Microcystin-producing blooms—a serious global public health issue$

The increase of human population and the consequent intensification of agricultural and industrial activities along with deficient water management have led to the enhancement of eutrophication in superficial freshwater bodies used for recreational purposes and as drinking water sources. The occurrence of phytoplanktonic blooms is also becoming more frequent worldwide. Environmental conditions such as higher temperature and pH values, low turbulence, and high nutrient inputs (particularly phosphorus (P), as well as nitrogen (N)) enhance the development of planktonic cyanobacteria in lakes and reservoirs, leading to formation of surface blooms that may accumulate as scum. The dominance of certain cyanobacteria at the surface is due to some advantageous characteristics such as lower nutrient (particularly nitrogen) requirements and buoyancy regulation in the water column for achieving better light and nutrient level conditions (Oliver and Ganf, 2000). The development of cyanobacterial blooms has become a serious problem because in the past decades many cyanobacteria have been reported to be able to produce secondary metabolites toxic to many organisms, including humans (Gorham and Carmichael, 1988; Codd et al., 1995; Codd, 2000; Briand et al., 2003; Haider et al., 2003; WHO, 2003). Cyanotoxins are very diverse in their chemical structure and toxicity (Dow and Swoboda, 2000; Kaebernick and Neilan, 2001; Briand et al., 2003), usually being classified as dermatotoxins (lipopolysaccharides, lyngbyatoxin-a, and aplysiatoxins), neurotoxins (anatoxin-a, homoanatoxin-a, anatoxin-a(s), and saxitoxins), and hepatotoxins (microcystins, nodularin, and cylindrospermopsin), according to the toxic effects ARTICLE IN PRESS $This paper was presented at the First World Environmental Education Congress, Espinho, Portugal (20th to 24th May 2003). *Corresponding author. E-mail addresses: (D.R. de Figueiredo), (M.J. Pereira). /$ - see front matter r 2004 Elsevier Inc. All rights reserved. doi:10.1016/v.2004.04.006 on animals. Microcystins are hepatotoxins to which special attention has been given not only due to their ability to cause acute poisonings but also due to their cancer promotion potential by chronic exposure of humans to low microcystin concentrations in drinking water (Ueno et al., 1996; Zhou et al., 2002), making production of these toxins a serious public health issue. The present study reviews some recent work made on microcystin toxicity on diverse organisms (including humans), factors influencing their production, and processes to eliminate them from drinking water. A retrospective concerning the occurrence of microcystinproducing blooms worldwide in the past 2 decades was also made. 2. Microcystin structure and synthesis Microcystins are cyclic heptapeptides with the general structure cyclo(-d-Ala-l-X-erythro-b-methyl-d-isoAspl-Y-Adda-d-isoGlu-N-methyldehydro-Ala). The aminoacid Adda (3-amino-9-methoxy-2,6,8-trimethyl-10- phenyldeca-4,6-dienoic acid) is considered responsible for the molecules hepatotoxicity (Dawson, 1998). There are more than 60 microcystin isoforms (Codd, 2000; Dow and Swoboda, 2000) in part due to the variable l-amino acids X and Y, but the most frequent and studied variant is microcystin-LR (MC-LR) with the variable amino acids leucine (L) and arginine (R). Other variants that also occur more frequently are MC-RR, MC-YR and MC-LA. These toxins occur in freshwaters worldwide and are mainly produced by colonial Microcystis spp. and filamentous Anabaena (An.) spp., Planktothrix/Oscillatoria (P. agardhii and P. rubescens), Anabaenopsis spp., Nostoc (N. rivulare), Aphanizomenon (Aph. flos-aquae) but also species belonging to the terrestrial genus Hapalosiphon (Codd et al., 1995; Dow and Swoboda, 2000; Kaebernick and Neilan, 2001). MC-LR, in particular, is known to be produced by species belonging to the genera Anabaena, Microcystis, Nostoc and Anabaenopsis (Dow and Swoboda, 2000; WHO, 2003) and MC-YR is produced by Microcystis aeruginosa, Microcystis viridis and Hapalosiphon spp. (Dow and Swoboda, 2000; WHO, 2003). MC-RR has been isolated from Oscillatoria agardhii, Microcystis aeruginosa and M. viridis, and MC-LA from Microcystis aeruginosa (Dow and Swoboda, 2000). There are no conclusive studies about the purpose of microcystins (secondary metabolites) synthesis but some results indicate that it may act as a chemical defence against grazing (Kurmayer and Ju¨ttner, 1999; Henning et al., 2001) or have an allelopathic effect over algal competitors (Kearns and Hunter, 2001) in addition to regulating endogenous protein phosphatases or being used as nitrogen reserve. Microcystins are produced nonribosomally through a microcystin synthetase complex (Kaebernick and Neilan, 2001) and their synthesis is an energy (ATP)- dependent process (Bickel and Lyck, 2001). The synthesis enzymatic complex is codified by an mcy genes cluster composed by two operons (mcyA–C and mcyD– J) (Kaebernick and Neilan, 2001) and it is present in toxic strains of the genus Microcystis but also in microcystin-producing strains of Anabaena, Nostoc and Planktothrix (Neilan et al., 1999), allowing the development o