Mineralogical and geomicrobial examination of soil contamination by radioactive Cs due to 2011 Fukushima Daiichi Nuclear Power Plant accident

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    aDepartment of Geology, Faculty of Science, Niigata University, Ikarashi-2, 8050, Niigata 950-2181, JapanbGraduate School of Science and Technology, Niigata UncDepartment of Chemistry, Faculty of Science, Niigata UdDepartment of Biology, Faculty of Education, Niigata UeDepartment of Environmental Sciences, Faculty of Scienf Fukushima-Higashi High School, Fukushima, Japan

    due to strong sorption of Cs by soil. Soil is fundamentally com-posed of minerals containing clay minerals and organic matters,and various organisms living in it.

    Cesium has a similar nature to other alkali metals such as K andbinds weakly to organic and inorganic ligands. Organic materials insoil are derived from plants and microorganisms. Organisms in thesoil are plants, lamentous and single-celled bacteria, algae, fungi,and small invertebrates such as protozoa, worms, insects and ani-

    stick et al., 2002;

    suggested that Csreleased inlkaline sol. 15% and

    ca. 70% of Cs remains after treatment (Hou et al., 2003). Ttype clay minerals show stronger sorption ability than 1:clay minerals and frayed edge sites in clay minerals mainlyCs (Sawhney, 1972; Ebel, 1980; Kitamura et al., 2008). The Cs sorp-tion characteristics by zeolite, e.g., clinoptilolite, is well known(e.g., Bailey et al., 1999). Clinoptilolite, which is highly selectivefor Cs, is used for removal of Cs from contaminated waters (Cheli-shchev, 1995). Therefore, current method for treatment of Cs is byion exchange of clinoptilolite offering ion exchange sites, moderateresistance to radiometric degradation and low solubility.

    Corresponding author. Tel.: +81 25 2626186.

    Physics and Chemistry of the Earth 5860 (2013) 5767

    Contents lists available at


    w.eE-mail address: akai@geo.sc.niigata-u.ac.jp (J. Akai).The Fukushima Daiichi Nuclear Power Plant accident hascaused wide soil contamination by radioactive Cs as Chernobylaccident did (e.g., Ebihara et al., 2012; Watanabe et al., 2012;UNSCEAR, 2008). It is well known that sorption of radioactiveCs in soil does not go so deep: Most of the Cs is less than10 cm deep (e.g., Arapis et al., 1997; Ohno et al., 2012). This is

    1992; Maes and Cremers, 1986; Cornell, 1993; BoNakano et al., 2003).

    Dissolution and extraction experiments havestrongly combined to clay minerals is not easilykinds of solutions; for example water, acid and aHowever, ammonium acetate releases Cs of ca1474-7065/$ - see front matter 2013 Elsevier Ltd. All rights reserved.http://dx.doi.org/10.1016/j.pce.2013.04.010manyutions.nallyhe 2:11 typeabsorbTEMleaves in Iitate village, Fukushima Pref. and bacterial strains of Bacillus subtillis, Rhodococus erythropolis,Streptomyces aomiensis and Actinomycetospora chlora were carried out. Non-radioactive 1% Cs solution(CsCl) was added to the culture media. Two types of strong or considerable bacterial uptakes of Cs werefound in bacterial cells. One is that Cs was contained mainly as globules inside bacteria and the other isthat Cs was absorbed in the whole bacterial cells. The globules consisted mainly of Cs and P. Based on allthese results, future diffusion and re-circulation behavior of Cs in the surface environment was discussed.

    2013 Elsevier Ltd. All rights reserved.

    1. Introduction mals. Clay minerals, especially 2:1 type clay minerals strongly ab-sorb Cs (Sawhney, 1972; Comans et al., 1991; Comans and Hockley,a r t i c l e i n f o

    Article history:Available online 25 April 2013

    Keywords:CesiumFukushimaLeavesRecirculationBacterial sorptioniversity, Ikarashi-2, 8050, Niigata 950-2181, Japanniversity, Ikarashi-2, 8050, Niigata 950-2181, Japanniversity, Ikarashi-2, 8050, Niigata 950-2181, Japance, Niigata University, Ikarashi-2, 8050, Niigata 950-2181, Japan

    a b s t r a c t

    Soil contamination by radioactive Cs from Fukushima Daiichi Nuclear Power Plant accident was investi-gated. Absorption and desorption experiments of Cs were conducted for several phyllosillicates (kaolin-ite, sericite, montmorillonite, vermiculite, chrysotile and biotite), zeolite and solid organic matter (deadand green leaves). The results conrmed the characteristic sorption and desorption of Cs by these mate-rials. The 2:1 type phyllosilicate, especially, vermiculite and montmorillonite absorbed Cs well. Heatedvermiculite for agricultural use and weathered montmorillonite also adsorbed Cs. Leaves also absorbedCs considerably but easily desorbed it. In summary, the relative capacity and strength of different mate-rials for sorption of Cs followed the order: zeolite (clinoptilolite) > 2:1 type clay mineral > 1:1 type claymineral > dead and green leaves. Culture experiments using bacteria of both naturally living on deadJinko Matsumoto fMineralogical and geomicrobial examinaradioactive Cs due to 2011 Fukushima Daccident

