Ann. Limnol. - Int. J. Lim. 51 (2015) 139–146
Ó EDP Sciences, 2015
DOI: 10.1051/limn/2015010
Available online at:
www.limnology-journal.org
Diversity of algae in a thallium and other heavy
metals-polluted environment
Bartosz J. Płachno1, Konrad Wołowski2*, Joanna Augustynowicz3 and Magdalena Łukaszek2
1
2
3
Department of Plant Cytology and Embryology, Jagiellonian University in Kraków, Gronostajowa 9 St., 30-387 Kraków, Poland
Department of Phycology, W. Szafer Institute of Botany, Polish Academy of Sciences, Lubicz 46 St., PL-31-512 Kraków, Poland
Faculty of Biotechnology and Horticulture, Institute of Plant Biology and Biotechnology, University of Agriculture in Kraków,
Al. 29 Listopada 54, 31-425 Kraków, Poland
Received 5 September 2014; Accepted 3 March 2015
Abstract – Thallium (Tl) compounds are extremely toxic to living organisms, including algae, but there is
a dearth of basic information regarding the mechanisms of action of Tl in the environment and its effects
on algae in natural conditions. This study examined algal diversity in an environment highly polluted by Tl.
Graniczna Woda stream is contaminated by Tl and other heavy metal compounds (Cd, Pb and Zn). There
we found 66 algae taxa representing five phyla, among which euglenophytes prevailed. We found that
euglenophytes, including Phacus species, can survive and can show high species diversity in the presence of
high Tl concentrations. The fact that these small organisms covered only by a pellicle are able to thrive in
such inhospitable habitat, shows a great plasticity of these organisms. It is unclear whether the algae of
Graniczna Woda stream have a broad tolerance to harmful conditions or rather represent new varieties/clones
that evolved in metal-contaminated waters and are adapted to this environment.
Key words: Euglenophytes / Cd / Zn / Pb / thallium / water pollution
Introduction
Thallium (Tl), a metallic element placed in group 13
(formerly 3A) of the periodic table on account of its high
density ( > 11.6 g.cmx3), is classified as a heavy metal. Its
name, from Greek, is connected with the green spectral
line that identified this element (Fleischer, 1997). Tl in the
environment exists at two oxidation states: the more stable
Tl(I) (e.g., Tl2O) and the less stable Tl(III) (e.g., Tl(OH)3).
The natural background level of Tl in the Earth’s crust is
put at 0.85 mg.kgx1, and its minerals, associated with K or
S, are quite rare but widespread. Its mean concentration
in natural water systems is 10 ng.dmx3 (Kabata-Penidias
and Mukherjee, 2007). Under the quality standards of
both the United States Environmental Protection Agency
(EPA) and the Polish Ministry of the Environment, the
maximum permitted concentration of Tl in surface waters
is 2 mg.dmx3. Anthropogenic sources of Tl in the environment are related mainly to coal combustion and ferrous
or nonferrous smelting (Peter and Viraraghavan, 2005).
Commercial use of Tl is associated with the manufacture
of refractive glass and formerly for pesticide production,
*Corresponding author: k.wolowski@botany.pl
and it is used as a radioisotope for scintigraphy
(Kabata-Pendias and Mickherjee, 2007). Both Tl(I)
and Tl(III) compounds are readily soluble and therefore
bioavailable. Tl compounds are extremely toxic to living
organisms. Its toxicity to mammals is higher than that of
Hg, Cd and Pb (Peter and Viraraghavan, 2005; Babula
et al., 2008). Up to 1984, however, Tl was not considered
an environmental pollutant. In Poland, research on the
effects of Tl on biota started in the late 1990s, focused
on plants and small mammals occurring in the vicinity of
Olkusz, a highly industrialized area in southern Poland
(e.g., Dmowski et al., 1998; Wierzbicka et al., 2004).
