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SHORT COMMUNICATIONS
Zinc Accumulation by the Slime Mold Fuligo septica (L.) Wiggers
in the Former Soviet Union and North Korea
Daniel A. Zhulidov, Richard D. Robarts,* Alexander V. Zhulidov, Olga V. Zhulidova,
Danila A. Markelov, Viktor A. Rusanov, and John V. Headley
Abstract
tributed Myxomycetes is Fuligo septica (L.) Wiggers,
which has been found almost everywhere (Stephenson
Samples of the slime mold Fuligo septica (L.) Wiggers were col-
and Stempen, 1994), even in deserts (Blackwell and
lected from an ecologically diverse selection of sites across the former
Gilbertson, 1984). They prevail in damp forests and in
USSR and in North Korea to determine their Zn concentrations.
Plasmodia were collected from trees, rocks, soils, the walls of buildings
old tree stumps, under fallen leaves and twigs, in wooden
and a variety of other materials and structures from 1990 to 1996.
wells, and cracks in damp wooden walls. They also peri-
The biomass collected ranged from 305 to 968 mg, whereas Zn concen-
odically occur on the soil surface on forest paths and
trations in plasmodia of F. septica ranged from 8400 to 23 000 mg
on trees and rocks. Despite their widespread abundance,
kg
⫺
1
dry wt. (mean and standard error ⫽ 14 200 ⫾ 860 mg kg
⫺
1
dry
predominantly ecological studies of these organisms are
wt.). No clear trend as to which areas produced F. septica with the
uncommon (Stephenson, 1988) and have usually been
highest Zn concentrations was discernable. Nor was it possible to
neglected in forest ecology studies (Seta
¨
la
¨
and Nuor-
identify any particular substrate on which F. septica grew that pro-
teva, 1989).
duced noticeably high Zn concentrations. For example, forest litter
Laboratory experiments have shown that high heavy
on which F. septica was found had Zn concentrations of only 25 to
metal concentrations in the slime mold, Physaruni poly-
130 mg kg
⫺
1
dry wt. Our data confirm the only other study showing
hyperaccumulation of Zn in F. septica, which was carried out in
cephaium, affect membrane potential, nuclear biochem-
Finland. This ability seems to be unique to this species, but how or
istry, and survival time (see references in Seta
¨
la
¨
and
why it does this, or why such high Zn concentrations are not toxic to
Nuorteva, 1989). However, Seta
¨
la
¨
and Nuorteva ana-
F. septica, are questions requiring future research.
lyzed dried museum specimens of Fuligo septica and
Lycogala epidendrum from Finland that had been col-
lected between 1860 and 1964 and found that F. septica
S
lime molds, or Myxomycetes, are fungus-like eu-
contained up to 11 000 mg Zn kg
⫺
1
dry wt., whereas L.
karyotes that are little studied. The plasmodia of
epidendrum contained a maximum Zn concentration of
Myxomycetes mainly obtain nutrients by ingesting food
only 82 mg kg
⫺
1
dry wt. In a follow-up study they mea-
particles such as bacteria, yeast cells, amoebae, flagel-
sured the metal concentrations of F. septica, seven other
lates, fungal mycelia, as well as algae and detritus (Gray
slime molds, and two unidentified slime mold plasmodia
and Alexopoulos, 1968). They may also feed in nature
collected from several Finnish sites. Fuligo septica con-
by absorbing dissolved substances, since they can be
tained between 4000 and 20 000 mg Zn kg
⫺
1
dry wt.,
grown on nutrient media, although this is still question-
causing the authors to comment that it was difficult to
able (Gray and Alexopoulos, 1968). Depending on the
understand how a living organism could tolerate such
species, the size of the plasmodia can vary from micro-
high metal concentrations.
scopic to several dozen centimetres in diameter (e.g.,
To our knowledge, Seta
¨
la
¨
and Nuorteva’s (1989) in-
Fuligo septica) and up to several square meters. The
vestigation has not been repeated in other parts of the
mass of some Myxomycetes can reach 30 g (Raven et
world, so it is not known whether their results were only
al., 1986).
typical for Finland or whether the ability of F. septica
One of the most consistently abundant and widely dis-
to accumulate very high Zn concentrations is a more
general phenomena that requires further study. We col-
lected samples of F. septica from a number of sites across
D.A. Zhulidov and V.A. Rusanov, Rostov Univ., Rostov-on-Don,
the former USSR and into North Korea and analyzed
Russia; R.D. Robarts, UNEP GEMS/Water Collaborating Centre,
Environment Canada, 11 Innovation Blvd., Saskatoon, SK, Canada
them for stored Zn concentrations.
