Accumulation of potassium, rubidium and caesium (133Cs and 137Cs in various fractions of soil and fungi in a Swedish forest.
ABSTRACT Radiocaesium ((137)Cs) was widely deposited over large areas of forest in Sweden as a result of the Chernobyl accident in 1986 and many people in Sweden eat wild fungi and game obtained from these contaminated forests. In terms of radioisotope accumulation in the food chain, it is well known that fungal sporocarps efficiently accumulate radiocaesium ((137)Cs), as well as the alkali metals potassium (K), rubidium (Rb) and caesium (Cs). The fungi then enhance uptake of these elements into host plants. This study compared the accumulation of these three alkali metals in bulk soil, rhizosphere, soil-root interface, fungal mycelium and sporocarps of mycorrhizal fungi in a Swedish forest. The soil-root interface was found to be distinctly enriched in K and Rb compared with the bulk soil. Potassium concentrations increased in the order: bulk soil<rhizosphere<fungal mycelium<soil-root interface<fungal sporocarps; and Rb concentration in the order: bulk soil<rhizosphere<soil-root interface<fungal mycelium<fungal sporocarps. Caesium was more or less evenly distributed within the bulk soil, rhizosphere and soil-root interface fractions, but was actively accumulated by fungi. Fungi showed a greater preference for Rb and K than Cs, so the uptake of (137)Cs could be prevented by providing additional Rb or K at contaminated sites. The levels of K, Rb, and Cs found in sporocarps were at least one order of magnitude higher than those in fungal mycelium. These results provide new insights into the use of transfer factors or concentration ratios. The final step, the transfer of alkali metals from fungal mycelium to sporocarps, raised some specific questions about possible mechanisms.
- SourceAvailable from: Klas Rosén[Show abstract] [Hide abstract]
ABSTRACT: Methods for cleaning up radioactive contaminated soils are urgently needed. In this study we investigated whether the use of arbuscular mycorrhizal (AM) fungi can improve (137)Cs uptake by crops. Barley, cucumber, perennial ryegrass, and sunflower were inoculated with AM fungi and grown in low-level radionuclide contaminated soils in a field experiment 70 km southwest of Chernobyl, Ukraine, during two successive years (2009-2010). Roots of barley, cucumber and sunflower plants were slightly or moderately infected with AM fungus and root infection frequency was negatively or non-correlated with (137)Cs uptake by plants. Roots of ryegrass were moderately infected with AM fungus and infection frequency was moderately correlated with (137)Cs uptake by ryegrass. The application of AM fungi to soil in situ did not enhance radionuclide plant uptake or biomass. The responsiveness of host plants and AM fungus combination to (137)Cs uptake varied depending on the soil, although mycorrhization of soil in the field was conditional and did not facilitate the uptake of radiocesium. The total amount of (137)Cs uptake by plants growing on inoculated soil was equal to amounts in plant cultivated on non-inoculated soil. Thus, the use of AM fungi in situ for bioremediation of soil contaminated with a low concentration of (137)Cs could not be recommended.Journal of environmental radioactivity 08/2013; 126C:14-19. · 1.47 Impact Factor
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ABSTRACT: The objectives of this study were to evaluate applicability of food waste compost (FWC) as a substrate for cultivation of Ganoderma lucidum, Lentinula edodes, and Pholiota adipose, and to determine contents of Ca, Mg, Na, and K in fruiting bodies (FB). FB yield per substrate in FWC-free controls was 53 ± 4 g/kg for G. lucidum, 270 ± 90 g/kg for L. edodes, and 1,430 ± 355 g/kg for P. adipose. Substrates supplemented with FWC showed the highest FB production at FWC content of 10% for G. lucidum (64 ± 6 g/kg), and 13% for L. edodes (665 ± 110 g/kg) and P. adipose (2,345 ± 395 g/kg), which were 1.2~2.5 times higher than the values for the controls. P. adipose contained higher amounts of mineral elements than the other species. Ca, Mg, Na, and K content in FB did not show a significant relation to FWC content.Mycobiology 12/2013; 41(4):210-3.
