Skip to main content
SpringerLink
Log in

100 kGy gamma-affected microbial communities within the ancient Arctic permafrost under simulated Martian conditions

  • Original Paper
  • Published:
Extremophiles Aims and scope Submit manuscript

Abstract

This research aimed to investigate the viability and biodiversity of microbial communities within ancient Arctic permafrost after exposure to a gamma-radiation dose of 100 kGy at low temperature (− 50 °C), low pressure (1 Torr) and dehydration conditions. The main objective was to assess the possibility for long-term survival of Earth-bound microorganisms in the subsurface of Martian regolith or inside small space bodies at constant absorption and accumulation of the gamma radiation dose. Investigated microbial communities had shown high resistance to a simulated Martian environment. After irradiation the total count of prokaryotic cells and number of metabolically active bacterial cells remained at the control level, while the number of bacterial CFUs decreased by 2 orders of magnitude, and the number of metabolically active cells of archaea decreased threefold. Besides, the abundance of culturable bacteria after irradiation was kept at a high level: not less than 3.7 × 105 cells/g. Potential metabolic activity of irradiated microbial communities in general were higher than in the control sample. A fairly high biodiversity of bacteria was detected in the exposed sample of permafrost, although the microbial community structure underwent significant changes after irradiation. In particular, actinobacteria populations of the genus Arthrobacter, which was not revealed in the control samples, became predominant in bacterial communities following the exposure. The results of the study testify that long-term preservation of microbial life inside Martian permafrost is possible. The data obtained can also be evaluated from the perspective of the potential for discovering viable Earth-bound microorganisms on other objects in the Solar system and inside of small bodies in outer space.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Arkhangelov AA (1977) The subsurface glaciation of the North of Kolyma lowland in the late Cenozoic era (article in Russian). Probl Cryolithol 4:26–57

    Google Scholar 

  • Arkhangelov AA, Kusnetsova TP, Kartashova GG, Konzkhin MA (1979) The genesis and formation of the late Pleistocene ice-rich silt formation in Kolyma Lowlands (on the example of Chukochiy Cape) (article in Russian). Probl Cryolithol 8:110–135

    Google Scholar 

  • Atlas RM (2010) Handbook of microbiological media. CRC Press, Boca Raton

    Book  Google Scholar 

  • Auerbach C (1976) Mutation research. Problems, results and perspectives. Chapman and Hall, London

    Google Scholar 

  • Bauermeister A, Moeller R, Reitz G, Sommer S, Rettberg P (2011) Effect of relative humidity on Deinococcus radiodurans’ resistance to prolonged desiccation, heat, ionizing, germicidal, and environmentally relevant UV radiation. Microb Ecol 61(3):715–722

    Article  CAS  PubMed  Google Scholar 

  • Baumstark-Khan C, Facius R (2002) Life under conditions of ionizing radiation. In: Horneck G, Baumstark-Khan C (eds) Astrobiology: the quest for the conditions of life. Springer, Berlin, pp 261–284

    Chapter  Google Scholar 

  • Beaty DW, Clifford SM, Borg LE, Catling DC, Craddock RA, Marais DJD, Farmer JD, Frey HV, Haberle RH, McKay CP, Newsom HE, Parker TJ, Segura T, Tanaka KL (2005) Key science questions from the second conference on early Mars: geologic, hydrologic, and climatic evolution and the implications for life. Astrobiology 5(6):663–689

    Article  PubMed  Google Scholar 

  • Cox MM, Battista JR (2005) Deinococcus radiodurans—the consummate survivor. Nat Rev Microbiol 3(11):882–892

    Article  CAS  PubMed  Google Scholar 

  • Dartnell LR, Desorgher L, Ward JM, Coates AJ (2007a) Modelling the surface and subsurface Martian radiation environment: implications for astrobiology. Geophys Res Lett 34:L02207

    Article  Google Scholar 

  • Dartnell LR, Desorgher L, Ward JM, Coates AJ (2007b) Martian subsurface ionising radiation: biosignatures and geology. Biogeosciences 4:545–558