As with other heavy metals, the effect of Tl on
organisms can be explained by its binding to –SH groups
of cysteine residues in proteins, leading to changes in the
activity of a broad range of enzymes. The most pronounced toxic effect of the Tl ion is related to the similarity
of Tl(I) to the potassium ion, due to their similar chemical
structure and properties. Monovalent Tl disrupts Kcontrolled activity of enzymes and membrane processes
such as the mitochondrial respiratory chain, and also
stabilization of ribosomes (Léonard and Gerber, 1997;
Arzate and Santamaria, 1998; Peter and Viraraghavan,
2005).
Article published by EDP Sciences
140
B. J. Płachno et al.: Ann. Limnol. - Int. J. Lim. 51 (2015) 139–146
Fig. 1. Oxbow of Graniczna Woda stream in the former De˛by Boruszowickie Reserve.
Unlike for the heavy metals Cd, Pb, Hg, Ni and Zn,
the literature contains little data on the effects of Tl on
plants. Only three plant species have been classified as
Tl hyperaccumulators, that is, plants able to accumulate
> 100 mg.kgx1 d.w. in natural conditions: Iberis intermedia Guersent, Biscutella laevigata L. (both from
the Brassicaceae family) and Silene latifolia Poir.
(Caryophyllaceae) (van der Ent et al., 2013). These are all
terrestrial species originating from southern France.
Studies showed that Tl can accumulate especially in plants
of the Brassicaceae family (Leblanc et al., 1999; Al-Najar
et al., 2005). There is far less information about aquatic
vegetation in Tl-contaminated environments, although
these organisms, immersed as they are, are far more exposed to harmful substances. In Synechocystis, Avery et al.
(1991) demonstrated competition between Tl(I) and
K ions, and Lustigman et al. (2000) showed Tl(I) toxicity
to the cyanobacterium Anacystis nidulans (Richter) Drouet
& Daily and the chlorophyte Chlamydomonas reinhardtii
P.A. Dang. Ralph and Twiss (2002) reported differential
toxicity of Tl to the unicellular chlorophyte Chlorella,
which depended on the oxidation state of the metal.
They observed the same degree of Chlorella growth
inhibition under treatment with Tl (III) at a dose of
2 r 10x13 [mol.dmx3] (4.1 r 10x2 ng.dmx3) and with
Tl(I) at a dose of 10x8 [mol.dmx3] (2.0 mg.dmx3). They
noted that Tl(III) toxicity was orders of magnitude greater
than Tl(I) to this phytoplankton but that the bioavailability of Tl(III) was significantly limited, and pointed
to the lack of fundamental information regarding Tl in the
environment. In experiments on Lemna minor L., Tl(I)
induced generation of reactive oxygen species, resulting in
damage to DNA and cell proteins (Babić et al., 2009).
The intrinsic toxicity of Tl and the mechanism of its
transport through the cell membrane were investigated
by Turner and Furniss (2012) in the marine alga
Ulva lactuca L.
Upper Silesia (southern Poland) is a highly contaminated mining and industrial region. Some watercourses in
this area, including Graniczna Woda stream, are polluted
by heavy metal compounds from chemical plants and
mines. Graniczna Woda stream was polluted by chemical
plants in the town of Tarnowskie Góry and by zinc smelters
in the town of Miasteczko Śla˛skie (Reczyńska-Dutka,
1986). In our latest work (Augustynowicz et al., 2014), we
conducted the Microtox1 toxicity test on the Graniczna
Woda strem and showed that studied water exhibited
second class of acute toxicity. In the above-mentioned
work, we also found high Tl pollution of the water in
Graniczna Woda stream with almost complete absence
of higher aquatic plants in its streambed. In the present
study, we examined there the diversity of algal flora. In an
unpolluted location in this area we had recorded a rich
algal flora in an earlier study (Wołowski et al., 2013a).
Material and methods
Study site
Material was obtained from Graniczna Woda stream
and its oxbow (Fig. 1) in the former De˛by Boruszowickie
Reserve near Tarnowskie Góry (Upper Silesia, Poland:
ca. 50x30kN/18x49kE). The stream bed is silty. The study
B. J. Płachno et al.: Ann. Limnol. - Int. J. Lim. 51 (2015) 139–146
141
Table 1. Algae taxa occurrence in De˛by Boruszowickie water bodies during sampling with comparison to the species occurrence in
Poland (rare – noted up to three times from Poland, often – noted four or more times from Poland).