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ABSTRACT: Radionuclide contamination in terrestrial ecosystems has reached a dangerous level. The major artificial radionuclide present in the environment is (137)Cs, which is released as a result of weapon production related to atomic projects, accidental explosions of nuclear power plants and other sources, such as reactors, evaporation ponds, liquid storage tanks, and burial grounds. The release of potentially hazardous radionuclides (radiocesium) in recent years has provided the opportunity to conduct multidisciplinary studies on their fate and transport. Radiocesium's high fission yield and ease of detection made it a prime candidate for early radio-ecological investigations. The facility setting provides a diverse background for the improved understanding of various factors that contribute toward the fate and transfer of radionuclides in the terrestrial ecosystem. In this review, we summarize the significant environmental radiocesium transfer factors to determine the damaging effects of radiocesium on terrestrial ecosystem. It has been found that (137)Cs can trace the transport of other radionuclides that have a high affinity for binding to soil particles (silts and clays). Possible remedial methods are also discussed for contaminated terrestrial systems. This review will serve as a guideline for future studies of the fate and transport of (137)Cs in terrestrial environments in the wake of the Fukushima Nuclear Power Plant disaster in 2011.Environmental Geochemistry and Health 05/2014; · 2.08 Impact Factor
Accumulation of potassium, rubidium and caesium (133Cs and137Cs) in various
fractions of soil and fungi in a Swedish forest
M. Vinichuka,c,⁎, A.F.S. Taylorb, K. Roséna, K.J. Johansona
aDepartment of Soil and Environment, Swedish University of Agricultural Sciences, P.O. Box 7014, SE-750 07, Uppsala, Sweden
bMacaulay Land Use Research Institute, Craigiebuckler, Aberdeen, AB15 8QH UK
cDepartment of Ecology, Zhytomyr State Technological University, 103 Cherniakhovsky Str., 10005, Zhytomyr, Ukraine
a b s t r a c t a r t i c l ei n f o
Received 4 September 2009
Received in revised form 12 February 2010
Accepted 12 February 2010
Available online 23 March 2010
Radiocaesium (137Cs) was widely deposited over large areas of forest in Sweden as a result of the Chernobyl
accident in 1986 and many people in Sweden eat wild fungi and game obtained from these contaminated
forests. In terms of radioisotope accumulation in the food chain, it is well known that fungal sporocarps
efficiently accumulate radiocaesium (137Cs), as well as the alkali metals potassium (K), rubidium (Rb) and
caesium (Cs). The fungi then enhance uptake of these elements into host plants. This study compared the
accumulation of these three alkali metals in bulk soil, rhizosphere, soil–root interface, fungal mycelium and
sporocarps of mycorrhizal fungi in a Swedish forest. The soil–root interface was found to be distinctly
enriched in K and Rb compared with the bulk soil. Potassium concentrations increased in the order: bulk
soilbrhizospherebfungal myceliumbsoil–root interfacebfungal sporocarps; and Rb concentration in the
order: bulk soilbrhizospherebsoil–root interfacebfungal myceliumbfungal sporocarps. Caesium was more
or less evenly distributed within the bulk soil, rhizosphere and soil–root interface fractions, but was actively
accumulated by fungi. Fungi showed a greater preference for Rb and K than Cs, so the uptake of137Cs could
be prevented by providing additional Rb or K at contaminated sites. The levels of K, Rb, and Cs found in
sporocarps were at least one order of magnitude higher than those in fungal mycelium. These results provide
new insights into the use of transfer factors or concentration ratios. The final step, the transfer of alkali
metals from fungal mycelium to sporocarps, raised some specific questions about possible mechanisms.
© 2010 Elsevier B.V. All rights reserved.
The mycelium of soil fungi plays a central role in the uptake of
nutrients from soil into plants via the formation of symbiotic
mycorrhizal associations (Read and Perez-Moreno, 2003). The fungi
enhance nutrient uptake into the host plant, both as a consequence of
the physical geometry of the mycelium and by the ability of the fungi
to mobilise nutrients from organic substrates through the action of
extracellular catabolic enzymes (Leake and Read, 1997). In addition to
acquiring essential macronutrients, mycorrhizal fungi are also very
efficient at taking up and accumulating microelements (Smith and
Read, 1997). Unfortunately, this ability includes accumulating non-
essential elements (Falandysz et al., 2007, 2008) and radionuclides,
retention, mobility and availability of these elements in forest
ecosystems (Nikolova et al., 1997; Rühm et al., 1997; Steiner et al.,
137Cs. This can have important consequences for the
The importance of fungi in radiocaesium migration in forest
systems is well documented (Rafferty et al., 1997). It has been
suggested that fungal mycelium may act as a sink for radiocaesium,
containing 20–30% of
Dighton et al., 1991; Brückmann and Wolters, 1994; Guillitte et al.,
1994; Nikolova et al., 2000). In previous work, we showed that
mycelium in organic soil layers contained 0.1–50% of the
Swedish forest soils (Vinichuk et al., 2005). In addition, mycelium
(particularly sporocarps) was shown to accumulate137Cs against a
background of low
concentrations in many fungi have been found to be 10 to 100 times
higher than in plants (Bakken and Olssen, 1990; Yoshida and
Muramatsu, 1998). Consequently, the consumption of sporocarps of
edible fungi (Skuterud et al., 1997) or of game animals that have
consumed large quantities of fungi with high
(Johanson et al., 1994) represents an important pathway by which
137Cs enters the human food system.
The chemical behaviour of137Cs could be expected to be similar to
that of stable caesium and also to that of K and Rb, which have rather
similar physicochemical properties, e.g. valence and ion diameter
(Bowen, 1979). Rubidium has often been used for studies on K uptake
and seems to emulate K to a high degree (Marschner, 1995). Both K
137Cs in soil inventories (Olsen et al., 1990;
137Cs activity concentrations.
Science of the Total Environment 408 (2010) 2543–2548
⁎ Corresponding author. Department of Soil and Environment, Swedish University of
Agricultural Sciences, P.O. Box 7014, SE-750 07, Uppsala, Sweden. Tel.: +46 18 67 14
42; fax: +46 18 67 28 95.