    Junji Akai a,, Nao Nomura b, Shin Matsushita b, Hisa

    Physics and Chem

    journal homepage: wwn of soil contamination bychi Nuclear Power Plant

    Kudo c, Haruo Fukuhara d, Shiro Matsuoka e,

    SciVerse ScienceDirect

    stry of the Earth

    l sevier .com/locate /pce

  • lated to enzyme necessity and afnity of K (Bossemeyer et al.,

    1991). Later, Kato et al. (2000) suggested Cs uptake by Streptomyces

    ry olividans TK-24 and Streptomyces sp. TOHO-2. Uptake of Cs by ac-tively metabolizing microorganisms may be proved more effec-tively, but microbial biosorption has suggested low Cs uptakeover zeolite use (Macaskie, 1991).

    Soil contamination by radioactive Cs from a reactor at the Fuku-shima Daiichi Nuclear Power Plant which resulted from meltdownof fuel rods, has spread over the wide area especially in FukushimaPrefecture. Regarding radioactive Cs behavior, many research stud-ies have been reported in relation to the Chernobyl accident andalso to nuclear weapons test effects in the 1960s (e.g., Lloyde andEncesah, 1999; Elles and Lee, 2002).

    First, this study described the basic data of Cs contamination inFukushima. Second, fundamental experiments of Cs sorption anddesorption by various clay minerals and leaves were conducted.Some previous studies on sorption of Cs by typical clay mineralspecies have been carried out (e.g., Hou et al., 2003). Therefore, thisstudy examined the Cs sorption properties by more varieties ofphyllosilicate types. Sorption of Cs by leaves was also compara-tively conducted. Desorption characteristics of Cs by clay mineralshave been reported and are well known. Then, we carried out thedesorption experiments from leaves in details. Thirdly, in orderto clarify the bacterial role in the environment, culture experi-ments were carried out using both a natural bacterial mixture liv-ing on the dead leaves in Iitate village, Fukushima Pref. and on fourpure strains. These strains were randomly selected among verycommonly found types of bacteria in the surface environments.All of these results lead to a clarication of the detailed formationprocess of the so-called hot spot where Cs is highly concentratedin local scales. Future diffusion and recirculation behaviour ofradioactive Cs in the surface environments, and the fate of Cs inthe future environments are nally discussed.

    2. Materials and methods

    This study is composed of sampling in the eld and laboratoryexperiments. So-called hot spot, where Cs is highly concentratedlocally, were found in the eld survey for sampling in Fukushimaprefecture. Using these samples, laboratory experiments wereconducted.

    2.1. Materials

    2.1.1. Soil and sandy dust specimens from highly Cs-concentratedareas

    Soils beneath the rain drainspout from house roof in Date city(sampled by S. Sato): Radiation intensity of b and c rays measured1989). Appanna et al. (1996) suggested that Cs was immobilizedby Pseudomonas uorescence as an insoluble precipitate when usingculture media containing ferric iron. However, the details for thesemicrobial processes are not fully claried, and more varieties ofexamples in different conditions are needed to be collected forwide interpretation of natural processes and also for remediationpossibilities. Another algal and fungal model system of Cs sorptionis also suggested (Harvey and Patrick, 1967; DeRome and Gadd,In general, the role of bacteria in surface environments isimportant due to the interaction between microbe and minerals.Regarding Cs contamination, bacterial behaviour has been re-viewed by Avery (1995, 2006). Because of the similarity of K andCs, both may be absorbed by the same metabolic pass. Escherichiacoli have characteristic K+ uptake transport systems which is re-


    58 J. Akai et al. / Physics and Chemistby the dosimeter (TGS-121/Aloka) was 60 lSv/h at the site and5 lSv/h at the position of 1 cm apart from the sample of ca.100 cc in the laboratory. Sandy dust sample on the housetop ofTachibana High School in Fukushima City was collected by Mat-sumoto. They were collected 20th March 2011 and the c-ray mea-surements were carried out 25th March 2011. Radiation intensityof b and c rays measured by dosimeter (Gamma Scout) was3.8 lSv/h at the position of 1 cm apart from the sample of ca.100 cc in the Laboratory. The sample used for c ray spectroscopywas 0.695 g. A soil sample with some black dead leaves was col-lected from the street gutter at Iitate village where there is a so-called hot spot. The radiation intensity of b and c rays measuredby dosimeter at this point was 132 lSv/h (b and c rays)

    2.1.2. Mineral and leaf samplesClay mineral species with their localities are shown below. 1.

    Kaolinite in Kanpaku; 2. Kaolinite in Hakurou, Hokkaidou; 3. Ser-pentine (chrysotile) in Oheyama, Kyoto; 4. Montmorillonite inOdo, Niigata; 5. Weathered montmorillonite (kaolinmontmoril-lonite) in Hanetsu, Niigata; 6. Vermiculite (Materials importedfrom China), 7. Heated vermiculite of (6), 8. Biotite in Ishikawa,Fukushima Pref.; 9. Sericite in Nabeyama (with impurity of kaolinmineral), 10. Chlorite in Kamioka, Gifu Pref. (with impurity ofantigorite). Natural zeolite samples (mineral species, locality in Ja-pan) were also prepared as follows.