Taxa
October
2008
Cyanophyta
Cyanophyceae
Oscillatoria sp. Vaucher ex Gomont
+
Phormidium sp. Kützing ex Gomont
+
Planktothrix agardhii (Gomont) Anagnostidis and Komárek
Heterokontophyta
Bacillariophyceae
Achnanthes sp. Bory de Saint-Vincent
Cyclotella sp. (Kützing) Brébisson
Eunotia bilunaris (Ehrenberg) Schaarschmidt
Eunotia exigua (Brébisson ex Kützing) Rabenhorst
Eunotia sp. Ehrenberg
+
Gomphonema parvulum (Kützing) Kützing
Navicula sp. Bory de Saint-Vincent
Nitzschia obtusa W.Smith
+
Nitzschia palea (Kützing) W.Smith
+
Pinnularia cf. ferrophila K. Krammer
Pinnularia nodosa (Ehrenberg) W.Smith
Pinnularia viridis (Nitzsch) Ehrenberg
+
Heterokontophyta
Xanthophyceae
Characiopsis subulata var. ensiformis (Hermann) Lemmermann
+
Tribonema sp. Derbès & Solier
+
Euglenophyta
Euglenophyceae
Euglena agilis H.J. Carter
Euglena archaeoviridis B. Zakrys and P.L. Walne
Euglena archaeoplastidiata M. Chadefaud
+
Euglena hemichromata Skuja
Euglena mutabilis F. Schmitz
+
Euglena sp. Ehrenberg
Lepocinclis spirogyroides Marin & Melkonian
+
Euglena viridis (O.F. Müller) Ehrenberg
Lepocinclis fusca (Klebs) Kosmala and Zakrys
+
Lepocinclis acus (O.F.Müller) Marin & Melkonian
Lepocinclis oxyuris (Schmarda) Marin and Melkonian
Lepocinclis ovum (Ehrenberg) Lemmermann
Monomorphina pyrum (Ehrenberg) Mereschkowsky
Petalomonas mediocanellata Stein
Phacus acuminatus Stokes
+
Phacus angustus Drezepolski
+
Phacus caudatus Hübner
+
Phacus curvicauda Svirenko
+
Phacus ichthydion Pochmann
Phacus indicus Skvortzov
Phacus inflexus (I. Kiselev) Pochmann
+
Phacus longicauda var. tortus Lemmermann
Phacus orbicularis Hübner
+
Phacus obolus Pochmann
Phacus parvulus Klebs
Phacus pleuronectes (O.F. Müller) Nitzsch
+
Phacus pusillus Lemmermann
Phacus unguis Pochmann
Trachelomonas bacillifera Playfair
Trachelomonas cervicula Stokes
Trachelomonas hispida (Perty) F.Stein
+
Trachelomonas oblonga Lemmermann
Trachelomonas perforata Awerinzew
Trachelomonas volvocinopsis Swirenko
May
2009
July
2010
June
2011
October
2011
Often
Often
Often
+
+
+
+
+
+
+
+
+
+
Reported from
Poland
+
+
+
+
+
+
+
+
Often
Often
Often
Often
Often
Often
Often
Often
Often
Rare
Often
Often
Often
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
Often
Rare
Rare
Often
Often
Often
Often
Often
Often
Often
Often
Often
Often
Rare
Often
Rare
Often
Often
Rare
Rare
Rare
Often
Often
Rare
Often
Often
Rare
Rare
Often
Often
Often
Often
Rare
Often
142
B. J. Płachno et al.: Ann. Limnol. - Int. J. Lim. 51 (2015) 139–146
Table 1. (Contd.)