E-mail address: Mykhailo.Vinichuk@mark.slu.se (M. Vinichuk).
0048-9697/$ – see front matter © 2010 Elsevier B.V. All rights reserved.
Contents lists available at ScienceDirect
Science of the Total Environment
journal homepage: www.elsevier.com/locate/scitotenv
and Rb show the same uptake kinetics and compete for transport
along gradients of concentrations in different compartments of soil
and organisms (Rodríguez-Navarro, 2000). However, the relationship
between K and Rb when taken up by fungi is not well understood
(Yamagata et al., 1959; Yoshida and Muramatsu, 1998).
Uptake of Cs is also related to uptake of K, particularly in fungi
(Bystrzejewska-Piotrowska and Bazal, 2008). Cs influx into cells and
its use of K transporters is discussed in great detail in the review by
White and Broadley (2000).
Myttenaere et al. (1993) summarised the relationship between
radiocaesium and K in forests and suggested the possible use of K as
an analogue for predicting radiocaesium behaviour. However, Cs has
not show good correlations with K in studies of alkali metal uptake
and it has been suggested that there is an alternative pathway for Cs
uptake into cells (Yoshida and Muramatsu, 1998). At the cellular level,
K is accumulated within cells andis the most important ion in creating
membrane potential and excitability.
The aim of the present study was to investigate the behaviour of
the three alkali metals K, Rb and Cs in bulk soil, fungal mycelium and
sporocarps. The important role that fungal mycelium plays in nutrient
uptake in forest soils, in particular its role in137Cs transfer between
soil and fungi, requires better understanding of the mechanisms
involved. An attempt was made to quantify the uptake and
distribution of the alkali metals in the soil–mycelium–sporocarp
compartments and to study the relationships between K, Rb and Cs in
the various transfer steps. Our starting hypothesis was that K uptake
could be used as an indicator of radiocaesium uptake in fungi.
2. Materials and methods
2.1. Sampling area
The study area was located in a forest ecosystem close to the
Forsmark nuclear power plant, on the east coast of central Sweden
(60°22′N, 18°13′E). The soil at the site is a sandy or clayey till and the
humus mainly occurs in the form of mull. Mosses dominate the
ground-layer vegetation. The field layer consists mainly of bilberry
(Vaccinium myrtillus L.), bracken (Pteridium aquilinum (L.) Kuhn.),
coltsfoot (Tussilago farfara L.), horsetail (Equisetum silvaticum L.) and
stone bramble (Rubus saxatilis L.). The tree layer comprises pure
Norway spruce (Picea abies (L.) H. Karst.) or spruce mixed with Scots
pine (Pinus sylvestris L.), both ca. 100 yrs old. For further details about
the site see Lundin et al. (2004). Ten sampling plots (approx. 10 m2
each) were established 20–50 m apart within this ecosystem, in an
area of approx. 2.0 ha. The dominant trees on plots 1–7 were spruce
and on plots 8–10 Scots pine.
2.2. Sampling of soil and fungi
Samples of soil and fungal sporocarps were collected from the 10
sampling plots in September–November 2003. Four replicate soil
samples were collected around and directly underneath fungal
sporocarps (from an area of about 0.5 m−2) within each 10 m2area.
After the removal of fresh leaves and litter, soil cores were taken to a
depth of 10 cm using a cylindrical steel tube with 5.7 cm diameter.
These soil cores were divided horizontally in the forest into two 5-cm
thick layers and stored in plastic bags at 4 °C until processed.
Sporocarps of the 12 different fungal species collected were
cleaned of any extraneous material, identified to species level in the
laboratory and the fresh material was transferred to 35 or 60 ml
plastic vials for determination of
below). The sporocarps were then dried at 35 °C to constant weight
for determination of Cs, K and Rb concentration. Portions of soil
samples taken from 0 to 5 and 5 to 10 cm depth were also used for
chemical analyses. We did not determine whether mycelia extracted
from the soil samples and sporocarps belonged to the same species,
137Cs activity concentration (see
but assumed that the majority of the prepared mycelia belonged to
the same species, with some inclusion of other species.
2.3. Preparation of fungal mycelium and fractionation of soil
Fungal structures were isolated from the soil samples (0–5 cm layer)
under a dissection microscope (magnification 64×) using forceps and by
The prepared fraction of mycelium contained aseptate and septate
hyphae, strands and rhizomorphs, sclerotia and a small number of
mycorrhizal root tips. The method for mycelium preparation is described
in Vinichuk and Johanson (2003). Mycelium samples were dried at 35 °C
to constant weight for determination of K, Rb and Cs. The amount of
mycelium obtained from each soil sample varied between 30 and 60 mg
DW per gram of soil.
The soil samples (0–5 cm layer) were also partitioned using the
method described by Gorban and Clegg (1996). Large roots, stones
and pieces of wood were removed and the remaining soil was gently
sieved through a 2 mm mesh. This sieved material was termed the
bulk soil fraction.