    1. Clinoptilolite in Itaya, Yamagata; 2. Mordenite in Kamihoro,Iwamizawa, Hokkaido.

    Leaf samples were used for sorption experiments. Varieties ofdead and green leaf samples were collected around Niigata Univer-sity, as follows; 1. Camellia (Camellia japonica), 2. Cherry treeSomei-yoshino (Cerasus yedoensis), 3.orange osmanthus (Osman-thus fragrans var. aurantiacus), 4. Reed (Phragmites australis), 5.Timothy, timothy grass (Phleum pretense), 6. Pine (Pinus thunbergii).

    2.1.3. BacteriaThe natural bacterial mixtures living on dead leaves obtained

    from the so-called hot spot of a street gutter at Iitate village, Fuku-shima Prefecture were collected.

    Pure bacterial strains of Rhodococus erythropolis (RIKEN BRC JCMNo. 9804), Streptomyces aomiensis (RIKEN BRC JCM No. 17986) andBacillus subtillis (RIKEN BRC JCM No. 18293) and Actinomycetosporachlora (RIKEN BRC JCM No. 17979) were obtained from JAPAN COL-LECTION OF MICROORGANISMS in RIKEN Bioresource Center.

    2.2. Experimental methods

    2.2.1. Radiation measurements and XRD analysisRadiation dosimeter of GM counter (Gamma Scourt) which

    measure a, b and c rays was used for eld and laboratory experi-ments. Radiation dosimeter of GM counter (TGS-121/Aloka) whichmeasure b and c rays were partly used for eld use. c-ray spec-trometry was carried out for identication and determinations ofradioisotopes. This is composed of a high purity Ge coupled witha multi-channel pulse-height analyzer. The resolution is 2.0 keVat 1332 keV c-ray of 60Co. Autoradiography was carried out usingBlack and White lm with sensitivity of ISO 400. Sandy dust parti-cles (Sample A) and Date soil sample (Sample B) were placed onthe lm and kept for 5 days in a dark room to develop. XRD (X-ray Diffraction) analysis was carried out using Ultima IV (Rigaku)for powdered samples.

    2.2.2. Sorption and desorption experiments by clay minerals, zeoliteand leaves

    For phyllosilicates, 10 ppm and 1% Cs solution were prepared asnon-radioactive CsCl solution. 1% solution is too high in a concen-tration for accidental contamination by Cs but this experiment was

    f the Earth 5860 (2013) 5767designed in order to check the fundamental capacity of sorption incomparison with other materials. Powdered phyllosilicate was putinto Cs solution. They were then stirred for 24 h and centrifuged for

  • analysis. 1 g of phyllosilicate was put in 40 cc of 10 ppm or 1% Cssolution and stirred for 24 h. They were centrifuged and the Cs con-centration was measured by Atomic Absorption Spectrometer (AA-6200: Shimadzu).

    Sorption experiments by zeolite samples were carried out forcomparison to clay minerals and leaf samples. Using 10 ppm and1% Cs solution (non-radioactive CsCl) and 1 g of zeolite, sampleswere put in 40 cc of 10 ppm or 1% Cs solution and stirred for24 h. The other conditions are the same as those described for clayminerals.

    Dead and green leaves were collected, washed with distilled

    types of solutions of 50 cc: Distilled water, NaOH (0.1 mol), HCl

    by CsCl. 10 cc of Sakurai medium and 40 cc of 1% Cs solution weremixed and used for natural bacteria in Iitate village. A small pieceof muddy dead leaf (square of ca. 5 mm) was added to culture solu-tion as a natural bacterial source. They were cultured at room tem-perature (25 C) for two weeks. Culture experiments of strains ofRIKEN BRC were carried out using 20 cc of corresponding mediumand 20 cc of 1% Cs solution. They were cultured at room tempera-ture (25 C) for 2 weeks.

    TEMEDS (Energy Dispersive Spectrometer) analysis was car-ried out as follows. TEM of JEM 2010 was operated at 200 kV.The EDS system used was Voyager IV (Noran Inst). Dead leaves

    The spectrum indicates the presence of 137Cs, 134Cs, 131I, 132Te,

    J. Akai et al. / Physics and Chemistry of the Earth 5860 (2013) 5767 59(0.1 mol), (NH4)2C2O4H2O (0.1 mol), KCl (0.1 mol), H2SO4(0.1 mol), HNO3 (0.1 mol).

