MINIREVIEW
Fungi and ionizing radiation from radionuclides
John Dighton1, Tatyana Tugay2 & Nelli Zhdanova2
1
Rutgers University Pinelands Field Station, NJ, USA; and 2Instiute of Microbiology and Virology, National Academy of the Sciences of the Ukraine,
Kiev, Ukraine
Correspondence: John Dighton, Rutgers
University Pinelands Field Station, PO Box
206, 501 Four Mile Road, New Lisbon, NJ
08064, USA. Tel.: 1609 894 8849; fax:
1609 894 0472; e-mail:
[email protected]
Received 2 November 2007; accepted 3 January
2008.
DOI:10.1111/j.1574-6968.2008.01076.x
Editor: Richard Staples
Keywords
radionuclides; mycorrhizae; remediation;
melanin; micro-fungi; radioadaptive properties.
Abstract
Radionuclides in the environment are one of the major concerns to human health
and ecotoxicology. The explosion at the Chernobyl nuclear power plant renewed
interest in the role played by fungi in mediating radionuclide movement in
ecosystems. As a result of these studies, our knowledge of the importance of fungi,
especially in their mycorrhizal habit, in long-term accumulation of radionuclides,
transfer up the food chain and regulation of accumulation by their host plants was
increased. Micro-fungi have been found to be highly resilient to exposure to
ionizing radiation, with fungi having been isolated from within and around the
Chernobyl plant. Radioresistance of some fungal species has been linked to the
presence of melanin, which has been shown to have emerging properties of acting
as an energy transporter for metabolism and has been implicated in enhancing
hyphal growth and directed growth of sensitized hyphae towards sources of
radiation. Using this recently acquired knowledge, we may be in a better position
to suggest the use of fungi in bioremediation of radioactively contaminated sites
and cleanup of industrial effluent.
Introduction
Radionuclide contamination has become a part of our
environment in the form of fallout from nuclear weapons,
waste from nuclear energy-generating industries and from
medical uses of radioisotopes. Fungi play a major role in
providing ecosystem services in terrestrial ecosystems
(Dighton, 2003) and it is in these systems that their
interaction with radionuclides has been most studied. The
International Commission on Radiological Protection recommendations on the ecological aspects of radionuclide
release (Coughtree, 1983), highlighted the importance of
organic soil horizons and their microbial communities
(fungi and bacteria) as potential accumulators of nutrient
elements and radionuclides within terrestrial ecosystems
(Heal & Horrill, 1983).
Radionuclide accumulation and movement in organic
horizons of forest soils may be related to fungal biomass
(Osburn, 1967) and where fungal activity is the pivotal
regulator in the interaction between ecosystem components
(Avila & Moberg, 1999; Fig. 1). Steinera et al. (2002) state
that ‘Fungi are one of the most important components of
forest ecosystems, since they determine to a large extent the
fate and transport processes of radionuclides . . .’. The
FEMS Microbiol Lett ]] (2008) 1–12
potential for macro-fruitbodies of higher fungi to hyperaccumulate radionuclides and heavy metals has led to
suggestions that they may be agents for bioremediation
(Gray, 1998). Despite nearly 50 years of investigation of
interactions between radionuclides and fungi, there is still
need for greater understanding of the nature of these
interactions, particularly from a molecular standpoint and
from the point of view of using fungal and plant–fungal
interactions in remediation of polluted systems (Zhdanova
et al., 2005b).
Fungal immobilization of radionuclides
Saprotrophic fungi present an enormous surface area of
hyphae to their surrounding environment, fitting them for
absorbing nutrient elements and radionuclides from the
environment. Microbial immobilization of radionuclides
from decomposing leaf litter and cellophane accumulated
almost three times the amount of radiocesium than sterile
equivalents (Witkamp & Barzansky, 1968). Measurement of
radiocesium incorporation into the fungus Trichoderma
viride from plant litters showed that the concentration factor
in fungi (ratio of radionuclide concentration in the fungus
to the concentration in the resource) decreased as the leaf
2008 Federation of European Microbiological Societies
Published by Blackwell Publishing Ltd. All rights reserved
c
2
J. Dighton et al.
Effect of casual agent
Fungi
Understorey
Tree litter
Animals
Soil mineral
horizon
Soil organic horizon
Tree leaves
Atmosphere
Increasing influence of casual agent
Fig. 1. A plot of the cause–effect relationship between components
(agents) of a forested ecosystem and their influence (effect) on mobility
of radionuclides, as derived from pathway analysis of the behavior of
radiocesium (modified from Avila & Moberg, 1999).
litters aged (2.36, 0.46 and 0.23 for litters of 4, 16 and 48
months of age) (Witkamp, 1968). The highest concentration
factor (4.31) was found from freshly fallen wood. This
provided basic evidence to suggest that fungi could mineralize radionuclides from these resources and translocate
them from the resource into their own biomass, thus
pointing to the potential significance of fungi in regulating
movement of radionuclides in the environment. In general,
it is thought that accumulation of radionuclide elements
follows that of nonradioactive elements. However, with the
discovery of isotope discrimination for a number of elements by a range of organisms, this may not hold true. The
ability of an organism to distinguish between isotopes has
led to new fields of ecology enabling nutrient cycling to be
more precise in identifying the source of nutrient acquired
from mixed sources (Henn & Chapela, 2001; Ruess et al.,
2004; Trudell et al., 2004; Hobbie, 2005).
Soil saprotrophic micro-fungi grow into and decompose
carbon based radioactive debris from the Chernobyl reactor
(Zhdanova et al., 1991). Cladosporium cladosporioides and
Penicillium roseopurpureum were shown to overgrow these
‘hot particles‘( o 1147 Bq of g-activity) and destroy them
within 50–150 days. Accumulation of released radionuclide
into fungal tissue from intact particles was greater for 152Eu
than 137Cs, but similar when the particles were ground in to
powder. Thus, capacity to acquire radionuclides in these
fungi is an interaction between the physical nature of the
radioactive source, fungal species and, presumably, their
enzymatic potential.
Grassland soil saprotrophic fungi have great potential for
uptake and accumulation of radiocesium fallout (Olsen
2008 Federation of European Microbiological Societies
Published by Blackwell Publishing Ltd. All rights reserved
c
et al., 1990; Dighton et al., 1991). Assuming an average
influx rate of 134 nmol Cs g 1 dry weight of mycelium, and
an estimate of hyphal biomass of 6 g dry weight m 2 of soil,
the fungal community of upland grass ecosystems in northern England would be able to take up between 350 and
804 nmol Cs m 1 h 1 of hyphae (Dighton et al., 1991; Dighton
& Terry, 1996) from micromolar concentrations in pore
water (Oughton, 1989). Once incorporated into microbial
(fungal and bacterial) biomass, a large percentage of the
radionuclide loading of organic soils is resistant to leaching,
with 40–80% of radiocaesium being retained, in comparison
to the rate of loss leaching from irradiated (Guillette et al.,
1994) or autoclaved soils (Sanches et al., 2000). In contrast,
in sandy mineral soils where microbial biomass accumulation is low, only an additional 0.005% of 137Cs is extracted
from these soils by sterilization (Cawse, 1983), indicative of
ion exchange but not microbial immobilization. Radiocesium immobilization into the abundant fungal mycelial
biomass of the Ah (O, upper organic) layer of spruce forests
causes retention and accumulation in upper soil horizons
and reduced leaching loss (Rommelt et al., 1990; Guillette
et al., 1990; Drissner et al., 1998; Baeza et al., 2002), where
fungi compete for Cs1 more strongly than plants by 10–150
times (Avery, 1996).
