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PubMed2000

Generation of antibodies directed against the low-immunogenic peptide-toxins microcystin-LR/RR and nodularin.

The preparation of antibodies against the liver toxin microcystin, as described here, is of major importance for its detection and purification in food and water, and for a therapeutic approach to neutralize the toxin by passive immunization. Microcystin-LR (MLR) and microcystin-RR (MRR) were purified from cyanobacterial cell materials by extraction, Sephadex LH-20-, ODS silica gel-, ionic exchange and RP-HPLC-chromatography. In order to reduce the toxicity for parenteral administration, microcystins were coupled by the carbodiimide method to poly-L-lysine (PLL(50.000)). Mice and rabbits were immunized with the conjugates in the presence of two lipopeptide immunoadjuvants (P(3)CSK(4) and P(3)CS-T(h)). High MLR-specific antibody levels were observed after parenteral coadministration of antigen and lipopeptides, whereas no anti-MLR antibodies were obtained with free microcystin or the microcystin-PLL(50.000)-conjugate in the absence of lipopeptide. In oral immunization, coadministration of antigen and adjuvants resulted in an accelerated development of anti MLR-specific antibodies and high antibody levels. Using the antisera, we could detect different microcystins and nodularin down to a concentration range of 10-50 ng/ml by a competitive inhibition ELISA; detection of microcystins in crude cell preparations was also possible. Furthermore, microcystins from different sources could be detected and discriminated from cyclic cyanopeptolines.

Administration, Oral↗

PubMed2006

Effect of process variables and natural organic matter on removal of microcystin-LR by PAC-UF.

The release of cyanobacterial toxins, such as microcystin-LR, in drinking water supplies is of increasing concern. In this study, we investigated the use of ultrafiltration (UF) combined with adsorption on powdered activated carbon (PAC) for the removal of microcystin-LR from drinking water. Process variables examined included PAC type, PAC dosage, membrane characteristics (material and pore size), and the presence of natural organic matter (NOM). Due to greater mesopore volume, wood-based activated carbon was up to 4-times more effective at removing microcystin-LR than coconut-based carbon, depending on contact time. Cellulose acetate (CA) membranes with a molecular weight cutoff (MWCO) of 20,000 Da did not reject or adsorb microcystin-LR. Membranes composed of polyethersulfone (PES) of similar pore size, on the other hand, adsorbed microcystin-LR presumably through hydrophobic interactions. A PES membrane with a MWCO of 5000 Da sorbed microcystin-LR, and also rejected 8.4% of the toxin through a size exclusion mechanism. When PAC was coupled to UF using PES membranes, greater removal of microcystin-LR occurred compared to when CA membranes were used due to sorption of the toxin to the PES membrane surface. The presence of Suwannee River fulvic acid (SRFA) reduced microcystin-LR removal by PAC-UF, primarily due to competition between SRFA and microcystin-LR for sites on the PAC surface.

Bacterial Toxins↗

PubMed1997

Evidence for a covalently bound form of microcystin-LR in salmon liver and Dungeness crab larvae.

The chemically unique nature of the C20 beta-amino acid (2S,3S,8S,9S)-3-amino-9-methoxy-2,6,8-trimethyl-10-phenyldeca-4,6- dienoic acid (Adda) portion of the microcystins has been exploited to develop a strategy to analyze for the total microcystin-LR (1; see Figure 1) burden in salmon liver and crab larvae tissues. Lemieux oxidation of microcystin-LR (1) gives 2-methyl-3-methoxy-4-phenylbutanoic acid (2), a unique marker for the presence of microcystins. The butanoic acid 2 can be isolated and detected by GC/MS from the livers of Atlantic salmon that received an ip injection of microcystin-LR (1) and from tissues of wild-caught crab larvae. The Lemieux oxidation-GC/MS results are compared with those from MeOH extraction-PPase analysis. Only approximately 24% of the total microcystin-LR (1) burden in salmon liver tissue is found to be extractable with MeOH. Similarly, the Lemieux oxidation-GC/MS method detected 10,000-fold greater microcystin concentrations in Cypress Island Dungeness crab larvae than did the MeOH extraction-PPase method. The disparity in microcystin concentrations measured by the two methods is taken as direct evidence for the existence of covalently bound microcystins in vivo.

