Abstract
Field experiments in a contaminated farmland in Nihonmatsu city, Fukushima were conducted to assess the effectiveness of the plant–microbe interaction on removal of radiocesium. Before plowing, 93.3 % of radiocesium was found in the top 5 cm layer (5,718 Bq kg DW−1). After plowing, Cs radioactivity in the 0–15 cm layer ranged from 2,037 to 3,277 Bq kg DW−1. Based on sequential extraction, the percentage of available radiocesium (water soluble + exchangeable) was fewer than 10 % of the total radioactive Cs. The transfer of 137Cs was investigated in three agricultural crops; komatsuna (four cultivars), Indian mustard and buckwheat, inoculated with a Bacillus or an Azospirillum strains. Except for komatsuna Nikko and Indian mustard, inoculation with both strains resulted in an increase of biomass production by the tested plants. The highest 137Cs radioactivity concentration in above-ground parts was found in Bacillus-inoculated komatsuna Nikko (121 Bq kg DW−1), accompanied with the highest 137Cs TF (0.092). Furthermore, komatsuna Nikko-Bacillus and Indian mustard-Azospirillum associations gave the highest 137Cs removal, 131.5 and 113.8 Bq m−2, respectively. Despite the beneficial effect of inoculation, concentrations of 137Cs and its transfer to the tested plants were not very high; consequently, removal of 137Cs from soil would be very slow.
References
Askbrant S, Melin J, Sandalls J, Rauret G, Vallejo R, Hinton T, Cremers A, Vandecastelle C, Lewyckyj N, Ivanov YA, Firsakova SK, Arkhipov NP, Alexakhin RM (1996) Mobility of radionuclides in undisturbed and cultivated soils in Ukraine, Belarus and Russia six years after the Chernobyl fallout. J Environ Radioact 31:287–312. doi:10.1016/0265-931X(95)00054-E
Bunzl K, Schimmack W, Belli M, Riccardi M (1997) Sequential extraction of fallout radiocesium from the soil: small scale and large scale spatial variability. J Radioanal Nucl Chem 226:47–53
Camps M, Rigol A, Hillier S, Vidal M, Rauret G (2004) Quantitative assessment of the effects of agricultural practices designed to reduce 137Cs and 90Sr soil-plant transfer in meadows. Sci Total Environ 332:23–38. doi:10.1016/j.scitotenv.2004.04.008
Chino M, Nakayama H, Nagai H, Terada H, Katata G, Yamazawa H (2011) Preliminary estimation of release amounts of 131I and 137Cs accidentally discharged from the Fukushima Dai-ichi Nuclear Power Plant into the atmosphere. J Nucl Sci Technol 48:1129–1134
Choudhary DK, Johri BN (2009) Interactions of Bacillus spp. and plants—with special reference to induced systemic resistance (ISR). Microbiol Res 164:493–513. doi:10.1016/j.micres.2008.08.007
Cook LL, Inouye RS, McGonigle TP, White GJ (2007) The distribution of stable cesium in soils and plants of the eastern Snake River Plain in southern Idaho. J Arid Environ 69:40–64. doi:10.1016/j.jaridenv.2006.08.014
Cook LL, Inouye RS, McGonigle TP (2009) Evaluation of four grasses for use in phytoremediation of Cs-contaminated arid land soil. Plant Soil 324:169–184. doi:10.1007/s11104-009-9942-z
Cremers A, Elsen A, De Preter P, Maes A (1988) Quantitative analysis of radiocaesium retention in soils. Nature 335:247–249
De Boulois H, Voets L, Delvaux B, Jakobsen I, Declerck S (2006) Transport of radiocaesium by arbuscular mycorrhizal fungi to Medicago truncatula under in vitro conditions. Environ Microbiol 8:1926–1934. doi:10.1111/j.1462-2920.2006.01070.x
Djedidi S, Kojima K, Yamaya H, Ohkama-Ohtsu N, Bellingrath-Kimura SD, Watanabe I, Yokoyama T (2014) Stable cesium uptake and accumulation capacities of five plant species as influenced by bacterial inoculation and cesium distribution in the soil. J Plant Res 127:585–597. doi:10.1007/s10265-014-0647-x
Dushenkov S, Mikheev A, Prokhnevsky A, Ruchko M, Sorochinsky B (1999) Phytoremediation of radiocesium-contaminated soil in the vicinity of Chernobyl, Ukraine. Environ Sci Technol 33:469–475
