Cyanobacterial toxins in Canadian freshwaters: A review

Abstract Cyanobacterial toxins are a serious water quality concern in productive water bodies worldwide. Microcystins (MCs), which are hepatotoxins, are prevalent in Canadian freshwaters while the occurrence of neurotoxins anatoxin-a, anatoxin-a(s) and saxitoxin appears to be much less common. Concentrations of microcystin-LR (MCLR), presumed to be the most common of the more than 70 MC analogues, are highly variable in phytoplankton assemblages of lakes and greatly influenced by phytoplankton species composition. The frequency of occurrence and concentrations of MC in lakes in western Canada tend to increase with lake trophic status as well as decreasing N:P ratio. Microcystins accumulate in the aquatic food web through feeding activities of invertebrates (i.e., filter-feeding by clams and grazing by zooplankton and gastropods). Eventual trophic transfer of MC to fish, and resulting mortalities have been documented. Human health may also be at risk. Conventional water treatment may adequately remove low MC concentrations from source water, but can fail to completely remove MCs when initial concentrations are high. To address human health concerns, Health Canada established a drinking water guideline of 1.5 μg/L of MCLR. More recently, it has been suggested that β/N-methylamino-L-alanine (BMAA), a non-protein amino acid produced by many species of cyanobacteria, may cause neuro-degenerative disease, thus representing a significant emerging health issue.

[1]  R. Zurawell,et al.  Microcystin-LR concentration in aquatic food web compartments from lakes of varying trophic status , 1996 .

[2]  Philip R. Cohen,et al.  Cyanobacterial microcystin‐LR is a potent and specific inhibitor of protein phosphatases 1 and 2A from both mammals and higher plants , 1990, FEBS letters.

[3]  P. Henriksen,et al.  Confirmation of anatoxin-a(s), in the cyanobacterium Anabaena lemmermannii, as the cause of bird kills in Danish lakes. , 1997, Toxicon : official journal of the International Society on Toxinology.

[4]  I. Falconer,et al.  Tumour promotion by Microcystis sp., a blue‐green alga occurring in water supplies , 1989, The Medical journal of Australia.

[5]  C. Holmes,et al.  Identification and characterization of hydrophobic microcystins in Canadian freshwater cyanobacteria. , 1993, Toxicon : official journal of the International Society on Toxinology.

[6]  S. França,et al.  Paralytic shellfish toxins in the freshwater cyanobacterium Aphanizomenon flos-aquae, isolated from Montargil reservoir, Portugal. , 2000, Toxicon : official journal of the International Society on Toxinology.

[7]  K. Beattie,et al.  Colorimetric protein phosphatase inhibition assay of laboratory strains and natural blooms of cyanobacteria: comparisons with high-performance liquid chromatographic analysis for microcystins. , 1997, FEMS microbiology letters.

[8]  Richard E. Moore,et al.  Investigations of a neurotoxic oscillatorialean strain (Cyanophyceae) and its toxin. Isolation and characterization of homoanatoxin‐a , 1992 .

[9]  Paul Alan Cox,et al.  A mechanism for slow release of biomagnified cyanobacterial neurotoxins and neurodegenerative disease in Guam. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[10]  P. Reichardt,et al.  Toxins extracted from an Alaskan isolate of Protogonyaulax sp. , 1980, Biochemical and biophysical research communications.

[11]  W. Carmichael,et al.  Production and characterization of antibodies against microcystins , 1989, Applied and environmental microbiology.

[12]  E. Prepas,et al.  Occurrence and toxicological evaluation of cyanobacterial toxins in Alberta lakes and farm dugouts , 1993 .

[13]  D. F. Jackson.  Algae, man and the environment , 1969 .

[14]  K. Mizuno,et al.  Monoclonal Antibody , 2020, Definitions.

[15]  S. Azevedo,et al.  The first evidence of paralytic shellfish toxins in the fresh water cyanobacterium Cylindrospermopsis raciborskii, isolated from Brazil. , 1999, Toxicon : official journal of the International Society on Toxinology.

[16]  E. Prepas,et al.  Chemical control of hepatotoxic phytoplankton blooms: Implications for human health , 1995 .

[17]  D. Cardo,et al.  Liver failure and death after exposure to microcystins at a hemodialysis center in Brazil. , 1998, The New England journal of medicine.

[18]  E. Prepas,et al.  In situ evaluation of options for chemical treatment of hepatotoxic cyanobacterial blooms , 1997 .

[19]  R. Kfir,et al.  Monoclonal antibody specific for cyanoginosin-LA: preparation and characterization. , 1986, Toxicon : official journal of the International Society on Toxinology.

