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Cyanotoxin contamination of semiarid drinking water supply reservoirs

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Abstract

Changing global climatic conditions and the continuous eutrophication of aquatic ecosystems have led to increased frequency, duration and toxicity of cyanobacterial blooms worldwide. This makes the provision of time series information on cyanotoxins extremely crucial for effective monitoring and management of water resources. The objective of the present study was to investigate seasonal and annual changes in microcystins (MCs), cylindrospermopsins (CYNs), saxitoxins (STXs), neo-saxitoxin (neo-STX) and anatoxin-a (ATX-a) concentrations in 11 public water supply reservoirs in the semiarid region of Brazil, from 2004 to 2011. Per time, at least one cyanotoxin was present in all the investigated reservoirs. High levels of MCs, CYNs, STXs and Neo-STX were detected simultaneously in Carpina, Duas Unas, Ipojuca, and Jucazinho reservoirs. All the investigated reservoirs had significant concentrations of MCs. The highest levels of MCs were found in Carpina (303,300.0 ng g−1) and Duas Unas (122,053.9 ng g−1) reservoirs, while the lowest concentration of the hepatotoxins was recorded in Ipojuca (10.3 ng g−1) reservoir. On the other hand, CYN was detected in four reservoirs, STXs and Neo-STX in ten reservoirs and ATX-a in two reservoirs. The first record of CYN in Carpina reservoir was obtained in 2006. In addition, Carpina reservoir had the highest concentration of STXs and Neo-STX in the dry and rainy seasons, respectively. The high concentration of cyanotoxins observed in most samples obtained from semiarid reservoirs in Brazil demonstrates the need for regular monitoring and updated management programs.

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Abbreviations

ATX-a:

Anatoxin-a

neo-STX:

Neo-saxitoxin

CYNs:

Cylindrospermopsins

MCs:

Microcystins

STXs:

Saxitoxins

References

  • Adeymo OM, Sirén AL (1992) Cardio-respiratory changes and mortality in the conscious rat induced by (+)- and (±)-anatoxin-a. Toxicon 30:899–905

    Article  Google Scholar 

  • Almeida VLS, Dantas EW, Melo-Júnior M, Bittencourt-Oliveira MC, Moura AN (2009) Zooplanktonic community of six reservoirs in northeast Brazil. Braz J Biol 69:57–65

    Article  Google Scholar 

  • Azevedo SMFO, Carmichael WW, Jochimsen EM, Rinehart KL, Lau S, Shaw GR, Eaglesham GK (2002) Human intoxication by microcystin during renal dialysis treatment in Caruaru. Toxicology 181–182:441–446

    Article  Google Scholar 

  • Babica P, Kohoutek J, Bláha L, Adamovsky O, Marsálek B (2006) Evaluation of extraction approaches linked to ELISA and HPLC for analyses of microcystin-LR, -RR and -YR in freshwater sediments with different organic material contents. Anal Bioanal Chem 85:1545–1551

    Article  Google Scholar 

  • Ballot A, Fastner J, Wiedner C (2010) Paralytic shellfish poisoning toxin-producing cyanobacterium aphanizomenon gracile in northeast Germany. Appl Environ Microbiol 76:1173–1180

    Article  Google Scholar 

  • Bittencourt-Oliveira MC, Piccin-Santos V, Kujbida P, Moura AN (2011a) Cylindrospermopsin in water supply reservoirs in Brazil determined by immunochemical and molecular methods. J Water Resour Prot 3:349–355

    Article  Google Scholar 

  • Bittencourt-Oliveira MC, Moura AN, Hereman TC, Dantas EW (2011b) Increase in straight and coiled Cylindrospermopsis raciborskii (Cyanobacteria) populations under conditions of thermal de-stratification in a shallow tropical reservoir. J Water Resour Prot 3:245–252

    Article  Google Scholar 

  • Bittencourt-Oliveira MC, Dias SN, Moura AN, Cordeiro-Araújo MK, Dantas EW (2012) Seasonal dynamics of cyanobacteria in a eutrophic reservoir (Arcoverde) in the semi-arid region of Brazil. Braz J Biol 72:533–544

    Article  Google Scholar 

  • Bittencourt-Oliveira MC, Piccin-Santos V, Moura AN, Aragão-Tavares NKC, Cordeiro-Araújo MK (2014) Cyanobacteria, microcystins and cylindrospermopsin in public drinking supply reservoirs of Brazil. An Acad Bras Cienc 86:297–309

    Article  Google Scholar 

  • Bláhová L, Oravec M, Marsálek B, Sejnohová L, Simek Z, Bláha L (2009) The first occurrence of the cyanobacterial alkaloi toxin cylindrospermopsin in the Czech Republic as determined by immunochemical and LC/MS methods. Toxicon 53:519–524

    Article  Google Scholar 

  • Bouvy M, Falcão D, Marinho M, Pagano M, Moura A (2000) Occurrence of Cylindrospermopsis (Cyanobacteria) in 39 Brazilian Tropical Reservoirs during the 1998 Drought. Aquat Microb Ecol 23:13–27

    Article  Google Scholar 

  • Bouvy M, Nascimento SM, Molica RJR, Ferreira A, Huszar V, Azevedo SMFO (2003) Limnological features in Tapacurá reservoir (northeast Brazil) during a severe drought. Hydrobiologia 493:115–130

    Article  Google Scholar 

  • Brasil (2011) Ministério da Saúde. Portaria No 2914, 12 de dezembro de 2011. Diário Oficial da República Federativa do Brasil, Poder Executivo, Brasília, DF, 12 dez. Seção 1, pp 39–46