    Article  CAS  Google Scholar 

  • Dartnell LR, Hunter SJ, Lovell KV, Coates AJ, Ward JM (2010) Low-temperature ionizing radiation resistance of Deinococcus radiodurans and Antarctic Dry Valley bacteria. Astrobiology 10(7):2010

    Article  Google Scholar 

  • Dieser M, Battista JR, Christner BC (2013) DNA double-strand break repair at − 15 °C. Appl Environ Microbiol 79(24):7662–7668

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • DiRuggiero J, Wierzchos J, Robinson CK, Souterre T, Ravel J, Artieda O, Souza-Egipsy V, Ascaso C (2013) Microbial colonisation of chasmoendolithic habitats in the hyper-arid zone of the Atacama Desert. Biogeosciences 10:2439–2450

    Article  Google Scholar 

  • El-Registan GI, Mulyukin AL, Nikolaev YA, Suzina NE, Gal’chenko VF, Duda VI (2006) Adaptogenic functions of extracellular autoregulators of microorganisms. Microbiology 75(4):380–389

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Ferreira AC, Nobre MF, Moore E, Rainey FA, Battista JR, daCosta MS (1999) Characterization and radiation resistance of new isolates of Rubrobacter radiotolerans and Rubrobacter xylanophilus. Extremophiles 3:235–238

    Article  CAS  PubMed  Google Scholar 

  • Garland JL, Mills AL (1991) Classification and characterization of heterotrophic microbial communities on the basis of patterns of community-level sole-carbon-source utilization. Appl Environ Microbiol 57(8):2351–2359

    CAS  PubMed  PubMed Central  Google Scholar 

  • Garland JL, Mills AL (1994) A community-level physiological approach for studying microbial communities. In: Ritz K, Dighton J, Giller KE (eds) Beyond the biomass: compositional and functional analysis of soil microbial communities. Wiley, Chichester, pp 77–83

    Google Scholar 

  • Gilichinsky D (2002) Permafrost as a microbial habitat. In: Bitton G (ed) Encyclopedia of environmental microbiology. Wiley, New York, pp 932–956

    Google Scholar 

  • Gilichinsky D, Vorobyova E, Erokhina I, Fyodorov-Davydov D, Chaikovskaya N (1992) Long-term preservation of microbial ecosystems in permafrost. Adv Space Res 12(4):255–263

    Article  CAS  PubMed  Google Scholar 

  • Giliichinsky DA, Wilson GS, Friedmann EI, McKay CP, Sletten RS, Rivkina EM, Vishnivetskaya TA, Erokhina LG, Ivanushkina NE, Kochkina GA, Shcherbakova VA, Soina VS, Spirina EV, Vorobyova EA, Fyodorov-Davydov DG, Hallet B, Ozerskaya SM, Sorokovikov VA, Laurinavichyus KS, Shatilovich AV, Chanton JP, Ostroumov VE, Tiedje JM (2007) Microbial populations in Antarctic permafrost. Astrobiology 7(2):275–311

    Article  Google Scholar 

  • Good IJ (1953) The population frequencies of species and the estimation of population parameters. Biometrika 40:237–264

    Article  Google Scholar 

  • Gorlenko MV, Kozhevin PA (1994) Differentiation of soil microbial communities by multisubstrate testing. Microbiology 63(2):158–161

    Google Scholar 

  • Gorlenko MV, Kozhevin PA (2005) Multisubstrate testing of natural microbial communities (book in Russian). MAKS Press, Moscow

    Google Scholar 

  • Gorlenko MV, Majorova TN, Kozhevin PA (1997) Disturbances and their influence on substrate utilization patterns in soil microbial communities. In: Insam H, Rangger A (eds) microbial communities. Springer, Berlin, pp 84–93

