Journal of Environmental Quality 31:1038-1042 (2002)
© 2002 American Society of Agronomy, Crop Science Society of America, and Soil Science Society of America
SHORT COMMUNICATION
Zinc Accumulation by the Slime Mold Fuligo septica (L.) Wiggers in the Former Soviet Union and North Korea
Daniel A. Zhulidova,c,
Richard D. Robarts*,b,
Alexander V. Zhulidova,c,
Olga V. Zhulidovad,
Danila A. Markelove,
Viktor A. Rusanova and
John V. Headleyf
a Rostov Univ., Rostov-on-Don, Russia
b UNEP GEMS/Water Collaborating Centre, Environment Canada, 11 Innovation Blvd., Saskatoon, SK, Canada S7N 3H5
c Centre for Preparation and Implementation of International Projects on Technical Assistance (CPPI), North Caucasus Branch, 200/1 Stachki Ave., Office 301, Rostov-on-Don, 344104, Russia
d Aquatest Ltd., Zhuravleva str., 44, Rostov-on-Don, 344022, Russia
e Moscow State Univ., Vorobevy Gory, Moscow, 119899, Russia
f National Water Research Inst., Environment Canada, 11 Innovation Blvd., Saskatoon, SK, Canada S7N 3H5
* Corresponding author (richard.robarts{at}ec.gc.ca)
Received for publication January 3, 2001.
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ABSTRACT
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Samples of the slime mold Fuligo septica (L.) Wiggers were collected from an ecologically diverse selection of sites across the former USSR and in North Korea to determine their Zn concentrations. Plasmodia were collected from trees, rocks, soils, the walls of buildings and a variety of other materials and structures from 1990 to 1996. The biomass collected ranged from 305 to 968 mg, whereas Zn concentrations in plasmodia of F. septica ranged from 8400 to 23000 mg kg-1 dry wt. (mean and standard error = 14200 ± 860 mg kg-1 dry wt.). No clear trend as to which areas produced F. septica with the highest Zn concentrations was discernable. Nor was it possible to identify any particular substrate on which F. septica grew that produced noticeably high Zn concentrations. For example, forest litter on which F. septica was found had Zn concentrations of only 25 to 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 Finland. This ability seems to be unique to this species, but how or why it does this, or why such high Zn concentrations are not toxic to F. septica, are questions requiring future research.
Abbreviations: GFAAS, graphite-furnace atomic-absorption spectrophotometry
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INTRODUCTION
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SLIME MOLDS, OR Myxomycetes, are fungus-like eukaryotes that are little studied. The plasmodia of Myxomycetes mainly obtain nutrients by ingesting food particles such as bacteria, yeast cells, amoebae, flagellates, fungal mycelia, as well as algae and detritus (Gray and Alexopoulos, 1968). They may also feed in nature by absorbing dissolved substances, since they can be grown on nutrient media, although this is still questionable (Gray and Alexopoulos, 1968). Depending on the species, the size of the plasmodia can vary from microscopic to several dozen centimetres in diameter (e.g., Fuligo septica) and up to several square meters. The mass of some Myxomycetes can reach 30 g (Raven et al., 1986).
One of the most consistently abundant and widely distributed Myxomycetes is Fuligo septica (L.) Wiggers, which has been found almost everywhere (Stephenson and Stempen, 1994), even in deserts (Blackwell and Gilbertson, 1984). They prevail in damp forests and in old tree stumps, under fallen leaves and twigs, in wooden wells, and cracks in damp wooden walls. They also periodically occur on the soil surface on forest paths and on trees and rocks. Despite their widespread abundance, predominantly ecological studies of these organisms are uncommon (Stephenson, 1988) and have usually been neglected in forest ecology studies (Setälä and Nuorteva, 1989).
Laboratory experiments have shown that high heavy metal concentrations in the slime mold, Physaruni polycephaium, affect membrane potential, nuclear biochemistry, and survival time (see references in Setälä and Nuorteva, 1989). However, Setälä and Nuorteva analyzed dried museum specimens of Fuligo septica and Lycogala epidendrum from Finland that had been collected between 1860 and 1964 and found that F. septica contained up to 11000 mg Zn kg-1 dry wt., whereas L. epidendrum contained a maximum Zn concentration of only 82 mg kg-1 dry wt. In a follow-up study they measured the metal concentrations of F. septica, seven other slime molds, and two unidentified slime mold plasmodia collected from several Finnish sites. Fuligo septica contained between 4000 and 20000 mg Zn kg-1 dry wt., causing the authors to comment that it was difficult to understand how a living organism could tolerate such high metal concentrations.
