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Original Articles

The colonization of an irradiated environment: the case of microbial biofilm in a nuclear reactor

ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon & ORCID Icon show all
Pages 108-121 | Received 25 Nov 2022, Accepted 19 Aug 2023, Published online: 03 Nov 2023

References

  • Alamri SA. 2010. Biodegradation of microcystin by a new Bacillus sp. isolated from a Saudi freshwater lake. Afr J Biotechnol. 9(39):6552–6559.
  • Albarracín VH, Gärtner W, Farias ME. 2013. UV resistance and photoreactivation of extremophiles from high altitude Andean Lakes. J Photochem Photobiol B: Biol. 1–4.
  • Alrumman SA, Hesham AEL, Alamri SA. 2016. Isolation, fingerprinting and genetic identification of indigenous PAHs degrading bacteria from oil-polluted soils. J Environ Biol. 37(1):75.
  • Ambrožič K, Žerovnik G, Snoj L. 2017. Computational analysis of the dose rates at JSI TRIGA reactor irradiation facilities. Appl Radiat Isot. 130:140–152. doi:10.1016/j.apradiso.2017.09.022
  • Arkatkar A, Juwarkar AA, Bhaduri S, Uppara PV, Doble M. 2010. Growth of Pseudomonas and Bacillus biofilms on pretreated polypropylene surface. Int Biodeterior Biodegrad. 64(6):530–536. doi:10.1016/j.ibiod.2010.06.002
  • 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. 41(1):19–34. doi:10.1269/jrr.41.19
  • Atamanyuk NI, Osipov DI, Tryapitsina GA, Deryabina LV, Stukalov PM, Ivanov IA, Pryakhin EA. 2012. Characteristics of phytoplankton in lake Karachay, a storage reservoir of medium-level radioactive waste. Health Phys. 103(1):47–49. doi:10.1097/HP.0b013e318249bebf
  • Baqué M, Viaggiu E, Scalzi G, Billi D. 2013. Endurance of the endolithic desert cyanobacterium Chroococcidiopsis under UVC radiation. Extremophiles. 17(1):161–169. doi:10.1007/s00792-012-0505-5
  • Battista JR. 2016. Radiation tolerance. eLS. Hoboken (NJ): Wiley; p. 1–10.
  • Bebout BM, Garcia-Pichel F. 1995. UV B-induced vertical migrations of cyanobacteria in a microbial mat. Appl Environ Microbiol. 61(12):4215–4222. doi:10.1128/aem.61.12.4215-4222.1995
  • Billi D, Baqué M, Verseux C, Rothschild L, de Vera JP. 2017. Desert cyanobacteria: potential for space and Earth applications. In: Stan-Lotter H, Fendrihan S, editors. Adaption of microbial life to environmental extremes. 2nd ed. Cham: Springer International Publishing; p. 133–146.
  • Billi D, Friedmann EI, Hofer KG, Caiola MG, Ocampo-Friedmann R. 2000. Ionizing-radiation resistance in the desiccation-tolerant cyanobacterium Chroococcidiopsis. Appl Environ Microbiol. 66(4):1489–1492. doi:10.1128/AEM.66.4.1489-1492.2000
  • Busse HJ, Wieser M, Buczolits S. 2015. Arthrobacter. In: Whitman WB, supervising editor. Bergey’s manual of systematics of archaea and bacteria. Hoboken (NJ): Wiley, in association with Bergey's Manual Trust.