S7N 3H5; A.V. Zhulidov, Centre for Preparation and Implementation
of International Projects on Technical Assistance (CPPI), North Cau-
Materials and Methods
casus Branch, 200/1 Stachki Ave., Office 301, Rostov-on-Don, 344104,
Russia; O.V. Zhulidova, Aquatest Ltd., Zhuravleva str., 44, Rostov-
Plasmodia of F. septica were collected in different regions
on-Don, 344022, Russia; D.A. Markelov, Moscow State Univ., Voro-
of the former USSR and from one area in North Korea be-
bevy Gory, Moscow, 119899, Russia; and J.V. Headley, National
tween 1990 and 1996 (Table 1, Fig. 1). Dr. T.P. Sizova of
Water Research Inst., Environment Canada, 11 Innovation Blvd.,
Saskatoon, SK, Canada S7N 3H5. Received 3 Jan. 2001. *Correspond-
ing author (richard.robarts@ec.gc.ca).
Abbreviations: GFAAS, graphite-furnace atomic-absorption spectro-
photometry.Published in J. Environ. Qual. 31:1038–1042 (2002).
1038
ZHULIDOV ET AL.: ZINC ACCUMULATION BY SLIME MOLD 1039
Table 1. Geographical location of sampling sites for Fuligo septica and zinc concentration in plasmodia. Numbers are collection site
locations shown in Fig. 1.
Weight of
Location and collection site no. Date F. septica Substrate Zn conc.
mg mg kg
⫺
1
dry wt.
Russia
European Russia
1. Murmansk oblast‡ 9 July 1992 567 Damp rock. 21 000
15 Aug. 1994† 385 Barn wall. 18 000
2. Karelia Republic 25 July 1990 743 Forest litter 12 500
10 Aug. 1992 648 Dry fallen tree 11 300
3. Arkhangelsk oblast‡ 14 Aug. 1990 638 Wall of a well 8 400
18 June 1991 585 Forest litter 10 200
5 Aug. 1995† 510 Dry fallen tree 9 600
4. Komi Republic 18 July 1995† 478 Forest path 15 300
5. Pskov oblast‡ 25 July 1995† 502 Forest path 10 100
6. Voronezh biosphere reserve 18 Aug. 1990 482 Old hay 8 800
23 Aug. 1990 509 Dry fallen aspen 10 400
2 Sept. 1990 836 Wall of a well 16 500
28 June 1991 627 Forest path 15 600
11 Oct. 1991 508 Forest litter 20 200
12 Aug. 1992 487 Dry aspen stump 16 000
14 July 1993 406 Wooden fence 18 700
18 Sept. 1994† 681 A path 9 300
20 Aug. 1995† 968 Wooden platform, Usman River 11 400
27 July 1996† 744 Side of an old boat, Usman River flood plain 19 700
7. Kursk biosphere reserve 12 Sept. 1990 589 Wall of a wooden house 10 400
8. Kursk oblast‡ 30 June 1991 466 Seim River flood plain, a path 11 300
9. Astrakhan biosphere reserve 28 Sept. 1992 673 Dead tree in flooded area 18 300
North Caucasus
10. Caucasus biosphere reserve 23 May 1993 835 Forest path 21 200
11. North Osetiya reserve 15 Sept. 1991 484 Fallen tree 23 000
Siberia
12. Western Siberia, Tobol River 12 Aug. 1992 571 Old tree, a swamp 10 000
13. Yakutiya Republic, town of Aldan 28 July 1993 456 Dead tree, a swamp 9 500
Lithuania
14. Village Ignalina 1 Aug. 1990 389 Old stump 10 200
Uzbekistan
15. Tashkent 14 May 1990 493 Wall of airport building 11 700
16. Zaamin reserve 10 June 1990 505 Wet rock 12 100
Kirgiziya
17. Village Khandarken 23 Aug. 1990 397 Wet rock 23 000
Tadzhikistan
18. Village Gissar 19 Sept. 1990 305 Road 22 200
Northern Korea
19. Mt. Mekhyan, near the “Exhibition
of International Friendship” Sept. 1990 317 A tree 9 600
† Sample was not given to T.P. Sizova for taxonomic identification.
‡ Oblast—usually translated as region, occasionally as province. Oblast is retained here to avoid confusion with generic usage of the word region. There
are 49 Oblasts in the Russian Federation.
Moscow University performed taxonomic identifications of F. (Zhulidov et al., 1997). The accuracy and precision of the
measurements were assessed using reference standards pre-septica using spores according to Sizova (1986).