To our knowledge, Setälä and Nuorteva's (1989) investigation has not been repeated in other parts of the world, so it is not known whether their results were only typical for Finland or whether the ability of F. septica to accumulate very high Zn concentrations is a more general phenomena that requires further study. We collected samples of F. septica from a number of sites across the former USSR and into North Korea and analyzed them for stored Zn concentrations.
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Materials and Methods
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Plasmodia of F. septica were collected in different regions of the former USSR and from one area in North Korea between 1990 and 1996 (Table 1, Fig. 1)
. Dr. T.P. Sizova of Moscow University performed taxonomic identifications of F. septica using spores according to Sizova (1986).
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Table 1. Geographical location of sampling sites for Fuligo septica and zinc concentration in plasmodia. Numbers are collection site locations shown in Fig. 1.
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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.
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Fuligo septica, and forest litter samples, were collected manually with utmost care using plastic instruments and placed in acid-cleaned Teflon-coated glass or polypropylene containers. The plasmodia selected for analysis were those that were the largest and easiest to separate from substrates. As the F. septica samples collected were in the soporiferous phase, they were usually easily detached from their substrate without scraping or cutting. Plasmodia that could not be detached without force were not collected to ensure that samples were not contaminated by attached substrate particles. Samples were dried at 40°C to a constant weight. Zinc concentration was determined using graphite-furnace atomic-absorption spectrophotometry (GFAAS; Perkin Elmer 3030, HGA-500) after samples were digested with a mixture of HNO3–HF–HClO4 (Zhulidov et al., 1997). The accuracy and precision of the measurements were assessed using reference standards prepared by the Hydrochemical Institute, Rostov-on-Don, Russia.
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Results and Discussion
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Fuligo septica was found and collected from rocks, trees, building walls, forest litter, and other material, including the side of an old boat in the Usman River flood plain (Table 1). The biomass collected ranged from 305 mg in Tadzhikistan to 968 mg near the Usman River. Zinc concentrations in plasmodia of F. septica ranged from 8400 to 23000 mg kg-1 dry wt. (mean and standard error = 14200 ± 860 mg kg-1 dry wt.) (Table 1). No clear trend as to which areas produced F. septica with the highest Zn concentrations was discernable, because the concentrations were highly variable for a given area [e.g., concentrations from the Voronezh Biosphere Reserve ranged between 8800 and 20200 mg kg-1 dry wt. (Table 1)]. It was also not possible to identify any particular substrate on which F. septica was found that produced noticeably higher Zn concentrations. In the case of forest litter, for example, F. septica was found to have concentrations ranging from 10200 to 20200 mg kg-1 dry wt. (Table 1).
Zinc concentrations in plasmodia of F. septica collected in Finland from 1860 to 1988 ranged from 2200 to 20000 mg kg-1 dry wt. (mean and standard error = 10800 ± 1250 mg kg-1 dry wt.) (Setälä and Nuorteva, 1989). Although the range of substrates from which Setälä and Nuorteva (1989) collected F. septica was more limited than ours, they similarly were unable to clearly identify one substrate that was responsible for very high Zn concentrations. For example, Zn concentrations in F. septica growing in moss carpets ranged from 4000 to 15000 mg kg-1 dry wt. On four occasions they also measured the Zn content of the hypothallus and sporophore of F. septica and found concentrations of 18000 to 31000 and 9700 to 14000 mg kg-1 dry wt., respectively. Setälä and Nuorteva (1989) speculated about whether Zn is necessary for the formation of the hypothallus or if it is secreted as a waste to the hypothallus to protect the sporophore and spores from metal toxicity, but were unable to reach a conclusion.