    They were stirred for 1 h and centrifuged, and the Cs concentra-tion was measured. Desorption ratio was calculated, using the fol-lowing equation:

    Desorption ratio % Absorbed Cs content Remaining Cs content=Absorbed Cs content 100

    2.2.3. Bacterial culture experiments and TEM (Transmission ElectronMicroscopy) observations

    The following culture media were prepared. Sakurai Mediumwas prepared as follows. 0.075 g of glucose, 0.3 g of polypeptonand 0.15 g of yeast extract were dissolved in 150 ml distilled water.Other Media for each corresponding bacterial strain was preparedas follows. For R. erythropolis, Bacto peptone (10 g), Yeast extract(5 g), Malt extract (5 g), Casamino acid (5 g), Glycerol (2 g), andMgSO4/7H2O were dissolved in 1 L of distilled water. For Strepto-mycesm aomiensis, Yeast extract (4 g), Malt extract (10 g) and Glu-cose (4 g) were dissolved in 1 L distilled water. For B. subtillis,Peptone (5 g), and Beef extract (3 g) were dissolved in 1 L distilledwater. For A. chlora, Yeast extract (1 g) and Oatmeal agar (20 g)were dissolved in 1 L distilled water. 1% Cs solution was preparedwater, and then air dried. The procedure was the same as inthe mineral sorption experiments. 1% and 10 ppm non-radioac-tive CsCl solutions were prepared. 5 g of the dried leaves wereput into the solutions (50 ml) and stirred for 24 h. The sampleswere centrifuged and the Cs concentration of the solution wasmeasured by Atomic Absorption Spectrometer (AA-6200:Shimadzu).

    Sorption ratio was calculated based on the following equation:

    Sorption ratio % Original Cs content in solution Remaining Cs content in solution=Original Cs content in solution 100

    Leave samples (1 g) were prepared by adsorbing Cs (1% Cs solu-tion; 50 cc) and drying. Then, they were immersed into variousFig. 1. Autoradiograph of Cs-contaminated materials. (a) Sandy dust from a housetop of Tdrainspout from a house roof in Date City, Fukushima Prefecture.etc. which have already been reported (MITI, 2011). 137Cs, 134Csand 131I are most well known. 132Te was also found in the Fukushi-ma City sample. Although 132Te has a half-life of 3.2 days, the peakof 132Te was still persistent on 25th March 2011. This means that atthe initial stage, much more 132Te must be present. The boilingin Iitate village were immersed in a small quantity of distilledwater and a drop of it was placed on carbon-coated perforatedmicrogrid and dried for TEM observation. A drop of the culturedproducts was placed on carbon-coated perforated microgrid anddried.

    3. Results

    3.1. Analysis of sandy dust sample from Tachibana High School andsoil sample from Date city

    The examined samples and obtained data in Fukushima City arevery fundamental as the early stage one of the Fukushima DaiichiNuclear Power Plant accident. The XRD analysis of the sandy dustsample from Tachibana High School showed that the constituentminerals were mainly quartz, feldspars, illite/mica, and very smallamounts of kaolin, vermiculite/chlorite and calcite. Soil samplecontained quartz, feldspars, illite/mica, vermiculite/smectite andvery small amounts of kaolin minerals. Furthermore, examinationby autoradiography was applied to both samples. Determinationof radioisotope nucleides by c-ray spectrometry was applied tothe sandy dust particles from Tachibana High School.

    Autoradiography was applied to the sandy dust and soil sam-ples in the middle of May 2011. Black dots in Fig. 1a indicate thesand particles with high coating of radioactive elements. Stronglydarkened shadows are grains with highly absorbed radioactive Cs.

    In Fig. 1b of soil specimens, rather continuous darkening isfound probably due to spacing between soil block sample and lmsurface. Strongly darkened grains are also found. Some white radialshadows are also found. There is a possibility that this is due toblocked radiation traces of b-ray by some mineral grains.

    c-ray spectrum was measured for the sample from FukushimaCity. Fig. 2 shows the c-ray spectrum taken at March 29, 2011for the sandy dust of Tachibana High School in Fukushima City.achibana High School in Fukushima City. (b) Small block of soil sample beneath the

  • 150 ppt in concentration.

    ry o3.2. Sorption and desorption experiments by clay minerals, zeolite andleaves

    3.2.1. Sorption experimentFundamental sorption experiments for varieties of phyllosili-temperature of Te is 1380 C and elements with relatively low boil-ing temperatures might be predominant. The radioactivity of 137Csin the sample was calculated to be 4.8 105 Bq/kg. The number ofCs atoms in the sample is 4.58 1011 which corresponds to theweight of Cs to be 105 pg (1.05 1010 g). This is equal to

    Fig. 2. c-ray Spectrum for the sandy dust of Tachibana High School in FukushimaCity.

    60 J. Akai et al. / Physics and Chemistcates were carried out, adding previously reported results for 2:1type clay minerals (Sawhney, 1972; Ebel, 1980; Comans et al.,1991; Kitamura et al., 2008).

    Fig. 3a and b indicate the results of sorption experiment of10 ppm and 1% Cs solutions for various clay mineral species,respectively. Slightly different sorption characteristics are found,but all kinds of phyllosilicates examined absorbed Cs well. 2:1 typeminerals strongly absorb Cs. Montmorillonite and vermiculiteshow stronger sorption properties among clay minerals. Heatedvermiculite of commercial use which is often used in agriculturalpurposes was also examined and adsorbed Cs as well as originalvermiculite.

    Weathered montomorillonite also absorbed Cs as well as non-weathered montomorillonite. Some uctuations may be due toimpurities contained in samples.

    Sorption experiments of Cs by natural zeolite were conducted.Fig. 3c and d indicate the results of Cs sorption by zeolite. Zeoliteshows strong sorption characteristics for 10 ppm and 1% Cs solu-tion. At 1% solutions, a clear difference is found among zeolite,phyllosilicate and leaves; zeolite has still strong sorption abilitythan phyllosilicate and solid organic materials.