Animals↗

PubMed1998

A photodetoxification mechanism of the cyanobacterial hepatotoxin microcystin-LR by ultraviolet irradiation.

When microcystin-LR was exposed to UV, three major nontoxic compounds were formed. These compounds were identified as [4(E),6(Z)-Adda5]- and [4(Z),6(E)-Adda5]microcystin-LR, which are geometrical isomers of the Adda [3-amino-9-methoxy-2,6,8-trimethyl-10-phenyl-4(E),6(E)-decadienoic acid] moiety of microcystin-LR, and a novel compound, tricyclo-Adda [(2S,3S,1'R,3'S,4'S,5'R,6'R,7'R)-3-amino-5-(4',6'-dimethyl-3'-methoxy tricyclo[5.4.0.0(1',5')]undeca-8',10'-dien-6'-yl)-2-methy l-4(E)-pentenoic acid]-containing microcystin-LR ([tricyclo-Adda5]microcystin-LR), which was formed by [2 + 2] addition between the benzene ring and the double bond at position 6-7 of the Adda moiety of the microcystin. The geometrical isomers were formed reversibly, and their equilibrium constants were almost the same. [Tricyclo-Adda5]microcystin-LR was also formed reversibly and was decomposed under UV light. These results suggest that the breakdown of microcystin-LR by UV irradiation proceeds via [tricyclo-Adda5]microcystin-LR.

Animals↗

PubMed2005

Electrochemical degradation of microcystin-LR.

Microcystin-LR present in drinking water sources poses a considerable threat to human health. Conventional oxidation treatment systems, such as photocatalysis and ferrate oxidation, demonstrated the formation of by-products detectable in the treated microcystin-LR solution. This study investigated an electrochemical approach for microcystin-LR oxidation. The oxidation rate of microcystin-LR increased with the current; the oxidation rate was 0.219 min(-1) and the half-life was 2.5 min at an applied current of 100 mA to treat 1.0 mgL(-1) of microcystin-LR solution. These results were almost the same as those obtained from the photocatalytic oxidation of a 0.055 mgL(-1) microcystin-LR solution. The average instantaneous current efficiency of currents from 30 to 150 mA was greatest at 100 mA because both the current and the microcystin-LR concentration limited the oxidation rate. In addition, no by-products were detected by HPLC, which suggests that the microcystin-LR can be decomposed completely by the indirect oxidation of the hydroxyl radicals formed during electrochemical treatment. We demonstrated that the electrochemical oxidation is a promising approach for the complete oxidation of microcystin-LR.

Bacterial Toxins↗

PubMed2004

Abundance of active and inactive microcystin genotypes in populations of the toxic cyanobacterium Planktothrix spp.

To investigate the abundance of active and inactive microcystin genotypes in populations of the filamentous cyanobacterium Planktothrix spp., individual filaments were grown as clonal strains in the laboratory and analysed for microcystin synthetase (mcy) genes and microcystin. Twenty-three green-pigmented strains of P. agardhii originating mostly from shallow water bodies fell into two groups, those possessing mcyA and those lacking mcyA. In contrast, all of the 49 strains that were assigned to the red-pigmented P. rubescens contained mcyA. One strain of P. agardhii and eight strains of P. rubescens contained the total microcystin synthetase gene cluster but were found inactive in microcystin synthesis. To investigate the natural abundance of inactive mcy genotypes in P. rubescens individual filaments sampled from Lake Irrsee and Lake Mondsee (Austria) were analysed directly for the presence of mcyA and microcystin by matrix-assisted laser desorption/ionisation time-of-flight mass spectrometry. All filaments assigned to P. rubescens contained mcyA. The proportion of inactive microcystin genotypes in populations with a low (Irrsee) or high density (Mondsee) of P. rubescens was 5% and 21%, each. The results of this study demonstrate that P. rubescens typically contain mcy genes whereas P. agardhii have a patchy distribution of mcy genes. In both species microcystin producers co-occur with non-microcystin producers due to the absence/inactivation of mcy genes.

Bacterial Proteins↗

PubMed1990

Isolation and characterization of hepatotoxic microcystin homologs from the filamentous freshwater cyanobacterium Nostoc sp. strain 152.

