Lapidus A, Copeland A, Kim E, Land M, Mavromatis K, Pitluck S, Richardson PM, Detter C, Brettin T, Saunders E, Lai B, Ravel B, Kemner KM, Wolf YI, Sorokin A, Gerasimova AV, Gelfand MS, Fredrickson JK, Koonin EV, Daly MJ (2007) Deinococcus geothermalis: the pool of extreme radiation resistance genes shrinks. PLoS One 2:e955. CrossRefGoogle Scholar
  62. 62.
    Ngo KV, Molzberger ET, Chitterni-Pattu S, Cox MM (2013) Regulation of Deinococcus radiodurans RecA protein function via modulation of active and inactive nucleoprotein filament states. J. Biol. Chem. 288:21351–21366.
  63. 63.
    Ghedira K, Othman H, Saied T, Baccar ZM, Hosni F, Hamzaoui AH, Thamaraiselvi K, Abdelmelek H, Srairi-Abid N, Costa MC, Sghaier H, Saleh HE-DM, Rahman ROM (2016) Insights into ionizing-radiation-resistant bacteria S-layer proteins and nanobiotechnology for bioremediation of hazardous and radioactive waste. Management of hazardous wastes. IntechOpen, Rijeka. Google Scholar
  64. 64.
    Fredrickson JK, Li SM, Gaidamakova EK, Matrosova VY, Zhai M, Sulloway HM, Scholten JC, Brown MG, Balkwill DL, Daly MJ (2008) Protein oxidation: key to bacterial desiccation resistance? ISME J 2:393–403. CrossRefGoogle Scholar
  65. 65.
    Daly M (2009) A new perspective on radiation resistance based on Deinococcus radiodurans. Nat Rev Microbiol 7:237–245CrossRefGoogle Scholar
  66. 66.
    Slade D, Radman M (2011) Oxidative stress resistance in Deinococcus radiodurans. Microbiol Mol Biol Rev 75:133–191. CrossRefGoogle Scholar
  67. 67.
    White O, Eisen JA, Heidelberg JF, Hickey EK, Peterson JD, Dodson RJ, Haft DH, Gwinn ML, Nelson WC, Richardson DL, Moffat KS, Qin H, Jiang L, Pamphile W, Crosby M, Shen M, Vamathevan JJ, Lam P, McDonald L, Utterback T, Zalewski C, Makarova KS, Aravind L, Daly MJ, Minton KW, Fleischmann RD, Ketchum KA, Nelson KE, Salzberg S, Smith HO, Venter JC, Fraser CM (1999) Genome sequence of the radioresistant bacterium Deinococcus radiodurans R1. Science 286:1571–1577CrossRefGoogle Scholar
  68. 68.
    Hess M (2003) Analysis of Deinococcus radiodurans mutants. University of Konstanz, Konstanz 84p. Google Scholar
  69. 69.
    Redon CE, Bonner WM (2011) High salt and DNA double-strand breaks. Proc Natl Acad Sci USA 108:20281–20282. CrossRefGoogle Scholar
  70. 70.
    Slade D, Lindner AB, Paul G, Radman M (2009) Recombination and replication in DNA repair of heavily irradiated Deinococcus radiodurans. Cell 136:1044–1055. CrossRefGoogle Scholar
  71. 71.
    Hassan FMN, Gupta RS (2018) Novel sequence features of DNA repair genes/proteins from Deinococcus species implicated in protection from oxidatively generated damage. Genes 9:149. CrossRefGoogle Scholar
  72. 72.
    Lai W-A, Kampfer P, Arun AB, Shen F-T, Huber B, Rekha PD, Young C-C (2006) Deinococcus ficus sp. nov., isolated from the rhizosphere of Ficus religiosa L. Int J Syst Evol Microbiol 56:787–791. CrossRefGoogle Scholar
  73. 73.
    Ghosal D, Omelchenko MV, Gaiadamakova EK, Matrosova VY, Vasilenko A, Venkateswaran A, Zhai M, Kostandarithes HM, Brim H, Makarova KS, Wackett LP, Fredrickson JK, Daly MJ (2005) How radiation kills cells: survival of Deinococcus radiodurans and Shewanella oneidensis under oxidative stress. FEMS Microbiol Rev 29:361–375Google Scholar
  74. 74.
    Chou FI, Tan ST (1990) Manganese (II) induces cell division and increases in superoxide dismutase and catalase activities in an aging deinococcal culture. J Bacteriol 172:2029–2035CrossRefGoogle Scholar
  75. 75.