[20]  W. Carmichael,et al.  Blood pressure and hepatocellular effects of the cyclic heptapeptide toxin produced by the freshwater cyanobacterium (blue-green alga) Microcystis aeruginosa strain PCC-7820. , 1988, Toxicon : official journal of the International Society on Toxinology.

[21]  I. Falconer,et al.  Effect of the cyanobacterial (blue-green algal) toxins from Microcystis aeruginosa on isolated enterocytes from the chicken small intestine. , 1992, Toxicon : official journal of the International Society on Toxinology.

[22]  W. Carmichael,et al.  Algal toxins and water‐based diseases , 1985 .

[23]  E. Prepas,et al.  Accumulation and elimination of cyanobacterial hepatotoxins by the freshwater clam Anodonta grandis simpsoniana , 1997 .

[24]  M. Kent.  Netpen liver disease (NLD) of salmonid fishes reared in sea water: species susceptibility, recovery, and probable cause. , 1990 .

[25]  D. Williams,et al.  Chemical and biological evidence links microcystins to salmon 'netpen liver disease'. , 1993, Toxicon : official journal of the International Society on Toxinology.

[26]  S. Watson,et al.  New Microcystin Concerns in the Lower Great Lakes , 2003 .

[27]  R. Sakai,et al.  Structures of three new cyclic heptapeptide hepatotoxins produced by the cyanobacterium (blue-green alga) nostoc sp. strain 1521 , 1990 .

[28]  K. Sivonen,et al.  Preliminary characterization of neurotoxic cyanobacteria blooms and strains from Finland , 1989 .

[29]  E. Prepas,et al.  Odorous Substances and Cyanobacterial Toxins in Prairie Drinking Water Sources , 1992 .

[30]  S. Hrudey,et al.  Quantitation of the microcystin hepatotoxins in water at environmentally relevant concentrations with the protein phosphatase bioassay. , 1994, Environmental science & technology.

[31]  J. Patočka,et al.  The toxins of Cyanobacteria. , 2001, Acta medica.

[32]  K. Sivonen,et al.  Toxic cyanobacteria (blue-green algae) in Finnish fresh and coastal waters , 1990, Hydrobiologia.

[33]  Geoffrey A. Codd,et al.  Immunoassay of hepatotoxic cultures and water blooms of cyanobacteria using Microcystis aeruginosa peptide toxin polyclonal antibodies , 1988 .

[34]  D. Botes,et al.  Isolation and characterization of four toxins from the blue-green alga, Microcystis aeruginosa. , 1982, Toxicon : official journal of the International Society on Toxinology.

[35]  M. Schwimmer.  Medical aspects of phycology , 1968 .

[36]  A. Zehnder,et al.  Toxicity of a unialgal culture of Microcystis aeruginosa. , 1958, Canadian journal of microbiology.

[37]  Ingrid Chorus,et al.  Cyanotoxins : occurrence, causes, consequences , 2001 .

[38]  A. Dabholkar,et al.  Ultrastructural changes in the mouse liver induced by hepatotoxin from the freshwater cyanobacterium Microcystis aeruginosa strain 7820. , 1987, Toxicon : official journal of the International Society on Toxinology.

[39]  N. R. Hunter,et al.  Anatoxin-a, a toxic alkaloid from Anabaena flos-aquae NRC-44h , 1977 .

[40]  P. Gorham,et al.  Isolation and identification of the fast-death factor in Microcystis aeruginosa NRC-1. , 1959, Canadian journal of biochemistry and physiology.

[41]  Y. Ueno,et al.  Detection of microcystins, a blue-green algal hepatotoxin, in drinking water sampled in Haimen and Fusui, endemic areas of primary liver cancer in China, by highly sensitive immunoassay. , 1996, Carcinogenesis.

[42]  W. Carmichael,et al.  Liver tumor promotion by the cyanobacterial cyclic peptide toxin microcystin-LR , 2005, Journal of Cancer Research and Clinical Oncology.

[43]  J. Eriksson,et al.  Structure and toxicity of a peptide hepatotoxin from the cyanobacterium Oscillatoria agardhii. , 1989, Toxicon : official journal of the International Society on Toxinology.

[44]  C. Holmes,et al.  A unified bioscreen for the detection of diarrhetic shellfish toxins and microcystins in marine and freshwater environments. , 1993, Toxicon : official journal of the International Society on Toxinology.

[45]  J. Raven,et al.  Algae and Human Affairs. , 1989 .

[46]  W. Carmichael,et al.  The pharmacology of anatoxin-a(s), a neurotoxin produced by the freshwater cyanobacterium Anabaena flos-aquae NRC 525-17. , 1986, Toxicon : official journal of the International Society on Toxinology.

[47]  M. Kent,et al.  Suspected toxicopathic hepatic necrosis and megalocytosis in pen-reared Atlantic salmon Salmo salar in Puget Sound, Washington, USA. , 1988 .