    In order to assess sorption of Cs to dead and green leaves, sorp-tion experiments were carried out. Fig. 4 indicates the results ofsorption experiment of 10 ppm and 1% Cs solution for various deadand green leaves. At 1% solution, some uctuations for each kind ofleaves are present, but all absorbed 8%1.6% of Cs. At a 10 ppmsolution, 5912.5% of Cs were absorbed. The general tendency isthat dead leaves absorb more than green leaves with someexceptions. However, the difference is not so large, and both deadand green leaves absorb Cs considerably, in general. Depending onthe kinds of leaves, a little difference is found. The reason is not al-ways clear: some leaves are coated with wax-like materials, andthe degree of degradation is different in each leaf. These factorsmay inuence the results. Green leaves have a still higher watercontent ratio than dead leaves. Therefore, a simple comparison be-tween green and dead leaves is difcult.

    3.2.2. Desorption experiment by leavesCs-desorption experiments of absorbed Cs in leaves by using

    distilled water and various chemical solutions showed that Cs is re-leased relatively easily (Fig. 5). This means that the combiningforce of Cs to leaves is not strong. In general, more Cs dissolvedfrom cherry leaves than pine leaves. There is a possibility that sur-face chemical conditions in leaves may be different, but more anal-yses are needed to verify this.

    3.2.3. Culture experiments using naturally living bacterial mixture toabsorb Cs

    For the rst time, original bacteria in Iitate village (a so-calledhot spot in the street gutter in Iitate village) was examined byTEM. Fig. 6a shows TEM image of predominant bacteria in thehighly Cs concentrated soil of 132 lSv/h (just on the dead leaf withsoil) indicating faint globules in bacterial cells. EDS spectrum(Fig. 6b) of the globule indicates the presence of Ca, P and smallamount of K. To check the bacterial behavior, culture experimentswere carried out using 1% Cs solution and Sakurai medium for sev-eral days. The products of the culture experiments were examinedby TEMEDS. Fig. 7a shows the TEM image of predominantlygrown bacteria. The size of the bacteria is 12 lm in length and0.40.5 lm in width, and rod-shaped and linked together in chain.Gene analysis for these bacteria was not carried out. However, leafsamples were once boiled at 100 C, and then cultured with Sakuraimedium; after this procedure, bacteria grew again. That is, thesebacteria have heat-resistant nature: thus, they are probablyspore-forming bacteria.

    Bacteria in Fig. 7a indicates that CsP globules are contained in-side the bacterial body. The EDS spectrum (Fig. 7b) shows the ana-lytical results of the globules. The globules may be mostly CsPcompound. Using quantitative analysis program in Voyager IV, Csconcentration in the globules was calculated to be Ca. 38 wt% whensupposed to be Cs phosphate. The spectrum of Fig. 9c indicatedcomposition of bacterial bodies other than the globule: Cs is alsocontained in relatively small quantities. These are the results ofculture for 5 days. In comparison, sorption of 10 ppm Cs solutionby bacteria also shows very small peak of Cs for the globules.

    3.2.4. Culture experiments using various bacteria to absorb CsFig. 8 shows some examples of Cs uptake by various bacteria.

    Considerable amounts of Cs were observed in EDS spectra. Glob-ules mainly composed of Cs and P phase, most likely Cs phos-phates, were also found in some cases (Fig. 8a, c, and e). B.subtillis cultured for 2 weeks contained globules of Cs and P, andRhodococcus of 5 days culture product and Streotomyces of 2 weeksculture product also showed globules in bacterial cells. On theother hand, Actinomycetospora showed bulk absorption of Cs wasfound in the whole bacterial body. The atomic number of Cs (55)is high, so Cs concentrated parts show darker contrast in TEMimages. Therefore, bacterial sorption of Cs is easily estimated viaTEM observation. Even if similar globules are found in both naturalbacteria in Iitate village and these pure RIKEN strains, the bacterialspecies from Iitate village is not determined. However, it is at least

    f the Earth 5860 (2013) 5767reported that varieties of bacteria may absorb Cs in various waysand Cs-absorption by bacteria is widely found in natural surfaceconditions.

  • try oJ. Akai et al. / Physics and Chemis4. Discussion

    4.1. Characteristics of soil contamination in Fukushima case

    Wide contamination by radioactive nuclides over Europe hasbeen spread by the Chernobyl accident (United Nations ScienticCommittee on the Effects of Atomic Radiation, 2008). The Fukushi-ma Daiichi Nuclear Power Plant accident occurred and radioactive

    Fig. 3. Experimental results of sorption of Cs from non-radioactive CsCl solutions byphyllosilicate. (b) Cs solution of 1% for phyllosilicate. (c) Cs solution of 10 ppm for zeolif the Earth 5860 (2013) 5767 61nucleides have spread again (MITI, 2011). This paper reports moreadditive data in Fukushima City, in the early stage of the accident.Especially, c-ray Spectrum for the sandy dust (collected 20thMarch 2011 and the measurement was carried out 25th March2011) showed relative abundance of 137Cs, 134Cs and 131I, etc.Furthermore, the presently observed low concentration of 132Teindicates that 132Te concentration was initially higher, becausehalf-life of 132Te is 3.2 days. 132Te changes to 132I. The boiling

    various types of phyllosilicate and natural zeolite. (a) Cs solution of 10 ppm forte. (d) Cs solution of 1% for zeolite.