A strain of the filamentous cyanobacterium Nostoc sp. isolated from a lake in Finland was found to produce at least nine hepatotoxic peptides with chemical and toxicological properties similar to those of the hepatotoxic hepta- and pentapeptides produced by other cyanobacteria. Toxins were isolated and purified by high-performance liquid chromatography. Amounts available for five of the purified toxins (P6, P14, P15, P16, and P18) were adequate for high-performance liquid chromatography amino acid analysis and determination of molecular weight by fast-atom bombardment-mass spectrometry (FAB-MS). Quantities of three toxins (P14, P15, and P16) were adequate for further analysis by high-resolution FAB-MS, FAB-MS/MS, and 1H-nuclear magnetic resonance. Analysis showed that the toxins are new types of microcystin-LR homologs. Microcystin-LR contains equimolar amounts of D-alanine, L-leucine, D-erythro-beta-methylaspartic acid, L-arginine, ADDA (3-amino-9-methoxy-2,6,8-trimethyl-10-phenyl-4,6-decadienoic acid), D-glutamic acid, and N-methyldehydroalanine (molecular weight [MW], 994). Nostoc sp. strain 152 was found to produce the following microcystin-LR homologs: (i) P6 contains an extra methylene group most probably due to the presence of N-methyldehydrobutyrine instead of N-methyldehydroalanine (MW, 1,008); (ii) P14 is O-acetyl-O-demethyl ADDA-microcystin-LR (MW, 1,022); (iii) P15 is 3-demethyl-O-acetylADDA-homoarginine-microcystin-LR (MW, 1,036); (iv) P16 is 3-demethyl-O-acetyl-O-demethylADDA-microcystin-LR (MW, 1,008); (v) P18 is 3-demethyl-O-acetyl-O-demethylADDA-homoarginine-microcystin- LR (MW, 1,022). The toxicities of the new microcystin homologs were not significantly different from those of microcystin-LR or demethylmicrocystin-LR.

Amino Acids↗

PubMed2001

The toxicology of microcystin-LR: occurrence, toxicokinetics, toxicodynamics, diagnosis and treatment.

Cyanobacterial blooms occur worldwide and present an increasing problem due to eutrophication of lakes. Microcystins, especially microcystin-LR, are microcyclic heptapeptide hepatotoxins and are the most common and potent toxins associated with cyanobacteria. Microcystin is rapidly taken up by hepatocytes through carrier-mediated transport. Once in the hepatocyte, microcystin causes structural damage to the cell indirectly by inhibiting protein phosphorylases 1 and 2A, which are needed for regulation of structural proteins of the cell. Acute liver hemorrhage and death occur with high doses of microcystin-LR, which is also a potent tumor promoter in laboratory rats. The significance of microcystin to human health has been debated; however, poisoning in humans has occurred due to contaminated dialysis water. Microcystin in contaminated drinking water may be the cause of elevated rates of primary liver cancer in some areas of China. Problems with hepatotoxic cyanobacteria have been most seen in livestock. Treatment of confirmed microcystin toxicosis in livestock is likely to be unrewarding, so prevention is important. Wild mammals, birds, fish, insects, and microinvertebrates may also be affected by microcystin.

Animal Diseases↗

PubMed1993

Hepatotoxin (microcystin) and neurotoxin (anatoxin-a) contained in natural blooms and strains of cyanobacteria from Japanese freshwaters.

Amounts of hepatotoxic microcystin and neurotoxic anatoxin-a were estimated in natural blooms and strains of cyanobacteria from freshwaters in Japan. A simultaneous analysis method of anatoxin-a and microcystin was applied to natural bloom samples, which has been dominated by several species and the strains of cyanobacteria which produced simultaneously both toxins. The natural blooms examined in the present study were mainly composed of Anabaena and Oscillatoria, but most also contained Microcystis and other cyanobacteria. Only one sample was almost unialgal, Anabaena spiroides, collected from Lake Sagami. The toxins in 14 samples collected from nine different natural blooms during 1988-1992 were identified as microcystins-RR, -YR, and -LR; desmethyl-7-microcystin-LR (7-DMLR); and anatoxin-a. Microcystins were the main toxins contained in these natural blooms, with anatoxin-a not being detected or of very little quantity. 7-DMLR was detected in samples only from Lake Kasumigaura. Five strains of Anabaena isolated from waters in Japan produced a small amount of anatoxin-a, but no microcystins. One half of the strains of Microcystis produced microcystins and/or anatoxin-a. This is the first study showing Microcystis producing both anatoxin-a and microcystins.