In addition to incorporation of radionuclides into cytoplasm by potassium replacement, the fungal cell wall has high
adsorptive capacity in ion-exchange sites. Dead mycelia (cell
walls) made into filters have been used to adsorb heavy metals
and radionuclides from industrial effluents (Tobin et al.,
1984; Singleton & Tobin, 1996). Potassium replacement is
species specific with suggestions that Rb and Cs replace K in
the filamentous fungus Fusarium solani (Das, 1991), but only
Rb, not Li, Na or Cs could replace K in the yeast Candida utilis
(Aiking & Tempest, 1977). Strontium behaves similarly to
calcium in biological systems. The wood decay fungus,
Resinicium bicolor, can absorb strontium from strontianite
sand and redeposit it in calcium oxalate crystals after
translocation through mycelial cords (Connolly et al., 1998),
thus altering the availability of strontium to other organisms.
Immobilization of radionuclides by fungi is species
dependent. Bio-sorption of radiothorium is higher in Rhizopus arrhizus, and Aspergillus niger than Penicilium italicum
and Penicilium acrysogenum (White & Gadd, 1990) and
Alternaria alternata has a greater uptake capacity than
Aspergillus pulverulens or Fusarium verticilloides for both
60
Co and 137Cs (Mahmoud, 2004). There also appears to be
a significant difference in Cs-uptake capacity between species of both mycorrhizal and saprotrophic basidiomycetes
(Clint et al., 1991). As a result, it is often difficult to
generalize on the efficiency of fungi per se of radionuclide
immobilization.
Accumulation of 90Sr by conidia or mycelium by a range
of micro-fungal species is greater in pigmented than in
FEMS Microbiol Lett ]] (2008) 1–12
3
Fungi and ionizing radiation
unpigmented species (Zhdanova et al., 1990). Mycelia of
light pigmented Moniliaceae accumulate 18–335 Bq g 1 of
90
Sr, but 20–1510 Bq g 1 for dark pigmented Dematiaceae.
Melanin has been shown to account for between 45% and
60% of 60Co and 137Cs incorporation into fungal hyphae
(Mahmoud, 2004).
Macro-fungi are known to translocate materials within
the fungal body, within their hyphae or in specialized
conductive rhizomporphs. Translocation of 14C and 32P
through hyphal systems of Rhizopus, Trichoderma and
Stemphylium is by diffusion (Olsson & Jennings, 1991), and
the direction of flow influenced by source–sink relations
(Olsson, 1995). Absorption of phosphorus by rhizomorphs
of Phallus impudicus and Mutinus canninus consisted of two
transport systems, one being cytoplasmic and the other
through cell walls (Jennings, 1990). In contrast to the
diffusion of C and P, translocation of 137Cs through hyphae
of Armillaria spp. and Schizophyllum commune has been
shown to be slower than that predicted by a diffusion model,
suggesting a possible mechanism for accumulation (Gray
et al., 1995, 1996). Preferential movement of radiocesium
and radiostrontium to the nutrient sinks of developing
basidiomycete fruitbodies has been demonstrated (Gray
et al., 1996; Baeza et al., 2002). Change in the chemical form
of radiostrontium from its site of acquisition as strontianite
sand and redeposition elsewhere as calcium oxalate crystals
after translocation through mycelial cords has been shown
in the wood decay fungus Resinicium bicolo (Connolly et al.,
1998). This suggests that fungi not only have the ability to
spatially redistribute materials, but can alter the chemical
form in which they are released to the environment, thus
altering potential availability to other organisms.
Many ectomycorrhizal symbioses occur in association
with basidiomycete fungi. These produce relatively large
fruiting structures (mushrooms) as well as extensive belowground mycelia. Thus, in addition to accumulation of
radionuclides in below-ground mycelia, translocation to,
and hyper-accumulation of radionuclides in mushrooms
has been shown. High levels of accumulation of radionuclides in mushrooms have been recorded many times,
especially following the Chernobyl accident (Table 1)
(Haselwandter, 1978; IJpelaar, 1980; Eckl et al., 1986; Elstner
et al., 1987; Guillette et al., 1987, 1994; Byrne, 1988; Dighton
& Horrill, 1988; Haselwandter et al., 1988; Horyna & Randa,
1988; Oolbekkink & Kuyper, 1989; Muramatsu et al., 1991;
Watling et al., 1993; Haselwandter & Berreck, 1994; Mietelski et al., 1994; Yoshida & Muramatsu, 1994; Grodzinskaya
et al., 1995; Malinowska et al., 2006). Although a variety of
radionuclides were released from Chernobyl, most of the
surveys relate to the radiocesium content of mushrooms;
however, it has been shown that the radionuclides 7Be, 60Co,
90
Sr, 95Zr, 95Nb, 100Ag, 125Sb, 144Ce, 226Ra and 238U also
accumulated in some mushroom species (Haselwandter &
Berreck, 1994). Accumulation into mushroom-forming
fungi can be a significant proportion of the radionuclide
loading of an ecosystem. A total of 490 Bq kg 1 of radiocesium was accumulated in mycorrhizal and saprotrophic
fungi of a Swedish boreal forest in contrast to the
138 Bq kg 1 contained in organic soil horizons, lichens,
mosses, ferns and angiosperms combined (Guillette et al.,
1994). The fungal loading represented some 78% of radiocesium in the combined ecosystem components measured.
In the years following the Chernobyl explosion, the fungal
contribution to the radionuclide body burden of humans
Table 1. Selected data of radionuclide accumulation in fruitbodies of a number of fungal species
Fungus
Isotope
Cortinarius praestans
Laccaria amethystine
Cortinarius armillatus
Agaricus spp.
Lycoperdon spp.
Various
Various
Various
Various
Various
Various
Lactarius rufus
Inocybe longicystis
Xercomus badius
Xercomus badius
Various
Various
137
FEMS Microbiol Lett ]] (2008) 1–12
Cs
137
Cs
137
Cs
110
Ag
110
Ag
Various
137
Cs
137
Cs
137
Cs
137
Cs
90
Sr, 2391240Pu
137
Cs
137
Cs
40
K
210
Pb
137
Cs
210
Pb
Concentration
(kBq kg 1 dry weight)
Source
0.5
43
44
0.05
0.56
0.09–947
0–33
1400–3700
0.3–20
300–1800
0–0.004
1.8–7.2
8.7–14.2
0.3–6.7
0.007–0.03
0–2.86
0.001–0.36
Byrne (1988)
Byrne (1988)
Byrne (1988)
Byrne (1988)
Byrne (1988)
Haselwandter & Berreck (1994)
Grodzinskaya et al. (1995)
Grodzinskaya et al. (1995)
Mietelski et al. (1994)
Mietelski et al. (1994)
Mietelski et al. (1994)
Dighton & Horrill (1988)
Dighton & Horrill (1988)
Malinowska et al. (2006)
Malinowska et al. (2006)
Kirchner & Daillant (1998)
Kirchner & Daillant (1998)
2008 Federation of European Microbiological Societies
Published by Blackwell Publishing Ltd. All rights reserved
c
4
was shown to have increased from 27% of the dietary
consumption in 1986 to up to 76% in 1988 as the quantity
of milk and meat in the diet declined (Horyna, 1991). Thus,
although data are limited it can be seen that fungi represent
a large ecosystem component of radionuclide accumulation
and potential transfer to food chains.
The Chernobyl explosion released 137Cs–134Cs in a 2 : 1
ratio, which has been used as a fingerprint to distinguish
137
Cs from pre- and post-Chernobyl sources. Using this
fingerprint, it was shown that a large proportion (up to
92%) of the 137Cs accumulated in mushrooms was of preChernobyl origin in the two ectomycorrhizal fungal species
Lactarius rufus and Inocybe longicytis (Dighton & Horrill,
1988). Similar figures of 13–69% of accumulated Cs from
pre-Chernobyl sources are reported in other mushroom
species (Byrne, 1988; Giovani et al., 1990). This suggests
that fungi could be long-term retainers of radionuclides in
the environment. Laboratory liquid culture studies show a
wide range of uptake and incorporation rates of radiocesium
into fungal mycelia. Three saprotrophic basidiomycetes,
Mycena polygramma, Cystoderma amianthinum and Mycena
sanguinolenta had the highest rates of accumulation compared with many ectomycorrhizal species (Clint et al., 1991).