  • ry o62 J. Akai et al. / Physics and Chemisttemperatures of Te and Cs are 1380 C and 670 C respectively, andtherefore, evaporation was above these temperatures. These com-positional characteristics are unique to Fukushima Daiichi and sug-gest a slight added health problem by radioactive 132I of latersupply after 131I. Half-life of 132I is 2.3 h.

    Fig. 4. Experimental results of sorption of Cs from non-radioactive CsCl solutions by var

    Fig. 5. Experimental results of desorption of non-radioactive Cs from leaf samples of psolutions.f the Earth 5860 (2013) 5767Autoradiography was preliminarily applied to sandy dust andthe results indicated the possibility of further wide use of thismethod to varieties of the contamination problem. For example,using these methods, vertical section of soil prole or sedimentsprole in river and/or ocean sediments can be visually examined.

    ious types of dead and green leaves. (a) Cs solution of 10 ppm. (b) Cs solution of 1%.

    ine (upper bar) and cherry trees (lower darker bar) by water and various chemical

  • try oJ. Akai et al. / Physics and Chemis4.2. Sorption and desorption characteristics

    In order to understand the combined process of natural envi-ronment, we must know the details of each key material whichbring Cs widely. So, fundamental characteristics of each key

    Fig. 6. TEM image and EDS spectrum of bacteria (a) TEM image of bacteria in the highlycells were found. (b) EDS spectrum of the globule. It indicates the presence of Ca, P and

    Fig. 7. TEM image and EDS spectra of cultured bacteria using a 1% non-radioactive Cs soinside the bacterial body. (b) EDS spectrum of the globules. (c) EDS spectrum of bacterif the Earth 5860 (2013) 5767 63material for Cs were examined, on the basis of previous knowl-edges on clay minerals (Schulz et al.,1960; Dolcater, 1968; Sawh-ney, 1972; Ebel, 1980; Comans et al., 1991; Ishikawa, 2007;Kitamura et al., 2008: Tsukada et al., 2008). And with regard toplant organic matters, Schulz et al., 1960; Tsukada et al., 2008)

    Cs concentrated soil in Iitate Village, Fukushima Pref. Faint globules in the bacteriala very small amount of K. The vertical scale is a log scale.

    lution. (a) TEM image of predominantly grown bacteria. Cs-P globules are containedal body other than globules.

  • Fig. 8. TEM images and EDS spectra of cultured strains of Bacillus subtillis, Rhodococus erythropolis, Streptomyces aomiensis and Actinomycetospora chlora. (a) TEM image ofBacillus subtillis (cultured for two weeks). CsP globules are contained inside bacterial body. (b) EDS spectrum of the globules of Bacillus subtillis (a). (c) TEM image ofRhodococus erythropolis (cultured for 5 days). Globules are contained inside the bacterial body. (d) EDS spectrum of the bacteria (c). (e) TEM image of Streptomyces aomiensis(cultured for 2 weeks). Cs is absorbed in the bacterial body. (f) EDS spectrum of Streptomyces aomiensis (e). (g) TEM image of Actinomycetospora chlora (cultured for 2 weeks).(h) EDS spectrum of Actinomycetospora chlora (g).

    64 J. Akai et al. / Physics and Chemistry of the Earth 5860 (2013) 5767

  • viewed by Appanna et al. (1996), where Cs was immobilized with

    viroprokley72),dy; A-Pauey an

    try oand microbes (Derks and Borst-Pauwels, 1979; Bossemeyer et al.,1989; Tomioka et al., 1992; Avery, 1995; Appanna et al., 1996; Katoet al., 2000).

    Sorption studies by phyllosilicate, zeolite and leaves showeddifferences in 10 ppm and 1%, although the actual concentrationof radioactive Cs following an accidental release may be in ppbor ppt level in the environment. Solid materials, for example, sandydust on the housetop of Tachibana High School contained Cs con-centrations of 150 ppt. When 1% concentration is applied, zeolite

    Fig. 9. Schematic model for the recirculation and fate of Cs in soils and the surface enpossible routes of Cs recirculation. 1, 2, and 3 indicate references relating to each(1972), Maes and Cremers (1986), Johnston and Tombacz (1990), Comans and HocComans et al. (1991), Kitamura et al. (2008). 3: Dolcater et al. (1968), Sawhney (19et al. (1960), Ejeckam and Sheriff (2005), Tsukada et al. (2008). 5: The present stu(1996), Avery (1995), Bossemeyer et al. (1989), Tomioka et al. (1992), Derks and Borstand Godd (1993), Derks and Borst-Pauwels (1979), deRome and Gadd (1991), HarvJ. Akai et al. / Physics and Chemisabsorbs more Cs than phyllosilicate and leaves; and the differencesin Cs sorption capacity became clear. This study showed the resultsof Cs adsorption by varieties of phyllosilicates that are not fully re-ported in the previous reports. In general, 2:1 type minerals ab-sorbed more Cs than 1:1 type, although some samples containedimpurity minerals. Montmorillonite absorbed Cs well. Weatheredmontmorillonite (kaolinmontmorillonite) still showed a largesorption capacity. Dead and green leaves also showed a consider-able amount of Cs sorption, but relatively less than phyllosilicate.

