Accumulation of Radioactive Cesium Released from Fukushima Daiichi Nuclear Power Plant in Terrestrial Cyanobacteria Nostoc commune

The Fukushima Daiichi Nuclear Power Plant accident released large amounts of radioactive substances into the environment and contaminated the soil of Tohoku and Kanto districts in Japan. Removal of radioactive material from the environment is an urgent problem, and soil purification using plants is being considered. In this study, we investigated the ability of 12 seed plant species and a cyanobacterium to accumulate radioactive material. The plants did not accumulate radioactive material at high levels, but high accumulation was observed in the terrestrial cyanobacterium Nostoc commune. In Nihonmatsu City, Fukushima Prefecture, N. commune accumulated 415,000 Bq/kg dry weight 134Cs and 607,000 Bq kg−1 dry weight 137Cs. The concentration of cesium in N. commune tended to be high in areas where soil radioactivity was high. A cultivation experiment confirmed that N. commune absorbed radioactive cesium from polluted soil. These data demonstrated that radiological absorption using N. commune might be suitable for decontaminating polluted soil.

Radioactive material was released into the environment in large quantities after the accident at the Fukushima Daiichi Nuclear Power Plant in March 2011, contaminating the soils of Tohoku and Kanto districts in Japan. According to the calculations of the Tokyo Electric Power Company, approximately 9.0×10 17 Bq of radioactive material was released by the accident (14). The level of this radioactive material is being monitored (1,12), and its accumulation by and effects on organisms have been reported (3,4).
Plants are primary producers and can accumulate radioactive material. Contamination of crops and wild plants is thus a major concern (7,9,13), but the details are poorly understood. For example, a sunflower that accumulated high levels of radioactive material was used to purify soil polluted after the Chernobyl Nuclear Power Plant accident that occurred in 1986 in Russia (2,5,10). However, a decontamination experiment using a sunflower performed by the Ministry of Agriculture, Forestry and Fisheries of Japan in 2011 was not successful (6).
While investigating the accumulation of radioactive material in wild plants and cyanobacterium in Iwaki City, Fukushima Prefecture, Japan, high accumulation was observed in the terrestrial cyanobacterium Nostoc commune. This species is a heterocystous blue-green algae that forms jelly-like clumps of polysaccharides. Radioactive material is expected to be deposited in these polysaccharides, simplifying its removal from the environment (11). Furthermore, it is reported that this species grows under high radiation exposure (8). In this study, we monitored the accumulation of radioactive material in N. commune.

Materials and Methods
Collection of seed plants and cyanobacterium N. commune Twelve species of seed plants and cyanobacterium N. commune were collected in 2012 from a site belonging to Iwaki Meisei University in Fukushima Prefecture, Japan. The site is approximately 45 km from the Fukushima Daiichi Nuclear Power Plant. N. commune was also collected from 34 habitats in Akita, Miyagi, Fukushima, Ibaraki, Tochigi, Chiba, Tokyo, Kyoto, Osaka, Yamaguchi, and Fukuoka prefectures, Japan, in 2011 and 2012 ( Fig. 1).

Detection of radioactive cesium and iodine
Field materials collected were transported to the laboratory in a polyethylene bag at 15-20°C to avoid damage during transportation. Plant and cyanobacterial samples were washed with water and dried at room temperature. Dried samples were desiccated at 60°C for 48 h, pulverized using a mill, and placed in U-8 plastic vials (Φ56 mm×68 mm high). Vials were stored in a desiccator until measurement. Radioactive cesium ( 134 Cs, 137 Cs) and iodine ( 131 I) were measured using a GEM40P4-76 Ge semiconductor detector (Seiko EG & G, Tokyo, Japan). Soil samples were dried at 60°C for 48 h, sifted through a Φ2.8 mm mesh, and placed in V-11 plastic vials (Φ128 mm×76 mm high). Levels of 134 Cs, 137 Cs, and 131 I were measured using a CAN-OSP-NAI NaI scintillation counter (Hitachi-Aloka Medical, Tokyo, Japan) or a Ge semiconductor detector.

Cultivation experiments
We used N. commune cultivated on Miyakojima Island, Okinawa, Japan, for this experiment. Dried N. commune (30 g) was soaked in distilled water for 1 h and then put on the surface of polluted sand or loam soil (1 kg) in a plastic box (40 cm length×32 cm width×7 cm height). The samples were cultivated outdoors for 30 days in November 2011. The concentration factor was calculated using the formula (radioactive cesium concentration in N. commune)/(radioactive cesium concentration in soil), where the cesium concentration was measured in Bq kg −1 dry weight (DW).

