Toxicity of Toxins in the The first report of animal deaths associated with scums of and some other was in Chroococcales the Polish Lake Barlewice in 1884. Since then Microcystis species have been associated with several incidences of Author: R. Bijkerk animal and human death and illness all over the world (Codd et al. 2005). Negative effects of Microcystis on growth, Cyanobacteria are commonly associated with water quali­ reproduction and survival of zooplankton have been ty problems, due to the ability of several species to form demonstrated but there are no universal patterns; adverse blooms or surface scums. These problems are not restricted effects on filtration rates may be due to mechanical inter­ to water bodies that suffer from eutrophication, although ference (Visser et al. 2005). Microcystin-LR may also act as incidence and intensity of nuisance blooms may be an allelopathic agent on aquatic macrophytes resulting in enhanced by nutrient enrichment (Reynolds & Walsby growth inhibition (Pflugmacher 2002). 1975, Paerl 1988a and b). Apart from being unesthetic, Not all Microcystis species are equally toxic and within cyanobacterial blooms may lead to serious health prob­ species toxic and non-toxic strains may coexist. A survey of lems in animals and humans, as the species most often 13 lakes distributed over nine European countries showed involved in bloom formation in the temperate zone, i.e. that M. aeruginosa and M. botrys had significantly higher members of the genera Anabaena, Aphanizomenon, proportions of microcystin containing colonies than other Microcystis and Planktothrix, are capable to produce strong species (Table 2). The production of toxins in populations toxins (Sivonen & Jones 1999). Among the order of M. novacekii and M. wesenbergii has been demonstrated Chroococcales sofar only few genera besides Microcystis in Japanese strains, but remains uncertain in European have shown this ability. The purpose of this chapter is to ones (d. Henriksen 2001). Thus, determination to the provide an actual species list of potentially toxic species level may be useful in risk assessment. Chroococcales and to give a brief introduction to the sub­ Microcystins are largely contained within the cyanobacter­ ject with suggestions for further reading. ial cell and extracellulair concentrations are generally low (Chorus 2001). In Microcystis the cellular contents of micro­ Toxins in the Chroococcales cystin may either be lower or higher at light, phosphorus Eight genera among the order Chroococcales contain or nitrogen limitation, depending on the strain. Moreover, species that must be considered potentially toxic (Table I), the amount of microcystin per unit dry weight is generally of which Microcystis is the most notorious in Dutch fresh higher when population density is low, that is at the onset waters. Toxic effects have primarily been associated with of the bloom (Kardinaal & Visser 2005). This suggests that the production of microcystins. These are cyclic heptapep­ toxic genotypes are gradually replaced by non-toxic ones tides that may cause liver damage (Sivonen & Jones 1999). in the coarse of summer, probably as a respons to decreas­ To date, approximately 75 different kinds of microcystins ing nutrient availability. This seems to contradict the have been discovered, of which microcystin-LR is one of observation that toxic potential is lower in small the most common (Sigma-Aldrich 2006). Neurotoxine, Microcystis colonies than in large (Kurmayer et al. 2003). An typical of Anabaena and some other Nostocales, have only identification to the species level, in this case a discrimina­ incidently been associated with Microcystis aeruginosa and tion between small colonies of M. aeruginosa and M. jlos­ Woronichinia naegeliana. A haemolytic toxin has been aquae, might elucidate a common mechanism. Important demonstrated in marine Synechococcus strains. A property to notice however is that toxicity of Microcystis may vary in of all cyanobacteria is the presence of cell wall bound space and time and may to a large extent be independent lipopolysaccharides (LPS), first identified in Anacystis nidu­ on the cell density estimated at the generic level. lans (Weise et al. 1970). Ingestion ofLPS may cause gas­ troenteritis and contact elicits irritant and allergenic Safety standards for surface waters responses in human and animal tissues (Sivonen & Jones Guidelines are appropriate to prevent adverse health 1999). Recent research has revealed an amount of other effects from exposure to cyanobacterial toxins during the bioactive peptides in Microcystis, not listed in Table I, with recreational use of surface water. First provisional stan­ possible adverse effects on other organisms (Namikoshi & dards are partly derived from the WHO drinking water Rinehart 1996). guidelines and are not only stated in concentration levels of microcystin-LR, but also in density levels of cyanobacte-