Fuligo septica, and forest litter samples, were collected man- pared by the Hydrochemical Institute, Rostov-on-Don, Russia.
ually with utmost care using plastic instruments and placed in
acid-cleaned Teflon-coated glass or polypropylene containers.
Results and Discussion
The plasmodia selected for analysis were those that were the
largest and easiest to separate from substrates. As the F. sep-
Fuligo septica was found and collected from rocks,
tica samples collected were in the soporiferous phase, they
trees, building walls, forest litter, and other material,
were usually easily detached from their substrate without
including the side of an old boat in the Usman River
scraping or cutting. Plasmodia that could not be detached
flood plain (Table 1). The biomass collected ranged
without force were not collected to ensure that samples were
from 305 mg in Tadzhikistan to 968 mg near the Usman
not contaminated by attached substrate particles. Samples
River. Zinc concentrations in plasmodia of F. septica
were dried at 40⬚C to a constant weight. Zinc concentration
ranged from 8400 to 23 000 mg kg
⫺
1
dry wt. (mean and
was determined using graphite-furnace atomic-absorption spec-
standard error ⫽ 14 200 ⫾ 860 mg kg
⫺
1
dry wt.) (Table
trophotometry (GFAAS; Perkin Elmer 3030, HGA-500) after
samples were digested with a mixture of HNO
3
–HF–HClO
4
1). No clear trend as to which areas produced F. septica
1040 J. ENVIRON. QUAL., VOL. 31, MAY–JUNE 2002
Fig. 1. Map of the former USSR and North Korea showing the sites were Fuligo septica was collected. Sampling sites are indicated by numbers
in circles and the legend is given in Table 1.
ZHULIDOV ET AL.: ZINC ACCUMULATION BY SLIME MOLD 1041
with the highest Zn concentrations was discernable, be-
Alpine pennygrass, Thlaspi caerulescens (J. Presl & C.
cause the concentrations were highly variable for a given
Presl), which can accumulate up to 25 000 mg Zn kg
⫺
1
area [e.g., concentrations from the Voronezh Biosphere
dry wt. of shoots (Watanabe, 1997). Seta
¨
la
¨
and Nuorteva
Reserve ranged between 8800 and 20 200 mg kg
⫺
1
dry
(1989) hypothesized that Zn possibly affords F. septica
wt. (Table 1)]. It was also not possible to identify any
protection from some more dangerous factors by acting
particular substrate on which F. septica was found that
as a coenzyme or enzyme activator in a detoxification
produced noticeably higher Zn concentrations. In the
system. Another possibility is that high Zn contents may
case of forest litter, for example, F. septica was found
protect F. septica from predators or phages. Inorganic
to have concentrations ranging from 10 200 to 20 200
tin, for example, has been shown to be effective in inacti-
mg kg
⫺
1
dry wt. (Table 1).
vating bacteriophage T4 (Doolittle and Cooney, 1992).
Zinc concentrations in plasmodia of F. septica col-
Whether F. septica actively hyperaccumulates Zn, or
lected in Finland from 1860 to 1988 ranged from 2200
simply binds it to the cell membrane, awaits experimen-
to 20 000 mg kg
⫺
1
dry wt. (mean and standard error ⫽
tal verification in laboratory cultures. Its ability to toler-
10 800 ⫾ 1250 mg kg
⫺
1
dry wt.) (Seta
¨
la
¨
and Nuorteva,
ate such high metal concentrations, what the upper con-
1989). Although the range of substrates from which
centration limit is, and why it hyperaccumulates Zn are
Seta
¨
la
¨
and Nuorteva (1989) collected F. septica was
also issues needing to be addressed in such experiments.
more limited than ours, they similarly were unable to
The identification of an active Zn sequestration mecha-
clearly identify one substrate that was responsible for
nism could lead to the cloning of the corresponding
very high Zn concentrations. For example, Zn concen-
genes and their use in bioremediation following implan-
trations in F. septica growing in moss carpets ranged
tation into plants with a larger biomass (cf. Watanabe,
from 4000 to 15 000 mg kg
⫺
1
dry wt. On four occasions
1997). Fuligo septica’s ability to hyperaccumulate Zn
they also measured the Zn content of the hypothallus
may also be significant in studies of toxic metal impacts
and sporophore of F. septica and found concentrations
in forest systems, such as in Europe (Seta
¨
la
¨
and Nuor-
of 18 000 to 31 000 and 9700 to 14 000 mg kg
⫺
1
dry
teva, 1989).