[48]  Y. Prairie,et al.  Empirical study of cyanobacterial toxicity along a trophic gradient of lakes , 2005 .

[49]  R. Zurawell,et al.  Tissue Distribution and Oral Dose Effects of Microcystin in the Freshwater Pulmonate Snail Lymnaea stagnalis jugularis (Say) , 2007, Journal of toxicology and environmental health. Part A.

[50]  E. Prepas,et al.  Role of chemical and physical variables in regulating microcystin-LR concentration in phytoplankton of eutrophic lakes , 2000 .

[51]  Paul Alan Cox,et al.  Biomagnification of cyanobacterial neurotoxins and neurodegenerative disease among the Chamorro people of Guam , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[52]  R. Zurawell,et al.  Elimination of the Cyanobacterial Hepatotoxin Microcystin from the freshwater Pulmonate Snail Lymnaea stagnalis jugularis (SAY) , 2006, Journal of toxicology and environmental health. Part A.

[53]  J. Fohlmeister,et al.  Sodium channels blocked by aphantoxin obtained from the blue-green alga, Aphanizomenon flos-aquae. , 1982, Toxicon : official journal of the International Society on Toxinology.

[54]  H. Paerl.  Nuisance phytoplankton blooms in coastal, estuarine, and inland waters1 , 1988 .

[55]  K. Sivonen,et al.  Anatoxin-a concentration inAnabaena andAphanizomenon under different environmental conditions and comparison of growth by toxic and non-toxicAnabaena-strains — a laboratory study , 1993, Journal of Applied Phycology.

[56]  W. Carmichael,et al.  Use of a colorimetric protein phosphatase inhibition assay and enzyme linked immunosorbent assay for the study of microcystins and nodularins. , 1994, Toxicon : official journal of the International Society on Toxinology.

[57]  V. Smith,et al.  Low Nitrogen to Phosphorus Ratios Favor Dominance by Blue-Green Algae in Lake Phytoplankton , 1983, Science.

[58]  W. Carmichael,et al.  MORPHOLOGICAL AND 16S rRNA GENE EVIDENCE FOR RECLASSIFICATION OF THE PARALYTIC SHELLFISH TOXIN PRODUCING APHANIZOMENON FLOS‐AQUAE LMECYA 31 AS APHANIZOMENON ISSATSCHENKOI (CYANOPHYCEAE) 1 , 2003 .

[59]  E. Prepas,et al.  VARIABILITY OF THE HEPATOTOXIN MICROCYSTIN‐LR IN HYPEREUTROPHIC DRINKING WATER LAKES 1 , 1995 .

[60]  Nigel Dudley,et al.  Pesticide Handbook , 1952, Agronomy Journal.

[61]  Kun Chen,et al.  Relationship between microcystin in drinking water and colorectal cancer. , 2002, Biomedical and environmental sciences : BES.

[62]  R. Zurawell,et al.  Hepatotoxic Cyanobacteria: A Review of the Biological Importance of Microcystins in Freshwater Environments , 2005, Journal of toxicology and environmental health. Part B, Critical reviews.

[63]  A. Hendriks,et al.  pH-DEPENDENT HYDROPHOBICITY OF THE CYANOBACTERIA TOXIN MICROCYSTIN-LR , 1999 .

[64]  P. Gorham.  Toxic Waterblooms of Blue-Green Algae. , 1960, The Canadian veterinary journal = La revue veterinaire canadienne.

[65]  Hanne Kaas,et al.  Toxic cyanobacteria in water. A guide to their public health consequences, monitoring, and management , 2000 .

[66]  F. Pomati,et al.  THE FRESHWATER CYANOBACTERIUM PLANKTOTHRIX SP. FP1: MOLECULAR IDENTIFICATION AND DETECTION OF PARALYTIC SHELLFISH POISONING TOXINS , 2000, Journal of phycology.

[67]  Dudley H. Williams,et al.  Structural studies on cyanoginosins-LR, -YR, -YA, and -YM, peptide toxins from Microcystis aeruginosa , 1985 .

[68]  W. Carmichael,et al.  Detection of an anatoxin-a(s)-like anticholinesterase in natural blooms and cultures of cyanobacteria/blue-green algae from Danish lakes and in the stomach contents of poisoned birds. , 1997, Toxicon : official journal of the International Society on Toxinology.

[69]  W. Carmichael,et al.  Cyanobacteria secondary metabolites--the cyanotoxins. , 1992, The Journal of applied bacteriology.

[70]  W. Carmichael,et al.  Anatoxins from clones of Anabaena flos-aquae isolated from lakes of western Canada: With 3 figures and 2 tables in the text , 1978 .