Endo S, Kimura S, Takatsuji T, Nanasawa K, Imanaka T, Shizuma K (2012) Measurement of soil contamination by radionuclides due to Fukushima Dai-ichi Nuclear Power Plant accident and associated cumulative external dose estimation. J Environ Radioact 111:18–27. doi:10.1016/j.jenvrad.2011.11.006
Endo S, Kajimoto T, Shizuma K (2013) Paddy-field contamination with 134Cs and 137Cs due to Fukushima Dai-ichi Nuclear Power Plant accident and soil-to-rice transfer coefficients. J Environ Radioact 116:59–64. doi:10.1016/j.jenvrad.2012.08.018
Entry JA, Watrud LS, Reeves M (1999) Accumulation of 137Cs and 90Sr from contaminated soil by three grass species inoculated with mycorrhizal fungi. Environ Pollut 104:449–457. doi:10.1016/S0269-7491(98)00163-8
Forsberg S, Strandmark M (2001) Migration and chemical availability of 137Cs and 90Sr in Swedish long-term experimental pastures. Water Air Soil Poll 127:157–171
Fuhrmann M, Lasat M, Ebbs S, Cornish J, Kochian L (2003) Uptake and release of cesium-137 by five plant species as influenced by soil amendments in field experiments. J Environ Qual 32:2272–2279
Gaspar L, Navas A (2013) Vertical and lateral distributions of 137Cs in cultivated and uncultivated soils on Mediterranean hillslopes. Geoderma 207–208:131–143. doi:10.1016/j.geoderma.2013.04.034
Glick BR (1995) The enhancement of plant growth by free-living bacteria. Can J Microbiol 41:109–117
Gray EJ, Smith DL (2005) Intracellular and extracellular PGPR: commonalities and distinctions in the plant–bacterium signaling processes. Soil Biol Biochem 37:395–412. doi:10.1016/j.soilbio.2004.08.030
Hamada N, Ogino H (2012) Food safety regulations: what we learned from the Fukushima nuclear accident. J Environ Radioact 111:83–99. doi:10.1016/j.jenvrad.2011.08.008
Hurek T, Reinhold-Hurek B (2003) Azoarcus sp. strain BH72 as a model for nitrogen-fixing grass endophytes. J Biotechnol 106:169–178. doi:10.1016/j.jbiotec.2003.07.010
Ishikawa NA, Tagami k, Uchida S (2008) Estimation of 137Cs plant root uptake using naturally existing 133Cs. J Nucl Sci Technol Supplement 6:146–151
Koarashi J, Atarashi-Andoh M, Matsunaga T, Sato T, Nagao S, Nagai H (2012) Factors affecting vertical distribution of Fukushima accident-derived radiocesium in soil under different land-use conditions. Sci Total Environ 431:392–401. doi:10.1016/j.scitotenv.2012.05.041
Kobayashi D, Okouchi T, Yamagami M, Shinano T (2014) Verification of radiocesium decontamination from farmlands by plants in Fukushima. J Plant Res 127:51–56. doi:10.1007/s10265-013-0607-x
Kuwahara C, Fukumoto A, Ohsone A, Furuya N, Shibata H, Sugiyama H, Kato F (2005) Accumulation of radiocesium in wild mushrooms collected from a Japanese forest and cesium uptake by microorganisms isolated from the mushroom-growing soils. Sci Total Environ 345:165–173. doi:10.1016/j.scitotenv.2004.10.022
Kuwahara C, Fukumoto A, Nishina M, Sugiyama H, Anzai Y, Kato F (2011) Characteristics of cesium accumulation in the filamentous soil bacterium Streptomyces sp. K202. J Environ Radioact 102:138–144. doi:10.1016/j.jenvrad.2010.11.004
Livens FR, Baxter MS (1988) Particle size and radionuclide levels in some west Cumbrian soils. Sci Total Environ 70:l–17. doi:10.1016/0048-9697(88)90248-3
Luksiene B, Marciulioniene D, Gudeliene I, Schönhofer F (2013) Accumulation and transfer of 137Cs and 90Sr in the plants of the forest ecosystem near the Ignalina nuclear power plant. J Environ Radioact 116:1–9. doi:10.1016/j.jenvrad.2012.09.005
Matsunaga T, Koarashi J, Atarashi-Andoh M, Nagao S, Sato T, Nagai H (2013) Comparison of the vertical distributions of Fukushima nuclear accident radiocesium in soil before and after the first rainy season, with physicochemical and mineralogical interpretations. Sci Total Environ 447:301–314. doi:10.1016/j.scitotenv.2012.12.087