    Chapter  Google Scholar 

  • Gorovaya AI, Skvortsov AV (1989) Radiomodifying effect of physiologically active humic substances (article in Russian). In: Rud GY (ed) Interuniversity thematic collection of scientific works. Kishinev Agricultural Institute

  • Halliwell B, Gutteridge JMC (2015) Free radicals in biology and medicine. Oxford University Press, New York

    Book  Google Scholar 

  • Harris DR, Pollock SV, Wood EA, Goiffon RJ, Klingele AJ, Cabot EL, Schackwitz W, Martin J, Eggington J, Durfee TJ, Middle CM, Norton JE, Popelars MC, Li H, Klugman SA, Hamilton LL, Bane LB, Pennacchio LA, Albert TJ, Perna NT, Cox MM, Battista JR (2009) Directed evolution of ionizing radiation resistance in Escherichia coli. J Bacteriol 191(16):5240–5252

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hassler DM, Zeitlin C, Wimmer-Schweingruber RF, Ehresmann B, Rafkin S, Eigenbrode JL, Brinza DE, Weigle G, Böttcher S, Böhm E, Burmeister S, Guo J, Köhler J, Martin C, Reitz G, Cucinotta FA, Kim M, Grinspoon D, Bullock MA, Posner A, Gómez-Elvira J, Vasavada A, Grotzinger JP, Science Team MSL (2014) Mars’ surface radiation environment measured with the Mars Science Laboratory’s Curiosity rover. Science 343(6169):1244797

    Article  PubMed  Google Scholar 

  • Jolivet E, L’Haridon S, Corre E, Forterre P, Prieur D (2003) Thermococcus gammatolerans sp. nov., a hyperthermophilic archaeon from a deep-sea hydrothermal vent that resists ionizing radiation. Int J Syst Evol Microbiol 53(3):847–851

    Article  CAS  PubMed  Google Scholar 

  • Kryazhevskikh NA, Demkina EV, Loiko NG, Baslerov RV, Kolganova TV, Soina VS, Manucharova NA, Gal’chenko VF, El’-Registan GI (2013) Comparison of the adaptive potential of the Arthrobacter oxydans and Acinetobacter lwoffii isolates from permafrost sedimentary rock and the analogous collection strains. Microbiology 82(1):29–42

    Article  CAS  Google Scholar 

  • Kudryashov YB, Berenfeld BS (1982) Fundamentals of radiation biophysics. Study book (book in Russian). MSU, Moscow

    Google Scholar 

  • Kuipers GK, Lafleur MVM (1998) Characterization of DNA damage induced by gamma-radiation derived water radicals, using DNA repair enzymes. Int J Radiat Biol 74(4):511–519

    Article  CAS  PubMed  Google Scholar 

  • Manaeva ES, Lomovtseva NO, Kostina NV, Gorlenko MV, Umarov MM (2014) Biological activity of soils in the settlements of southern (Microtus rossiaemeridionalis) and bank (Clethrionomys glareolus) voles. Biol Bull 41(1):80–88

    Article  CAS  Google Scholar 

  • Manucharova NA, Vlasenko AN, Men’ko EV, Zvyagintsev DG (2011) Specificity of the chitinolytic microbial complex of soils incubated at different temperatures. Microbiology 80(2):205–215

    Article  CAS  Google Scholar 

  • 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(3):633–637

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McNamara NP, Black HIJ, Beresford NA, Parekh NR (2003) Effects of acute gamma irradiation on chemical, physical and biological properties of soils. Appl Soil Ecol 24(2):117–132

    Article  Google Scholar 

  • Mileikowsky C, Cucinotta FA, Wilson JW, Gladman B, Horneck G, Lindegren L, Melosh J, Rickman H, Valtonen M, Zheng JQ (2000) Natural transfer of viable microbes in space: 1. From Mars to Earth and Earth to Mars. Icarus 145(2):391–427

