Variation in life history responses of Daphnia to toxic Microcystis aeruginosa

Hietala, Jaana; Reinikainen, Marko; Walls, Mari

doi:10.1093/plankt/17.12.2307

Cited by 63 publications

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“…THE JOURNAL OF EXPERIMENTAL BIOLOGY 2796 cyanobacteria on Daphnia are reflected by, for example, reduced growth, survival and reproduction (Lampert, 1981; Demott et al, 1991;Hietala et al, 1995;Nogueira et al, 2004;Trubetskova and Haney, 2006; Dao et al, 2010). However, one possible way to reduce toxic effects is to biotransform the toxin MC-LR by conjugation to the tripeptide glutathione (GSH) via the enzyme glutathione S transferase (GST) (Pflugmacher et al, 1998).…”

Section: Discussionmentioning

confidence: 99%

Transgenerational effects of microcystin-LR onDaphnia magna

Ortiz-Rodríguez

Dao

Wiegand

2012

Journal of Experimental Biology

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SUMMARYAnthropogenic and climate factors increase the frequency of problematic cyanobacterial blooms in freshwater. Among other toxins, some cyanobacteria produce microcystins (MCs), which inhibit phosphatases type 1 and type 2A and provokes oxidative stress. Toxic cyanobacteria affect the growth, survival and reproduction of zooplankton, particularly those from the genus Daphnia, which have a central position in pelagic food webs. However, one possibility to ameliorate effects is to biotransform MC via glutathione S transferase (GST) to a less toxic glutathione conjugate. This process was hypothesised to underlie the ability of Daphnia to withstand MC and to explain the enhanced tolerance of the offspring from mothers exposed to toxic cyanobacteria. Thus we conducted multigenerational experiments with D. magna, exposing the parental generation to MC for 1 or 7days and determining the enzyme-mediated tolerance to MC in their offspring by assessing the acute effect of MC on biotransformation and antioxidant and metabolism enzymes, and through 21day chronic tests on toxicity and growth. Seven days of exposure of the parental generation to MC induced higher activity of GST and malate dehydrogenase in the offspring and enabled them to increment the catalase activity when challenged with MC, whereas 1day of exposure of the parental generation did not. Offspring from non-exposed and 1-day-exposed mothers suffered decreased survival when exposed to MC compared with offspring from 7-day-exposed mothers; survival was correlated with the elevated activity of GST, malate dehydrogenase and catalase, suggesting maternal transfer of activation factors. However, increased survival occurred at the expense of individual growth. These results suggest that transgenerational effects are provoked by MC in D. magna, which may explain the observed acquirement of enhanced tolerance over generations.Key words: microcystin, cyanobacterial toxin, transgenerational effect, Daphnia, zooplankton. THE JOURNAL OF EXPERIMENTAL BIOLOGY 2796 cyanobacteria on Daphnia are reflected by, for example, reduced growth, survival and reproduction (Lampert, 1981; Demott et al., 1991;Hietala et al., 1995;Nogueira et al., 2004;Trubetskova and Haney, 2006; Dao et al., 2010). However, one possible way to reduce toxic effects is to biotransform the toxin MC-LR by conjugation to the tripeptide glutathione (GSH) via the enzyme glutathione S transferase (GST) (Pflugmacher et al., 1998). MCs are conjugated to GSH through the terminal methylene of N-methyldehydroalanine (Kondo, 1992), which is the moiety that binds to the active center of protein phosphatases (MacKintosh, 1995). The resulting conjugate is less toxic (Metcalf et al., 2000) and more hydrophilic, for easier transportation or excretion (Pflugmacher et al., 2001). This MC-LR detoxification process has been described in several aquatic organisms ranging from plants to invertebrates (including Daphnia magna) to fish (Pflugmacher et al., 1998;Wiegand and Pflugmacher, 2005). Three major families of prote...

