Vesa O. Sipiä
Finnish Institute of Marine Research
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Phycologia | 2001
Harri Kankaanpää; Vesa O. Sipiä; Jorma S. Kuparinen; Jennifer L. Ott; Wayne W. Carmichael
Abstract During 2–12 August 1999, the development of a surface bloom dominated by the cyanobacterium Nodularia spumigena was followed in the western Gulf of Finland, Baltic Sea. Intense surface scums of aggregated N. spumigena existed on calm days. The low-nutrient N. spumigena-dominated water mass was separated by a front from a nutrient-rich water mass dominated by Aphanizomenon cf. flos-aquae (Nostocales, Cyanobacteria). Owing to inadequate mixing of the two water masses, it is likely that N. spumigena growth was based mainly on the use of internal phosphorus stores. Signs of cell decay were observed on 5 August, and the proportion of empty filaments in the community increased towards the end of the survey period. A high number of Nitzschia spp. (Bacillariophyceae) was recorded within the N. spumigena aggregates on 8 August, suggesting nutrient leakage from the N. spumigena filaments. Senescence of N. spumigena and a decrease in the proportion of intact N. spumigena cells in dry material resulted in decreasing concentrations of cell-bound nodularin (NODLN), from 2.1 to 0.5 g kg−1 dry weight. No clear temporal trends in NODLN concentrations (< 0.5–2.6 μg l−1) were observed in Gulf waters. We hypothesize that the bloom was linked to a fish kill that occurred during the same time period. Threespine sticklebacks (Gasterosteus aculeatus, Gasterosteiformes, Gasterosteidae) were found floating on the surface during the water-bloom. The sticklebacks contained approximately 35–170 μg NODLN kg−1 dry weight (microcystin-LR equivalents). Empty N. spumigena cells and trace amounts of NODLN were also found in surficial sediment, indicating that toxin-producing N. spumigena had reached the seafloor.
Aquatic Toxicology | 2002
Harri Kankaanpää; Pekka J. Vuorinen; Vesa O. Sipiä; Marja Keinänen
Nodularin (NODLN) is a cyclic pentapeptide hepatotoxin that is regularly produced in high amounts by the cyanobacterium Nodularia spumigena in the Baltic Sea, and can bioaccumulate in Baltic biota. Baltic sea trout (Salmo trutta m. trutta L.) were exposed orally to a single dose of food containing NODLN (125 mg/kg ww) from N. spumigena (strain AV1, from the Baltic Sea). The level of exposure was 210-620 (average 440) microg NODLN per kg bw. Based on an 8-day survey under laboratory conditions, NODLN-like compounds accumulated in trout liver, with increasing liver concentrations (from 19 microg/kg on day 1 up to 1200 microg/kg on day 8 as measured with the EnviroLogix ELISA kit) during the experiment. Thus, accumulation of NODLN-like compounds in liver increased from 0.05% of the total NODLN dose administered on day 1 to 0.53% on day 8. However, the ELISA test kit is also sensitive to metabolites of algal hepatotoxins. In the HPLC chromatograms, no NODLN peak was detected after 24 h that also suggested NODLN absorbed in trout was metabolized or bound rapidly. According to ELISA, NODLN-like compounds also accumulated in trout muscle in lower quantities (from 125 to 34 microg/kg dw). Histopathology revealed complete loss of liver architecture after 1-2 days of the single oral dose. From day 4 to 8, there was partial recovery of liver cells. NODLN did not affect thiamine levels or water content of trout liver. The results showed that NODLN rapidly induces severe but reversible liver damage. Apparently NODLN accumulated in trout liver from cyanobacteria in the intestine, but was detoxified rapidly. On the basis of discrepancies between the histopathology and ELISA, and on the other hand, between the HPLC and ELISA methods, analysis of NODLN and its metabolites in biological tissue needs to be improved.