McGrath SP, Zhao FJ (2003) Phytoextraction of metals and metalloids from contaminated soils. Curr Opin Biotechnol 14:277–282. doi:10.1016/S0958-1669(03)00060-0
Mimura T, Mimura M, Kobayashi D, Komiyama C, Sekimoto H, Miyamoto M, Kitamura A (2014) Radioactive pollution and accumulation of radionuclides in wild plants in Fukushima. J Plant Res 127:5–10. doi:10.1007/s10265-013-0599-6
Ministry of Agriculture, Forestry and Fisheries (MAFF) of Japan (2013). http://www.maff.go.jp/mobile/kinkyu/tohoku_saigai/08/2011/1109/110914/110914_gijutu_betu01.html and http://www.s.affrc.go.jp/docs/press/pdf/110914-09.pdf. In Japanese
Morino Y, Ohara T, Nishizawa M (2011) Atmospheric behavior, deposition, and budget of radioactive materials from the Fukushima Dai-ichi Nuclear Power Plant in March 2011. Geophys Res Lett 38:L00G11. doi:10.1029/2011GL048689
Nadeem SM, Ahmad M, Zahir ZA, Javaid A, Ashraf M (2013) The role of mycorrhizae and plant growth promoting rhizobacteria (PGPR) in improving crop productivity under stressful environments. Biotech Adv 32:429–448. doi:10.1016/j.biotechadv.2013.12.005
Nakamaru Y, Uchida S (2008) Distribution coefficients of tin in Japanese agricultural soils and the factors affecting tin sorption behavior. J Environ Radioact 99:1003–1010. doi:10.1016/j.jenvrad.2007.11.012
Nakano M, Yong RN (2013) Overview of rehabilitation schemes for farmlands contaminated with radioactive cesium released from Fukushima power plant. Eng Geol 155:87–93. doi:10.1016/j.enggeo.2012.12.010
Ohmori Y, Inui Y, Kajikawa M et al (2014) Difference in cesium accumulation among rice cultivars grown in the paddy field in Fukushima Prefecture in 2011 and 2012. J Plant Res 127:57–66. doi:10.1007/s10265-013-0616-9
Ohno T, Muramatsu Y, Miura Y, Oda K, Inagawa N et al (2012) Depth profiles of radioactive cesium and iodine released from the Fukushima Dai-ichi Nuclear Power Plant in different agricultural fields and forests. Geochem J 46:287–295. doi:10.2343/geochemj.2.0204
Puhakainen M, Riekkinen I, Heikkinen T, Jaakkola T, Steinnes E, Rissanen K, Suomela M, Thørring H (2001) Effect of chemical pollution on forms of 137Cs, 90Sr and 239,240Pu in Arctic soil studied by sequential extraction. J Environ Radioact 52:17–29
Rigol A, Roig M, Vidal M, Rauret G (1999) Sequential extractions for the study of radiocesium and radiostrontium dynamics in mineral and organic soils from western Europe and Chernobyl area. Environ Sci Tech 33:887–895
Rogers RD, Williams SE (1986) Vesicular arbuscular mycorrhizal—influence on plant uptake of cesium and cobalt. Soil Biol Biochem 18:371–376
Sakai M, Gomi T, Nunokawa M, Wakahara T, Onda Y (2014) Soil removal as a decontamination practice and radiocesium accumulation in tadpoles in rice paddies at Fukushima. Environ Pollut 187:112–115. doi:10.1016/j.envpol.2014.01.002
Schmidt CS, Alavi M, Cardinale M, Müller H, Berg G (2012) Stenotrophomonas rhizophila DSM14405T promotes plant growth probably by altering fungal communities in the rhizosphere. Biol Fertil Soils 48:947–960. doi:10.1007/s00374-012-0688-z
Smolders E, Tsukada H (2011) The transfer of radiocesium from soil to plants: mechanisms, data, and perspectives for potential countermeasures in Japan. Integrat Environ Assess Manag 7:379–381
Spezzano P (2005) Distribution of pre- and post-Chernobyl radiocaesium with particle size fractions of soils. J Environ Radioact 83:117–127. doi:10.1016/j.jenvrad.2005.02.002
Tanaka K, Iwatani H, Sakaguchi A, Takahashi Y, Onda Y (2013) Local distribution of radioactivity in tree leaves contaminated by fallout of the radionuclides emitted from the Fukushima Daiichi Nuclear Power Plant. J Radioanal Nucl Chem 295:2007–2014