  • Chapon V, Piette L, Vesvres M-H, Coppin F, Marrec CL, Christen R, Theodorakopoulos N, Février L, Levchuk S, Martin-Garin A, et al. 2012. Microbial diversity in contaminated soils along the T22 trench of the Chernobyl experimental platform. Appl Geochem. 27(7):1375–1383. doi:10.1016/j.apgeochem.2011.08.011
  • Cheptsov VS, Vorobyova EA, Manucharova NA, Gorlenko MV, Pavlov AK, Vdovina MA, Lomasov VN, Bulat SA. 2017. 100 kGy gamma-affected microbial communities within the ancient Arctic permafrost under simulated Martian conditions. Extremophiles. 21(6):1057–1067. doi:10.1007/s00792-017-0966-7
  • Conn HJ, Dimmick I. 1947. Soil bacteria similar in morphology to Mycobacterium and Corynebacterium. J Bacteriol. 54(3):291–303. doi:10.1128/jb.54.3.291-303.1947
  • Daly MJ, Gaidamakova EK, Matrosova VY, Vasilenko A, Zhai M, Venkateswaran A, Hess M, Omelchenko MV, Kostandarithes HM, Makarova KS, et al. 2004. Accumulation of Mn (II) in Deinococcus radiodurans facilitates gamma-radiation resistance. Science. 306(5698):1025–1028. doi:10.1126/science.1103185
  • Daly MJ. 2009. A new perspective on radiation resistance based on Deinococcus radiodurans. Nat Rev Microbiol. 7(3):237–245. doi:10.1038/nrmicro2073
  • DSMZ. 2014; [accessed May 26]. https://www.dsmz.de/collection/catalogue/microorganisms/culture-technology/list-of-media-for-microorganisms.
  • Egas C, Barroso C, Froufe HJC, Pacheco J, Albuquerque L, da Costa MS. 2014. Complete genome sequence of the radiation-resistant bacterium Rubrobacter radiotolerans RSPS-4. Stand Genomic Sci. 9(3):1062–1075. doi:10.4056/sigs.5661021
  • Fredrickson JK, Zachara JM, Kennedy DW, Kukkadapu RK, McKinley JP, Heald SM, Liu C, Plymale AE. 2004. Reduction of TcO4− by sediment-associated biogenic Fe (II). Geochim Cosmochim Acta. 68(15):3171–3187. doi:10.1016/j.gca.2003.10.024
  • Fricke H. 1952. Effect of ionizing radiation on protein denaturation. Nature. 169(4310):965–966. doi:10.1038/169965a0
  • Fujii M, Takano Y, Kojima H, Hoshino T, Tanaka R, Fukui M. 2010. Microbial community structure, pigment composition, and nitrogen source of red snow in Antarctica. Microb Ecol. 59(3):466–475. doi:10.1007/s00248-009-9594-9
  • Fuma S, Kawaguchi I, Kubota Y, Yoshida S, Kawabata ZI, Polikarpov GG. 2012. Effects of chronic γ-irradiation on the aquatic microbial microcosm: equi-dosimetric comparison with effects of heavy metals. J Environ Radioact. 104:81–86. doi:10.1016/j.jenvrad.2011.09.005
  • Gao B, Gupta RS. 2012. Phylogenetic framework and molecular signatures for the main clades of the phylum Actinobacteria. Microbiol Mol Biol Rev. 76(1):66–112. doi:10.1128/MMBR.05011-11
  • Ghorbal SKB, Chourabi K, Maalej L, Ammar AB, Ouzari H-I, Hassen A, Jaafoura H, Chatti A. 2019. Pseudomonas aeruginosa swarmer cells adaptation toward UVc radiations. Front Microbiol. 10:556. doi:10.3389/fmicb.2019.00556
  • Han J-I, Choi H-K, Lee S-W, Orwin PM, Kim J, Laroe SL, Kim T-G, O'Neil J, Leadbetter JR, Lee SY, et al. 2011. Complete genome sequence of the metabolically versatile plant growth-promoting endophyte Variovorax paradoxus S110. J Bacteriol. 193(5):1183–1190. doi:10.1128/JB.00925-10
  • Hing JN, Jong BC, Liew PWY, Elly Ellyna R, Shamsudin S. 2022. Gamma radiation dose–response of gram-positive and gram-negative bacteria. Malay Appl Biol. 51(5):107–112. doi:10.55230/mabjournal.v51i5.2370
  • Horneck G, Klaus DM, Mancinelli RL. 2010. Space microbiology. Microbiol Mol Biol Rev. 74(1):121–156. doi:10.1128/MMBR.00016-09