Amino Acid Sequence↗

PubMed1995

Reliable and sensitive method for determination of microcystins in complicated matrices by frit-fast atom bombardment liquid chromatography/mass spectrometry.

A reliable and sensitive method for determination of hepatotoxic microcystins in complicated matrices by frit-fast atom bombardment liquid chromatography/mass spectrometry (Frit-FAB LC/MS) is described. Immonium ions of constituent amino acids, which were obtained together with molecular ion species by FAB mass spectral analysis of standard microcystins RR, YR, LR, and [D-Asp3] and [Dha7]microcystins LR using flow injection system composed of Frit-FAB probe, showed potential for reliable identification of microcystins by Frit-FAB LC/MS. Frit-FAB LC/MS using a microbore column provided not only the baseline separation of standard microcystins RR, YR, and LR but 200-fold higher sensitivity than that using conventional column. Furthermore, when a selected ion monitoring (SIM) technique was used, the detection limits of microcystins RR, YR, and LR were 300, 350, and 400 pg, respectively, at a signal-to-noise ratio of 5:1, and calibration curves of each microcystin showed a linear relationship from 2 ng to 50 ng. Finally, identification and quantitative analyses of microcystins in water samples were carried out.

Chromatography, Liquid↗

PubMed2005

Diversity of hepatotoxic microcystins and bioactive anabaenopeptins in cyanobacterial blooms from Greek freshwaters.

Microcystins (MCs) and anabaenopeptins from 26 cyanobacterial bloom samples dominated mainly by the genus Microcystis and collected from seven Greek freshwaters were identified and quantified by high-performance liquid chromatography coupled to a diode array detector. All the samples analyzed contained microcystins; in 27% of the samples anabaenopeptins were detected but not anabaenopeptilide (A). In each sample 1-7 microcystins and up to two anabaenopeptins (anabaenopeptins A and B) were identified. MC-RR and MC-LR were the predominant microcystins, followed by MC-YR. MC-LA and demethylated variants of MC-LR and MC-RR also were present but were not abundant. Total content of microcystin and anabaenopeptin varied from 40 to 2565 microg g(-1) freeze-dried material (mean 674.5 microg g(-1)) and from undetectable to 48 microg g(-1) freeze-dried material (mean 6.2 microg g(-1)), respectively. Qualitative and quantitative variation in the microcystins in the samples indicates there may be geographical trends in the distribution of microcystins. This study reports for the first time (1) the widespread occurrence of several different microcystins in Greek freshwaters and (2) quantitative data on the anabaenopeptins produced in natural cyanobacterial populations.

Chromatography, High Pressure Liquid↗

PubMed1999

Hepatic toxicity and persistence of ser/thr protein phosphatase inhibition by microcystin in the little skate Raja erinacea.

Microcystin-induced ser/thr protein phosphatase (PP) inhibition and toxicity were examined in the little skate (Raja erinacea), an evolutionarily primitive marine vertebrate. As in mammals, PP inhibition and toxicity were exclusively hepatocellular, but were much more persistent in the skate. A dose of 63 microg/kg given iv to adult male skates resulted in the near complete inhibition of hepatic PP activity at 24 h. PP activity was still 95% inhibited 7 days after dosing in skates given 125 microg/kg microcystin. Mortality occurred at doses of 500 microg/kg or more. Hepatic lesions were only seen in animals with fully inhibited PP activity in liver. The histological changes seen at 125 microg/kg were mild periportal inflammatory changes increasing in severity together with hepatocyte necrosis at higher doses of microcystin. Microcystin persisted and could be detected in plasma up to 7 days after dosing. This finding shows that, in the skate, as in mammals, the liver is the only organ capable of uptake of microcystin, since there was no significant inhibition of PP activity in the rectal gland and small decreases in PP activity of the kidney that were not time or dose dependent. In vitro microcystin caused dose-dependent inhibition of PP activity in isolated skate hepatocytes, while it was without effect in cultured rectal glands. Uptake of microcystin and the accompanying inhibition of PP activity in skate hepatocytes was prevented by the addition of a series of organic dyes and bile acids. The spectrum of inhibitors of microcystin uptake in skate is similar to that seen in the rat, indicating common features of the carrier(s) in these diverse species.