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Section: Discussionmentioning

confidence: 99%

Transgenerational effects of microcystin-LR onDaphnia magna

Ortiz-Rodríguez

Dao

Wiegand

2012

Journal of Experimental Biology

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“…1). Studies showing considerable intraspecific variation in how diets containing cyanotoxins affect grazer fitness are not uncommon (Hietala et al 1995;Hairston et (Sarnelle 1993). Our assay using the compound-treated dried algae showed that particle-bound microcystin-LR, within the natural concentration range found in lakes, negatively affected the population growth rate of the Baker Lake Daphnia clone, but did not affect the fitness of the clone from Lake Sixteen.…”

Section: Discussionmentioning

confidence: 71%

“…In addition, significant interspecific and intraspecific variation exists in the ability of zooplankton to feed and reproduce on different cyanobacterial species and genotypes (Hietala et al 1995;Nandini and Rao 1998). Furthermore, the patchy nature of freshwater habitats and the clonal nature of many zooplankton and all cyanobacteria provide ample opportunity for selection of both deterrence and tolerance in grazers and prey, thus producing considerable variance within and between sites Wilson et al 2005).…”

Section: Discussionmentioning

confidence: 99%

A direct test of cyanobacterial chemical defense: Variable effects of microcystin‐treated food on two Daphnia pulicaria clones

Wilson

Hay

2007

Limnology & Oceanography

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To determine the direct effects of microcystin on the fitness of herbivorous zooplankton, we experimentally added microcystin-LR to freeze-dried cells of palatable Chlorella and fed these compound-treated cells to two clones of Daphnia pulicaria that had shown differing responses to a diet containing a strain of Microcystis aeruginosa that produces microcystin. The Daphnia that performed better on a diet containing live Microcystis showed reduced population growth when exposed to microcystin-LR-treated Chlorella, whereas the Daphnia that performed poorly on the diet containing live Microcystis was not affected by the experimental diet containing microcystin-LR. This is the first study to unambiguously show that some Daphnia strains are and some strains are not harmed by the consumption of microcystin-LR. These surprising results were not generated by interference from lipophilic secondary metabolites in Microcystis. When the crude lipophilic extract of Microcystis was added to dried Chlorella cells, it enhanced the fitness of both Daphnia clones. We hypothesize that the Daphnia clone more tolerant to live cells may upregulate resistance when cued by the presence of the live Microcystis cells, but not by microcystin-LR alone. Alternatively, the Daphnia clone that grew well on a diet containing live Microcystis may sequester compounds from Microcystis that defend the cyanobacteria from autotoxicity; these compounds would have been unavailable to Daphnia consuming freeze-dried Chlorella treated with microcystin-LR alone. Thus, microcystin-LR can suppress Daphnia fitness when consumed; however, the effects of microcystin vary across clones of herbivorous zooplankton and the consequences of this variance should not be overlooked when considering zooplankton-cyanobacteria interactions.Blooms of cyanobacteria threaten aquatic communities and global water supplies (Paerl 1988) because they produce secondary metabolites that can harm or kill fishes, livestock, and humans (Carmichael 1992). Some of the more commonly studied cyanotoxins include cyclic peptides that target mammalian livers (e.g., microcystin and cylindrospermopsin), nerve synapses (e.g., anatoxin-a), and gastrointestinal tracts (e.g., lyngbyatoxin-a) (Carmichael 1992; Chorus and Bartram 1999;Zurawell et al. 2005). Despite a large correlative literature suggesting that cyanotoxins may deter feeding by zooplankton (Lampert 1987;Watanabe et al. 1996;Zurawell et al. 2005), the effect of cyanobacterial secondary metabolites on ecologically relevant organisms, such as herbivorous zooplankton, is equivocal (Wilson et al. 2006a). There are no direct empirical tests of how cyanobacterial secondary metabolites affect grazers consuming these compounds.Cyanobacteria have been proposed to lower zooplankton grazing rates in three basic ways: (1) by occurring as large colonial and filamentous morphologies that clog filtering appendages or are otherwise inedible, (2) by being nutritionally deficient, and (3) by producing toxic secondary metabolites ( (4) fed diets ...