  • Islam E, Sar P. 2016. Diversity, metal resistance and uranium sequestration abilities of bacteria from uranium ore deposit in deep earth stratum. Ecotoxicol Environ Saf. 127:12–21. doi:10.1016/j.ecoenv.2016.01.001
  • Kämpfer P, Rainey FA, Andersson MA, Nurmiaho Lassila EL, Ulrych U, Busse HJ, Weiss N, Mikkola R, Salkinoja-Salonen M. 2000. Frigoribacterium faeni gen. nov., sp. nov., a novel psychrophilic genus of the family Microbacteriaceae. Int J Syst Evol Microbiol. 50(1):355–363. doi:10.1099/00207713-50-1-355
  • Kausar J, Ohyama Y, Terato H, Ide H, Yamamoto O. 1997. 16S rRNA gene sequence of Rubrobacter radiotolerans and its phylogenetic alignment with members of the genus Arthrobacter, gram-positive bacteria, and members of the family Deinococcaceae. Int J Syst Bacteriol. 47(3):684–686. doi:10.1099/00207713-47-3-684
  • Krisko A, Radman M. 2013. Biology of extreme radiation resistance: the way of Deinococcus radiodurans. Cold Spring Harb Perspect Biol. 5(7):a012765. doi:10.1101/cshperspect.a012765
  • La Duc MT, Kern R, Venkateswaran K. 2004. Microbial monitoring of spacecraft and associated environments. Microb Ecol. 47(2):150–158. doi:10.1007/s00248-003-1012-0
  • Leonardo T, Farhi E, Boisson AM, Vial J, Cloetens P, Bohic S, Rivasseau C. 2014. Determination of elemental distribution in green micro-algae using synchrotron radiation nano X-ray fluorescence (SR-nXRF) and electron microscopy techniques – subcellular localization and quantitative imaging of silver and cobalt uptake by Coccomyxa actinabiotis. Metallomics. 6(2):316–329. doi:10.1039/c3mt00281k
  • Lloyd JR, Renshaw JC. 2005. Bioremediation of radioactive waste: radionuclide–microbe interactions in laboratory and field-scale studies. Curr Opin Biotechnol. 16(3):254–260. doi:10.1016/j.copbio.2005.04.012
  • Makarova KS, Omelchenko MV, Gaidamakova EK, Matrosova VY, Vasilenko A, Zhai M, Lapidus A, Copeland A, Kim E, Land M, et al. 2007. Deinococcus geothermalis: the pool of extreme radiation resistance genes shrinks. PLOS One. 2(9):e955. doi:10.1371/journal.pone.0000955
  • 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. doi:10.1128/jb.178.3.633-637.1996
  • McLeod MP, Warren RL, Hsiao WWL, Araki N, Myhre M, Fernandes C, Miyazawa D, Wong W, Lillquist AL, Wang D, et al. 2006. The complete genome of Rhodococcus sp. RHA1 provides insights into a catabolic powerhouse. Proc Natl Acad Sci U S A. 103(42):15582–15587. doi:10.1073/pnas.0607048103
  • 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(1–2):1–9. doi:10.1016/j.apsoil.2007.03.011
  • Miwa H, Ahmed I, Yoon J, Yokota A, Fujiwara T. 2008. Variovorax boronicumulans sp. nov., a boron-accumulating bacterium isolated from soil. Int J Syst Evol Microbiol. 58(Pt 1):286–289. doi:10.1099/ijs.0.65315-0
  • Moeller R, Horneck G, Facius R, Stackebrandt E. 2005. Role of pigmentation in protecting Bacillus sp. endospores against environmental UV radiation. FEMS Microbiol Ecol. 51(2):231–236. doi:10.1016/j.femsec.2004.08.008
  • Moeller R, Reitz G, Li Z, Klein S, Nicholson WL. 2012. Multifactorial resistance of Bacillus subtilis spores to high-energy proton radiation: role of spore structural components and the homologous recombination and non-homologous end joining DNA repair pathways. Astrobiology. 12(11):1069–1077. doi:10.1089/ast.2012.0890
  • Moissl C, Osman S, La Duc MT, Dekas A, Brodie E, DeSantis T, Venkateswaran K. 2007. Molecular bacterial community analysis of clean rooms where spacecraft are assembled. FEMS Microbiol Ecol. 61(3):509–521. doi:10.1111/j.1574-6941.2007.00360.x