Animals↗

PubMed2003

Dynamics of microcystin-degrading bacteria in mucilage of Microcystis.

To reveal the process of degradation of hepatotoxic microcystin produced in Microcystis cells during the Microcystis bloom period, we used fluorescence in situ hybridization (FISH) to analyze the population dynamics of microcystin-degrading bacteria in Microcystis mucilage. We designed and applied an oligonucleotide probe targeted to the 16S rRNA sequence of strain Y2 of a microcystin-degrading bacterium (MCD-bacterium), which was isolated from Lake Suwa, Japan. In both the 1998 and 1999 tests, FISH clearly showed that MCD-bacteria existed in the mucilage and that, when a high concentration of cell-bound microcystin was detected, MCD-bacteria exceeded 10% of the sum of bacteria hybridized with group-specific probes. The concentration of MCD-bacteria was highest in summer 1998, when a toxic species, M. viridis, was dominant. There was a high correlation between the number of MCD-bacteria in the mucilage and the concentration of cell-bound microcystin in the lake. Our results suggest that MCD-bacteria responded to changes in the concentration of microcystin and degraded the microcystin when it was released from Microcystis cells. We also analyzed changes in the bacterial community structure associated with the Microcystis colonies by using domain- and group-specific oligonucleotide probes. Changes in the concentrations of the Cytophaga/Flavobacterium group and delta-Proteobacteria, which can degrade macromolecules derived from Microcystis cells, were synchronized with changes in the concentration of Microcystis. The results not only suggest the significant role of MCD-bacteria in detoxification, but also demonstrate a possible sequence of degradation from Microcystis cells to microcystin maintained in the cell, which is then carried out by bacterial consortia in the mucilage.

Adhesives↗

PubMed1995

Mass spectral analyses of microcystins from toxic cyanobacteria using on-line chromatographic and electrophoretic separations.

The application of capillary electrophoresis and of reversed-phase liquid chromatography coupled to electrospray mass spectrometry is presented for the analysis of microcystins isolated from toxic strains of Microcystis aeruginosa. The separation performance of these two techniques is compared in terms of both sensitivity and of resolution of closely related microcystins. Quantitation of microcystin-LR present at low micrograms/ml concentrations in cell extracts is demonstrated using both techniques. A marked advantage of capillary electrophoresis over liquid chromatography was its ability to resolve different desmethyl microcystin-LR analogues. Identification of these positional isomers was facilitated using capillary electrophoresis combined with tandem mass spectrometry (MS-MS). Rationalization of fragment ions observed in MS-MS spectra of microcystins was made possible through comparison with 15N labelled microcystins obtained from stable isotope feeding experiments. The potential of tandem mass spectrometry in providing selective detection of microcystins in cell extracts, and in structural characterization of novel microcystins, was also investigated.

Amino Acid Sequence↗

PubMed1996

Separation of toxic peptides (microcystins) in capillary electrophoresis, with the aid of organic mobile phase modifiers.

A capillary electrophoretic (CE) method incorporating sodium dodecyl sulphate (SDS)-organic modifier solvents in the CE buffer was developed for the detection of toxic cyclic heptapeptide toxins (microcystins) produced by blue-green algae (cyanobacteria). The applicability of these run buffers for the analysis of microcystins was evaluated and optimum conditions for separation were determined. The migration times, elution order and selectivity of the toxic peptides were influenced by modifying the composition of the electrophoretic buffer with organic solvents [0 to 20% (v/v)]. At maximum addition, the organic solvents with the exception of acetonitrile, increased the viscosity of the buffer solution. In contrast to the migration time of the other microcystins, that of microcystin-RR was not increased by the addition of 2-propanol to the buffer solution. Rather, microcystin-RR eluted more quickly with the increase in 2-propanol, thereby effecting changes in the elution order of the microcystins. In addition, this solvent resulted in comigration of microcystin-LR and microcystin-YR. No significant relationship was found between the elution order and separation and the structure of the toxic peptides studied in micellar electrokinetic capillary chromatography with an organic modifier in the buffer solution; but there is an agreement between the effects of the organic modifiers and their dipole moments. Parameters such as linearity, sensitivity and reproducibility were also evaluated. High-efficiency separations of toxic peptide molecules having equal or nearly equal mass to charge ratios have been achieved using SDS as an additive to the running buffer. The influence of the pH has been examined.

