Inducible tolerance to dietary protease inhibitors in<i>Daphnia magna</i>

Elert, Eric von; Zitt, Anja; Schwarzenberger, Anke

doi:10.1242/jeb.068742

Cited by 45 publications

(62 citation statements)

References 56 publications

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“…Additionally, our study indicates that such adaptation also appears within an ecosystem with a different spatial distribution of blooms. These new facets of the Daphnia-Microcystis interaction may be crucial for the stabilisation of the top-down effect of grazers in the trophic structure, for the limitation of microcystin accumulation by Daphnia and thus for the reduction of the contribution of daphniids to the transfer of toxins to higher trophic levels in food webs [6], [9], [46].…”

Section: Discussionmentioning

confidence: 99%

Response of Daphnia's Antioxidant System to Spatial Heterogeneity in Cyanobacteria Concentrations in a Lowland Reservoir

et al. 2014

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Many species and clones of Daphnia inhabit ecosystems with permanent algal blooms, and they can develop tolerance to cyanobacterial toxins. In the current study, we examined the spatial differences in the response of Daphnia longispina to the toxic Microcystis aeruginosa in a lowland eutrophic dam reservoir between June (before blooms) and September (during blooms). The reservoir showed a distinct spatial pattern in cyanobacteria abundance resulting from the wind direction: the station closest to the dam was characterised by persistently high Microcystis biomass, whereas the upstream stations had a significantly lower biomass of Microcystis. Microcystin concentrations were closely correlated with the cyanobacteria abundance (r = 0.93). The density of daphniids did not differ among the stations. The main objective of this study was to investigate how the distribution of toxic Microcystis blooms affects the antioxidant system of Daphnia. We examined catalase (CAT) activity, the level of the low molecular weight antioxidant glutathione (GSH), glutathione S-transferase (GST) activity and oxidative stress parameters, such as lipid peroxidation (LPO). We found that the higher the abundance (and toxicity) of the cyanobacteria, the lower the values of the antioxidant parameters. The CAT activity and LPO level were always significantly lower at the station with the highest M. aeruginosa biomass, which indicated the low oxidative stress of D. longispina at the site with the potentially high toxic thread. However, the low concentration of GSH and the highest activity of GST indicated the occurrence of detoxification processes at this site. These results demonstrate that daphniids that have coexisted with a high biomass of toxic cyanobacteria have effective mechanisms that protect them against the toxic effects of microcystins. We also conclude that Daphnia's resistance capacity to Microcystis toxins may differ within an ecosystem, depending on the bloom's spatial distribution.

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Section: Discussionmentioning

confidence: 99%

Response of Daphnia's Antioxidant System to Spatial Heterogeneity in Cyanobacteria Concentrations in a Lowland Reservoir

et al. 2014

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“…Control liposomes were produced according to [25] and subsequently enriched tenfold through centrifugation and subsequent resuspension in 1 ml liposome buffer [47]. For passive loading of the liposomes with microcystin, 500 μl of this suspension were added to 3 μg MC-LR and incubated for four h at 60°C.…”

Section: Methodsmentioning

confidence: 99%

“…Schwarzenberger et al [14] found that the tolerance of different Daphnia genotypes depended on the residual activity of proteases; increased gene expression and enhanced activity of the non-inhibited protease type also seemed to play a role. Von Elert et al [25] demonstrated that tolerance to cyanobacterial protease inhibitors was acquired by remodelling the affected digestive protease type.…”