    Ferreira AC, Nobre MF, Rainey FA, Silva MT, Wait R, Burghardt J, Chung AP, da Costa MS (1997) Deinococcus geothermalis sp. nov. and Deinococcus murrayi sp. nov., two extremely radiation-resistant and slightly thermophilic species from hot springs. Int J Syst Bacteriol 47:939–947CrossRefGoogle Scholar
  76. 76.
    Spiers AJ (2014) A mechanistic explanation linking adaptive mutation, niche change, and fitness advantage for the wrinkly spreader. Int J Evol Biol 2014:675432.
  77. 77.
    Mao J, Tang Q, Zhang Z, Wang W, Wei D, Huang Y, Liu Z, Shi Y, Goodfellow M (2007) Streptoyces radiopugnans sp. nov., a radiation-resistant actinomycete isolated from radiation polluted soil in China. Int J Syst Evol Microbiol 57:2578–2582. CrossRefGoogle Scholar
  78. 78.
    Mohammadipanah F, Wink J (2016) Actinobacteria from arid and desert habitats: diversity and biological activity. Front. Microbiol. 6.
  79. 79.
    Bhave SV, Shanbhag PV, Sonawane SK, Parab RR, Mahajan GB (2013) Isolation and characterization of halotolerant Streptomyces radiopugnans from Antarctica soil. Lett Appl Microbiol 56:348–355. CrossRefGoogle Scholar
  80. 80.
    Stonesifer J, Baltz RH (1985) Mutagenic DNA repair in Streptomyces. Proc Natl Acad Sci USA 82:1180–1183CrossRefGoogle Scholar
  81. 81.
    Hoff G, Bertrand C, Piotrowski E, Thibessard A, Leblond P (2018) Genome plasticity is governed by double strand break DNA repair in Streptomyces. Sci Rep 8:5272CrossRefGoogle Scholar
  82. 82.
    Lee J-J, Park S-J, Lee Y-H, Lee S-Y, Ten LN, Jung H-Y (2017) Hymenobacter aquaticus sp. nov., a radiation-resistant bacterium isolated from a river. Int J Syst Evol Microbiol 67:1206–1211. CrossRefGoogle Scholar
  83. 83.
    Collins MD, Hutson RA, Grant IR, Patterson MF (2000) Phylogenetic characterization of a novel radiation-resistant bacterium from irradiated pork: description of Hymenobacter actinosclerus sp. nov. Int J Syst Evol Microbiol 50:731–734CrossRefGoogle Scholar
  84. 84.
    Lee JJ, Srinivasan S, Lim S, Joe M, Lee SH, Kwon SA, Kwon YJ, Lee J, Choi JJ, Lee HM, Auh YK, Kim MK (2014) Hymenobacter swuensis sp. nov., a gamma-radiation-resistant bacteria isolated from mountain soil. Curr Microbiol 68:305. CrossRefGoogle Scholar
  85. 85.
    Srinivasan S, Lee S-Y, Kim MK, Jung H-Y (2017) Complete genome sequence of Hymenobacter sp. GD25A, a gamma radiation-resistant bacteria isolated from soil. Mol Cell Toxicol 13:65–72CrossRefGoogle Scholar
  86. 86.
    Seybold CA, Herrick JE, Brejda JJ (1999) Soil resilience: a fundamental component of soil quality. Soil Sci 164:224–234CrossRefGoogle Scholar
  87. 87.
    Caplin N, Willey N (2018) Ionizing radiation, higher plants, and radioprotection: from acute high doses to chronic low doses. Front Plant Sci 9:847. CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Matthew Chidozie Ogwu
    • 1
    • 2
  • Sathiyaraj Srinivasan
    • 3
  • Ke Dong
    • 4
  • Dhamodharan Ramasamy
    • 1
  • Bruce Waldman
    • 1
    • 5
    Email author
  • Jonathan M. Adams
    • 6
    Email author
  1. 1.School of Biological SciencesSeoul National UniversityGwanak-guRepublic of Korea
  2. 2.Department of Plant Biology and BiotechnologyUniversity of BeninBenin CityNigeria
  3. 3.Department of Bio and Environmental Technology, Division of Environmental and Life Science, College of Natural ScienceSeoul Women’s UniversityNowon-guRepublic of Korea
  4. 4.Department of Life SciencesKyonggi UniversitySuwonRepublic of Korea
  5. 5.Department of Integrative BiologyOklahoma State UniversityStillwaterUSA
  6. 6.School of Geographic and Oceanographic SciencesNanjing UniversityNanjingPeople’s Republic of China

Personalised recommendations