  • 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. doi:10.1089/ast.2014.1278
  • Nagar V, Pansare Godambe L, Shashidhar R. 2017. Radiation sensitivity of planktonic and biofilm‐associated Shigella spp. and Aeromonas spp. on food and food‐contact surfaces. Int J Food Sci Technol. 52(1):258–265. doi:10.1111/ijfs.13277
  • Panitz C, Frösler J, Wingender J, Flemming HC, Rettberg P. 2019. Tolerances of Deinococcus geothermalis biofilms and planktonic cells exposed to space and simulated Martian conditions in low earth orbit for almost two years. Astrobiology. 19(8):979–994. doi:10.1089/ast.2018.1913
  • Pavlopoulou A, Savva GD, Louka M, Bagos PG, Vorgias CE, Michalopoulos I, Georgakilas AG. 2016. Unraveling the mechanisms of extreme radioresistance in prokaryotes: lessons from nature. Mutat Res Rev Mutat Res. 767:92–107. doi:10.1016/j.mrrev.2015.10.001
  • Pepe-Ranney C, Koechli C, Potrafka R, Andam C, Eggleston E, Garcia-Pichel F, Buckley DH. 2016. Non-cyanobacterial diazotrophs mediate dinitrogen fixation in biological soil crusts during early crust formation. ISME J. 10(2):287–298. doi:10.1038/ismej.2015.106
  • Piotrowska-Seget Z, Cycoń M, Kozdroj J. 2005. Metal-tolerant bacteria occurring in heavily polluted soil and mine spoil. Appl Soil Ecol. 28(3):237–246. doi:10.1016/j.apsoil.2004.08.001
  • Rao S, Chan OW, Lacap-Bugler DC, Pointing SB. 2016. Radiation-tolerant bacteria isolated from high altitude soil in Tibet. Indian J Microbiol. 56(4):508–512. doi:10.1007/s12088-016-0604-6
  • Ravnik M, Jeraj R. 2003. Research reactor benchmarks. Nucl Sci Eng. 145(1):145–152. doi:10.13182/NSE03-A2370
  • Reddy GS, Prakash JS, Prabahar V, Matsumoto GI, Stackebrandt E, Shivaji S. 2003. Kocuria polaris sp. nov., an orange-pigmented psychrophilic bacterium isolated from an Antarctic cyanobacterial mat sample. Int J Syst Evol Microbiol. 53(Pt 1):183–187. doi:10.1099/ijs.0.02336-0
  • Rivasseau C, Farhi E, Compagnon E, de Gouvion Saint Cyr D, van Lis R, Falconet D, Kuntz M, Atteia A, Couté A. 2016. Coccomyxa actinabiotis sp. nov. (Trebouxiophyceae, Chlorophyta), a new green microalga living in the spent fuel cooling pool of a nuclear reactor. J Phycol. 52(5):689–703. doi:10.1111/jpy.12442
  • Romanovskaya VA, Rokitko PV, Mikheev AN, Gushcha NI, Malashenko YR, Chernaya NA. 2002. The effect of γ-radiation and desiccation on the viability of the soil bacteria isolated from the alienated zone around the Chernobyl Nuclear Power Plant. Microbiology. 71(5):608–613. doi:10.1023/A:1020575223365
  • Sajjad W, Ahmad M, Khan S, Ilyas S, Hasan F, Celik C, McPhail K, Shah AA. 2017. Radio-protective and antioxidative activities of astaxanthin from newly isolated radio-resistant bacterium Deinococcus sp. strain WMA-LM9. Ann Microbiol. 67(7):443–455. doi:10.1007/s13213-017-1269-z
  • Salter SJ, Cox MJ, Turek EM, Calus ST, Cookson WO, Moffatt MF, Turner P, Parkhill J, Loman NJ, Walker AW. 2014. Reagent and laboratory contamination can critically impact sequence-based microbiome analyses. BMC Biol. 12:1–2. doi:10.1186/s12915-014-0087-z
  • Schink B. 2002. Synergistic interactions in the microbial world. Antonie Van Leeuwenhoek. 81(1–4):257–261. doi:10.1023/a:1020579004534
  • Shanson DC. 1989. Disinfection and sterilization. In: Shanson DC, editor. Microbiology in Clinical Practice. 2nd ed. Guildford: Butterworth-Heinemann; p. 610–625.