[71]  L. Fabbro,et al.  A decision-making framework for ecological impacts associated with the accumulation of cyanotoxins (cylindrospermopsin and microcystin) , 2005 .

[72]  W. Carmichael,et al.  Paralytic shellfish poisons produced by the freshwater cyanobacterium Aphanizomenon flos-aquae NH-5. , 1986, Toxicon : official journal of the International Society on Toxinology.

[73]  M. Watanabe,et al.  Hepatotoxin (microcystin) and neurotoxin (anatoxin-a) contained in natural blooms and strains of cyanobacteria from Japanese freshwaters. , 1993, Natural toxins.

[74]  E. Prepas,et al.  Hepatic and renal pathology of intraperitoneally administered microcystin-LR in rainbow trout (Oncorhynchus mykiss). , 1996, Toxicon : official journal of the International Society on Toxinology.

[75]  W. Carmichael,et al.  Phycotoxins from blue-green algae , 1980 .

[76]  Kenneth H. Nicholls,et al.  Univariate Step-trend and Multivariate Assessments of the Apparent Effects of P Loading Reductions and Zebra Mussels on the Phytoplankton of the Bay of Quinte, Lake Ontario , 2002 .

[77]  I. Falconer,et al.  Biological half-life, organ distribution and excretion of 125-I-labelled toxic peptide from the blue-green alga Microcystis aeruginosa. , 1986, Australian journal of biological sciences.

[78]  J. Bartram,et al.  Health risks caused by freshwater cyanobacteria in recreational waters. , 2000, Journal of toxicology and environmental health. Part B, Critical reviews.

[79]  J. Howell,et al.  Symptoms and pathology produced by toxic Microcystis aeruginosa NRC-1 in laboratory and domestic animals. , 1965, Canadian journal of comparative medicine and veterinary science.

[80]  C. Scrimgeour,et al.  Identification of anatoxin-A in benthic cyanobacteria (blue-green algae) and in associated dog poisonings at Loch Insh, Scotland. , 1992, Toxicon : official journal of the International Society on Toxinology.

[81]  J. Eriksson,et al.  Hepatocellular uptake of 3H-dihydromicrocystin-LR, a cyclic peptide toxin. , 1990, Biochimica et biophysica acta.

[82]  W. Carmichael,et al.  Microcystin-LR-induced Ultrastructural Changes in Rats , 1990, Veterinary pathology.

[83]  K. Sivonen,et al.  The effect of water treatment processes on the removal of hepatotoxins fromMicrocystis andOscillatoria cyanobacteria: A laboratory study , 1989 .

[84]  C. Huber.  The crystal structure and absolute configuration of 2,9‐diacetyl‐9‐azabicyclo[4,2,1]non‐2,3‐ene , 1972 .

[85]  J. V. Smith,et al.  Oral toxicity of a bloom of the Cyanobacterium microcystis Aeruginosa administered to mice over periods up to 1 year. , 1988, Journal of toxicology and environmental health.

[86]  P. Henriksen,et al.  Saxitoxins (PSP toxins) in Danish lakes , 2000 .

[87]  C. Holmes,et al.  Liquid chromatography-linked protein phosphatase bioassay; a highly sensitive marine bioscreen for okadaic acid and related diarrhetic shellfish toxins. , 1991, Toxicon : official journal of the International Society on Toxinology.

[88]  D. Steffensen,et al.  Paralytic shellfish poisons from Australian cyanobacterial blooms , 1994 .

[89]  S. Orrenius,et al.  Rapid microfilament reorganization induced in isolated rat hepatocytes by microcystin-LR, a cyclic peptide toxin. , 1989, Experimental cell research.

[90]  W. Carmichael,et al.  Blue-green algae (Microcystis aeruginosa) hepatotoxicosis in dairy cows. , 1987, American journal of veterinary research.

[91]  J. Yates,et al.  Structural characterization of toxic cyclic peptides from blue-green algae by tandem mass spectrometry. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[92]  M. L. Fidalgo,et al.  PSP toxins from Aphanizomenon flos-aquae (cyanobacteria) collected in the Crestuma-Lever reservoir (Douro river, northern Portugal). , 2001, Toxicon : official journal of the International Society on Toxinology.

[93]  Robert E. Carlson,et al.  Potential Links Between Eutrophication and the Formation of Carcinogens in Drinking Water , 1988 .

[94]  R. Zurawell,et al.  Influence of lake trophic status on the occurrence of microcystin-LR in the tissue of pulmonate snails , 1999 .

[95]  R. Bidigare,et al.  Diverse taxa of cyanobacteria produce beta-N-methylamino-L-alanine, a neurotoxic amino acid. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[96]  P. Cohen,et al.  Okadaic acid: a new probe for the study of cellular regulation. , 1990, Trends in biochemical sciences.