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Distribution and Toxicity of Cylindrospermopsis

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Distribution and Toxicity of Cylindrospermopsis Limnetica 23(1-2) 11/10/04 10:19 Página 145 145 CORE Distribution and toxicity of Cylindrospermopsis raciborskiiMetadata, citation and similar papers at core.ac.uk Provided by Diposit Digital de Documents(Cyanobacteria) de la UAB in Portuguese freshwaters Martin L. Saker1*, Isabel C. G. Nogueira1 and Vitor M. Vasconcelos1 1Departamento de Zoologia e Antropologia, Faculdade de Ciências, Praça Gomes Teixeira, Porto 4050 Portugal and Centro Interdisciplinar de Investigação Marinha e Ambiental, Rua dos Bragas 177, 4050 Porto, Portugal. *Departmento de Zoologia e Antropologia. Faculdade de Ciências. Praça Gomes Teixeira. 4050 Porto. Portugal. Phone: +351 22 3401813. Fax: +351 22 3390608. Email: [email protected] ABSTRACT The cyanobacterium Cylindrospermopsis racborskii has become increasingly prevalent in freshwaters worldwide. This species is of concern from a water quality perspective due to its known ability to produce a potent hepatotoxic alkaloid cylindrosper- mopsin, which has been implicated in outbreaks of human sickness and cattle mortality. C. raciborskii isolates from Brazil have also been found to produce the highly toxic paralytic shellfish poisons (PSP’s). In this paper we report the toxicity of four isolates of C. raciborskii taken from three reservoirs and one river in Portugal as well as the occurrence of this species in other water bodies used for potable and recreational purposes. All four isolates grown in pure culture in the laboratory were found to be toxic in the mouse bioassay at 8 – 24 hours after intraperitoneal administration of single doses ranging from 1337 to 1572 mg kg-1. Histological examination showed liver damage as the primary lesion, in addition to some inflammation in the intestine. HPLC/MS tests for the presence of cylindrospermopsin, microcystins and PSP toxins were negative. The available evidence suggests that another toxin may be present. This report constitutes the first report of toxic C. raciborskii in Europe and draws attention to our need for increased monitoring of this cyanobacterium in water bodies used for potable and recrea- tional purposes. Keywords: Cyanobacteria, Cylindrospermopsis, freshwaters, toxicity, Portugal RESUMEN La cianobacteria Cylindrospermopsis racborskii ha incrementado su presencia en agua dulce por todo el mundo. Esta especie es de gran importancia debido a su conocida capacidad para producir un alcaloide hepatotóxico, cilindrospermopsina. Esta toxina es responsable de enfermedades en humanos y mortalidad en ganado. Cepas de C. raciborskii aisladas de Brasil se ha demostrado que tienen capacidad para producir la toxina paralytic shellfish poisons (PSP’s). En este trabajo hemos estudiado la presencia de esta especie en agua dulce con usos recreacionales y de abastecimiento en Portugal. De las cuatro cepas C. raciborskii aisladas de tres embalses y de un río estudiamos la toxicidad con bioensayos en ratones. Todas presentaron toxici- dad al cabo de las 8 – 24 horas tras inyección intraperitoneal, la dosis presenta un rango de concentración de 1337 a 1572 mg kg-1. La examinación histológica reveló daños en el hígado y señales inflamatorias en el intestino. Los análisis con HPLC/MS revelaron la ausencia de cilindrospermopsina, microcistinas y PSP, sugiriendo que otra toxina podría estar presente para las cepas aisladas y cultivadas en laboratorio. Este artículo es el primero acerca de la toxicidad de C. raciborskii en Europa y refleja la necesidad de aumentar el monitoreo de esta cyanobacteria en el agua potable y con fines recreativos. Palabras clave: Cianobacteria, Cylindrospermopsis, aguas continentasles, toxicidad, Portugal INTRODUCTION recent review of the worldwide occurrence of C. raciborskii by Padisák (1997) highlighted the The freshwater, planktonic cyanobacterium increasing number of reports of this species from Cylindrospermopsis raciborskii (Order Nosto- many temperate European countries including cales) was originally described as a species of Austria (Dokulil & Mayer, 1996), France (Briand only tropical interest (Woloszynska, 1912). A et al., -In press; Couté et al., 1997), Germany Limnetica 23(1-2): 145-152 (2004) © Asociación Española de Limnología, Madrid. Spain. ISSN: 0213-8409 Limnetica 23(1-2) 11/10/04 10:19 Página 146 146 Saker et al. (Krienitz & Hegewald, 1996), Greece (Hindák & using the taxonomic descriptions of Baker (1991) Moustaka, 1988), Hungary (Padisák, 1997), and Komárek & Kling (1991) were taken from Spain (Romo & Miracle, 1994) and Slovakia three reservoirs (Odivelas Reservoir, Caia (Horecká & Komárek, 1979). Reservoir and Maranhão Reservoir) and one river This species is of concern from a water quality (Ardila River) in the south of Portugal