Aquatic Toxicology | 2003
Kari K. Lehtonen; Harri Kankaanpää; Sari Leiniö; Vesa O. Sipiä; Stephan Pflugmacher; Eva Sandberg-Kilpi
In this laboratory study the effects of the cyanobacterium Nodularia spumigena (strain AV1) that produces hepatotoxic nodularin (NODLN), non-toxic Nodularia sphaerocarpa (strain UP16f) and purified NODLN on the infaunal clam Macoma balthica from the Baltic Sea were examined. N. sphaerocarpa (2.4 and 12.5 mg dw l(-1)), N. spumigena (4 and 20 mg dw l(-1), intracellular NODLN content ca. 4 and 20 microg l(-1)) and purified NODLN (10 and 50 microg l(-1)) were applied in experimental tanks at 24 h intervals for 96 h. Water samples were taken during the experiment for the measurement of soluble NODLN concentrations. The concentrations of total hepatotoxins in the soft tissues were analysed with enzyme-linked immunosorbent assay (ELISA) and NODLN with high-performance liquid chromatography/diode array detection (HPLC/DAD). Acetylcholinesterase (AChE) activity was measured from the foot tissue samples taken at 0, 24 and 96 h. In the water phase, 60-100% of NODLN in the pure-toxin treatments and all the NODLN in N. spumigena treatments appeared as a yet unidentified form with NODLN-like spectral characteristics. The compound was present in similar quantities also in the non-toxic N. sphaerocarpa treatments. In the toxic N. spumigena treatments the tissue concentration of hepatotoxic NODLN-like compounds (measured with ELISA) increased from the control levels of 0.16 to 16.6 microg g(-1) dw (24 h), reaching 30.3 microg g(-1) dw at 96 h. However, <5% of the toxin detected by ELISA could be shown to be NODLN in HPLC/DAD analysis. Matrix-assisted laser desorption/ionisation-time of flight mass spectrometry (MALDI-TOF/MS) analyses revealed no NODLN-glutathione (GSH) conjugates in the tissues of M. balthica. Combining the responses in the AChE activity recorded after 24 and 96 h exposure, increases by 46% (N. spumigena) and 36% (soluble NODLN) compared with the control activity were observed in the low-level toxic exposures. Oppositely, decreases by 19% (N. spumigena) and 27% (soluble NODLN) of control activity were observed in the high-level exposures. Only the differences between the increased and decreased AChE activities were statistically significant, with individuals exposed to high levels expressing approximately 55% of the activity of those exposed to low concentrations. The results show that M. balthica readily ingests toxic N. spumigena and that accumulation of peptides takes place rapidly, which has potential food chain effects through toxin enrichment. However, it appears that M. balthica is at least partly able to metabolise NODLN. In addition to hepatotoxicity, NODLN seems to induce concentration-dependent neurotoxic effects; this must be taken into consideration when applying AChE activity as a biomarker of specific anthropogenic contamination (e.g. organophosphate and carbamate pesticides).
Journal of Chromatography B | 2003
Krister Karlsson; Vesa O. Sipiä; Harri Kankaanpää; Jussi Meriluoto
Samples of mussels and flounders from the Baltic Sea were analysed for nodularin content on two different LC-MS instruments (triple quadrupole and ion trap). The triple quadrupole instrument was well suited for the quantitative analysis. The limit of detection in the selected ion recording mode was 5 pg and in the multiple reactant monitoring mode 500 pg on column for extracts of Nodularia spumigena. The fragmentation patterns of nodularin-R and desmethylnodularin-R were recorded and shown to be similar to those of microcystins. LC-MS proved to be an excellent tool for the analyses of cyanobacterial hepatotoxins in complex matrices.