  • Shivaji S, Chaturvedi P, Begum Z, Pindi PK, Manorama R, Padmanaban DA, Shouche YS, Pawar S, Vaishampayan P, Dutt CBS, et al. 2009. Janibacter hoylei sp. nov., Bacillus isronensis sp. nov. and Bacillus aryabhattai sp. nov., isolated from cryotubes used for collecting air from the upper atmosphere. Int J Syst Evol Microbiol. 59(Pt 12):2977–2986. doi:10.1099/ijs.0.002527-0
  • Shuryak I. 2019. Review of microbial resistance to chronic ionizing radiation exposure under environmental conditions. J Environ Radioact. 196:50–63. doi:10.1016/j.jenvrad.2018.10.012
  • Siasou E, Johnson D, Willey NJ. 2017. An extended dose–response model for microbial responses to ionizing radiation. Front Environ Sci. 5:6. doi:10.3389/fenvs.2017.00006
  • Siezen RJ. 2011. Microbial sunscreens. Microb Biotechnol. 4(1):1–7. doi:10.1111/j.1751-7915.2010.00241.x
  • Silva AJ, Benitez JA. 2016. Vibrio cholerae biofilms and cholera pathogenesis. PLoS Negl Trop Dis. 10(2):e0004330. doi:10.1371/journal.pntd.0004330
  • Singh SP, Häder DP, Sinha RP. 2010. Cyanobacteria and ultraviolet radiation (UVR) stress: mitigation strategies. Ageing Res Rev. 9(2):79–90. doi:10.1016/j.arr.2009.05.004
  • Snoj L, Kavčič A, Žerovnik G, Ravnik M. 2010. Calculation of kinetic parameters for mixed TRIGA cores with Monte Carlo. Ann Nucl Energy. 37(2):223–229. doi:10.1016/j.anucene.2009.10.020
  • Snoj L, Trkov A, Jaćimović R, Rogan P, Žerovnik G, Ravnik M. 2011. Analysis of neutron flux distribution for the validation of computational methods for the optimization of research reactor utilization. Appl Radiat Isot. 69(1):136–141. doi:10.1016/j.apradiso.2010.08.019
  • Stoeckel M, Lücking G, Ehling-Schulz M, Atamer Z, Hinrichs J. 2016. Bacterial spores isolated from ingredients, intermediate and final products obtained from dairies: thermal resistance in milk. Dairy Sci Technol. 96(4):569–577. doi:10.1007/s13594-016-0279-0
  • Suzuki KI, Collins MD, Iijima E, Komagata K. 1988. Chemotaxonomic characterization of a radiotolerant bacterium, Arthrobacter radiotolerans: description of Rubrobacter radiotolerans gen. nov., comb. nov. FEMS Microbiol Lett. 52(1–2):33–39. doi:10.1111/j.1574-6968.1988.tb02568.x
  • Suzuki Y, Banfield JF. 2004. Resistance to, and accumulation of, uranium by bacteria from a uranium-contaminated site. Geomicrobiol J. 21(2):113–121. doi:10.1080/01490450490266361
  • Tamponnet C, Martin-Garin A, Gonze M-A, Parekh N, Vallejo R, Sauras-Yera T, Casadesus J, Plassard C, Staunton S, Norden M, et al. 2008. An overview of BORIS: bioavailability of radionuclides in soils. J Environ Radioact. 99(5):820–830. doi:10.1016/j.jenvrad.2007.10.011
  • Thakur RK, Shirkot P. 2017. Exploration of Western Himalayan region for identification of gold nanoparticles synthesizing bacteria. bioRxiv. 164103.