Results and Discussion
We investigated soil contamination by radioactive material at a site of Iwaki Meisei University. In April 2012, the radioactivity was distributed within the top 10 cm of topsoil ( Table 1). The concentration of 137 Cs was 2,530 Bq kg −1 DW at depths of 0-5 cm, 424 Bq kg −1 DW at 5-10 cm, 31 Bq kg −1 DW at 10-15 cm, and 5 Bq kg −1 DW at 15-20 cm. 131 I was not detected, perhaps because of its short half-life (8.02 days).
In all the 12 seed plant species studied, we detected relatively low concentrations of radioactive cesium ( Table  2). Accumulation levels in larger plants such as Solidago canadensis var. scabra tended to be lower than in smaller plants. In S. canadensis var. scabra, the concentrations of 137 Cs were 78 Bq kg −1 DW in shoots and 100 Bq kg −1 DW in roots. In contrast, the small plant Vicia sativa ssp. nigra accumulated 557 Bq kg −1 DW 137 Cs in shoots and 1,520 Bq kg −1 DW in roots. We believe that V. sativa ssp. nigra absorbed more radioactive cesium because of its small root system. Overall, more radioactive material accumulation was concentrated in the roots than in the shoots. In the shoots, 134 Cs levels were 29-410 Bq kg −1 DW and 137 Cs levels were 43-557 Bq kg −1 DW. In the roots, 134 Cs levels were not detected (ND) to 1,120 Bq kg −1 DW and 137 Cs levels were ND-1,520 Bq kg −1 DW. These data suggested that seed plants generally do not easily transport radioactive cesium into shoots. In contrast, high concentrations of 134 Cs (32,300 Bq kg −1 DW) and 137 Cs (46,200 Bq kg −1 DW) were observed in terrestrial cyanobacterium N. commune.    N. commune grows throughout the year. We believe that the cyanobacteria sampled from Nihonmatsu existed at the time of the nuclear accident.
Relatively high concentrations of cesium were also detected in the samples from Miyagi, Ibaraki, and Chiba prefectures surrounding Fukushima. In Abiko City (Chiba Prefecture), approximately 200 km from the power plant, 5,380 Bq kg −1 DW 134 Cs and 7,590 Bq kg −1 DW 137 Cs were detected in N. commune. Abiko City was reported to have high levels of radioactivity in rain after the accident. In contrast, radioactive cesium was not detected in samples from Osaka, Yamaguchi, and Fukuoka prefectures; cesium released after the accident probably did not reach these areas.
The concentration of radioactive cesium in N. commune tended to be high where soil contamination was high. Growing on the soil surface, N. commune appeared to have been strongly exposed to radioactivity. As shown in supplementary Fig. 1, the radioactive cesium concentrations in the soil and in N. commune were directly proportional and relatively well correlated.
N. commune might absorb radioactive cesium from polluted soil or contaminated rainwater. To clarify how radioactive cesium was absorbed by N. commune, we cultivated the cyanobacterium in polluted sand and loam soils.
Radioactive cesium was not detected from N. commune cultivated on Miyakojima Island, which was used for the experiment. During the experimental period, there were three rain showers, but radioactive cesium was not detected in rainwater. The temperature ranged 6-25°C. After 30 days, growth of N. commune was not observed, but it had absorbed radioactive cesium (Table 3 These results suggested that wild N. commune directly absorbed radioactively contaminated rainwater. However, N. commune absorbed more radioactive cesium from the soil than the seed plants. The 134 Cs concentration factors were  0.07-0.39 in sunflower and 0.02-0.07 in soybean (5).
Removal of radioactive material from the environment is an urgent problem in affected areas, and soil decontamination using living organisms is being considered. In microbes, cesium-accumulating bacteria have been isolated (15,16), but collecting these bacteria from polluted soil is difficult.
In this study, we demonstrated that the terrestrial cyanobacterium N. commune can absorb high levels of radioactive cesium. Because N. commune forms jelly-like clumps, it can be easily collected from the soil surface. Furthermore, its weight decreases by about 90% when N. commune is dried. Radiological absorption by N. commune may be a viable strategy for decontaminating polluted soil. We will perform decontamination experiments using N. commune in the future.