Seasonal succession of cyanobacterial protease inhibitors and Daphnia magna genotypes in a eutrophic Swedish lake

Schwarzenberger, Anke; D’hondt, Sofie; Vyverman, Wim; Elert, Eric von

doi:10.1007/s00027-013-0290-y

Cited by 24 publications

(33 citation statements)

References 54 publications

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“…BM25. However, this cyanobacterium has been shown to inhibit chymotrypsins (Schwarzenberger et al, 2013), and actually three different chymotrypsin inhibitors were identified in our study: micropeptin DR1056, micropeptin DR1006 and micropeptin MM978. Such protease inhibitors have been found in many blooms worldwide (Jakobi et al, 1996;Jakobi et al, 1995;Agrawal et al, 2001;Czarnecki et al, 2006), suggesting that they are among the most frequent cyanobacterial secondary metabolites.…”

Section: Discussionmentioning

confidence: 60%

“…We previously identified the micropeptins underlying the inhibition of chymotrypsins by BM25 (Schwarzenberger et al, 2013) and demonstrated that cyanobacteria produce more (P depletion) or less (N depletion) of these protease inhibitors under nutrient depletion. These findings are in full agreement with the carbon-nutrient balance hypothesis according to which the relative availability of carbon and nutrients affects the production of secondary metabolites (Stamp, 2003): because micropeptins are cyclic peptides that contain nitrogen but no phosphorus (Adiv et al, 2010), N-depleted growth of the cyanobacterium led to reduced synthesis of micropeptins, while P depletion resulted in nonlimiting availability of carbon and nitrogen, which then fuelled the increased synthesis of the protease inhibitors.…”

Section: Discussionmentioning

confidence: 99%

“…strain BM25 originates from Lake Bysjön in Southern Skania, Sweden (kindly provided by Ineke van Gremberghe, Ghent University, Ghent, Belgium). BM25 has been shown to inhibit D. magna chymotrypsins (but not trypsins) in vitro (Schwarzenberger et al, 2013). The cyanobacterium was cultivated semi-continuously at 20°C and constant light (50μEm…”

Section: Methodsmentioning

confidence: 99%

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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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Section: Discussionmentioning

confidence: 60%

Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

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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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“…Interestingly, both tolerant clones and the clone used in the transcriptome stemmed from the same population with frequent cyanobacterial blooms [24]. Therefore, local adaptation of this population to microcystins due to higher transporter-gene regulation is plausible.…”

Section: Resultsmentioning

confidence: 99%

“…Therefore, it is a key issue to elucidate the underlying molecular mechanisms of Daphnia ’s ability to tolerate cyanobacterial toxins and to therefore possibly suppress cyanobacterial blooms [19]. Toxic cyanobacterial secondary metabolites that frequently occur in cyanobacterial blooms are the well-studied microcystins and serine protease inhibitors [23, 24]. Both toxin types have been shown to negatively affect Daphnia [13, 14].…”

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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Inhibition of gut digestive proteases by cyanobacterial diets decreases infection in a Daphnia host–parasite system

Sánchez,

von Elert,

Monell

et al. 2024

Ecology and Evolution

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Secondary metabolites produced by primary producers have a wide range of functions as well as indirect effects outside the scope of their direct target. Research suggests that protease inhibitors produced by cyanobacteria influence grazing by herbivores and may also protect against parasites of cyanobacteria. In this study, we asked whether those same protease inhibitors produced by cyanobacteria could also influence the interactions of herbivores with their parasites. We used the Daphnia‐Metschnikowia zooplankton host‐fungal parasite system to address this question because it is well documented that cyanobacteria protease inhibitors suppress trypsin and chymotrypsin in the gut of Daphnia, and because it is known that Metschnikowia infects via the gut. We tested the hypothesis that Daphnia gut proteases are necessary for Metschnikowia spores to be released from their asci. We then also tested whether diets that decrease trypsin and chymotrypsin activity in the guts of Daphnia lead to lower levels of infection. Our results show that chymotrypsin promotes the release of the fungal spores from their asci. Moreover, a diet that strongly inhibited chymotrypsin activity in Daphnia decreased infection levels, particularly in the most susceptible Daphnia clones. Our results support the growing literature that cyanobacterial diets can be beneficial to zooplankton hosts when challenged by parasites and uncover a mechanism that contributes to the protective effect of cyanobacterial diets. Specifically, we demonstrate that host chymotrypsin enzymes promote the dehiscence of Metschnikowia spores; when cyanobacteria inhibit the activity of chymotrypsin in hosts, this most likely traps the spore inside the ascus, preventing the parasite from puncturing the gut and beginning the infection process. This study illustrates how secondary metabolites of phytoplankton can protect herbivores against their own enemies.

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Seasonal succession of cyanobacterial protease inhibitors and Daphnia magna genotypes in a eutrophic Swedish lake

Cited by 24 publications

References 54 publications

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

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

Deciphering the genetic basis of microcystin tolerance

Inhibition of gut digestive proteases by cyanobacterial diets decreases infection in a Daphnia host–parasite system

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