between perspective due to its ability to produce toxic com- July to October 1999. The location of the four pounds that can potentially affect the health of source water bodies are shown in figure 1. humans and other animals. The tricyclic alkaloid Isolation into pure culture was by transferen- cylindrospermopsin has been reported to be produ- ce of single trichomes as previously described ced by C. raciborskii strains from Australia (Saker et al., 1999a) into sterile plastic 10 ml (Hawkins et al., 1997; Saker et al., 1999a,b; Saker centrifuge tubes containing 5 ml of Z8 media & Griffiths, 2000) and Thailand (Li et al., 2001). (Kotai, 1972) modified by the omission of all This compound causes severe liver damage in the combined forms of nitrogen. Cultures were mouse bioassay (Hawkins et al., 1985; Hawkins et maintained at 20 ± 1oC and incident light inten- al., 1997; Ohtani et al., 1992) with symptoms cle- sity of 10 µmol m-2 s-1 provided by cool white arly distinguishable from those of some other cya- fluorescent tubes (14:10; light:dark cycle). nobacterial hepatotoxins including nodularin and Cultures in the late exponential growth phase microcystin. Cylindrospermopsin has been impli- (100 ml) were used to inoculate 6 L culture cated in outbreaks of human sickness (Bourke et flasks containing 4 L of nitrogen replete Z8 al., 1983; Byth, 1980) and cattle mortality (Saker medium. The flasks were incubated under the et al., 1999b; Thomas et al., 1998) and in recogni- conditions described above and at the end of the tion of its potency, a water quality guideline value exponential growth phase, these cultures were of 1 µg L-1 has been proposed (Shaw et al., 2000). harvested by gravity filtration onto GF/C filter Paralytic shellfish poisons (PSP´s) including neo- paper, frozen and freeze dried. saxitoxin, saxitoxin and gonyautoxin 2/3 isomers, 50 ml sub-samples of the C. raciborskii cultu- similar to those produced by another freshwater res were preserved with Lugols´ solution for mor- cyanobacterium Anabaena circinalis, have also phological measurement of vegetative cells and been detected in isolates of C. raciborskii from heterocysts, using a Leica DM LB image analysis Brazil (Lagos et al., 1999). These toxins have been system. For each of the morphological variables, implicated in the death of humans and other ani- > 30 measurements were taken. End cells were mals (Ressom et al., 1994). excluded from the analysis due to the greater In this paper, we investigate the distribution variability in end cell shape (Singh, 1962). of C. raciborskii in a range of Portuguese fresh- waters and report on the toxicity of four isolates Mouse bioassay of C. raciborskii taken from one river and three reservoirs in Portugal and grown in pure culture. Freeze dried biomass (ca. 145 - 160 mg) from the The toxicity of these isolates has been investiga- four C. raciborskii isolates was sonicated in 5 ml ted by mouse bioassay (intraperitoneal (i.p) of physiological saline, on ice, at 50 Hz for five administration) and by HPLC/MS. minutes. Sonicated cell suspensions were inspec- ted microscopically (to ensure complete cell lysis) and 1ml administered intra-peritoneally to each of METHODS two white male Charles River mice (23 – 25 g weight). Two control animals were dosed with Isolation and culture of C. raciborskii 1ml of physiological saline and another two mice with 1ml of a sonicated cell suspension of Cylindrospermopsis raciborskii (Woloszy´nska) Ankistrodesmus falcatus (Corda) Ralfs in physio- Seenayya and Subba Raju isolates, identified logical saline. All mice were observed regularly. Limnetica 23(1-2) 11/10/04 10:19 Página 147 Cylindrospermopsis raciborskii in Portugal 147 Moribund mice were necropsied by cervical dis- location. Portions of cecum, liver, lung, kidney and upper and lower intestine were immediately removed, washed with Dulbecco´s buffered saline (Sigma), fixed in Boiun fixative (Sigma), and included in paraffin. Sections (5 – 7 µm) were stained with haematoxilin and eosin and analysed with a HP Leica DMLB optical microscope with and 100x, 400x and 1000x magnification. HPLC analysis of toxins For the analysis of microcystins, lyophilised C. raciborskii samples were sonicated in 20 % methanol, filtered (0.2 µm) and analysed using a Shimadzu LC6-AD HPLC system equipped with a Shimadzu SPD-M10A diode array detec- tor. An Altima C18 column (150mm x 4.6 mm, 5 µm) was used with a 1 mL per minute linear gradient of 15 % to 45 % methanol / 8 mM Ammonium acetate in 30 mins. Microcystins if present were identified by their characteristic UV spectrum and quantified by comparison to a microcystin-LR standard (Calbiochem # B28160). The detection limits using this techni- que were generally less than 0.5 µg L-1. For the analysis of saxitoxins, lyophilised algal samples were sonicated in 1 % acetic acid,
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