    Article  CAS  PubMed  Google Scholar 

  • Mulyukin AL, Demkina EV, Kozlova AN, Soina VS (2001) Synthesis of anabiosis autoinducers by non-spore-forming bacteria as a mechanism regulating their activity in soil and subsoil sedimentary rocks. Microbiology 70(5):535–541

    Article  CAS  Google Scholar 

  • 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(12):1076–1090

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nicholson WL, Munakata N, Horneck G, Melosh HJ, Setlow P (2000) Resistance of Bacillus endospores to extreme terrestrial and extraterrestrial environments. Microbiol Mol Biol Rev 64(3):548–572

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Osman S, Peeters Z, La Duc MT, Mancinelli R, Ehrenfreund P, Venkateswaran K (2008) Effect of shadowing on survival of bacteria under conditions simulating the Martian atmosphere and UV radiation. Appl Environ Microbiol 74(4):959–970

    Article  CAS  PubMed  Google Scholar 

  • Parro V, de Diego-Castilla G, Moreno-Paz M, Blanco Y, Cruz-Gil P, Rodríguez-Manfredi JA, Fernández-Remolar D, Gómez F, Gómez MJ, Rivas LA, Demergasso C, Echeverría A, Urtuvia VN, Ruiz-Bermejo M, García-Villadangos M, Postigo M, Sánchez-Román M, Chong-Díaz G, Gómez-Elvira J (2011) A microbial oasis in the hypersaline Atacama subsurface discovered by a life detector chip: implications for the search for life on Mars. Astrobiology 11(10):969–996

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pavlov AK, Blinov AV, Konstantinov AN (2002) Sterilization of Martian surface by cosmic radiation. Planet Space Sci 50(7):669–673

    Article  CAS  Google Scholar 

  • Pavlov AK, Kalinin VL, Konstantinov AN, Shelegedin VN, Pavlov AA (2006) Was Earth ever infected by martian biota? Clues from radioresistant bacteria. Astrobiology 6(6):911–918

    Article  CAS  PubMed  Google Scholar 

  • Pavlov AK, Shelegedin VN, Vdovina MA, Pavlov AA (2010) Growth of microorganisms in Martian-like shallow subsurface conditions: laboratory modeling. Int J Astrobiol 9(1):51–58

    Article  CAS  Google Scholar 

  • Pavlov AA, Vasilyev G, Ostryakov VM, Pavlov AK, Mahaffy P (2012) Degradation of the organic molecules in the shallow subsurface of Mars due to irradiation by cosmic rays. Geophys Res Lett 39(13):L13202

    Article  Google Scholar 

  • Pitonzo BJ, Amy PS, Rudin M (1999a) Effect of gamma radiation on native endolithic microorganisms from a radioactive waste deposit site. Radiat Res 152(1):64–70

    Article  CAS  PubMed  Google Scholar 

  • Pitonzo BJ, Amy PS, Rudin M (1999b) Resuscitation of microorganisms after gamma irradiation. Radiat Res 152(1):71–75

    Article  CAS  PubMed  Google Scholar 

  • Rainey FA, Ray K, Ferreira M, Gatz BZ, Nobre MF, Bagaley D, Rash BA, Park M-J, Earl AM, Shank NC, Small AM, Henk MC, Battista JR, Kämpfer 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(9):5225–5235

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rivkina EM, Kraev GN, Krivushin KV, Laurinavichus KS, Fyodorov-Davydov DG, Kholodov AL, Shcherbakova VA, Gilichinsky DA (2006) Methane in permafrost of Northeastern Arctic (article in Russian). Earth Cryosphere 10(3):23–41

    Google Scholar 

  • Romanovskaya VA, Rokitko PV, Malashenko YR, Krishtab TP, Chernaya NA (1999) Sensitivity of soil bacteria isolated from the alienated zone around the chernobyl nuclear power plant to various stress factors. Microbiology 68(4):465–469