wt., respectively. Seta
¨
la
¨
and Nuorteva (1989) speculated
about whether Zn is necessary for the formation of
Acknowledgments
the hypothallus or if it is secreted as a waste to the
Part of this work was done as part of the Environmental
hypothallus to protect the sporophore and spores from
Project between the former USSR State Committee of Hydro-
metal toxicity, but were unable to reach a conclusion.
meteorology and the Hydrometeorological Service of North
Are the high Zn concentrations in F. septica the result
Korea. The Hydrochemical Institute, Federal Russian Service
of environmental contamination in the former USSR,
for Hydrometeorology and Environmental Monitoring; the
or does this slime mold have a unique characteristic?
Kajima Foundation, Japan and the Association of Canadian
Seta
¨
la
¨
and Nuorteva (1989) measured the Zn concentra-
Community Colleges, Partnerships for Tomorrow Programme
provided funding. The authors are grateful to Dr. T.P. Sizova,
tions in plasmodia of slime mold species other than F.
Moscow University; Prof. P. Nuorteva, University of Helsinki,
septica [Lycogala epidenrum L. (Trien), Symphytocar-
Finland; Prof. M.A. Rish and Dr. S. Urmanov, Fergana, State
pus flaccidus (Morgan), Tubifera ferruginosa (Batsch),
University, Uzbekistan; Prof. A.A. Kist, Prof. R.A. Kulmatov,
Amaurochaete atra (Albert. & Schweinitz), Ceratiomyxa
and Dr. U. Rakhmatov, Institute of Nuclear Physics, Academy
fruticulosa (O.F. Muller), and Stemonitis sp.] in Finland
of Science of Uzbekistan; Dr. N. Katargin, Vernadsky Institute
and found it ranged from 23 to 570 mg kg
⫺
1
dry wt.
of Geochemistry and Analytical Chemistry, Moscow, Russia;
Therefore, the high Zn concentrations of F. septica
Dr. A.A. Gusev, Administration of Kursk Region, Russia; as
found by Seta
¨
la
¨
and Nuorteva (1989) and ourselves
well as to the authorities and staff of the Voronezh Biosphere
seem to be due to a unique ability of F. septica. Zinc
Reserve (Dr. V.A. Semyonov, Dr. V. Kazmin, and Dr. V.
concentrations in the forest litter from sites where we
Emetz), Olekminsk Reserve (Dr. Yu. Rozhkov), North Ose-
tiya Reserve (Dr. A. Lipkovich), Russia; and Zaamin Reserve,
collected plasmodia ranged from 25 to 130 mg kg
⫺
1
Uzbekistan for their assistance in our work. We also thank Dr.
dry wt., whereas the plasmodia collected at these sites
Yu. Novozhilov, Komarov Botanical Institute, St. Petersberg,
contained 10 200 to 20 000 mg kg
⫺
1
dry wt. (Table 1).
Russia, for discussions about slime molds and Dr. J.R. Law-
Unfortunately, we do not have Zn concentration data
rence, National Water Research Institute, Environment Can-
for the other substrates where we collected plasmodia.
ada, and three anonymous reviewers for comments on an
The high Zn concentrations found by Seta
¨
la
¨
and Nuor-
earlier draft of the manuscript.
teva (1989) in museum samples of F. septica showed
that high Zn concentrations in F. septica were occurring
References
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Blackwell, M., and R.L. Gilbertson. 1984. Distribution and sporulation
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a plausible explanation for the very high Zn concentra-
Microbiol. Ecol. 10:369–377.
tions in F. septica.
Doolittle, M.M., and J.J. Cooney. 1992. Inactivation of bacteriophage
T4 by organic and inorganic tin compounds. J. Ind. Microbiol.
This conclusion raises a second question: Why does
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Gray, W.D., and C.J. Alexopoulos. 1968. Biology of the myxomycetes.
these not toxic to the organism? While we were not
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accumulated high metal concentrations, similar levels
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Seta
¨
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of Zn hyperaccumulation have been reported in the
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septica (L.) Wiggers and some other slime molds (Myxomycetes ).
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Zhulidov, A.V., J.V. Headley, R.D. Robarts, A.M. Nikanorov, A.A.
Stephenson, S.L. 1988. Distribution and ecology of Myxomycetes in
Ischenko, and M.A. Champ. 1997. Concentrations of Cd, Pb, Zn
temperate forests: I. Patterns of occurrence in the upland forests
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Bull. 35:242–251.
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of slime molds. Timber Press, Portland, OR.
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