Environmental Toxicology and Chemistry | 2006
Vesa O. Sipiä; Olli Sjövall; Terhi Valtonen; Deborah L. Barnaby; Geoffrey A. Codd; James S. Metcalf; Mikael Kilpi; Olli Mustonen; Jussi Meriluoto
Nodularin (NODLN) is a cyanobacterial hepatotoxin that may cause toxic effects at very low exposure levels. The NODLN-producing cyanobacterium Nodularia spumigena forms massive blooms in the northern Baltic Sea, especially during the summer. We analyzed liver and muscle (edible meat) samples from common eider (Somateria mollissima), roach (Rutilus rutilus L.), and flounder (Platichthys flesus L.) for NODLN-R by liquid chromatography/mass spectrometry (LC-MS) and enzyme-linked immunosorbent assay (ELISA). Thirty eiders, 11 roach, and 15 flounders were caught from the western Gulf of Finland between September 2002 and October 2004. Eiders from April to June 2003 were found dead. The majority of samples were analyzed by LC-MS and ELISA from the same sample extracts (water:methanol:n-butanol, 75:20:5, v:v:v). Nodularin was detected in 27 eiders, nine roach, and eight flounders. Eider liver samples contained NODLN up to approximately 200 microg/kg dry weight and muscle samples at approximately 20 microg/kg dry weight, roach liver samples 20 to 900 microg NODLN/kg dry weight and muscle samples 2 to 200 microg NODLN/kg dry weight, and flounder liver samples approximately 5 to 1,100 microg NODLN/kg dry weight and muscle samples up to 100 microg NODLN/kg dry weight. The NODLN concentrations found in individual muscle samples of flounders, eiders, and roach (1-200 microg NODLN/kg dry wt) indicate that screening and risk assessment of NODLN in Baltic Sea edible fish and wildlife are required for the protection of consumers health.
Environmental Toxicology and Chemistry | 2004
Vesa O. Sipiä; Krister Karlsson; Jussi Meriluoto; Harri Kankaanpää
Nodularin (NODLN) is a cyclic pentapeptide hepatotoxin produced by the cyanobacterium Nodularia spumigena, which occurs regularly in the Baltic Sea during the summer season. Nodularia blooms have caused several animal kills in the Baltic Sea area, and NODLN has been found in mussels and fish caught from the northern Baltic Sea in 1996 to 2002. We analyzed liver samples of common eider (Somateria mollissima) for NODLN by enzyme-linked immunosorbent assay (ELISA) and liquid chromatography/mass spectrometry (LC-MS). Eiders feed extensively on mussel and can be exposed to NODLN by contaminated mussels. Fifteen eiders were shot and collected from three different sites in the western Gulf of Finland (northern Baltic Sea) in August and September 2002. Analyses by ELISA and LC-MS showed that eider liver samples contained 3 to 180 microg NODLN/kg dry weight and 0.1 to 5.8 microg NODLN/liver (dry wt). This is the first documentation of NODLN in seabirds and additional evidence for the transfer of NODLN in different parts of the Baltic Sea food web.
Aquatic Ecosystem Health & Management | 2002
Vesa O. Sipiä; Kirsti Lahti; Harri Kankaanpää; Pekka J. Vuorinen; Jussi Meriluoto
Nodularin, a cyclic pentapeptide hepatotoxin closely related to microcystins, is produced by the toxic brackish water cyanobacterium Nodularia spumigena which regularly forms blooms in the Baltic Sea. Baltic herring ( Clupea harengus membras L.) and salmon ( Salmo salar L.) were caught in the Baltic Sea during 1997 to assess levels of nodularin and microcystins resulting from the blooms. The total toxin content in herring muscle and salmon liver was measured with an enzyme-linked immunosorbent assay. Despite exceptionally heavy blooms of toxic Nodularia in the Baltic Sea during the summer of 1997, Baltic herring and salmon contained very low quantities of nodularin and microcystins (2.5-6.5 ng g -1 dry weight, not corrected for recovery, [30%]). These concentrations do not pose a health threat to humans, based on the World Health Organization value of tolerable daily intake. Moreover, the concentrations we found in salmon and herring were much lower than those reported for livers of European flounder ( Platichthys flesus L.) or Atlantic cod ( Gadus morhua L.) from the Baltic Sea during 1996-1999. We suspect that cyanobacterial hepatotoxins do not effectively accumulate in herring and salmon.