Are the high Zn concentrations in F. septica the result of environmental contamination in the former USSR, or does this slime mold have a unique characteristic? Setälä and Nuorteva (1989) measured the Zn concentrations in plasmodia of slime mold species other than F. septica [Lycogala epidenrum L. (Trien), Symphytocarpus flaccidus (Morgan), Tubifera ferruginosa (Batsch), Amaurochaete atra (Albert. & Schweinitz), Ceratiomyxa fruticulosa (O.F. Muller), and Stemonitis sp.] in Finland and found it ranged from 23 to 570 mg kg-1 dry wt. Therefore, the high Zn concentrations of F. septica found by Setälä and Nuorteva (1989) and ourselves seem to be due to a unique ability of F. septica. Zinc concentrations in the forest litter from sites where we collected plasmodia ranged from 25 to 130 mg kg-1 dry wt., whereas the plasmodia collected at these sites contained 10200 to 20000 mg kg-1 dry wt. (Table 1). Unfortunately, we do not have Zn concentration data for the other substrates where we collected plasmodia. The high Zn concentrations found by Setälä and Nuorteva (1989) in museum samples of F. septica showed that high Zn concentrations in F. septica were occurring before the environment was subjected to modern pollution. Environmental contamination does not seem to be a plausible explanation for the very high Zn concentrations in F. septica.
This conclusion raises a second question: Why does F. septica accumulate such high Zn levels and why are these not toxic to the organism? While we were not able to find reports of other species of slime molds that accumulated high metal concentrations, similar levels of Zn hyperaccumulation have been reported in the Alpine pennygrass, Thlaspi caerulescens (J. Presl & C. Presl), which can accumulate up to 25000 mg Zn kg-1 dry wt. of shoots (Watanabe, 1997). Setälä and Nuorteva (1989) hypothesized that Zn possibly affords F. septica protection from some more dangerous factors by acting as a coenzyme or enzyme activator in a detoxification system. Another possibility is that high Zn contents may protect F. septica from predators or phages. Inorganic tin, for example, has been shown to be effective in inactivating bacteriophage T4 (Doolittle and Cooney, 1992).
Whether F. septica actively hyperaccumulates Zn, or simply binds it to the cell membrane, awaits experimental verification in laboratory cultures. Its ability to tolerate such high metal concentrations, what the upper concentration limit is, and why it hyperaccumulates Zn are also issues needing to be addressed in such experiments. The identification of an active Zn sequestration mechanism could lead to the cloning of the corresponding genes and their use in bioremediation following implantation into plants with a larger biomass (cf. Watanabe, 1997). Fuligo septica's ability to hyperaccumulate Zn may also be significant in studies of toxic metal impacts in forest systems, such as in Europe (Setälä and Nuorteva, 1989).
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ACKNOWLEDGMENTS
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Part of this work was done as part of the Environmental Project between the former USSR State Committee of Hydrometeorology and the Hydrometeorological Service of North Korea. The Hydrochemical Institute, Federal Russian Service for Hydrometeorology and Environmental Monitoring; the Kajima Foundation, Japan and the Association of Canadian Community Colleges, Partnerships for Tomorrow Programme provided funding. The authors are grateful to Dr. T.P. Sizova, Moscow University; Prof. P. Nuorteva, University of Helsinki, Finland; Prof. M.A. Rish and Dr. S. Urmanov, Fergana, State University, Uzbekistan; Prof. A.A. Kist, Prof. R.A. Kulmatov, and Dr. U. Rakhmatov, Institute of Nuclear Physics, Academy of Science of Uzbekistan; Dr. N. Katargin, Vernadsky Institute of Geochemistry and Analytical Chemistry, Moscow, Russia; Dr. A.A. Gusev, Administration of Kursk Region, Russia; as well as to the authorities and staff of the Voronezh Biosphere Reserve (Dr. V.A. Semyonov, Dr. V. Kazmin, and Dr. V. Emetz), Olekminsk Reserve (Dr. Yu. Rozhkov), North Osetiya Reserve (Dr. A. Lipkovich), Russia; and Zaamin Reserve, Uzbekistan for their assistance in our work. We also thank Dr. Yu. Novozhilov, Komarov Botanical Institute, St. Petersberg, Russia, for discussions about slime molds and Dr. J.R. Lawrence, National Water Research Institute, Environment Canada, and three anonymous reviewers for comments on an earlier draft of the manuscript.
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REFERENCES
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ABSTRACT
INTRODUCTION