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“…Differences in the sensitivity between several Daphnia clones and species exposed to aqueous extracts or purified toxins and toxic and non-toxic cells of cyanobacteria were found in other studies [11,[16][17][18][19]. However, few studies tested the effects of ANTX-a(s) producer strains of cyanobacteria on Daphnia.…”

Section: Effects Of An Anatoxin-a(s)-producing Strain Of Anabaena Spimentioning

confidence: 89%

Effects of an Anatoxin-a(s)-Producing Strain of Anabaena spiroides (Cyanobacteria) on the Survivorship and Somatic Growth of Two Daphnia similis Clones

Abreu¹,

Ferrão-Filho²

2013

JEP

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The toxicity of an anatoxin-a(s) producer strain of Anabaena spiroides (ITEP-024) was estimated through sub-chronic bioassays with two clones of Daphnia similis (Labtox and Itajubá), both with intact cells and aqueous extracts of lyophilized material. Animals were grown as clonal cultures in the lab with mineral water plus 20% lake water. The concentrations used in the bioassays were 0.125, 0.25, 0.375, 0.50 and 1.00 mg·L −1 for intact cell cultures and 10, 25, 50 and 100 mg·L −1 for aqueous extracts. Controls with nutritive food were used. The bioassays lasted 72 hours for the aqueous extracts and 96 hours for the intact cell cultures, with measurements of survivorship every day and body length at the beginning and at the end of the bioassays. Both kinds of samples affected survivorship and growth rate of both Daphnia clones, with the intact cell samples being more effective than aqueous extracts. Regarding survivorship, the clone Itajubá was more sensitive to aqueous extracts than the clone Labtox (LC 50 = 54.4 and 83.1 mg·L −1 , respectively). No significant difference was found between clones in the intact cell bioassays. Regarding growth rates, a significant difference was found between clones in both samples. However, growth rate was significantly decreased in much lower concentrations of intact cells than in aqueous extracts of cyanobacteria. A stimulus of growth was found in the lower concentration (10 mg·L −1 ) of aqueous extracts, which is consistent with a hormetic response. In spite of its known high neurotoxicity to mice, ITEP-024 strain caused any effect on mobility of both clones. The effects on survivorship and growth of Daphnia caused by ITEP-024 strain in much higher concentrations of aqueous extracts suggests that uptake of toxins from the water are not so effective as the uptake trough the gut when intact cells are ingested.

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Variation in life history responses of Daphnia to toxic Microcystis aeruginosa

Cited by 63 publications

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Transgenerational effects of microcystin-LR onDaphnia magna

Transgenerational effects of microcystin-LR onDaphnia magna

A direct test of cyanobacterial chemical defense: Variable effects of microcystin‐treated food on two Daphnia pulicaria clones

Effects of an Anatoxin-a(s)-Producing Strain of <i>Anabaena spiroides</i> (Cyanobacteria) on the Survivorship and Somatic Growth of Two <i>Daphnia similis</i> Clones

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Variation in life history responses of Daphnia to toxic Microcystis aeruginosa

Cited by 63 publications

References 0 publications

Transgenerational effects of microcystin-LR onDaphnia magna

Transgenerational effects of microcystin-LR onDaphnia magna

A direct test of cyanobacterial chemical defense: Variable effects of microcystin‐treated food on two Daphnia pulicaria clones

Effects of an Anatoxin-a(s)-Producing Strain of &lt;i&gt;Anabaena spiroides&lt;/i&gt; (Cyanobacteria) on the Survivorship and Somatic Growth of Two &lt;i&gt;Daphnia similis&lt;/i&gt; Clones

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Effects of an Anatoxin-a(s)-Producing Strain of <i>Anabaena spiroides</i> (Cyanobacteria) on the Survivorship and Somatic Growth of Two <i>Daphnia similis</i> Clones