Accumulation varied between about 100 and 250 nmol g 1
dry weight of fungus per hour. However, if the uptake is
expressed on a hyphal surface area basis, the ranking of
species differs, and the uptake values range from 0.1 to
2.5 nmol m 2 hyphal area per hour. This suggests that
acquisition of radionuclides by fungi may be influenced by
growth conditions in soil and the consequential foraging
strategy of the mycelium (Rayner, 1991; Ritz, 1995).
Fungal regulation of radionuclide uptake
by plants
Mycorrhizal symbioses occur in about 95% of all vascular
plant species. In addition to benefits of improved water and
nutrient acquisition, defense against root herbivory and root
pathogens, mycorrhizae are also able to mediate uptake or
radionuclides by plants. Evidence for enhanced uptake of
radionuclides by arbuscular mycorrhizae is somewhat conflicting (Haselwandter & Berreck, 1994). Sweet clover and
Sudan grass showed a slight, but statistically insignificant,
increase in uptake of 137Cs and 60Co by mycorrhizal plants
(Rogers & Williams, 1986), but mycorrhizal Agrostis tenuis
by Glomus mosseae significantly decreased the Cs content of
shoots (Berreck & Haselwandter, 2001). Increased competition between K and Cs in soil, by adding K fertilizer, led to
further suppression of Cs uptake. Glomus mosseae arbuscular mycorrhizal soybeans significantly increased 90Sr uptake
from soil, but uptake of radiocesium into shoots of mycorrhizal Festuca ovina was reduced (Jackson et al., 1973).
The protective effect of mycorrhizae was also shown in
2008 Federation of European Microbiological Societies
Published by Blackwell Publishing Ltd. All rights reserved
c
J. Dighton et al.
transformed carrot root in association with Glomus mycorrhizae, where uptake of radiocesium was strongly correlated
to fungal hyphal length. These mycorrhizal fungal hyphae
have a greater uptake capacity than the root, resulting in
preferential hyphal accumulation in the fungus rather than
in the host plant (de Boulois et al., 2005). However, in this
root culture system, there was no shoot to act as a nutrient
sink; thus the conclusions drawn must bear in mind that
aspect of plant physiology. This effect is plant–species
dependent, as no mycorrhizal enhancement of 134Cs uptake
occurred in clover, Eucalyptus or maize. Instead, mycorrhizae enhanced the uptake of 65Zn in maize (Joner et al.,
2004). Similarly, mycorrhizae increased 137Cs uptake by leek,
but not by ryegrass (Rosén et al., 2005). In grasses, there was
a similar enhanced translocation of radiocesium into shoots
of arbuscular mycorrhizal Festuca ovina, but not into clover
(Trifolium repens), as shown by one experiment (Dighton &
Terry, 1996). In contrast, there was a decrease in the Cs
translocated to the shoots of Agrostis tenuis in the presence
of arbuscular mycorrhizae (Berreck & Haselwandter, 2001).
It is known that the addition of potassium to soil reduces Cs
uptake by plants. The Cs concentration in shoots of Agrostis
was found to be approximately half in plants grown in soil
with amendments of 100 kg ha 1 of potassium to soil,
compared with no K addition and this declined to about
30% over the subsequent 6 weeks (Berreck & Haselwandter,
2001). Thus, the inferences on cesium uptake by plants must
be moderated in relation to the potassium supply, which
acts as a competing ion.
Ericoid mycorrhizal heather plants (Calluna vulgaris)
accumulated less radiocesium than nonmycorrhizal plants
(Clint & Dighton, 1992), indicative of the accumulation in
fungal components in the root. However, mycorrhizal plants
allowed a greater proportion of the Cs to be translocated to
shoots compared with nonmycorrhizal plants. A similar
18% higher shoot accumulation of 137Cs in mycorrhizal
heather compared with nonmycorrhizal plants was observed
by Strandberg & Johansson (1998). Elevated levels of radionuclide in roots compared with shoots in mycorrhizal
plants, suggests that the mycorrhizal fungi accumulate
radiocesium in the fungal tissue in a manner similar to that
shown for heavy metals and ectomycorrhizae (Denny &
Wilkins, 1987a, b). This concept has been reviewed in terms
of competition between radiocesium and potassium in
mycorrhizal Agrostis tenuis symbioses (Berreck & Haselwandter, 2001). They showed that mycorrhizal development
in plant roots reduced Cs uptake by the plant at moderate
nutrient levels in the soil, which suggests that the protective
mechanism is due to sequestration of Cs in the extraradical
hyphae of the mycorrhizal fungus and a reduced translocation into the host plant. They also demonstrated that, for
this fungal plant interaction, there was no benefit of adding
potassium to reduce Cs uptake.
FEMS Microbiol Lett ]] (2008) 1–12
5
Fungi and ionizing radiation
Effects of radionuclides on fungi
The influence of ionizing radiation on yeast cells has
dominated the literature on effects on the genetics and
physiology of fungi. Short term (80 min) exposure of yeast
to 50 Gy of X- and g-radiation elicits the up-regulation of
genes responsible for DNA repair, cell rescue defense,
protein and cell fate and metabolism (Bennett et al., 2001;
Game et al., 2005; Kimura et al., 2006). Both Bennett et al.
(2001) and Game et al. (2005) identified genes involved in
DNA repair using X-rays to simulate the general effects of
ionizing radiation. Game et al. (2005) also shows that the
absence of the DOT1 gene, which is important in the
production of histone #3 protein and the methylation of
lysine-79 reduces effective repair of damaged DNA. The upregulation of specific DNA repair genes were identified using
micro-arrays on X-ray (50 Gy) treated yeast (Kimura et al.,
2006).
Studies on filamentous fungi have mainly been in association with food irradiation. Threshold levels of g-irradiation
suggest that 1.5–4 kGy is sublethal for hyphal growth,
whereas it requires 2.5–5 kGy to effect suppression of spore
germination in Aspergillus niger, Aspergillus flavus and
Fusarium oxysporum (Attaby et al., 2001). However, at these
doses amyloytic and proteolytic activity of these fungi is
reduced. Aflatoxin production by Aspergillus niger, Aspergillus fumigatus, Aspergillus flavus and Penicillium expansum
isolated from apples, was increased at 0.5 kGy, but decreased
above 1.2 kGy of irradiation (Afifi et al., 2003).
Ecological studies on fungal communities have been
conducted at sites of artificially elevated radiation levels. A
total of 41 mycelial fungal species were isolated from soil in
the atomic-weapons Nevada Test Site, USA (Durrell &
Shields, 1960). Between 1997 and 2004, 155 micro-fungi
have been isolated from 49 inner locations of the reactor
room of the Chernobyl Atomic Electric Station (CHAES),
where radiation exposure from a-, b- and g-emitting
239
Pu, 2401241Pu, 241Am, 244Cm and 137Cs has been in the
range of 1.5 10 4–10 000 Gy (Zhdanova et al., 2001,
2005a). Examples of the fungal isolates from Chernobyl are
shown in Table 2 along with the radiation dose at the site of
isolation.