The soil aggregates containing roots that remained on the sieve
were further crumbled and gently squeezed between the fingers,
resulting in separation of more soil from the roots — this was termed
the rhizosphere fraction. The residue, which was called the soil–root
interface fraction, consisted of the finest roots with adhering soil
particles. The method is fully described in Nikolova et al. (2000). In
total, nine samples of bulk soil fraction and mycelium, 12 samples of
fungal sporocarps and six samples of rhizosphere and soil–root
interface fraction were analysed for K, Rb and Cs.
2.4. Chemical analyses and radiometry
Soil organic matter content (OMC) was determined by heating a
known mass of soil to 550 °C. Soil pH was determined in a 1:5 soil:
water suspension (5 g of soil). The137Cs activity concentrations in the
bulk soil samples and sporocarps were determined using well-
calibrated HP-Ge detectors at the low background laboratory at the
Department of Soil and Environment. This laboratory participates in
intercomparison studies organised by the Swedish Radiation Protec-
tion Authority. The measuring time employed was chosen in order to
obtain a statistical error due to the random process of decays ranging
between 5 and 10%. The137Cs activity concentrations were corrected
to sampling date and expressed as Bq kg−1DW.
For element analyses, a 2.5 g portion of each sample was mixed
with 5 ml HNO3+0.5 ml 30% hydrogen peroxide. The mixture was
then digested using a microwave oven and thereafter diluted with MQ
water and analysed using an inductively coupled plasma technique.
Alkali metals were analysed in the laboratories of ALS Scandinavia, a
company within the ALS Laboratory Group. The analyses were
accompanied by rigorous quality control measures. Plant certified
reference material, peach leaves NIST 1547 (NIST, Gaithenburg, USA),
which has matrix close enough to fine roots and fungal material was
used for accuracy assessment giving recoveries 97–101; 97.5–99.4
and 93.7–102.5% for K, Rb and Cs respectively. For soil CRM SO-2
(heavymetalsinsoil) havebeenusedwhichhasno certified valuesfor
K, Rb or Cs. Detailed procedure of measurements is available in
Rodushkin et al. (2008). Element concentrations in analysed fractions
are reported as mg kg−1DW. The transfer factor (TFg) was calculated
as137Cs activity concentration in sporocarps (Bq kg−1) divided by
137Cs ground deposition (Bq m−2) for the 0–10 cm soil layer.
2.5. Statistical analyses
Data were analysed using one-way analyses of variance. The data
were log10-transformed prior to analysis in order to achieve normality.
M. Vinichuk et al. / Science of the Total Environment 408 (2010) 2543–2548
were sought using Pearson correlation coefficients. All statistical
3.1. Soil characteristics
Soil pH was rather high at the site. The mean pH in the 0–5 cm layer
was 5.2 (range 3.8–6.9) and in the 5–10 cm layer 5.1 (range 3.6–7.1).
The highest soil pH values (6.5–6.9) for the entire 0–10 cm layer were
found in plots 1, 2 and 5, while the pH values in the other plots were in
the range 3.7–5.1.
Soil organic matter content (OMC) at the study site was also high.
The mean OMC in the 0–5 cm layer was 66.2% (range 36.4–97.7),
while in the 5–10 cm layer it was 52.9% (range 21.2–96.6). Plots 5,
8 and 9 had very high OMC values for the 0–10 cm soil layer (84.0,
85.9 and 97.7%, respectively). The pH and OMC values were not
correlated to the uptake of alkali metals in either fungal sporocarps or
3.2. Potassium, Rb and Cs concentrations in soil and fungal
Concentrations of K, Rb and Cs in bulk soil were not significantly
differentfrom those in therhizosphere, althoughthevaluesforall three
elements were slightly higher in the rhizosphere fraction (Table 1).
interface and fungal mycelium fractions than in the bulk soil and
rhizosphere fraction. There were significant 3.5-fold and 2.5-fold in-
respectively. Caesium concentrations varied considerably among
samples and no significant differences were found among the different
fractions analysed. The concentration ratio data (CR, defined as
concentration of the element (mg kg−1DW) in a specific fraction or
fungi divided by concentration of the element (mg kg−1DW) in bulk
in fungal material was more evident, particularly in the sporocarps
Sporocarp:bulk soil concentration ratios, K:Rb and K:Сs ratios in
fungi,137Cs activity concentrations andsoil tofungi transferfactorsfor
the sporocarps analysed are shown in Table 3. The concentration
ratios for each element varied considerably between the species
sampled. In general, the saprotrophic fungus Hypholoma capnoides
had the lowest values and Sarcodon imbricatus the highest. The
sporocarps of the latter species had particularly high values of Rb and
For137Cs, TFg for the species of fungi studied varied between 0.13
in Lactarius trivialis and 5.56 in Cortinarius armeniacus, with a mean
value of about 1.3 (Table 3).
When comparing concentration ratios of K, Rb and Cs, it emerged
that fungal sporocarps accumulated greater amounts of these
elements than mycelium. For example, K concentrations in fungal
sporocarps collected from the same plots where soil samples and
mycelium were extracted were about 15 times higher than the K
concentrations found in mycelium. The concentrations of Rb in fungal
sporocarps were about 18-fold higher than in the corresponding
fungal mycelium and those of Cs about 7-fold higher.