Environmental Pollution | 2009
Harri Kankaanpää; Olli Sjövall; Maija Huttunen; Miikka Olin; Krister Karlsson; Kirsi Hyvärinen; Laura Sneitz; Janne Härkönen; Vesa O. Sipiä; Jussi Meriluoto
This seven-year survey was primarily targeted to quantification of production of nodularin-R (NOD-R), a cyclic pentapeptide hepatotoxin, in Baltic Sea cyanobacteria waterblooms. Additionally, NOD-R and microcystin-LR (MC-LR; a cyclic heptapeptide toxin) sedimentation rates and NOD-R sediment storage were estimated. NOD-R production (70-2450 microg m(-3); approximately 1 kg km(-2) per season) and sedimentation rates (particles; 0.03-5.7 microg m(-2)d(-1); approximately 0.3kg km(-2) per season) were highly variable over space and time. Cell numbers of Nodularia spumigena did not correlate with NOD-R quantities. Dissolved NOD-R comprised 57-100% of total NOD-R in the predominantly senescent, low-intensity phytoplankton blooms and seston. Unprecedentedly intensive MC-LR sedimentation (0.56 microg m(-2)d(-1)) occurred in 2004. Hepatotoxin sedimentation rates highly exceeded those of anthropogenic xenobiotics. NOD-R storage in surficial sediments was 0.4-20 microg kg(-1) ( approximately 0.1 kg km(-2)). Loss of NOD-R within the chain consisting of phytoplankton, seston and soft sediments seemed very effective.
Chromatographia | 2002
Harri Kankaanpää; K. M. Vuorensola; Vesa O. Sipiä; Jussi Meriluoto
SummaryHigh-performance liquid chromatography (HPLC) was applied in the analysis of nodularin (NODLN), a potent, bioaccumulable hepatotoxin. The behaviour of NODLN in biological matrices and possibility to analyse biota samples for NODLN content was examined using a conventional HPLC/diode array detector method that uses C18 solid-phase cartridge clean up. Tissues of European flounder, blue mussel (spiked and naturally contaminated), clam (exposed to NODLN in an aquariuml and mouse (subjected to i. p. administration of NODLN) were analysed. UV detection was 5 times more sensitive than electrochemical detection. Recovery of NODLN from spiked tissues was 59% for mussel, 53% for flounder, and 44–75% for mouse tissues. NODLN was detected in clams exposed with NODLN, but not in naturally contaminated mussels where NODLN conjugation occurs. Through the use of spectral processing, free NODLN was unambiguously identified from tissue samples. The HPLC method showed limits of quantification between 90 and 150 μg NODLN kg−1 dw. The method proved applicable for routine tissue analysis and can be used in the monitoring of acutely toxic NODLN levels.
Archives of Environmental Contamination and Toxicology | 2009
Pekka J. Vuorinen; Vesa O. Sipiä; Krister Karlsson; Marja Keinänen; Ambrose Furey; Orla Allis; Kevin J. James; Ulla Perttilä; Eija Rimaila-Pärnänen; Jussi Meriluoto
Nodularin (NODLN) is a cyclic pentapeptide hepatotoxin produced by the cyanobacterium Nodularia spumigena, which occurs regularly in the Baltic Sea during the summer season. In this study flounder (Platichthys flesus L.) was orally exposed to NODLN either as a single dose or as three repeated doses 3xa0days apart. Liver and bile samples of the fish were taken 4xa0days after the last dose. Liver glutathione-S-transferase (GST) activity was also measured and the histopathology of the liver was investigated. The liver of the exposed fish was analyzed by liquid chromatography-mass spectrometry for NODLN concentration. The content of NODLN-like compounds in the bile was analyzed by enzyme-linked immunosorbent assay. NODLN exposure caused slightly incoherent liver architecture and degenerative cell changes in both groups. The mean liver GST activity was significantly higher in the repeatedly dosed flounders than in the singly dosed flounders or in the control. In conclusion, the significantly lower NODLN concentration and the increased GST activity in the liver of the repeatedly dosed flounders compared to the singly dosed flounders suggest that NODLN is rapidly detoxificated. The absence of NODLN glutathione conjugates and the low concentrations of NODLN-like compounds in the bile indicate that detoxification products disintegrate or they are rapidly excreted.