During the last 18 years about, 2000 strains of 180 species
of 92 genera of fungi have been isolated from around
Chernobyl (Zhdanova et al., 2000, 2005b). The richness of
fungal species declined with increasing radiation, indicating
that the community consists of radio-resistant and
susceptible species. Radio-resistant species of Penicillium,
Fusarium, Chrysosporium, Scopulariopsis, Hyalodendron,
Verticillium, Mucor made up to 70–80% of fungal frequency
and Aspergillus versicolor, Aspergillus niger, Hormoconis
resinae, C. sphaerospermum, C. herbarum, C. cladosporioides,
Alternaria alternata, Aureobasidium pullulans, Penicillium
FEMS Microbiol Lett ]] (2008) 1–12
Table 2. List of fungal species isolated from within and around the
Chernobyl nuclear reactor in relation to radiation exposure at site of
isolation (where fungi are in intimate contact with the substrate) and
directional growth towards a collimated beam of ionizing radiation
(tropism)
Species (isolate number)
Radioactivity
of substrate
(Gy 10 3)
Tropism
Penicillium steckii (Pst2)
Penicillium hirsutum (Phir1)
Cladosporium cladosporioides (Ccl4)
Penicillium lanosum (Plan10)
Aspergillus versicolor (Aver43)
Aspergillus versicolor (Aver54)
Cladosporium sphaerospermum (Cshp35)
Cladosporium sphaerospermum (Csph70)
Hormoconis resinae (Hres30)
Aspergillus versicolor (Aver55)
Aspergillus versicolor (Aver57)
Cladosporium sphaerospermum (Csph21)
Hormoconis resinae (Hres52)
Hormoconis resinae (Hres61)
Hormoconis resinae (Hres21)
Penicillium aurantiogriseum (P aur 60)
Aspergillus versicolor (Aver101)
Aspergillus versicolor (Aver102)
Penicillium spinulosum (Pspin85)
Penicillium spinulosum (Pspin87)
Hormoconis resinae (Hres11)
Hormoconis resinae (Hres76)
Hormoconis resinae (Hres77)
Cladosporium herbarum (Cher80)
2
2
3
2
5.5
9.8
3.5
4
4
25
50
10.5
12
20
30
38
10 000
10 000
3000
10 000
150
1000
3000
10 000
Positive
Positive
Positive
Positive
Positive
Positive
Positive
Positive
Positive
Positive
Positive
Positive
Positive
Positive
Positive
Positive
No tropism
No tropism
No tropism
No tropism
No tropism
No tropism
No tropism
No tropism
aurantiogriseum, Penicilium spinulosum, Acremonium strictum made up 10–50% of the frequency.
Despite differences in the habitat between sampling sites,
there is a trend of change in dominance of fungal species
with radiation level (Zhdanova et al., 1990, 1991, 1994,
1995, 2000). Both Chaetomium aureum and Paecilomyces
lilacinus are indicators of high levels of radionuclide
contamination (3.7 106–3.7 108 Bq kg 1) of soil in
woodland ecosystems, Acremonium strictum and Arthrinium
phaeospermum bioindicators at mid level of pollution
(3.7 103–3.7 105 Bq kg 1) and Myrothecium roridum
and Metarhizium anisopliae as bioindicators of low contamination (o 3.7 102 Bq kg 1).
Intense radiation within the 10 km CHAES alienation
zone led to simpler soil fungal communities being dominated by melanized fungal species (Zhdanova et al., 1995).
Melanin may provide a radiological protective mechanism,
as seen in the response of lichen fungi to UV light (Durrell &
Shields, 1960; Zhdanova et al., 1978; Gauslaa & Solhaug,
2001). Many (25%) fungal species from the Nevada Test Site
contained melanin or other pigments (Durrell & Shields,
1960) and up to 40% of all fungi isolated from the
2008 Federation of European Microbiological Societies
Published by Blackwell Publishing Ltd. All rights reserved
c
6
J. Dighton et al.
I
A. ver 432
A
20
B
B
10
A. ver 57
25
0
Cont
Sn
Radionuclide
Cs
A. ver 43
II
15
Hyphal length (mm)
III
A
A
Hyphal length (mm)
Hyphal length (mm)
30
BC
AB
20
A
15
10
5
0
Cont
A
10
Sn
Radionuclide
5
0
Cont
Sn
Radionuclide
Cs
Chernobyl reactor room also contained melanin or other
pigments (Zhdanova et al., 2000). These noticeably exceeded
the ratio found in other, clean environments. The most
frequently occurring pigmented species were Cladosporium
sphaerospermum, C. herbarum, Hormoconis resinae, Alternaria alternate and Aureobasidium pullulans. The predominance of melanized fungi suggests that the possession of
pigmentation may lead to the evolution of radio-adaptation
(Tugay, 2006; Tugay et al., 2006b).
Genetic damage to fungi isolated from the fourth-reactor
rooms during 1997–1998 have been revealed in Alternaria
alternata and C. sphaerospermum, where their genetic composition is more monotonous than those of their natural
populations (Burlakova et al., 2001). This is taken to suggest
that in elevated radioactive conditions, surviving fungal
strains have either increased radio-stability or the community composition changes to a reduced species diversity to
that of solely resistant species, thus lowering genetic diversity. The search for specific genetic markers connected with
increased radio-resistance and, in particular, with genes of
resistance is underway (Mironenko et al., 2000).
When grown under the influence of ionizing radiation, of
the 13 fungal strains isolated from sites of contrasting levels
of radioactive pollution, nine strains (69%) showed an
increase in spore germination in the presence of ionizing
radiation from 137Cs and six strains (46%) exposed to 121Sn
(Tugay et al., 2006a). Of these, five strains (48%) showed
enhanced conidial germination as under exposure to mixed
g1b radiation, and five (48%) showed activation under the
influence of just one type of radiation. In contrast, fungi
2008 Federation of European Microbiological Societies
Published by Blackwell Publishing Ltd. All rights reserved
c
Cs
Fig. 2. Hyphal extension of three isolates of
Aspergillus versicolor isolated from contrasting
levels of radiation exposure, when grown in the
presence of g-ionizing radiation at 2 105 Bq
with 27 keV from 121Sn and 662 keV from 137Cs.
I is an isolate from a control area, II is an isolate
from an exposure of 55 mR h 1 and III from
500 mR h 1. Post hoc means separation tests
(Tukey’s test) are represented by letters where
bars indicated by different letters are statistically
significantly different. Data from Tugay et al.
(2006a).
isolated from radioactively clean locations did not show
radiostimulation of conidial germination.
When exposed to ionizing radiation, hyphal extension
rates are enhanced in fungi isolated from radioactively
contaminated areas (Tugay et al., 2006a; Fig. 2). The
mechanism of this action has been demonstrated in Cryptococcus neoformans to be related to the ability of melanized
forms to facilitate electron transfer to elicit coupled oxidation of NADPH and reduction of ferricyanide (Dadachova
et al., 2007).
Observations of fungi growing over and decomposing
radioactive ‘hot’ particles (Zhdanova, 1991), indicated the
presence of preferential growth of some fungal species
towards the particle (radiotropism) as a response to radiation alone (Zhdanova et al., 1994; Vember et al., 1999; Tugay
et al., 2003, 2004, 2005; Tugay, 2006). By exposing fungal
hyphae to collimated beams of ionizing radioactive emissions from 32P (b emissions) and 109Cd (g emissions) at
c. 2 108 Bq, the directional growth of hyphae emerging
from conidiospores was followed (Zhdanova et al., 2004). Of
the 27 fungal/radiation interactions, 18 (66.7%) showed
positive stimulation of growth towards the radiation source
(low mean return angle) and eight showed no response. Of
the fungal species isolated from radioactively contaminated
sites, 86% of the interactions showed positive directional
growth to the radiation beam, whereas few from less
contaminated areas showed a response. In this study,
directed growth occurred in the absence of any chemical
influence of the radioactive source, because the source was
physically separated from the fungal culture; fungi are
FEMS Microbiol Lett ]] (2008) 1–12
7
Fungi and ionizing radiation
P. lil 1941
A
75
B
B
50
25
0
B
50
B
25
0
Control
Cd
P
Chernobyl soil 3.2 × 10 Bq kg
Control
Cd
Cl. cl 4
Mean return angle (°)
75
A
A
A
50
P
Hot particle 1.5 × 10 Bq
P. hirz 1
25
0
A
100
B
B
50
0
Control
Cd
P
Control
Hot particle 6 × 10 Bq
influenced solely by clean b and g emissions. An example of
the data for Penicillium species is shown in Fig. 3. The
underlying mechanisms of this directed growth are, as yet,
not fully known. There are suggestions that that the fungal
hyphae are able to use the energy for metabolism (Dadachova
et al., 2007) although other physiological responses cannot
be discounted. A survey of directional growth attributes of
fungal isolates in relation to radiation levels at the source of
isolation shows a hormetic response (Calabrese & Baldwin,
2000; Pelevina et al., 2003; Petin et al., 2003) where directional growth is maximal at moderate irradiation levels and
is lowest at no or high levels at the site of isolation (Dighton
et al., 2008). Although hormetic responses to radiation have
been shown in a number of organisms (Calabrese &
Baldwin, 2000), its existence and importance is still subject
to debate. Melanin or other natural quinine pigments in the
fungal cell wall may act as the radiation receptor for this
response. Melanin has the capacity to change biochemical
pathways in fungal cells when exposed to UV light and
radiation (Durrell & Shields, 1960; Zhdanova et al., 1978;
Huselton & Hill, 1990; Gauslaa & Solhaug, 2001; Tugay
et al., 2006b; Dadachova et al., 2007). This may explain why
there is a greater proportion of melanized fungal species in
soils subjected to long-term low levels of ionizing radiation
(Zhdanova et al., 1995).