3.3. Relationships between K, Rb and Cs in soil and fungi
There were no significant correlations between K in soil and in
either mycelium (r=0.452, ns) or in sporocarps (r=0.338, ns).
Sporocarp Rb and Cs concentrations were unrelated to soil concen-
trations, but both elements in mycelium were correlated to soil
concentrations (Rb: r=0.856, p=0.003; Cs: r=0.804, p=0.009).
There was a close positive correlation (r=0.946, pb0.001)
between the K:Rb ratio in soil and in fungal mycelium (Fig. 1b). This
relationship was also apparent between soil and sporocarps but was
weak and not significant (r=0.602, ns) (Fig. 1b). The K:Cs ratio in soil
and fungal components showed a somewhat different pattern, with
that in mycelium being closely positively correlated (r=0.883,
p=0.01) to the K:Cs ratio in soil (Fig. 1a). The K:Cs ratio in fungal
sporocarps was relatively weakly and non-significantly correlated to
that in soil.
No significant correlations were found between the concentrations
of the three elements in fungi and soil pH or soil organic mattercontent
(data not shown).
4.1. Potassium, Rb and Cs concentrations in soil and fungi
Potassium is an obligatory component of living cells, all of which
depend on K+uptake, and also eventually on K+flux, to grow and
maintain life. Potassium transport in fungi is reviewed in depth by
Rodríguez-Navarro (2000). In the present study, potassium concen-
tration increased in the order: bulk soilbrhizospherebfungal myce-
liumbsoil–root interfacebfungal sporocarps, and was significantly
higher in the soil–root interface fraction and fungi than in bulk soil.
According to Tyler (1982), the high concentrations of K in fungal
sporocarps may reflect a demand for this element as a major cation in
osmoregulation and also indicates that K is an important element in
regulating the productivity of sporophore formation in fungi.
Rubidium concentrations increased in the order bulk soilbrhizo-
spherebsoil–root interfacebfungal myceliumbfungal sporocarps. The
concentrations of Rb were slightly but significantly higher in the soil–
root interface fraction than in bulk soil and thus fungi seemed to have
highest preference for this element, since the accumulation of Rb by
fungi, and especially fungal sporocarps, was very pronounced.
Rubidium concentrations in sporocarps were more than one order
of magnitude higher than those in mycelium extracted from soil of the
same plots where fungal sporocarps were sampled. The high ability of
Mean concentrations of K, Rb and Cs (mg kg−1DW, (standard deviation)) in soil fractions and fungi.
Element Bulk soil Rhizosphere Soil root–interface Fungal myceliumFruit bodies
0.8 (0.8) a
Means within rows with different letters are significantly different (pb0.001).
Concentration ratios CRs (defined as concentration of the element (mg kg−1DW) in
the specific fraction divided by concentration of the element (mg kg−1DW) in bulk
soil) (mean values (standard deviation)).
Element Rhizosphere Soil root–interface Fungal mycelium Fruit bodies
M. Vinichuk et al. / Science of the Total Environment 408 (2010) 2543–2548
fungi to accumulate Rb is well documented. Studies by Yoshida and
Muramatsu (1998) have demonstrated that mushrooms accumulate
at least one order of magnitude higher concentrations of Rb than
plants growing in the same forest.
Caesium concentrations increased in the order: soil–root inter-
facebbulk soilbrhizospherebfungal myceliumbfungal sporocarps,
and were only significantly higher in fungi compared with bulk soil.
Stable Cs was more or less evenly distributed within bulk soil,
rhizosphere and soil–root interface fractions, indicating no Cs
enrichment of those forest compartments. Fungi showed a tendency
to accumulate Cs, giving a mean concentration ratio of about 2:1 for
mycelium and about 40 for sporocarps. Thus, Cs concentrations in
sporocarps were nearly one order of magnitude higher than those in
mycelium. Similar behaviour of137Cs was observed in our previous
studies (Vinichuk and Johanson, 2003; Vinichuk et al., 2004), where
137Cs activity increased in the order: soilbmyceliumbfungal spor-
ocarps. The differences between fungal species in their preferences for
uptake of137Cs or stable Cs seem to reflect the location of the fungal
mycelium relative to that of caesium within the soil profile (Rühm
et al., 1997). Stable Cs is thought to be less available for uptake since it
is contained in mineral compounds and is difficult for fungi or plants
to access. The concentration ratio for stable Cs in mushrooms has been
reported to be lower than that for137Cs (Yoshida and Muramatsu,
1998). The differing behaviour of the natural and radioactive forms of
Cs may also derive from their disequilibrium in the ecosystem
(Horyna and Řanad, 1988).
For all three alkali metals studied, the levels of K, Rb, Cs and137Cs
in sporocarps were at least one order of magnitude higher than those
in fungal mycelium.
4.2. Preferences in alkali metal uptake by fungi
Studiesof uptakemechanisms andaffinityfor alkali metalsin fungi
are scarce, but some results are reviewed by White and Broadley
(2000) and Rodríguez-Navarro (2000). Terada et al. (1998) studied
the mechanism of
Pleurotus ostreatus (Fr.) Kummer Y-l in a laboratory experiment and
concluded that Cs uptake by mycelia was affected by the presence of K
and Rb, while K uptake by mycelia was affected by Cs. Furthermore, in
an experiment with pure cultures of mycorrhizal fungi, Olsen et al.