    Phyllosilicates strongly absorb Cs and do not release Cs easily,but leaves desorb Cs relatively easily. These characteristics deter-mine the Cs behavior in the environment. Slight differences amongthe leaf species, dead and green leaves are present, but it can begenerally said that all dead and green leaves absorb a considerableamount of Cs and release Cs even by water relatively easily.

    4.3. Interaction between microbes and minerals

    Interaction between microbes and minerals is an important as-pect for the surface environmental process. Biological process-re-lated Cs diffusion effect into the ground has been theoreticallysuggested in the study of the Chernobyl accident and soil contam-ination (Matisoff, 1995). In this study, geomicrobilogical effects onCs behaviour are also suggested. The bacteria found may obtainnutrients from dead leaves, etc. A previous study on the biowea-thering of biotite (Akai, 2008) indicated that bacteria actively ab-sorb K on the cleavage surface of biotite from Ishikawa,Fukushima Prefecture, Japan. Therefore, sorption of Cs instead ofK in Iitate village is suggested, and the observed results (Fig. 9athe cell pellet of Pseudomonas uorescens in the presence of ferriciron. All the results of this study suggest that the bacterial absorp-tion and later transportation of Cs by bacteria may play some rolein the surface behavior of Cs.

    4.4. Formation of a so-called hot spotand b) are reasonably interpreted. Other examples have been re-

    nment. Solid arrows indicate transfer of Cs. Arrows with dashed lines indicate somecess. 1: Wauters et al. (1996), Elles (2002), Stauton and Roubaud (1997), Sawney(1992), Arapis et al. (1997). 2: The present study: Sawhney (1972), Ebel (1980),Ishikawa (2007), Schulz et al. (1960), Cornell (1993). 4: The present study; Schulzppanna et al. (1996), Staunton et al. (2002). 6: The present study; Appanna et al.wels (1979), Kato et al. (2000). 7: Matisoff (1995), Avery et al. (1992, 1993), Perkinsd Patrick (1967). 8: IAEA (1995), Delvaux et al. (2000), Lembrechts (1993).f the Earth 5860 (2013) 5767 65As is well known, Cs concentrated area (so-called hot spot) isformed in various scales in Japan: for several km to less than 1 min size. The following four steps are described as important forthe formation of a Cs hot spot. Step I: Cs is present probably asa ne solid phase or gaseous phase in emission from the powerplant accident. Step II: Cs may be present as a solution when thesolid Cs phase fell onto the ground or is in the air with water phase.Step III: Cs in the solution meets minerals or other materials, e.g.,plants and other organic materials containing dead and greenleaves, etc. Then, Cs is strongly absorbed to minerals and softly ab-sorbed to organic matters containing dead leaves. This is related tothe strong absorbing property of clay minerals and soft absorbingin organic matters for Cs. Step IV: Cs diffusion and recirculationbehavior are interpreted to be involved in the transportation ofCs as solid grains of minerals and some solid organic substances.These grains may be transported, accumulated and again depositedby water ow, wind, or articial transportation, burning, etc. Largeparts of step IV correspond to the fundamental process of erosion,transportation and sedimentation in the surface area, as is the casein natural sedimentological processes in geology, containing com-ponents of human activity.

    4.5. Recirculation process and the fate of Cs in the future

    Based on the results of this study and previous literatures thefollowing fundamental schematic gure can be drawn (Fig. 9). Itsuggests the possible Cs diffusion and recirculation in the surfaceenvironment.

  • and Tombacz, 1990; Elles and Lee, 2002). Then the Cs is ion-ex-changed with cations in interlayer sites, e.g., K in mica with time.

    tion of every environment.

    ry oThe ion-exchangeable form of Cs is known to be reduced less than50% after 1 year, and relative abundances of Cs are estimated as fol-lows: Cs rmly xed to minerals, is 70%, Cs in ionexchangeablestate is 10% and Cs in a form that is combined to organic matter,is 20% (Tsukada et al., 2008). Cs is softly absorbed to organic mat-ter, e.g., dead leaves and fumus. The fate of the Cs in the organicmatter, especially in dead leaves, will be released later and theymay then be transferred to minerals or plants. The fate of Cs maydepend on soil types and relative abundance and quantities of con-stituent minerals.