Mycoremediation
Remediation of contaminated areas is usually approached
by phytoremediation (Raskin & Ensley, 2000). Fungi have
FEMS Microbiol Lett ]] (2008) 1–12
A
75
100
Mean return angle (°)
Fig. 3. Mean return angle of hyphal extension
from spores of isolates of Penicillum spp.,
isolated from sites with a range of radioactive
pollution. A small mean return angle denotes
preferential hyphal growth towards the
collimated beam of radiation emitted from a
109
Cd (g-) or 32P (b-) source at c. 2 108 Bq at a
distance of 3 cm from the fungi. Post hoc means
separation tests (Tukey’s test) are represented by
letters where bars indicated by different letters
are statistically significantly different. Data from
Zhdanova et al. (2004).
P. hirz 3
100
Mean return angle (°)
Mean return angle (°)
100
Cd
P
Chernobyl soil 4 × 10 Bq kg
been shown to be useful adsorbers of heavy metal and
radionuclide contaminants of industrial effluents, where
dead mycelia have been used as filters (Tobin et al., 1984;
Singleton & Tobin, 1996). The propensity of fungal hyphae
to adsorb and absorb radionuclides may provide an alternative means to effect radionuclide cleanup. Air-lifted bioreactor systems containing live cultures of Rhizopus arrhizua
(R. oryzae) and Aspergillus niger removed about 90–95% of
radiothorium from solution (White & Gadd, 1990).
Fruitbodies of ectomycorrhizal basidiomycete fungal are
accumulators or hyper-accumulators of radionuclides and
could be harvested in order to remove radionuclide contaminants from a site (Gray, 1998). However, high accumulation in mushrooms poses an environmental problem in
that consumption by animals or humans results in radionuclide transfer up the food chain (Watling et al., 1993;
Barnett et al., 2001), especially in a boreal coniferous
ecosystem in Sweden, where they are a major component of
ecosystem biomass (Guillette et al., 1994).
Concluding remarks
Fungi appear to be very resistant to radionuclides in the
environment. Part of this resistance may be the smaller
amount of DNA per nucleus than mammalian cells, but
evidence from comparative studies between pigment and
nonpigmented fungi suggest there may be other factors that
confer radioresistance. Melanin pigment may provide some
protection against ionizing radiation and be integral to the
absorption and retention of radionuclides (Bohac et al.,
2008 Federation of European Microbiological Societies
Published by Blackwell Publishing Ltd. All rights reserved
c
8
1989; Rafferty et al., 1997; Mahmoud, 2004). Owing to the
long-lived and extensive hyphal network and biomass in
upper soil horizons of forest ecosystems [up to 2 ton ha 1 of
hyphae (Zvyagintsev, 1987, 1999)], fungi are very efficient in
absorbing radionuclides, and are an important component
of long term accumulation of radionuclides (Avery, 1996;
Avila & Moberg, 1999; Steinera et al., 2002). This may be
why radionuclide adsorption/desorption models do not
conform to observed patterns, as mycorrhizal fungi mediate
soil-to-plant transfer rates (Drissner et al., 1998). Internal
translocation of radionuclides to and hyper-accumulation
into harvestable fruit bodies of macro-fungi has potential
for environmental remediation but needs further evaluation
(Gray, 1998). Ectomycorrhizal association of fast growing
Ponderosa and Monterey pines accumulate 6.3–8.3% of the
137
Cs and 1.5–4.5% of the 90Sr from a rooting medium
(Entry et al., 1993), incorporating three to five times more
90
Sr than nonmycorrhizal seedlings (Entry et al., 1994).
Models of radionuclide accumulation into fungal fruitbodies predict an ecological half life of 3–8 years (Rühm
et al., 1998), but other models (Avila et al., 1999) suggest this
is a gross underestimation (Shaw et al., 2005). Thus, there
are theoretical grounds to consider plant/mycorrhizal symbioses for remediation, although field evaluation of their
potential has yet to occur.
Ionizing radiation causes genetic alteration in cells and
induces cell repair mechanisms. In mycelial fungi, melanin,
and possibly other pigments, may be important in providing
radioresistance. Melanin has also been implicated in the
growth response of radiologically adapted fungal isolates
(Tugay, 2006; Dadachova et al., 2007) and in the directional
growth stimulation that directs fungi to sources of radioactivity (Zhdanova et al., 2004). Dadachova et al. (2007)
speculate that fungi may be somewhat autotrophic, which
would allow them to be grown as a food source in space
stations, gaining energy from the high levels of ionizing
radiation. In these fungi are, we really looking at a new form
or autotrophism?
Thus, although we have accumulated a large body of
knowledge regarding the sequestration and distribution of
radionuclides in fungal components of the soil ecosystem,
more information and validation of existing models of
fungal retention are needed. Although the use of fungi in
phytoremediation is not usually considered (Raskin &
Ensley, 2000), the role of mycorrhizal fungi in soil-to-plant
transfer and accumulation for phyto- or mycoremediation
needs further attention (Gray, 1998; Rosén et al., 2005).
Acknowledgements
Part of the work reported here was conducted under receipt
of a grant from the National Science Foundation (IBN
0134795) awarded to the senior author.
2008 Federation of European Microbiological Societies
Published by Blackwell Publishing Ltd. All rights reserved
c
J. Dighton et al.
References
Afifi AE, Foaad MA & Fawzi EM (2003) Effect of gamma
irradiation on elimination of aflatoxins produced by apple
mycoflora in apple fruits. Acta Microbiol Polenica 52: 349–386.
Aiking H & Tempest DW (1977) Rubidium as a probe for
function and transport of potassium in the yeast Candida utilis
NCYC-321 grown in chemostat culture. Arch Microbiol 115:
215.
Attaby HSH, Mahmoud ML & Botros HW (2001) Studies on the
use of ionizing radiation in preservation and storage of African
sorghum grains I. Effect of gamma radiation on the fungi
associated with Sorghum bicolor grains. Egyptian J Microbiol
36: 255–273.
Avery SV (1996) Fate of caesium in the environment: distribution
between the abiotic and biotic components of aquatic and
terrestrial ecosystems. J Environ Radioactivity 30: 139–171.
Avila R & Moberg L (1999) A systematic approach to the
migration of 137Cs in forest ecosystems using interaction
matrices. J Environ Radioactivity 45: 217–282.
Avila R, Johanson KJ & Bergström R (1999) Model of the seasonal
variations of fungi ingestion and 137Cs activity concentrations
in roe deer. J Environ Radioactivity 46: 99–112.