Taxa
October
2008
Chlorophyta
Chlorophyceae
Chlamydomonas sp. Ehrenberg
Desmodesmus armatus (R.Chodat) E.Hegewald
+
Desmodesmus sp. (R.Chodat) S.S.An, T.Friedl and E.Hegewald
+
Oedogonium sp. Link ex Hirn
+
Scenedesmus ecornis (Ehrenberg) Chodat
+
Scenedesmus cf. armatus (R.Chodat) R.Chodat
+
Scenedesmus intermedius Chodat
+
Scenedesmus sempervirens Chodat
+
Scenedesmus sp. Meyen
+
Stigeoclonium tenue (C.Agardh) Kützing
Ulothrix sp. Kützing
Chlorophyta
Trebouxiophyceae
Microthamnion kuetzingianum Nägeli ex Kützing
Chlorophyta
Ulvophyceae
Ulothrix sp. Kützing
Chlorophyta
Zygnematophyceae
Closterium moniliferum Ehrenberg ex Ralfs
+
Closterium ehrenbergii Meneghini ex Ralfs
+
stream is in the Stoła River basin, which has the annual
discharge of 1.46 m3.sx1 (Program of the Environmental
Protection for the Tarnowskie Góry community). Part of
the oxbow borders the peat bog. The fieldwork was done
during the 2008, 2009, 2010 and 2011 vegetation seasons,
together with studies on the occurrence of carnivorous
Utricularia in this area. Samples for taxonomic research
were taken once a year (except in 2011 when sampling
was done twice) using a plankton net (0.25 mm mesh) and
a big pipette (phytobenthos). The samples were placed in
35 ml plastic containers and refrigerated. Fresh samples
or samples fixed with 4% formaldehyde were observed
with a Nikon ECLIPSE 600 light microscope with
Nomarski phase contrast. The collected water samples
were transported to the W. Szafer Institute of Botany
(Polish Academy of Sciences) in Cracow, where they were
analyzed as previously described (Wołowski et al., 2011).
Chemical analysis of water samples
Inductively coupled plasma mass spectrometry (ICPMS) (ELAN 6100, Perkin Elmer) (PN-EN ISO 99631:2001) as well as titration methods (PN-ISO 9297:1994;
PN-EN ISO 17294-1:2007) were applied to measure the
chemical composition of samples. The spectrometer was
calibrated to the ICP multi-element standard (Merck).
Results
Water chemistry analyses showed the following
average amounts of elements (mg.dmx3): inorganic
C 78.17, N 7.41, P 0.45, S 151.03, K 36.07, Fe 0.86,
May
2009
July
2010
June
2011
+
+
October
2011
+
+
+
+
+
+
+
+
Often
Often
Often
Often
Often
Often
Often
Rare
Often
Often
Often
Often
+
+
Reported from
Poland
+
Often
Often
Often
Mg 8.71, Mn 0.26, Ca 123.10. The amounts of heavy
metals and metalloids such as Cr, Ni, Cu, Zn, Ag, Hg,
As and Se did not exceed the relevant norms. For Cd
(0.06 mg.dmx3) the upper limit was exceeded by a factor
of 16 (Polish standard) or 40 (US EPA standard), for
Pb (0.05 mg.dmx3) by a factor of 7 (US EPA standard)
and for Zn (1.06 mg.dmx3) by a factor of 10 (US EPA
standard). The concentration of Tl (0.24 mg.dmx3)
exceeded the surface-water limits most spectacularly: by a
factor of 120 under both Polish and US EPA standards
(Rozporza˛dzenie Ministra Środowiska z dn. 9 listopada
2011 r.; US EPA Water Quality Standards, 2013). In
the group of biogenic substances, the upper limits were
x3
(Polish standard
exceeded for NOx
3 at 7.15 mg.dm
3x
x3
j 5 mg.dm ) and for PO4 at 0.45 mg.dmx3 (Polish
standard j 0.31 mg.dmx3). Other water parameters
were as follows: pH 7.0–7.5, electrical conductivity
1.04 mS.cmx1 and redox potential (Eh) 258 mV.
We identified 66 algal taxa representing five phyla
(Table 1). The euglenophytes of Graniczna Woda
stream showed great diversity, including 9 species
of Euglena, 5 of Trachelomonas, 15 of Phacus, 4 of
Lepocinclis, and one each of Monomorphina and
Petalomonas (see Fig. 2). Among the other algal groups
were 3 taxa of Cyanophyceae, 2 of Xanthophyceae, 14 of
Bacillariophyceae and 15 of green algae (Chlorophyceae).
