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

Abstract

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 9.0×10¹⁷ 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).

Fig. 1.

Locations of the collection sites of the Nostoc commune investigated in the present study.

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 (¹³⁴Cs, ¹³⁷Cs) and iodine (¹³¹I) 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 ¹³⁴Cs, ¹³⁷Cs, and ¹³¹I 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 ¹³⁷Cs 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. ¹³¹I was not detected, perhaps because of its short half-life (8.02 days).

Table 1.

Radioactivity concentration of ¹³⁴Cs and ¹³⁷Cs in the soil of Iwaki Meisei University, Iwaki City, Fukushima. Soil was collected in April 2012

Depth	134Cs (Bq kg−1 DW)	137Cs (Bq kg−1 DW)
0–5 cm	1,630±298a	2,530±461
5–10 cm	250±73	424±86
10–15 cm	16±14	31±11
15–20 cm	4±1	5±1
20–25 cm	NDb	6±2
25–30 cm	ND	ND

^a3σ counting error.

^bnot detected.

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 ¹³⁷Cs 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 ¹³⁷Cs 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, ¹³⁴Cs levels were 29–410 Bq kg⁻¹ DW and ¹³⁷Cs levels were 43–557 Bq kg⁻¹ DW. In the roots, ¹³⁴Cs levels were not detected (ND) to 1,120 Bq kg⁻¹ DW and ¹³⁷Cs 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 ¹³⁴Cs (32,300 Bq kg⁻¹ DW) and ¹³⁷Cs (46,200 Bq kg⁻¹ DW) were observed in terrestrial cyanobacterium N. commune.

Table 2.

Radioactivity concentration of ¹³⁴Cs and ¹³⁷Cs in wild plants and cyanobacterium grown in Iwaki Meisei University, Iwaki City, Fukushima

Species	Collection dates	Shoot		Root
		134Cs (Bq kg−1 DW)	137Cs (Bq kg−1 DW)	134Cs (Bq kg−1 DW)	137Cs (Bq kg−1 DW)
Dicotyledoneae
Artemisia indica var. maximowiczii	16 April 2012	91±12a	184±15	63±9	76±9
Bidens pilosa var. pilosa	13 October 2012	55±10	93±11	541±51	1,040±61
Cerastium glomeratum	2 May 2012	39±11	59±11	NDb	125±28
Hypochaeris radicata	2 June 2012	227±16	354±19	192±18	308±21
Petasites japonicus	16 April 2012	124±21	174±25	128±12	171±13
Rumex acetosa	24 April 2012	93±11	141±13	206±10	314±12
Solidago canadensis var. scabra	8 June 2012	54±6	78±7	61±8	100±9
Veronica persica	2 May 2012	78±10	136±12	ND	244±64
Vicia sativa subsp. nigra	2 May 2012	410±21	557±24	1,120±48	1,520±53
Monocotyledoneae
Poa annua	8 May 2012	172±17	219±20	506±39	691±43
Dactylis glomerata	15 June 2012	29±7	43±7	106±21	182±22
Imperata cylindrica	26 June 2012	73±11	129±12	101±17	214±21
Cyanobacteria
Nostoc commune	24 April 2012	32,300±101	46,200±125

^a3σ counting error.

^bnot detected.

N. commune was collected from 34 habitats between August 2011 and October 2012. The radioactivity concentrations of ¹³⁴Cs and ¹³⁷Cs are summarized in supplementary Table 1. The ¹³⁴Cs concentrations ranged from not detectable (ND) to 415,000 Bq kg⁻¹ DW, while the ¹³⁷Cs concentrations ranged from ND to 607,000 Bq kg⁻¹ DW. Radioactive iodine ¹³¹I was not detected in any samples. High radioactive cesium levels were observed in the samples from Fukushima Prefecture, where the Fukushima Daiichi Nuclear Power Plant is located. In particular, 415,000 Bq kg⁻¹ DW ¹³⁴Cs and 607,000 Bq kg⁻¹ DW ¹³⁷Cs were detected in N. commune from Nihonmatsu, where soil contamination was high (5,460 Bq kg⁻¹ DW ¹³⁴Cs, 6,330 Bq kg⁻¹ DW ¹³⁷Cs). However, much lower radioactivity levels (28,300 Bq kg⁻¹ DW ¹³⁴Cs, 39,800 Bq kg⁻¹ DW ¹³⁷Cs) were detected in the cyanobacterial sample from Koriyama, although soil radioactivity was very high there (26,500 Bq kg⁻¹ DW ¹³⁴Cs, 33,200 Bq kg⁻¹ DW ¹³⁷Cs). 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 ¹³⁴Cs and 7,590 Bq kg⁻¹ DW ¹³⁷Cs 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). In polluted sand (4,980 Bq kg⁻¹ DW ¹³⁴Cs, 6,070 Bq kg⁻¹ DW ¹³⁷Cs), N. commune accumulated 3,100 Bq kg⁻¹ DW ¹³⁴Cs and 4,420 Bq kg⁻¹ DW ¹³⁷Cs. The concentration factors were 0.62 for ¹³⁴Cs and 0.73 for ¹³⁷Cs. Similarly, in polluted loam soil (785 Bq kg⁻¹ DW ¹³⁴Cs, 962 Bq kg⁻¹ DW ¹³⁷Cs), the cyanobacterium contained 183 Bq kg⁻¹ DW ¹³⁴Cs and 246 Bq kg⁻¹ DW ¹³⁷Cs, giving concentration factors of 0.23 for ¹³⁴Cs and 0.26 for ¹³⁷Cs. The concentration factors in the sand were higher than those in the loam soil. The reasons for this difference between soil types should be examined in the future.

Table 3.

Radioactivity concentration of ¹³⁴Cs and ¹³⁷Cs in Nostoc commune grown in polluted soil. N. commune was cultivated outdoors for 30 days

Soil type	Soil		Nostoc commune		Concentration factor
	134Cs (Bq kg−1 DW)	137Cs (Bq kg−1 DW)	134Cs (Bq kg−1 DW)	137Cs (Bq kg−1 DW)	134Cs	137Cs
Sand	4,980±300a	6,070±365	3,100±47	4,420±55	0.62	0.73
Loam	785±48	962±58	183±12	246±14	0.23	0.26

^a3σ counting error.

The concentration factors for wild N. commune, shown in supplementary Table 1, were 0.85–76.01 for ¹³⁴Cs and 0.98–95.89 for ¹³⁷Cs, but were much lower for cultivated N. commune (0.23 and 0.62 for ¹³⁴Cs, 0.26 and 0.73 for ¹³⁷Cs). 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 ¹³⁴Cs 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 cyano-bacterium 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.