(1990) found that some species showed a preference for Cs over K.
Experiments with yeast (Conway and Duggan, 1958) showed a
preference for K over Cs and the affinity for alkali metal uptake
decreased in the order: K+NRb+NCs+followed by Na+and Li+, with
a relative ratio of 100:42:7:4:0.5. Our findings indicate that fungi
(mycelium and sporocarps) prefer Rb and K to Cs. Based on the CR
values obtained for fungal sporocarps (Table 3), the alkali metals
studied can be ranked in the order: Rb+NK+NCs+, with a relative
ratio of 100:57:32, which is within the range mentioned above and
that derived from the Yoshida and Muramatsu (1998) data
(100:88:50). The preference for an alkali metal depends on the
nutritional status of the organism, which at least partly explains the
137Cs and Cs accumulation by the mushroom
Elementconcentration ratios (mg kg−1dwinfungi)/ (mg kg−1dwinbulksoil),K:RbandK:Сs ratiosinfungi(mg kg−1dw) /(mg kg−1dw),137Csactivityconcentrations(Bq kg−1dw)
and transfer factors (Bq kg−1dw) / (Bq m2) for fungal sporocarps.a
Plot SpeciesKRb CsK:Rb
aMean background deposition was 5.6 kBq m2.
Fig. 1. Ratio of (a) K:Cs and (b) K:Rb (b) in fungal sporocarps (♦, solid line) and soil mycelium (○, dotted line) in relation to that in the soil in which they were growing.
M. Vinichuk et al. / Science of the Total Environment 408 (2010) 2543–2548
differences reported between field experiments and laboratory
experiments with a good nutrient supply.
The mycorrhizal species Sarcodon imbricatus was found to be the
most efficient in accumulating K, Rb and Cs, in agreement with results
from other studies. For example, Tyler (1982) studied the litter-
decomposing fungus Collybia peronata and reported a mean CR for Rb
of 41, while the mean CR for Rb in Amanita rubescens, which is
probably mycorrhizal with beech (Fagus sylvatica L.), was above 100.
However, Römmelt et al. (1990) reported lower
mycorrhizal species, which means that mycorrhizal species do not
necessarily accumulate alkali metals more efficiently than sapro-
Accumulation of stable and radioactive caesium by fungi is
apparently species-dependent. Studies by de Meijer et al. (1988)
showed that the variation in concentrations of stable and radioactive
caesium in fungi of the same species is generally larger than the
variation between different species. According to Dahlberg et al.
(1997) the variation in137Cs levels within the same genet of Suillus
varegatus was as large as within non-genet populations of this species.
Our data indicated two orders of magnitude variation in Cs uptake,
with the highest CR value in e.g. S. imbricatus (256) and the lowest in
Lactarius deterrimus (2.6). However, some studies (Seeger and
Schweinshaut, 1981) have reported the highest accumulation of
stable Cs in Cortinariaceae sp.
In the second part of the study we investigated the competition
between K, Rb and Cs in the various transfer steps and attempted to
estimate the relationships between the concentrations of these three
elements in soil, mycelia and fungal sporocarps. The lack of a
significant correlation between K in soil and in either mycelium or
sporocarps may indicate a demand for essential K in fungi, regardless
of the concentration of this element in soil. Indeed, Yoshida and
Muramatsu (1998) came to a similar conclusion, suggesting that K
concentration in fungi seemed to be controlled within a narrow range,
regardless of the fungal species. This also supports the claim that K
uptake by fungi is self-regulated by the internal nutritional require-
ments of the fungus (Baeza et al., 2004). In the case of mycorrhizal
fungi, the nutritional requirements of the fungus and of its host plant
are both relevant.
The relationships observed between K:Rb and K:Cs ratios in fungal
sporocarps and soil mycelia with respect to the soil in which they
were growing (Fig. 1) also indicate differences in uptake of these
alkali metals by fungi. The closest positive correlations between K:Rb
ratios in fungal mycelium and in soil may indicate similarities in the
uptake mechanism of these two elements by fungi. The relationships
found between K:Cs ratios in soil mycelium and in soil were less
pronounced. The K:Cs ratio in mycelium was positively correlated
with that in soil but this correlation was less significant, while the
correlation between soil K:Cs ratio and that found in sporocarps was
also positive but not significant. These findings are in good agreement
with the suggestion by Yoshida and Muramatsu (1998) that since Cs
does not showa good correlationwithK, theremight be an alternative
pathway for Cs uptake into cells and the mechanism of Cs uptake by
fungi could be similar to that for Rb.
High efficiency of Rb uptake by fungi may also indicate that Rb, but
not Cs, eventually replaces essential K due to K limitation (Brown and
Cs does not (Wallace, 1970 and references therein). It has been shown
that forest plants apparently discriminate between K+and Rb+in soils
and a shortage of K+favours the uptake of the closely related Rb+ion
(Nyholm and Tyler, 2000), whereas increasing K+availability in the
system decreases Rb+uptake (Drobner and Tyler, 1998).