    CAS  Google Scholar 

  • Rummel JD, Beaty DW, Jones MA, Bakermans C, Barlow NG, Boston PJ, Chevrier VF, Clark BC, de Vera J-PP, Gough RV, Hallsworth JE, Head JW, Hipkin VJ, Kieft TL, McEwen AS, Mellon MT, Mikucki JA, Nicholson WL, Omelon CR, Peterson R, Roden EE, Lollar BS, Tanaka KL, Viola D, Wray JJ (2014) A new analysis of Mars “special regions”: findings of the second MEPAG Special Regions Science Analysis Group (SR-SAG2). Astrobiology 14(11):887–968

    Article  PubMed  Google Scholar 

  • Sher AV (1971) Mammals and stratigraphy of the Far Northeast USSR and North America (book in Russian). Nauka, Moscow

    Google Scholar 

  • Smith HD, McKay CP (2005) Drilling in ancient permafrost on Mars for evidence of a second genesis of life. Planet Space Sci 53(12):1302–1308

    Article  Google Scholar 

  • Stotzky G, Mortensen JL (1959) Effect of gamma radiation on growth and metabolism of microorganisms in an organic soil. Proc Soil Sci Soc Am 23:125–127

    Article  CAS  Google Scholar 

  • Takai K, Inagaki F, Horikoshi K (2004) Distribution of unusual archaea in subsurface biosphere. In: Wilcock WSD, DeLong EF, Kelley DS, Baross JA, Cary SC (eds) The subseafloor biosphere at mid-ocean ridges, geophysical monograph 144. American Geophysical Union, Washington, DC, pp 369–381

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30(12):2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tauscher C, Schuerger AC, Nicholson WL (2006) Survival and germinability of Bacillus subtilis spores exposed to simulated Mars solar radiation: implications for life detection and planetary protection. Astrobiology 6(4):592–605

    Article  CAS  PubMed  Google Scholar 

  • Tesfai AT, Beamer SK, Matak KE, Jaczynski J (2011) Radio-resistance development of DNA repair deficient Escherichia coli DH5α in ground beef subjected to electron beam at sub-lethal doses. Int J Radiat Biol 87(6):571–578

    Article  CAS  PubMed  Google Scholar 

  • Vago JL, Westall F, Pasteur Instrument Teams, Landing Site Selection Working Group, and Other Contributors, Coates AJ, Jaumann R, Korablev O, Ciarletti V, Mitrofanov I, Josset J-L, De Sanctis MS, Bibring J-P, Rull F, Goesmann F, Steininger H, Goetz W, Brinckerhoff W, Szopa C, Raulin F, Westall F, Edwards HGM, Whyte LG, Fairén AG, Bibring J-P, Bridges J, Hauber E, Ori GG, Werner S, Loizeau D, Kuzmin RO, Williams RME, Flahaut J, Forget F, Vago JL, Rodionov D, Korablev O, Svedhem H, Sefton-Nash E, Kminek G, Lorenzoni L, Joudrier L, Mikhailov V, Zashchirinskiy A, Alexashkin S, Calantropio F, Merlo A, Poulakis P, Witasse O, Bayle O, Bayón S, Meierhenrich U, Carter J, García-Ruiz JM, Baglioni P, Haldemann A, Ball AJ, Debus A, Lindner R, Haessig F, Monteiro D, Trautner R, Voland C, Rebeyre D, Goulty D, Didot F, Durrant S, Zekri E, Koschny D, Toni A, Visentin G, Zwick M, van Winnendael M, Azkarate M, Carreau C, The ExoMars Project Team (2017) Habitability on early Mars and the search for biosignatures with the ExoMars Rover. Astrobiology 17(6–7):471–510

    Article  Google Scholar 

  • Verseux C, Baqué M, Cifariello R, Fagliarone C, Raguse M, Moeller R, Billi D (2017) Evaluation of the resistance of Chroococcidiopsis spp. to sparsely and densely ionizing irradiation. Astrobiology 17(2):118–125

    Article  CAS  PubMed  Google Scholar 

  • Vorobyova EA, Soina VS, Mulukin AL (1996) Microorganisms and enzyme activity in permafrost after removal of long-term cold stress. Adv Space Res 18(12):103–108