The euglenophytes dominated among the observed algae
in every sampling year, and they also were the group
with the highest diversity, numbering 37 taxa. Some
of them are taxa rarely noted from Poland: Euglena
archaeoviridis B. Zakrys & P.L. Walne, Euglena archaeoplastidiata M. Chadefaud, Petalomonas mediocanellata
Stein, Phacus angustus Drezepolski, Phacus ichthydion
B. J. Płachno et al.: Ann. Limnol. - Int. J. Lim. 51 (2015) 139–146
143
Fig. 2. Euglenophytes documented in samples from Graniczna Woda stream: (A) Phacus indicus, (B) Phacus acuminatus, (C) Phacus
alatus, (D) Phacus curvicauda, (E) Phacus obolus, (F) Phacus parvulus, (G) Phacus caudatus, (H) Phacus unguis, (I) Phacus longicauda
var. tortus, (J) Euglena mutabilis, (K) Euglena hemichromata, (L) Euglena archaeoviridis, (M) Trachelomonas bacillifera, (N)
Monomorphina pyrum. Scale bar = 10 mm.
Pochmann, Phacus indicus Skvortzow, Phacus inflexus
(Kiselev) Pochmann, Phacus obolus Pochmann, Phacus
pusillus Lemmermann, Phacus unguis Pochmann and
Trachelomonas perforata Awerinzew. The other determined algal taxa are often reported from contaminated
waters.
In the area we examined, the water chemistry analyses
clearly indicated contamination with biogenic compounds
and heavy metals (Tl, Cd, Zn and Pb). This is the first
time so many Phacus taxa (15) have been recorded in
such a contaminated habitat; Phacus caudatus Hübner,
Phacus curvicauda Svirenko and Phacus parvulus Klebs
were recorded repeatedly throughout the study. Among
the euglenas, Euglena mutabilis F. Schmitz, Euglena viridis
(O.F. Müller) Ehrenberg, E. archaeoplastidiata Chadefaud
and Euglena agilis H.J. Carter were constant in the study
area. E. agilis occurred en masse in the pallmeloid stage
at sampling time in summer 2011. Trachelomonas hispida
(Perty) F. Stein was noted in almost every studied
sample. Diatoms were equally represented, and Nitzschia
palea (Kützing) W. Smith and Pinnularia viridis (Nitzsch)
Ehrenberg were noted in every sample. Among the
15 Chlorophyceae taxa the one most commonly noted
was Desmodesmus sp. We observed that the shape
and arrangement of the chloroplasts in E. viridis and
E. mutabilis varied and did not always fit the classical
description, and that the dimensions of euglenophyte
specimens were at their lower limits.
144
B. J. Płachno et al.: Ann. Limnol. - Int. J. Lim. 51 (2015) 139–146
Discussion
Previously we studied algal flora in the JeleniakMikuliny Reserve, situated in the same large forest
complex as De˛by Boruszowickie. The area of the
Jeleniak-Mikuliny reserve consists of two shallow, overgrown water ponds lying in the lowland between
two sand dunes. In this reserve, we found 96 algal
taxa [Cyanophyceae (4) Bacillariophyceae (20),
Chrysophyceae (1), Raphidophyceae (1), Xanthophyceae
(1), Cryptophyceae (2), Dinophyceae (1), Euglenophyceae
(24), Chlorophyceae (19), Zygnematophyceae (27)] and 11
morphotypes of chrysophyte stomatocysts (Wołowski
et al., 2013a). The algal flora of polluted Graniczna
Woda stream was poorer, with 66 species. It is known
that heavy metal pollution alters algal diversity and also
community structure. Different species may be more or
less tolerant to pollution and some may dominate in a
polluted environment (Say and Whitton, 1980; Whitton
et al., 1981; Podda et al., 2013; Trzcińska and PawlikSkowrońska, 2013). Some cyanobacteria of the genera
Oscillatoria, Phormidium, Plectonema and Schizothrix are
often abundant in alkaline waters polluted by heavy metal
compounds (Say and Whitton, 1980; Whitton et al., 1981).