Baeza A, Guillén FJ & Hernández S (2002) Transfer of 134Cs and
85
Sr to Pleurotus eryngii fruiting bodies under laboratory
conditions: a compartmental model approach. Bull Environ
Contam Toxicol 69: 817–828.
Bennett CB, Lewis LK, Karthikeyan G, Lobachev KS, Jin YH,
Sterling JF, Snipe JR & Resnick MA (2001) Genes required for
ionizing radiation resistance in yeast. Nat Genet 29: 426–434.
Barnett CL, Beresford NA, Frankland JC, Self PL, Howard BJ &
Marriott JVR (2001) Radiocaesium intake in Great Britain as a
consequence of the consumption of wild fungi. The Mycologist
15: 98–104.
Berreck M & Haselwandter K (2001) Effect of the arbuscular
mycorrhizal symbiosis upon uptake of cesium and other
cations by plants. Mycorrhiza 10: 275–280.
Bohac JD, Krivolutskii A & Antonova TB (1989) The role of
fungi in the biogenous migration of elements and in the
accumulation of radionuclides. Agric Ecosyst Environ 28:
31–34.
Burlakova EB, Michailov VF & Mazurik VK (2001) System of an
oxidation-reduction homeostasis at the instability genome
induced by radiation. Rad Biol Radioecol 41: 489–499.
Byrne AR (1988) Radioactivity in fungi in Slovenia, Yugoslavia,
following the Chernobyl accident. J Environ Radioactivity 6:
177–183.
Calabrese EJ & Baldwin LA (2000) Radiation hormesis: its
historical foundations as a biological hypothesis. Human Exper
Toxicol 19: 41–75.
Cawse PA (1983) The accumulation of caesium-137 and
plutonium-2391240 in soils of Great Britain, and transfer to
vegetation. Ecological Aspects of Radionuclide Release
(Coughtree PJ, Bell JNB & Roberts TM, eds), pp. 47–62.
Blackwell Scientific Publications, Oxford, UK.
FEMS Microbiol Lett ]] (2008) 1–12
9
Fungi and ionizing radiation
Clint GM & Dighton J (1992) Uptake and accumulation of
radiocaesium by mycorrhizal and non-mycorrhizal heather
plants. New Phytol 122: 555–561.
Clint GM, Dighton J & Rees S (1991) Influx of 137Cs into hyphae
of basidiomycete fungi. Mycolog Res 95: 1047–1051.
Connolly JH, Shortle WC & Jellison J (1998) Translocation and
incorporation of strontium carbonate derived strontium into
calcium oxalate crystals by the wood decay fungus Resinicium
bicolor. Can J Bot 77: 179–187.
Coughtree PJ (ed) (1983) Ecological Aspects of Radionuclide
Release, p. 279. Blackwell Scientific Publications, Oxford.
Dadachova E, Bryan R, Huang X, Moadel T, Schweitzer AD, Aisen
P, Nosanchuk JD & Casadevall A (2007) Ionizing radiation
changes the electronic properties of melanin and enhances the
growth of melanized fungi. PLoS ONE 2: e457. doi:10.1371/
journal.pone.0000457.
Das J (1991) Influence of potassium in the agar medium on the
growth pattern of the filamentous fungus Fusarium solani.
Appl Environ Microbiol 57: 3033.
de Boulois HD, Delvaux B & Declerck S (2005) Effects of
arbuscular mycorrhizal fungi on the root uptake and
translocation of radiocaesium. Environ Poll 134: 515–524.
Denny HJ & Wilkins DA (1987a) Zinc tolerance in Betula spp. I.
Effects of external concentration of zinc on growth and uptake.
New Phytol 106: 517–524.
Denny HJ & Wilkins DA (1987b) Zinc tolerance in Betula spp. IV.
The mechanism of ectomycorrhizal amelioration of zinc
toxicity. New Phytol 106: 545–553.
Dighton J (2003) Fungi in Ecosystem Processes, pp. 333–355.
Marcel Dekker, New York.
Dighton J & Horrill AD (1988) Radiocaesium accumulation in
the mycorrhizal fungi Lactarius rufus and Inocybe longicystis,
in upland Britain. Trans Br Mycol Soc 91: 335–337.
Dighton J, Clint GM & Poskitt JM (1991) Uptake and
accumulation of 137Cs by upland grassland soil fungi: a
potential pool of Cs immobilization. Mycol Res 95: 1052–1056.
Dighton J & Terry GM (1996) Uptake and immobilization of
caesium in UK grassland and forest soils by fungi following the
Chernobyl accident. Fungi and Environmental Change
(Frankland JC, Magan N & Gadd GM, eds), pp. 184–200.
Cambridge University Press, Cambridge.
Dighton J, Tugay T & Zhdanova NN (2008) Interactions of Fungi
and Radionuclides in Soil. Microbiology of Extreme Soils (Dion
P & Nautiyal CS, eds),) Springer, in press.
Drissner J, Bürmann W, Enslin F, Heider R, Klemt E, Miller R,
Schick G & Zibold G (1998) Availability of caesium
radionuclides to plants – classification of soils and role of
mycorrhiza. J Environ Radioactivity 41: 19–32.
Durrell LW & Shields LA (1960) Fungi isolated in culture from
soils of the Nevada test site. Mycologia 52: 636–641.
Eckl P, Hoffman W & Turk R (1986) Uptake of natural and manmade radionuclides by lichens and mushrooms. Radiation
Environ Biophys 25: 43–54.
Elstner EF, Fink R, Holl W, Lengfelder E & Ziegler H (1987)
Natural and Chernobyl-caused radioactivity in mushrooms,
FEMS Microbiol Lett ]] (2008) 1–12
mosses and soil-samples of defined biotops in SW Bavaria.
Oecologia 73: 553–558.
Entry JA, Rygiewicz PT & Emmingham WH (1993)
Accumulation of cesium-137 and strontium-90 in Ponderosa
pine and Monteray pine seedlings. J Environ Qual 22: 742–746.
Entry JA, Rygiewicz PT & Emmingham WH (1994) 90Sr uptake
by Pinus ponderosa and Pinus radiata seedlings inoculated with
ectomycorrhizal fungi. Environ Poll 86: 201–206.
Game JC, Williamson MS & Baccari C (2005) X-ray survival
characteristics and genetic analysis for nine Saccharomyces
deletion mutants that show altered radiation sensitivity.
Genetics 169: 51–63.
Gauslaa Y & Solhaug KA (2001) Fungal melanins as a sun screen
for symbiotic green algae in the lichen Lobaria pulmonaria.
Oecologia 126: 462–471.
Giovani C, Nimis PL, Land P & Padovani R (1990) Investigation
of the performance of macromycetes as bioindicators of
radioactive contamination. Transfer of Radionuclides in
Natural and Semi-Natural Environments (Desmet G,
Nassimbeni P & Belli M, eds), pp. 485–491. Elsevier Applied
Science, London.
Gray SN (1998) Fungi as potential bioremediation agents in soil
contaminated with heavy or radioactive metals. Biochem Soc
Trans 26: 666–670.
Gray SN, Dighton J, Olsson S & Jennings DH (1995) Real-time
measurement of uptake and translocation of 137Cs within
mycelium of Schizophyllum commune Fr. by autoradiography
followed by quantitative image analysis. New Phytol 129:
449–465.
Gray SN, Dighton J & Jennings DH (1996) The physiology of
basidiomycete linear organs III. Uptake and translocation of
radiocaesium within differentiated mycelia of Armillaria spp.
growing in microcosms and in the field. New Phytol 132:
471–482.
Grodzinskaya AA, Berreck M, Wasser SP & Haselwandter K
(1995) Radiocaesium in fungi: accumulation pattern in the
Kiev district of Ukraine including the Chernobyl zone.
Sydowia 10: 88–96.
Guillette O, Fraiture A & Lambinon J (1990) Soil-fungi
radiocaesium transfers in forest ecosystems. Transfer of
Radionuclides in Natural and Semi-Natural Environments
(Desmet G, Nassimbeni P & Belli M, eds), pp. 468–476.