Stable Cs uptake was not correlated with K uptake, suggesting that
the uptake mechanisms of these two alkali metal ions by fungi may
differ. No correlation between K and137Cs in fungi has been found in
studies carried out elsewhere (Ismail, 1994; Yoshida and Muramatsu,
40K content for
The results provide some new insights into the use of transfer
factors or concentration ratios. The transfer of alkali metals from
fungalmycelium tosporocarpsraised someparticularquestionsabout
possible transfer mechanisms.
The concentrations of the three stable alkali elements K, Rb and Cs
and the activity concentration of137Cs were determined in various
components of forest ecosystem − bulk soil, rhizosphere, soil–root
interface fraction, fungal mycelium and fungal sporocarps. The soil–
root interface fraction was found to be distinctly enriched with K and
Rb compared with bulk soil. Potassium concentration increased in the
order: bulk soilbrhizospherebfungal myceliumbsoil–root interfa-
cebfungal sporocarps, while Rb concentration increased in the order:
bulk soilbrhizospherebsoil–root interfacebfungal myceliumbfungal
sporocarps. Caesium was more or less evenly distributed within bulk
soil, rhizosphere and soil–root interface fractions, indicating no Cs
enrichment of those forest compartments.
The uptake of K, Rb and Cs during the entire transfer process
gradient. For all three alkali metals studied, the levels of K, Rb and Cs
were at least one order of magnitude higher in sporocarps compared
with fungal mycelium. Potassium uptake seemed to be regulated by
fungal nutritional demands for this element. Fungi showed a high
preference for uptake of Rb and K compared with Cs. According to their
efficiency of uptake by fungi, the three elements may be ranked in the
order: Rb+NK+NCs+, with a relative ratio 100:57:32.
The mechanism of Cs uptake by fungi could be similar to that for
Rb, whereas that the K uptake mechanism may be different.
We would like to express our thanks to Dr. I. Nikolova for her
assistance with experiments and to the staff of theAnalytica laboratory,
Luleå, forICP-AES and ICP-SFMS analyses. We thanks associate editor of
the journal of the Science of the Total Environment Dr. J. Bennett for
valuable comments on the manuscript. The project was financially
supported by SKB (Swedish Nuclear Fuel and Waste Management Co).
Baeza A, Hernández S, Guillén FJ, Moreno G, Manjón JL, Pascual R. Radiocaesium and
naturalgammaemitters inmushroomscollectedinSpain.Sci Total Environ2004;318
Bakken RL, Olssen RA. Accumulation of radiocaesium in fungi. Can J Microbiol 1990;36:
Bowen HJM. Environmental chemistry of the elements. London, UK: Academic Press;
Brown GR, Cummings SP. Potassium uptake and retention by Oceanomonas baumannii
at low water activity in the presence of phenol. FEMS Microbiol Lett 2001;205(1):
Brückmann A, Wolters V. Microbial immobilisation and recycling of137Cs in the organic
layers of forest ecosystems: relationship to environmental conditions, humification
and invertebrate activity. Sci Total Environ 1994;157:249–56.
Bystrzejewska-Piotrowska G, Baza1 MA. A study of mechanisms responsible for
incorporation of cesium and radiocesium into fruitbodies of king oyster mushroom
(Pleurotus eryngii). J Environ Radioact 2008;99:1185–91.
Conway EJ, Duggan F. A cation carrier in the yeast cell wall. Biochem J 1958;69:265–74.
Dahlberg A, Nikolova I, Johanson KJ. Intraspecific variation in137Cs activity concentration
in sporocarps of Suillus variegatus in seven Swedish populations. Mycol Res 1997;101
de Meijer RJ, Aldenkamp FJ, Jansen AE. Resorption of cesium radionuclides by various
fungi. Oecologia 1988;77:268–72.
Dighton J, Clint GM, Poskitt J. Uptake and accumulation of137Cs by upland grassland soil
fungi: a potential pool of Cs immobilisation. Mycol Res 1991;95(9):1052–6.
Drobner U, Tyler G. Conditions controlling relative uptake of potassium and rubidium
by plants from soils. Plant Soil 1998;201:285–93.
Falandysz J, Kunito T, Kubota R, Bielawski L, Mazur A, Falandysz JJ, et al. Selected
elements in Brown Birch Scaber Stalk Leccinum scabrum. J Environ Sci Health Part A
M. Vinichuk et al. / Science of the Total Environment 408 (2010) 2543–2548
Falandysz J, Kunito T, Kubota R, Gucia M, Mazur A, Falandysz JJ, et al. Some mineral
constituents of Parasol Mushroom (Macrolepiota procera). J Environ Sci Health Part B
Gorban GR, Clegg S. A conceptual model for nutrient availability in the mineral soil–root
system. Can J Soil Sci 1996;76:125–31.
Guillitte O, Melin J, Wallberg L. Biological pathways of radionuclides originating from the
Chernobyl fallout in a boreal forest ecosystem. Sci Total Environ 1994;157:207–15.