Electrophoresis, Capillary↗

PubMed1992

Two methyl ester derivatives of microcystins, cyclic heptapeptide hepatotoxins, isolated from Anabaena flos-aquae strain CYA 83/1.

Cultured cells of Anabaena flos-aquae strain CYA 83/1, isolated from Lake Edlandsvatn, Norway, produced two microcystin mono-methyl ester derivatives (1 and 2) at the D-Glu unit in addition to microcystin-LR (3), [D-Asp3]microcystin-LR (4), microcystin-RR (5), and [D-Asp3]microcystin-RR (6). Structures of these compounds were assigned based on their amino acid analysis with a Waters Pico Tag HPLC system plus fast atom bombardment mass spectrometry (FABMS), including tandem FABMS, analysis on the two new microcystins, [D-Glu(OCH3)6]microcystin-LR (1) and [D-Asp3, D-Glu(OCH3)6]microcystin-LR (2). Toxicity data were not obtained for 1 and 2 because of the small amounts isolated from the cells.

Amino Acid Sequence↗

PubMed1995

Detection of cyanobacterial toxins (microcystins) in waters of northeastern Wisconsin by a new immunoassay technique.

The development of reliable, sensitive immunoassay techniques for detection of microcystins in water is becoming increasingly important. We have developed an enzyme-linked immunosorbent assay (ELISA) potentially able to detect microcystins at concentrations as low as 95 pg microcystin/ml water. The procedure uses antibodies extracted from the eggs of immunized chickens, eliminating the need to collect blood from laboratory rabbits. The antibody is able to recognize microcystin-LR, and -RR, and may recognize other forms of microcystin. The newly developed ELISA technique was utilized to measure the amount of microcystin in waters of northeastern Wisconsin. Of the water samples analyzed, 87% contained measurable amounts of microcystin (0.2-200 ng/ml). Organisms of the genus Microcystis were identified most frequently from microcystin-containing waters. The distribution of microcystin-producing cyanobacterial strains was apparently random throughout the sampling area.

Animals↗

PubMed2004

Assimilation and depuration of microcystin-LR by the zebra mussel, Dreissena polymorpha.

Zebra mussels (Dreissena polymorpha) are an important component of the foodweb of shallow lakes in the Netherlands, amongst others in Lake IJsselmeer, an international important wetland. Large numbers of ducks feed on these mussels in autumn and winter. The mussels are filter feeders and are exposed to high densities of cyanobacteria in summer and autumn. Mussels and cyanobacteria both thrive in Lake IJsselmeer. Apparently the mussels are somehow protected against accumulation of harmful quantities of cyanobacterial toxins. In this study, we investigated the assimilation of the cyanobacterial toxin microcystin-LR (MC-LR) in zebra mussels when fed the toxic cyanobacterium Microcystis aeruginosa as sole food or in a mixture with the eustigmatophyte Nannochloropsis limnetica. After 3 weeks of assimilation we studied the depuration of MC-LR during 3 weeks when the food of the mussels was free of cyanobacteria. These assimilation/depuration experiments were combined with grazing experiments, using the same food treatments. Microcystins were analyzed using liquid chromatography-mass spectrometry (LC-MS); in addition, covalently bound MC were analyzed using the MMPB method. The mussels showed higher clearance rates on Microcystis than on Nannochloropsis. No selective rejection of either phytoplankton species was observed in the excretion products of the mussels. Zebra mussels fed Microcystis as single food, assimilated microcystin-LR relatively fast, and after 1 week the maximum value of free unbound microcystin assimilation (ca. 11 microg g DW(-1)) was attained. For mussels, fed with the mixed food, a maximum of only 3.9 microg g DW(-1) was recorded after 3 weeks. Covalently bound MC never reached high values, with a maximum of approximately 62% of free MC in the 2nd week of the experiment. In the depuration period microcystin decreased rapidly to low values and after 3 weeks only very low amounts of microcystin were detectable. The amount of toxin that accumulated in the mussels would appear to be high enough to cause (liver) damage in diving ducks. However, death by exposure to microcystin seems unlikely. Mussels seem efficient in minimizing the assimilation of microcystin. If it were not for this, mass mortalities of ducks in shallow lakes in the Netherlands would presumably occur on a much more widespread scale than is currently observed.

Analysis of Variance↗