Transgenerational effects of microcystin-LR onDaphnia magna

Abstract

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...

Offspring performance of Daphnia magna after short-term maternal exposure to mixtures of microcystin and ammonia

“…The inhibiting effect on cyanobacteria biomass was particularly evident in ponds lacking planktivorous fish (Chislock et al 2013). Many previous studies found that Daphnia could develop tolerance to cyanobacteria and its toxicants through pre-exposure (Gustafsson and Hansson 2004;Jiang et al 2013;Ortiz-Rodriguez et al 2012).…”

“…In addition, detrimental effects were also observed in the performance of progeny from MC-LRexposed mothers (Dao et al 2010), which might be because more energy was allocated to resist MC-LR; hence, energy used for growth would be reduced. However, Daphnia might be capable of developing tolerance to MC-LR due to having the mechanisms of transformation and antioxidant enzymes (Ortiz-Rodriguez et al 2012). Development of tolerance to toxic cyanobacteria by Daphnia has been observed in both natural eutrophic lakes (Hairston et al 2001;Hairston et al 1999;Sarnelle 2005) and laboratory studies (Gustafsson and Hansson 2004).…”

“…Development of tolerance to toxic cyanobacteria by Daphnia has been observed in both natural eutrophic lakes (Hairston et al 2001;Hairston et al 1999;Sarnelle 2005) and laboratory studies (Gustafsson and Hansson 2004). Tolerance to MC-LR could even be inherited by the future generations: for example, progeny from mothers which suffered from MC-LR survived better when being exposed to the toxicant again (Ortiz-Rodriguez et al 2012).…”

CYP-dependent induction of glutathione S-transferase in Daphnia similis exposed to a disperse azo dye

“…Although there is no information regarding the mechanisms controlling GST induction in Daphnia, the limited literature available shows that GST activity induction can be observed under different chemical stress conditions. GST induction has been suggested as one important survival strategy in D. magna exposed to microcystin-L-R over generations (Ortiz-Rodríguez et al 2012). Ikenaka et al (2006) studied the metabolism of pyrene in D. magna, and showed that SKF-525A prevented CYP activity.…”

The neurotoxin BMAA in aquatic systems : analysis, occurrence and effects

“…In case adaptation occurs, offspring from exposed mothers can have an increased fitness when exposed to cyanobacteria compared to offspring from unexposed mothers [181]. This increased fitness might be caused by microcystin-LR induced maternal transfer of detoxification enzyme activation, which results in higher offspring survival under exposed conditions [182]. As shown for D. carinata, this maternally transferred inducible tolerance is clone specific, and could come at the expense of reduced fitness under unexposed conditions [183].…”