    Article  CAS  Google Scholar 

  • Vorobyova E, Soina V, Gorlenko M, Minkovskaya N, Zalinova N, Mamukelashvili A, Gilichinsky D, Rivkina E, Vishnivetskaya T (1997) The deep cold biosphere: facts and hypothesis. FEMS Microbiol Rev 20:277–290

    Article  CAS  Google Scholar 

  • Wassmann M, Moeller R, Reitz G, Rettberg P (2010) Adaptation of Bacillus subtilis cells to archean-like UV climate: relevant hints of microbial evolution to remarkably increased radiation resistance. Astrobiology 10(6):605–615

    Article  CAS  PubMed  Google Scholar 

  • Wierzchos J, de los Ríos A, Ascaso C (2012) Microorganisms in desert rocks: the edge of life on Earth. Int Microbiol 15:171–181

    Google Scholar 

  • Willerslev E, Hansen AJ, Rønn R, Brand TB, Barnes I, Wiuf C, Gilichinsky D, Mitchell D, Cooper A (2004) Long-term persistence of bacterial DNA. Curr Biol 14(1):R9–R10

    Article  CAS  PubMed  Google Scholar 

  • Yardin MR, Kennedy IR, Thies JE (2000) Development of high quality carrier materials for field delivery of key microorganisms used as bio-fertilisers and bio-pesticides. Radiat Phys Chem 57:565–568

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors express their gratitude to D.A. Gilichinsky, now deceased, for the provision of samples of ancient permafrost. The authors are also grateful to D.S. Karlov for the help with experiments and thank the anonymous reviewers for the help in improving the MS. The research was partially supported by the Grant no. 14-50-00029 of the Russian Science Foundation (in part of microbiological analyses), by the Program of Fundamental Research #7 RAS (in part of gamma-irradiation of permafrost samples) as well as the Act 211 Government of the Russian Federation, Agreement no. 02.A03.21.0006 (in part of molecular-biological analyses).

Author information

Authors and Affiliations

  1. Lomonosov Moscow State University, GSP-1, Leninskie Gory 1/12, Moscow, 119991, Russia

    Vladimir S. Cheptsov, Elena A. Vorobyova, Natalia A. Manucharova & Mikhail V. Gorlenko

  2. Space Research Institute, Russian Academy of Sciences, 84/32 Profsoyuznaya Str., Moscow, 117997, Russia

    Vladimir S. Cheptsov & Elena A. Vorobyova

  3. Ioffe Physical-Technical Institute, Russian Academy of Sciences, Polytechnicheskaya Str. 26, St. Petersburg, Russia

    Anatoli K. Pavlov & Maria A. Vdovina

  4. S.-Petersburg State Polytechnical University, Polytechnicheskaya Str. 29, St. Peterburg, 195251, Russia

    Vladimir N. Lomasov

  5. Petersburg Nuclear Physics Institute Named by B.P. Konstantinov of National Research Centre “Kurchatov Institute”, Gatchina, 188300, Russia

    Sergey A. Bulat

  6. Institute of Physics and Technology, Ural Federal University, Ekaterinburg, 620002, Russia

    Sergey A. Bulat

Authors
  1. Vladimir S. Cheptsov
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Elena A. Vorobyova
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Natalia A. Manucharova
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mikhail V. Gorlenko
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Anatoli K. Pavlov
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Maria A. Vdovina
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Vladimir N. Lomasov
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Sergey A. Bulat
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Vladimir S. Cheptsov.

Additional information

Communicated by A. Oren.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cheptsov, V.S., Vorobyova, E.A., Manucharova, N.A. et al. 100 kGy gamma-affected microbial communities within the ancient Arctic permafrost under simulated Martian conditions. Extremophiles 21, 1057–1067 (2017). https://doi.org/10.1007/s00792-017-0966-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00792-017-0966-7

Keywords

Search

Navigation