Horyna J, Řanad Z. Uptake of radiocaesium and alkali metals by mushrooms. J Radioanal
Nuclear Chem 1988;127:107–20.
Ismail SS. Distribution of Na, K, Rb, Cs and137Cs in some Austrian higher fungi. Biol Trace
Elem Res 1994;43–5:707–14.
Johanson KJ, Bergström R, Eriksson O, Erixon A. Activity concentrations of Cs-137 in
moose and forage plants in mid-Sweden. J Environ Radioact 1994;22:251–67.
Leake JR, Read DJ. Mycorrhizal fungi in terrestrial habitats. In: Wicklow DT, Söderström B,
editors. The mycota IV: environmental and microbial relationship. Berlin: Springer-
Verlag; 1997. p. 281–301.
Lundin L, Lode E, Stendahl J, Merklund PA, Björkvald L, Thorstensson A. Soils and site
types in the Forsmark area. SKB-rapport; 2004. 102 pp.
Marschner H. Mineral nutrition of higher plants. 2nd ed. London, UK: Academic press;
Myttenaere C, Schell WR, Thiry Y, Sombre L, Ronneau C, van der Stegen de Schriek J.
Modelling of Cs-137 cycling in forests: recent developments and research needed.
Sci Total Environ 1993;136:77–91.
Nikolova I, Johanson K, Dahlberg A. Radiocaesium in fruitbodies and mycorrhizae in
ectomycorrhizal fungi. J Environ Radioact 1997;37:115–25.
Nikolova I, Johanson KJ, Clegg S. The accumulation of
partment of forest soils. J Environ Radioact 2000;47:319–26.
Nyholm NEI, Tyler G. Rubidium content of plant, fungi and animals closely reflects
potassium and acidity conditions of forest soils. Forest Ecol Manag 2000;134:89–96.
Olsen RA, Joner E, Bakken LR. Soil fungi and the fate of radiocaesium in the soil
ecosystem — a discussion of possible mechanisms involved in the radiocaesium
accumulation in fungi, and the role of fungi as a Cs-sink in the soil. In: Desmet G,
Nassimbeni P, Belli M, editors. Transfer of radionuclides in natural and semi-natural
environment. Luxemburg: Elsevier Applied Science; 1990. p. 657–63.
137Cs and K from forest litter. Soil Biol Biochem 1997;29(11/12):1673–81.
Read DJ, Perez-Moreno J. Mycorrhizas and nutrient cycling in ecosystems — a journey
towards relevance? New Phytol 2003;157:475–92.
137Cs in the biological com-
Rodríguez-Navarro A. Potassium transport in fungi and plants. Biochim Biophys Acta
Rodushkin I, Engström E, Sörlin D, Baxter D. Levels of inorganic constituents in raw nuts
and seeds on the Swedish market. Sci Total Environ 2008;392:290–304.
RömmeltR,HierscheL,SchallerG, Wirth E. Influence ofsoil fungi(basidiomycetes)onthe
P, Belli M, editors.Transferof radionuclides innaturaland seminaturalenvironments.
London: Elsevier; 1990. p. 152160.
Rühm W,KammererL, Hiersche L, Wirth E.The137Cs/134Csratio infungiasanindicator of
the major mycelium location in forest soil. J Environ Radioact 1997;35(2):129–48.
Seeger R, Schweinshaut P. Vorkommen von caesium in höheren pilzen. Sci Total Environ
Skuterud L, Travnicova IL, Balonov MI, Strand P, Howard B. Contribution of fungi to radio-
caesium intake by rural populations in Russia. Sci Total Environ 1997;193(3):237–42.
Smith SE, Read DJ. Mycorrhizal symbiosis. 2nd ed. London: Academic Press; 1997.
Steiner M, LinkovI,YoshidaS.Theroleof fungiinthe transfer andcycling ofradionuclides
in forest ecosystems. J Environ Radioact 2002;58:217–41.
Terada H, Shibata H,Kato F, Sugiyama H.Influence of alkali elements on the accumulation
of radiocesium by mushrooms. J Radioanal Nucl Chem 1998;235(1–2):195–200.
Trans Br Mycol Soc 1982;79:239–41.
of Ukraine. J Environ Radioact 2003;64:27–43.
VinichukMM, Johanson KJ, Taylor AFS.137Cs inthe fungal compartment of Swedish forest
soils. Sci Total Environ 2004;323:243–51.
Vinichuk M, Johanson K, Rosén K, Nilsson I. Role of fungal mycelium in the retention of
radiocaesium in forest soils. J Environ Radioact 2005;78:77–92.
Wallace A. Monovalention carrier effects on transport of86Rb and137Cs into bush bean
plants. Plant Soil 1970;32:526–30.
White PJ, Broadley MR. Mechanisms of caesium uptake by plants. Review. New Phytol
Yamagata N, Yamagata T, Matsuda S. The different distribution of rubidium and cesium
in natural plants. Bull Chem Soc Jpn 1959;32(4):407–14.
Yoshida S,MuramatsuY.Concentrationofalkaliandalkalineearthelements inmushrooms
M. Vinichuk et al. / Science of the Total Environment 408 (2010) 2543–2548