    Bacterial absorption of Cs has been reported (Avery, 1995;Derks and Borst-Pauwels, 1979). E. coli has several well-character-ized K uptake transport systems, which are required for enzymeactivation (Bossemeyer et al., 1989). Uptake of Cs by activelymetabolizing microorganisms has been proven successfully. Inbiomass of Rhizopus arrhizus and Penicillium chrysogenu, uptakeby an energy-independent process was suggested to be moreimportant than energy-dependent uptake (Harvey and Patrick,1967; deRome and Gadd, 1991). Cs is expected to persist in a mo-bile form in the environment with accumulation of the Cs bymicroorganisms, which may be related to passing radionuclideto higher trophic levels in the food chain (Avery, 1995). Bacteriamay attack and obtain nutrients from dead leaves etc. So Cs inor on the dead leaves may be transferred into bacteria. Cs mayalso get into plants. Other organisms such as cyanobacteria andeukaryotic algae Chlorella salina (Very et al., 1992, 1993) and fun-gi biomass (Perkins and Godd, 1993) also accumulate Cs. So,microorganisms able to absorb Cs may be ubiquitously habitedin surface conditions, often on dead leaves, etc. From the resultsof this study and previous reports, wide bacterial absorption ofCs was suggested for Fukushima area even if the quantity is notalways so much.

    The relative strength of bonding to phyllosilicates is in the orderof Cs > NH4+ > K+ (Sawhney, 1972). If extreme K+ is supplied, K+ willbe used by plants, and the nal Cs concentration in the plant maybecome low. But if extreme NH4 is used, then Cs will be released,and Cs will be absorbed more by plant.

    Thus, Fig. 9 schematically sketches the future fate of Cs diffu-sion and recirculation in the environment. That is, Cs diffusesand is xed to various materials (minerals, organic matter contain-ing leaves, bacteria, microorganisms, plants, etc.) when Cs encoun-ters them in the solution state. Then, absorbed Cs does not remainin the same materials but diffuses to some extent for a long time,according to strength of sorption. Weakly absorbed Cs, for exampleto green and dead leaves, may be transferred probably to 2:1 phyl-losilicate via bacteria or through natural decay. Cs-xed clay min-erals may also behave as ne sedimentary grains in the surfacegeological process. Thus, a hot spot where radioactive Cs is highlyconcentrated is formed and/or Cs will migrate into the environ-ment. Conditions for formation of the hot spot depend on differ-ent situations in varieties of the sites. Correlations of each factor,such as the presence of clay minerals, dead and green leaves, mi-crobes, pore water depend on a variety of situations.

    5. Summary

    Soil contamination by radioactive Cs in Fukushima region wasWhen a Cs solution corresponding to the above mentioned stepIII meets minerals, it is strongly absorbed to these minerals con-taining phyllosilicates by the weak hydration energy (Johnston

    66 J. Akai et al. / Physics and Chemistexamined from the standpoint of environmental mineralogy. Add-ing to obtained fundamental data for Fukushima City in an earlystage, the following new points were claried.References

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    We thank Mr. Shigeki Chiba of Hobara High School, FukushimaPref., Mr. Nobuo Kuromori of Chishitu-Kisho Kogyou Company andMr. Shinnichi Satoh of Fukushima University Student for their helpin collecting samples and Mr. Shoki Yamada of Niigata UniversityStudent for his help in drawing gures. We thank BAMI Co., Ltd.in Fukushima and NITTAI Co., Ltd. in Okayama for supplying ver-miculite samples, and JIHKURAITO Co., Ltd. in Yamagata for sup-plying the Itaya zeolite sample. We thank Dr. Hossain Anawar forhis kind and detailed comments to the manuscript to improvingit. This work was supported by Grants-in-Aid for Scientic Re-search by JSPS (Challenging Exploratory Research). We alsoacknowledge many citizens of Wakamiya Cho, Nihonmatsu City,and Fukushima Pref. for their cooperation in cleaning Cs-contami-nated spots and sampling. We appreciate careful and kind com-ments of anonymous reviewers for this manuscript.1. Comparative sorption experiments of Cs by wide varieties ofphyllosilicates containing serpentine, heated vermiculite andweathered montmorillonit, dead and green leaves, and zeolitewere carried out. Strength and capacity for sorption of Cs is inthe order of zeolite > 2:1 type clay > 1:1 type clay > leaves.

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    5. The future diffusion and recirculation behavior of Cs in the envi-ronment were discussed using a schematic model gure. Theconcrete process of hot spot formation depends on each situa-

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    Mineralogical and geomicrobial examination of soil contamination by radioactive Cs due to 2011 Fukushima Daiichi Nuclear Power Plant accident1 Introduction2 Materials and methods2.1 Materials2.1.1 Soil and sandy dust specimens from highly Cs-concentrated areas2.1.2 Mineral and leaf samples2.1.3 Bacteria

    2.2 Experimental methods2.2.1 Radiation measurements and XRD analysis2.2.2 Sorption and desorption experiments by clay minerals, zeolite and leaves2.2.3 Bacterial culture experiments and TEM (Transmission Electron Microscopy) observations

    3 Results3.1 Analysis of sandy dust sample from Tachibana High School and soil sample from Date city3.2 Sorption and desorption experiments by clay minerals, zeolite and leaves3.2.1 Sorption experiment3.2.2 Desorption experiment by leaves3.2.3 Culture experiments using naturally living bacterial mixture to absorb Cs3.2.4 Culture experiments using various bacteria to absorb Cs

    4 Discussion4.1 Characteristics of soil contamination in Fukushima case4.2 Sorption and desorption characteristics4.3 Interaction between microbes and minerals4.4 Formation of a so-called hot spot4.5 Recirculation process and the fate of Cs in the future

    5 SummaryAcknowledgmentsReferences


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