Tang S, Liao S, Guo J, Song Z, Wang R, Zhou X (2011) Growth and cesium uptake responses of Phytolacca americana Linn. and Amaranthus cruentus L. grown on cesium contaminated soil to elevated CO2 or inoculation with a plant growth promoting rhizobacterium Burkholderia sp. D54, or in combination. J Hazard Mater 198:188–197. doi:10.1016/j.jhazmat.2011.10.029
Tomioka N, Uchiyama H, Yagi O (1992) Isolation and characterization of cesium accumulating bacteria. Appl Environ Microbiol 58:1019–1023
Tripathi AK, Nagarajan T, Verma SC, Le Rudulier D (2002) Inhibition of biosynthesis and activity of nitrogenase in Azospirillum brasilense Sp7 under salinity stress. Curr Microbiol 44:363–367. doi:10.1007/s00284-001-0022
Tsukada H, Hasegawa H, Hisamatsu S, Yamasaki S (2002) Transfer of 137Cs and stable Cs from paddy soil to polished rice in Aomori Japan. J Environ Radioact 59(3):351–363. doi:10.1016/S0265-931X(01)00083-2
Tsukada H, Takeda A, Hisamatsu S, Inaba J (2008) Concentration and specific activity of fallout 137Cs in extracted and particle-size fractions of cultivated soils. J Environ Radioact 99:875–881. doi:10.1016/j.jenvrad.2007.11.014
Vandebroek L, Van Hees M, Delvaux B, Spaargaren O, Thiry Y (2009) Acid extraction as a predictive tool of radiocaesium interception potential (RIP) in a worldwide scale. Radioprotection 44:635–638
Vandenhove H (2013) Phytoremediation options for radioactively contaminated sites evaluated. Ann Nucl Energy 62:596–606. doi:10.1016/j.anucene.2013.02.005
Vandenhove H, Sweeck L (2011) Soil vulnerability for cesium transfer. Integr Environ Assess Manag 7:374–378
Varskog P, Naeumann R, Steinnes E (1994) Mobility and plant availability of radioactive Cs in natural soil in relation to stable Cs, other alkali elements and soil fertility. J Environ Radioact 22:43–53. doi:10.1016/0265-931X(94)90034-5
Vinichuk M, Mårtensson A, Ericsson T, Rosén K (2013) Effect of arbuscular mycorrhizal (AM) fungi on 137Cs uptake by plants grown on different soils. J Environ Radioact 115:151–156. doi:10.1016/j.jenvrad.2012.08.004
Wensling LA, Harsh JB, Ward TE, Palmer CD, Hamilton MA, Boyle JS, Flury M (2005) Cesium desorption from illite as affected by exudates from rhizosphere bacteria. Environ Sci Technol 39:4505–4512
Willey NJ, Martin MH (1995) Annual patterns of Cs-133 concentration in British upland vegetation. Chemosphere 30:717–724. doi:10.1016/0045-6535(94)00437-Y
Yoshihara T, Matsumura H, Hashida S, Nagaoka T (2013) Radiocesium contaminations of 20 wood species and the corresponding gamma-ray dose rates around the canopies at 5 months after the Fukushima nuclear power plant accident. J Environ Radioact 115:60–68. doi:10.1016/j.jenvrad.2012.07.002
Zhu YG, Smolders E (2000) Plant uptake of radiocesium: a review of mechanisms, regulation and application. J Exp Bot 51:1635–1645
Acknowledgments
This study was supported by the Special Research Fund of the Ministry of Education, Culture, Sports, Science and Technology (MEXT), Japan titled “Research and development of security and safe crop production to reconstruct agricultural lands in Fukushima Prefecture based on novel techniques to remove radioactive compounds using advanced bio-fertilizer and plant protection strategies”. This work was also supported by a Grant-in-Aid for Scientific Research (B):24380176 from the Japan Society for the Promotion of Science (JSPS).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Djedidi, S., Terasaki, A., Aung, H.P. et al. Evaluation of the possibility to use the plant–microbe interaction to stimulate radioactive 137Cs accumulation by plants in a contaminated farm field in Fukushima, Japan. J Plant Res 128, 147–159 (2015). https://doi.org/10.1007/s10265-014-0678-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10265-014-0678-3