Elsevier Applied Science, London.
Guillette O, Melin J & Wallberg L (1994) Biological pathways of
radionuclides originating from the Chernoyl fallout in a boreal
forest ecosystem. Sci Tot Environ 157: 207–215.
Guillette O, Gasia MC, Lambinon J, Fraiture A, Colard J &
Kirchmann R (1987) La radiocontamination des champignons
sauvages en Belgique et au Grand -Duche de Luxembourg
apres l’ accident nucleaire de tchernobyl. Mem Soc Roy Bot Belg
9: 79–93.
Haselwandter K (1978) Accumulation of the radioactive nuclide
137
Cs in fruitbodies of basidiomycetes. Health Phys 34:
713–715.
2008 Federation of European Microbiological Societies
Published by Blackwell Publishing Ltd. All rights reserved
c
10
Haselwandter K & Berreck M (1994) Accumulation of
radionuclides in fungi. Metal Ions in Fungi (Winkelmann G &
Winge DR, eds), pp. 259–277. Marcel Dekker, New York.
Haselwandter K, Bereck M & Brunner P (1988) Fungi as
bioindicators of radiocaesium contamination. Pre- and postChernobyl activities. Trans Br Mycol Soc 90: 171–176.
Heal OW & Horrill AD (1983) Terrestrial ecosystems: an
ecological context for radionuclide research. Ecological Aspects
of Radionuclide Release (Coughtree PJ, ed), pp. 31–46.
Blackwell Scientific Publications, Oxford.
Henn MR & Chapela IH (2001) Ecophysiology of 13C and 15N
isotopic fractionation in forest fungi and the roots of the
saprotrophic-mycorrhizal divide. Oecologia (Berlin) 128:
480–487.
Hobbie EA (2005) Using isotopic tracers to follow carbon and
nitrogen cycling of fungi. The Fungal Community: Its
Organization and Role in the Ecosystem, 3rd edn (Dighton J,
White JF & Oudemans P, eds), pp. 361–381. CRC Taylor &
Francis, Boca Raton.
Horyna J (1991) Wild mushrooms – the most significant source
of internal contamination. Isotopenpraxis 27: 23–24.
Horyna J & Randa Z (1988) Uptake of radiocesium and alkali
metals by mushrooms. J Radionuclide Chem 127: 107–120.
Huselton CA & Hill HZ (1990) Melanin photosensitizes
ultraviolet light (UVC) DNA damage in pigmented cells.
Environ Molec Mutagenesis 16: 37–43.
IJpelaar P (1980) Het Caesium-137 gehalte van verschillende
paddestoelsoorten. Coolia 23: 86–91.
Jackson NE, Miller RH & Franklin RE (1973) The influence of
vesicular-arbuscular mycorrhizae on uptake of 90Sr from soil
by soybeans. Soil Biol Biochem 5: 205–212.
Jennings DH (1990) The ability of basidiomycete mycelium to
move nutrients through the soil ecosystem. Nutrient Cycling in
Terrestrial Ecosystems: Field Methods, Applications and
Interpretation (Harrison AF, Ineson P & Heal OW, eds),
pp. 233–245. Elsevier, Amsterdam.
Joner EJ, Roos P, Jansa J, Frossard E, Leyval C & Jakobsen I (2004)
No significant contribution of arbuscular mycorrhizal fungi to
transfer of radiocesium from soil to plants. Appl Environ
Microbiol 70: 6512–6517.
Kimura S, Ishidou E, Kurita S, Suzuki Y, Shibato J, Rakwal R &
Iwahashi H (2006) DNA microarray analyses reveal a postirradiation differential time-dependent gene expression profile
in yeast cells exposed to X-rays and g-rays. Biochem Biophys
Res Comm 346: 51–60.
Kirchner G & Daillant O (1998) Accumulation of 210Pb, 226Ra
and radioactive cesium by fungi. Sci Total Environ 222: 63–70.
Mahmoud YA-G (2004) Uptake of radionuclides by some fungi.
Mycobiology 32: 110–114.
Malinowska E, Szefer P & Bojanowski R (2006) Radionuclide
content in Xercomus badius and other commercial mushrooms
from several regions in Poland. Food Chem 97: 19–24.
Mietelski JW, Jasinska M, Kubica B, Kozak K & Macharski P
(1994) Radioactive contamination of Polish mushrooms.
Sci Total Environ 157: 217–226.
2008 Federation of European Microbiological Societies
Published by Blackwell Publishing Ltd. All rights reserved
c
J. Dighton et al.
Mironenko NV, Alekhina IA, Zhdanova NN & Bulat SA (2000)
Intraspecific variation in gamma-radiation resistance and
genomic structure in the filamentous fungus Alternaria
alternata: a case study of strains inhabiting Chernobyl Reactor
No. 4. Ecotox Environ Safety 45: 177–187.
Muramatsu Y, Yoshida S & Sumia M (1991) Concentrations of
radiocesium and potassium in basidiomycetes collected in
Japan. Sci Tot Environ 105: 29–39.
Olsen RA, Joner E & Bakken LR (1990) Soil fungi and the fate of
radioceasium 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. Transfer
of Radionuclides in Natural and Semi-Natural Environments
(Desmet G, Nassimbeni P & Belli M, eds), pp. 657–663.
Elsevier Applied Science, London.
Olsson S (1995) Mycelial density profiles of fungi on
heterogenous media and their interpretation in terms of
nutrient reallocation patterns. Mycol Res 99: 143–153.
Olsson S & Jennings DH (1991) Evidence for diffusion being the
mechanism of translocation in the hyphae of three moulds.
Exp Mycol 15: 302–309.
Oolbekkink GT & Kuyper TW (1989) Radioactive caesium from
Chernobyl in fungi. The Mycologist 3: 3–6.
Osburn WS (1967) Ecological concentration of nuclear fallout in
a Colorado mountain watershed. Radiological Concentration
Process (Aberg B & Hungate FP, eds), pp. 675–709. Pergamon
Press, New York.
Oughton DH (1989) The Environmental Chemistry of
Radiocaesium and Other Nuclides. PhD thesis, University of
Manchester, UK.
Pelevina II, Aleschnko AV, Antoschina MM, Gotlib VJ,
Kudriashova OV, Semenova LP & Serebryanyi AM (2003) The
reaction of cell population to low level of irradiation. Rad Biol
Radioecol 43: 161–166.
Petin VG, Morozov II, Kabakova N & Gorshkova TA (2003) Some
effects of radiation hormesis for bacterial and yeast cells. Rad
Biol Radioecol 43: 176–178.
Rafferty B, Dawson D & Kliashtorn A (1997) Decomposition in
two pine forests: the mobilization of 137Cs and K from forest
litter. Soil Biol Biochem 29: 1673–1681.
Raskin I & Ensley BD (eds) (2000) Phytoremediation of Toxic
Metals: Using Plants to Clean up the Environment, p. 304. John
Wiley & Sons Inc., New York.
Rayner ADM (1991) The challenge of the individualistic
mycelium. Mycologia 83: 48–71.
Ritz K (1995) Growth responses of some fungi to spatially
heterogeneous nutrients. FEMS Microbiol Ecol 16: 269–280.
Rogers RD & Williams SE (1986) Vesicular-Arbuscular
mycorrhiza: influence on plant uptake of cesium and cobalt.
Soil Biol Biochem 18: 371–376.
Rommelt R, Hiersche L, Schaller G & Wirth E (1990) Influence of
soil fungi (Basidiomycetes) on the migration of Cs 1341137
and Sr 90 in coniferous forest soils. Transfer of Radionuclides in
Natural and Semi-Natural Environments (Desmet G,
FEMS Microbiol Lett ]] (2008) 1–12
11
Fungi and ionizing radiation
Nassimbeni P & Belli M, eds), pp. 152–160. Elsevier Applied
Science, London.