18 Table 1. Species of the Chroococcales that are considered as potentially toxic with the kind of toxins involved However, it should be realized that some of the listed species might be misidentified.

taxon hepatotoxlns .....rot ..... hemolytic toxins Irritant totoxlns source microcystln anatoxin .-....- Ii-'Ysaccharkles Coelosphaerium kuetzingianum + + 14 aponina j + + - , 6, 14 Microcystis aeruginosa 1 + (+) I + 2,10,12,13,15,16, 20, 21 Microcystis botrys + + 17, 20 Microcystis flos-aquae I + + 20 Microcystis ichthyoblabe 1 + j + 2,5, 10, 20 Microcystis novacekii + + 10 J I i 1- Microcystis ponniformis 1) 1 + + 20 L J ! Microcystis viridis I + I + - 3,4, 10,15,16,18,20,21 I Microcystis wesenbergii J + 1 + 2, 9, 10, 16, 20 Radiocystis femandoi IT I + + 19 Snowella lacustris I + + 1 1,17 1 - Synechococcus sp. ~ J + + , 8 Synechocystis sp. I + + - 7,11 J I Woronichinia naegeliana + (+) + + 14,16, 17 I I t if Tropical species If Marine species I I 1

rial cells (Falconer et al. 1999). At a level of 20 000 cells per Table 2. Percentage of microcystin containing colonies in a survey of 13 European lakes (After Via-Drdorika et al. 2003). ml (> 10 ]lg/l microcystin-LR) there is a low probability of adverse effects (mainly irritative or allergenic effects). This SpecIes 'MIToxle Microcystis aeruginosa 72 probability is moderate at a level of 100 000 cells per ml Microcystis botrys 90 (>20 ]lg/l microcystin-LR). In scums characterized by a Microcystis flos-aquae I 50 thousand- to million-fold concentration of the cyanobacte­ Microcystis ichthyoblabe I 20 Microcystis ponniformis 53 rial population, there is a high risk of adverse health I Microcystis viridis I 17 effects. In the Dutch guideline the same microcystin con­ Microcystis wesenbergii I 0 centration levels are used (Health Council of the Netherlands 2001). The guidelines are currently subject of discussion for sev­ T (2004) Characteristics of microcystin produc­ eral reasons (Chorus 2005). It became clear that health tion in the cell cycle of Microcystis viridis. effects of recreational exposure may not be related to the Environm Toxicology 19(1): 20-25 . toxins analyzed but to exposure time and cyanobacterial 4 Kaya K & Watanabe MM (1990) Microcystin cell density (Pilotto et al. 1997). Next to microcystin-LR sev­ composition of an axenic clonal strain of eral other toxins have to be considered in water safety Microcystis viridis and Microcystis viridis-contain­ plans. Therefore, future standards may either involve ing waterblooms in Japanese fresh waters. J Appl cyanobacterial biomass or one to two cyanotoxins (Chorus PhycoI2:173-178. 2005)· 5 Kurmayer R, Christiansen G & Chorus I (2003) The abundance of microcystin-producing geno­ References table I types correlates positively with colony size in I Berg K, Skulberg OM, Skulberg R, Underdal B & Microcystis sp. and determines its microcystin net Willen T (1986) Observations of toxic blue-green production in Lake Wannsee. Appl Environ algae (Cyanobacteria) in some Scandinavian MicrobioI69(2): 787-795. lakes. Acta Vet Scand 27: 440-452. 6 Kutt EC & Martin DF (1975) Report on a bio­ 2 Fastner J, Erhard M & von Di:ihren H (2001) chemical red tide repressive agent. Environ Lett Determination of oligopeptide diversity within a 9(2): 195-208. natural population of Microcystis spp. 7 Lincoln EP & Carmichael WW (1981) (Cyanobacteria) by typing single colonies by Preliminary tests of toxicity of Synechocystis sp. matrix-assisted laser desorption ionization-time Grown on wastewater medium. In: Carmichael of flight mass spectrometry. Appl Environm WW (ed) The water environment. Algal toxins MicrobioI67(II): 5069-5076. and health. Plenum Press, New York. Pp 223-230. 3 Kameyama K, Sugiura N, lnamori Y & Maekawa 8 Mitsui A, Rosner D, Goodman A, Reyes-Vasquez

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