  • Theodorakopoulos N, Février L, Barakat M, Ortet P, Christen R, Piette L, Levchuk S, Beaugelin-Seiller K, Sergeant C, Berthomieu C, et al. 2017. Soil prokaryotic communities in Chernobyl waste disposal trench T22 are modulated by organic matter and radionuclide contamination. FEMS Microbiol Ecol. 93(8). doi:10.1093/femsec/fix079
  • Thornley MJ, Horne RW, Glauert AM. 1965. The fine structure of Micrococcus radiodurans. Arch Mikrobiol. 51(3):267–289. doi:10.1007/BF00408143
  • [UNSCEAR Report] United Nations Scientific Committee on the Effects of Atomic Radiation. 2000. Sources and effects of ionizing radiation, United Nations Scientific Committee on the Effects of Atomic Radiation (UNSCEAR) 2000 Report, Volume I: report to the General Assembly, with Scientific Annexes-Sources. New York (NY): United Nations.
  • Vaishampayan P, Probst A, Krishnamurthi S, Ghosh S, Osman S, McDowall A, Ruckmani A, Mayilraj S, Venkateswaran K. 2010. Bacillus horneckiae sp. nov., isolated from a spacecraft-assembly clean room. Int J Syst Evol Microbiol. 60(Pt 5):1031–1037. doi:10.1099/ijs.0.008979-0
  • Verseux C, Baqué M, Lehto K, de Vera JPP, Rothschild LJ, Billi D. 2016. Sustainable life support on Mars – the potential roles of cyanobacteria. Int J Astrobiol. 15(1):65–92. doi:10.1017/S147355041500021X
  • Weisburg WG, Barns SM, Pelletier DA, Lane DJ. 1991. 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol. 173(2):697–703. doi:10.1128/jb.173.2.697-703.1991
  • Willems A, De Ley J, Gillis M, Kersters K. 1991. Comamonadaceae, a new family encompassing the acidovorans rRNA complex, including Variovorax paradoxus gen. nov., comb. nov., for Alcaligenes paradoxus (Davis 1969). Int J Syst Evol Microbiol. 41(3):445–450.
  • Wilson KH, Blitchington RB, Greene RC. 1990. Amplification of bacterial 16S ribosomal DNA with polymerase chain reaction. J Clin Microbiol. 28(9):1942–1946. doi:10.1128/jcm.28.9.1942-1946.1990
  • Zakrzewska A, van Eikenhorst G, Burggraaff JEC, Vis DJ, Hoefsloot H, Delneri D, Oliver SG, Brul S, Smits GJ. 2011. Genome-wide analysis of yeast stress survival and tolerance acquisition to analyze the central trade-off between growth rate and cellular robustness. Mol Biol Cell. 22(22):4435–4446. doi:10.1091/mbc.E10-08-0721
  • Zavilgelsky GB, Abilev SK, Sukhodolets VV, Ahmad SI. 1998. Isolation and analysis of UV and radio-resistant bacteria from Chernobyl. J Photochem Photobiol B. 43(2):152–157. doi:10.1016/S1011-1344(98)00099-2
  • Zhdanova NN, Zakharchenko VA, Vember VV, Nakonechnaya LT. 2000. Fungi from Chernobyl: mycobiota of the inner regions of the containment structures of the damaged nuclear reactor. Mycol Res. 104(12):1421–1426. doi:10.1017/S0953756200002756