Rosén K, Zhong Weiliang Z & Mårtensson A (2005) Arbuscular
mycorrhizal fungi mediated uptake of 137Cs in leek and
ryegrass. Sci Tot Environ 338: 283–290.
Ruess L, Haggblom MM, Langel R & Scheu S (2004) Nitrogen
isotope ratios and fatty acid composition as indicators of
animal diets in belowground systems. Oecologia (Berlin) 139:
336–346.
Rühm W, Steiner M, Kammerer L, Hiersche L & Wirth E (1998)
Estimating future radiocaesium contamination of fungi on the
basis of behaviour patterns derived from past instances of
contamination. J Environ Radioactivity 39: 129–147.
Sanches AL, Parekh NR, Dodd BA & Ineson P (2000) Microbial
component of radiocaesium retention in highly organic soils.
Soil Biol Biochem 32: 2091–2094.
Shaw G, Venter A, Avila R et al. (2005) Radionuclide migration
in forest ecosystems – results of a model validation study.
J Environ Radioactivity 84: 285–296.
Singleton I & Tobin JM (1996) Fungal interactions with metals
and radionuclides for environmental bioremediation. Fungi
and Environmental Change (Frankland JC, Magan N & Gadd
GM, eds), pp 282–298. Cambridge University Press,
Cambridge.
Steinera M, Linkovb M & Yoshida S (2002) The role of fungi in
the transfer and cycling of radionuclides in forest ecosystems.
J Environ Radioactivity 58: 217–241.
Strandberg M & Johansson M (1998) 134Cs in heather seed plants
grown with and without mycorrhiza. J Environ Radioactivity
40: 175–184.
Tobin JM, Cooper DG & Neufeld RJ (1984) Uptake of metal ions
by Rhizopus arrhizus biomass. Appl Environ Microbiol 47:
821–824.
Trudell SA, Rygiewicz PT & Edmonds RL (2004) Patterns of
nitrogen and carbon stable isotope ratios in macrofungi,
plants and soils in two old-growth conifer forests. New Phytol
164: 317–335.
Tugay TI (2006) Features of evince of adaptable reactions at
micromycetes, isolated from radioactively polluted territories.
Abstract of XII meeting of Ukrainian Botany Society, 15–18 May,
Odessa, p 26.
Tugay TI, Zhdanova NN, Retchits TI, Zheltonozhsky VA &
Sadovnikov LV (2003) Influence of low level ionizing
irradiation on spread of radiotropism among fungi. Sci Pap
Inst Nuc Res 2: 72–79.
Tugay TI, Zheltonozhsky VA & Sadovnikov LV (2004) Response
reactions of fungi under exposure of ionizing irradiation. Sci
Pap Inst Nuc Res 2: 132–138.
Tugay TI, Zhdanova NN, Zheltonozhsky VA, Sadovnikov LV &
Telichko MV (2005) Response reactions of the fungi, isolated
from inner locations of ‘‘Ukryttya’’, which have different levels
of radioactivity. Sci Pap Inst Nuc Res 1: 128–136.
Tugay TI, Zhdanova NN, Zheltonozhsky VA, Sadovnikov LV &
Dighton J (2006a) The influence of ionizing radiation on spore
FEMS Microbiol Lett ]] (2008) 1–12
germination and emergent hyphal growth response reactions
of microfungi. Mycologia 98: 521–527.
Tugay T, Zhdanova N, Zheltonozhsky V & Sadovnikov L (2006b)
Influence of small dozes radiation on antioxidant activity
of anamorphic fungal species Aspergillus versicolor and
Paecilomyces lilacinus, having radio adaptive properties.
Abstract of the 35th Annual Meeting of the European Radiation
Research Society 22–25 August, Kiev 2006, p 84.
Vember VV, Zhdanova NN & Tugay TI (1999) Irradiation
influence on the physiologo-biochemical properties of
Cladosporium cladosporioides (Fres.) de Vries strains which
differ in radiotropism sign. Microbiologichny Zhurnal 61:
25–32.
Watling R, Laessoe T, Whalley AJS & Lepp NW (1993)
Radioactive caesium in British mushrooms. Bot J Scotl 46:
487–497.
White C & Gadd GM (1990) Biosorption of radionuclides by
fungal biomass. J Chem Tech Biotech 49: 331–343.
Witkamp M (1968) Accumulation of 137Cs by Trichoderma viride
relative to 137Cs in soil organic matter and soil solution. Soil
Sci 106: 309–311.
Witkamp M & Barzansky B (1968) Microbial immobilization of
137
Cs in forest litter. Oikos 19: 392–395.
Yoshida S & Muramatsu Y (1994) Accumulation of radiocesium
in basidiomycetes collected from Japanese forests. Sci Tot
Environ 157: 197–205.
Zhdanova NN, Melezhik AV, Vasilevskaya AI & Pokhodenko VD
(1978) Formation and disappearance of photo induced
paramagnetic centers in melanin-containing fungi. News Acad
Sci USSA 4: 576–581.
Zhdanova NN, Vasilevskaya AA, Sadnovikov YuS & Artyshkova
LA (1990) The dynamics of micromycete complexes
contaminated with soil radionuclides. Mikologia i
Fitopatologiya 24: 504–512.
Zhdanova NN, Lashko TN, Redchitz TI, Vasiliveskaya AI,
Bosisyuk LG, Sinyavskaya OI, Gavrilyuk VI & Muzalev PN
(1991) Interaction of soil micromycetes with ‘hot’ particles
in the model system. Microbiologichny Zhurnal 53: 9–17.
Zhdanova NN, Redchitz TI, Krendayaskova VG, Lacshko TN,
Gavriluk VI, Muzalev PI & Sherbachenko AM (1994) Tropism
under the influence of ionizing radiation. Mikologia i
Fitopatologiya 28: 8–13.
Zhdanova NN, Vasilevskaya AI, Artyshkova LV, Sadovnikov YuS,
Gavrilyuk VI & Dighton J (1995) Changes in the micromycete
communities in soil in response to pollution by long-lived
radionuclides emitted by in the Chernobyl accident. Mycol Res
98: 789–795.
Zhdanova NN, Zakharchenko VA, Vember VV & Nakonechnaya
LT (2000) Fungi from Chernobyl: mycobiota of the inner
regions of the containment structures of the damaged nuclear
reactor. Mycol Res 104: 1421–1426.
Zhdanova NN, Fomina M, Redchitz T & Olsson S (2001)
Chernobyl effect: growth characteristics of soil fungi
Cladosporium cladosporioides (Fresen) de Vries with and
without positive radiotropism. Polish J Ecol 49: 309–318.
2008 Federation of European Microbiological Societies
Published by Blackwell Publishing Ltd. All rights reserved
c
12
Zhdanova NN, Tugay T, Dighton J, Zheltonozhsky V &
McDermott P (2004) Ionizing radiation attracts fungi. Mycol
Res 108: 1089–1096.
Zhdanova NN, Zaharchenko VA, Tugay NI & Karpenko YV
(2005a) Fungi lesion of inner locations object Shelter. Problems
Nuclear Power Plants’ Safety Chornobyl 3: 78–86.
Zhdanova NN, Zakharchenko VA & Haselwandter K (2005b)
Radionuclides and fungal communities. The Fungal
2008 Federation of European Microbiological Societies
Published by Blackwell Publishing Ltd. All rights reserved
c
J. Dighton et al.
Community: Its Organization and Role in the Ecosystem
(Dighton J, White JF & Oudemans P, eds), pp. 759–768. CRC
Press, Baton Rouge.
Zvyagintsev DG (1987) Soil and Microorganisms. MGU, Moscow,
256pp.
Zvyagintsev DG (1999) Structure and functioning of a complex
soil microorganisms: Structurally functional role of soil in
biosphere. M.:GEOC 101–112.
FEMS Microbiol Lett ]] (2008) 1–12