Section: Introductionmentioning

confidence: 99%

Deciphering the genetic basis of microcystin tolerance

et al. 2014

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BackgroundCyanobacteria constitute a serious threat to freshwater ecosystems by producing toxic secondary metabolites, e.g. microcystins. These microcystins have been shown to harm livestock, pets and humans and to affect ecosystem service and functioning. Cyanobacterial blooms are increasing worldwide in intensity and frequency due to eutrophication and global warming. However, Daphnia, the main grazer of planktonic algae and cyanobacteria, has been shown to be able to suppress bloom-forming cyanobacteria and to adapt to cyanobacteria that produce microcystins. Since Daphnia’s genome was published only recently, it is now possible to elucidate the underlying molecular mechanisms of microcystin tolerance of Daphnia.ResultsDaphnia magna was fed with either a cyanobacterial strain that produces microcystins or its genetically engineered microcystin knock-out mutant. Thus, it was possible to distinguish between effects due to the ingestion of cyanobacteria and effects caused specifically by microcystins. By using RNAseq the differentially expressed genes between the different treatments were analyzed and affected KOG-categories were calculated. Here we show that the expression of transporter genes in Daphnia was regulated as a specific response to microcystins. Subsequent qPCR and dietary supplementation with pure microcystin confirmed that the regulation of transporter gene expression was correlated with the tolerance of several Daphnia clones.ConclusionsHere, we were able to identify new candidate genes that specifically respond to microcystins by separating cyanobacterial effects from microcystin effects. The involvement of these candidate genes in tolerance to microcystins was validated by correlating the difference in transporter gene expression with clonal tolerance. Thus, the prevention of microcystin uptake most probably constitutes a key mechanism in the development of tolerance and adaptation of Daphnia. With the availability of clear candidate genes, future investigations examining the process of local adaptation of Daphnia populations to microcystins are now possible.Electronic supplementary materialThe online version of this article (doi:10.1186/1471-2164-15-776) contains supplementary material, which is available to authorized users.

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“…These serine proteases represent the most important digestive enzymes in the gut of D. magna (Von Elert et al, 2004). When ingested with food particles, protease inhibitors negatively affect Daphnia by decreasing protease activity and reducing somatic growth (Lürling, 2003;Rohrlack et al, 1999;Von Elert et al, 2012;Schwarzenberger et al, 2012). The inhibition of digestive enzymes by these protease inhibitors should result in lower availability of amino acids.…”

Section: Introductionmentioning

confidence: 99%

Effect of nutrient limitation of cyanobacteria on protease inhibitor production and fitness ofDaphnia magna

Schwarzenberger

Sadler

Elert

2013

Journal of Experimental Biology

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SUMMARYHerbivore-plant interactions have been well studied in both terrestrial and aquatic ecosystems as they are crucial for the trophic transfer of energy and matter. In nutrient-rich freshwater ecosystems, the interaction between primary producers and herbivores is to a large extent represented by Daphnia and cyanobacteria. The occurrence of cyanobacterial blooms in lakes and ponds has, at least partly, been attributed to cyanotoxins, which negatively affect the major grazer of planktonic cyanobacteria, i.e. Daphnia. Among these cyanotoxins are the widespread protease inhibitors. These inhibitors have been shown (both in vitro and in situ) to inhibit the most important group of digestive proteases in the gut of Daphnia, i.e. trypsins and chymotrypsins, and to reduce Daphnia growth. In this study we grew cultures of the cyanobacterium Microcystis sp. strain BM25 on nutrient-replete, N-depleted or P-depleted medium. We identified three different micropeptins to be the cause for the inhibitory activity of BM25 against chymotrypsins. The micropeptin content depended on nutrient availability: whereas N limitation led to a lower concentration of micropeptins per biomass, P limitation resulted in a higher production of these chymotrypsin inhibitors. The altered micropeptin content of BM25 was accompanied by changed effects on the fitness of Daphnia magna: a higher content of micropeptins led to lower IC 50 values for D. magna gut proteases and vice versa. Following expectations, the lower micropeptin content in the Ndepleted BM25 caused higher somatic growth of D. magna. Therefore, protease inhibitors can be regarded as a nutrientdependent defence against grazers. Interestingly, although the P limitation of the cyanobacterium led to a higher micropeptin content, high growth of D. magna was observed when they were fed with P-depleted BM25. This might be due to reduced digestibility of P-depleted cells with putatively thick mucilaginous sheaths. These findings indicate that both the grazer and the cyanobacterium benefit from P reduction in terms of digestibility and growth inhibition, which is an interesting starting point for further studies.

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Inducible tolerance to dietary protease inhibitors inDaphnia magna

Cited by 45 publications

References 56 publications

Response of Daphnia's Antioxidant System to Spatial Heterogeneity in Cyanobacteria Concentrations in a Lowland Reservoir

Response of Daphnia's Antioxidant System to Spatial Heterogeneity in Cyanobacteria Concentrations in a Lowland Reservoir

Deciphering the genetic basis of microcystin tolerance

Effect of nutrient limitation of cyanobacteria on protease inhibitor production and fitness ofDaphnia magna

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