Thus we might expect such taxa to be very abundant in the
alkaline, metal-polluted water of Graniczna Woda stream,
but we observed Oscillatoria sp. and Phormidium sp.
during only one season. The low occurrence of filamentous
cyanobacteria may also be related to a lack of N limitation
(as the mean N: mean P was 16.4:1 which is very close
to the Redfield ratio of 16:1) (see Reynolds, 1984), or to
the presence of other organic compounds that were
present in the studied water.
The high diversity of euglenoids in Graniczna Woda
stream indicates high tolerance of Tl by these algae. Years
of research on euglenophytes have shown that they are
remarkably tolerant to various kinds of pollution with
heavy metals such as Fe, Zn, Cu, Cd, Mn, Pb, Ni and Al
(Albergoni et al., 1980; Tam et al., 1981; Fasulo et al.,
1983; Walne and Kivic, 1990). They have also been
found in waters polluted with diesel oil (Dennington
et al., 1975), phenol (Pawlitz and Werner, 1978) and
herbicides and insecticides (Poorman, 1973; Butler, 1977),
and can survive in highly radioactive water (Lackley,
1968). Euglenophytes are also found living under very high
salinity, for example, in Great Salt Lake (Jones, 1944).
Several features help euglenophytes to survive in an
unfavorable environment, such as fast reproduction
(division), formation of cysts (Hindák et al., 2000) and
mixotrophy. Euglenophytes thrive very well in eutrophic
water and as a consequence they are often used as
bioindicators of water contamination (Starmach, 1983;
Sládeček and Sládečková, 1996; Wołowski, 1998, 2011,
Wołowski and Hindák, 2005). They usually inhabit
a-mesosaprobic and polysaprobic waters.
The contamination of the studied stream with organic
phosphates and nitrates explains the abundant occurrence
of euglenophytes. It is known that high concentrations
of heavy metals limit a site’s availability to different
groups of organisms but in this case they apparently had
no major effect on the algal taxa that occurred in De˛by
Boruszowickie.
It is generally known that acidophilic E. mutabilis
(Lane and Burris, 1981) and Euglena gracilis (Cook, 1968)
are able to grow in highly polluted habitats. E. mutabilis
colonizes highly acidified waters, tolerates pH of ca. 1, and
can be dominant among the eukaryotes in habitats such as
the metal-contaminated ponds of the Smoking Hills region
of the Canadian Arctic (Tam et al., 1981; Havas and
Hutchinson, 1983) and acidic post-mining ponds contaminated with heavy metals (Wołowski et al., 2008, 2013b). In
the investigated area of De˛by Boruszowickie, E. mutabilis
was present but did not develop en masse. Probably its
growth was limited by the high pH (7–7.5) of the water.
Our results confirm the higher tolerance spectrum of
E. mutabilis. Presumably the very low pH of post-mining
ponds also limits the growth of euglenophytes, such
as Phacus species, which prefer slightly acidic or neutral
water.
We found no literature data about the occurrence of
these Phacus species in waters contaminated with heavy
metals, including Tl. Ph. caudatus and Ph. curvicauda are
common, well-known species that occur in waters polluted
with organic compounds. There are somewhat fewer
records published for Ph. parvulus, which occurred in
Graniczna Woda stream throughout the studied period.
That this small organism covered only by a pellicle can
thrive in such an inhospitable habitat is an intriguing
finding.
Future studies should determine whether the algae
of Graniczna Woda stream accumulate heavy metals
or possess physiological adaptations endowing them
with a mechanism to effectively exclude harmful heavy
metals.
Acknowledgements. We would like to thank Michael Jacobs for
improving the English version of the manuscript. For this
research, K.W. received funding from the Polish Ministry of
Science and Higher Education/National Science Centre (grant N
N304 220135), K.W. and M.Ł. received funding from the
statutory fund of the Institute of Botany, Polish Academy of
Sciences, and J.A. received funding from the National Science
Centre (grant DEC-011/03/B/NZ9/00952). B.J. Płachno gratefully acknowledges granting of a Scholarship for Outstanding
Young Scientists from the Minister of Science and Higher
Education. The authors are very grateful to the reviewers for
their valuable comments on the manuscript.
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