  • Bricelj VM, Connell L, Konoki K, Mac Quarrie SP, Scheuer T, Catterall WA et al (2005) Sodium channel mutation leading to saxitoxin resistance in clams increases risk of PSP. Nature 434:763–767

    Article  Google Scholar 

  • Carmichael WW (1994) The toxins of cyanobacteria. Sci Am 270:78–86

    Article  Google Scholar 

  • Chellappa NT, Câmara FRA, Rocha O (2009) Phytoplankton community: indicator of water quality in the Armando Ribeiro Gonçalves Reservoir and Pataxó Channel, Rio Grande do Norte, Brazil. Braz J Biol 69:241–251

    Article  Google Scholar 

  • Costa IAS, Azevedo SMFO, Senna PAC, Bernardo RR, Costa SM, Chellappa NT (2006) Occurrence of toxin-producing cyanobacteria blooms in a Brazilian semiarid reservoir. Braz J Biol 66:211–219

    Article  Google Scholar 

  • Dantas EW, Moura AN, Bittencourt -Oliveira MC (2011) Cyanobacterial blooms in stratified and destratified eutrophic reservoirs in semi-arid region of Brazil. An Acad Bras Cienc 83:1327–1338

    Article  Google Scholar 

  • Devlin JP, Edwards OE, Gorham PR, Hunter NR, Pike RK, Stavric B (1977) Anatoxin-a, a toxic alkaloid from Anabaena-flos-aquae NRC-44H. Can J Chem 55:1367–1371

    Article  Google Scholar 

  • Ding W-X, Shen H-M, Zhu H-G, Lee B-L, Ong C-N (1999) Genotoxicity of microcystic cyanobacteria extract of a water source in China. Mutat Res 442:69–77

    Article  Google Scholar 

  • Dörr FA, Rodríguez V, Molica R, Henriksen P, Krock B, Pinto E (2010) Methods for detection of anatoxin-a (s) by liquid chromatography coupled to electrospray ionization-tandem mass spectrometry. Toxicon 55:92–99

    Article  Google Scholar 

  • Fonseca JR, Vieira PCS, Kujbida P, Costa da, I. A. S (2015) Cyanobacterial occurrence and detection of microcystins and saxitoxins in reservoirs of the Brazilian semi-arid. Acta Limnol Bras 27:78–92

    Article  Google Scholar 

  • Foss AJ, Aubel MT (2015) Using the MMPB technique to confirm microcystin concentrations in water measured by ELISA and HPLC (UV, MS, MS/MS). Toxicon 104:91–101

    Article  Google Scholar 

  • Froscio SM, Humpage AR, Burcham PC, Falconer IR (2003) Cylindrospermopsin-induced protein synthesis inhibition and its dissociation from acute toxicity in mouse hepatocytes. Environ Toxicol 18:243–251

    Article  Google Scholar 

  • Furtado ALFF, Calijuri MC, Lorenzi AS, Honda RY, Genuário DB, Fiore MF (2009) Morphological and molecular characterization of cyanobacteria from a Brazilian facultative wastewater stabilization pond and evaluation of microcystin production. Hydrobiologia 627:195–209

    Article  Google Scholar 

  • Genuário DB, Silva-Stenico ME, Welker M, Beraldo Moraes LA, Fiore MF (2010) Characterization of a microcystin and detection of microcystin synthetase genes from a Brazilian isolate of Nostoc. Toxicon 55:846–854

    Article  Google Scholar 

  • Genuário DB, Lorenzi AS, Agujaro LF, Isaac RL, Azevedo MTP, Cantúsio Neto R, Fiore MF (2016) Cyanobacterial community and microcystin production in a recreational reservoir with constant Microcystis blooms. Hydrobiologia 779:105–125

    Article  Google Scholar 

  • Henrie T, Plummer S, Roberson JA (2017) Occurrence and state approaches for addressing cyanotoxins in US drinking water. J Am Water Works Assoc 109:40–47

    Article  Google Scholar 

  • Jochimsen EM, Carmichael WW, An J, Cardo DM, Cookson ST, Holmes CE, Antunes BC, Filho M, Lyra DA, Barreto TM, Azevedo VST, S. M. F. O., and Jarvis WR (1998) Liver failure and death after exposure to microcystins at a hemodialysis center in Brazil. N Engl J Med 338:873–878

    Article  Google Scholar 

  • Lagos N, Onodera H, Zagatto PA, Andrinolo D, Azevedo SMFO, Oshima Y (1999) The first evidence of paralytic shellfish toxins in the freshwater cyanobacterium Cylindrospermopsis raciborskii, isolated from Brazil. Toxicon 37:1359–1373

    Article  Google Scholar 

  • Lira GAST, Araújo EL, Bittencourt-Oliveira MC, Moura AN (2011) Phytoplankton abundance, dominance and coexistence in an eutrophic reservoir in the state of Pernambuco, Northeast Brazil. An Acad Bras Cienc 83:1313–1326

    Article  Google Scholar 

  • Matsunaga S, Moore RE, Niemczura WP, Carmichael WW (1989) Anatoxin-a(s), a potent anticholinesterase from Anabena flos-aquae. J Am Chem Soc 111:8021–8023

    Article  Google Scholar 

  • Meriluoto J, Spoof L, Codd GA (eds) (2017) Handbook of cyanobacterial monitoring and cyanotoxin analysis. Wiley, New York

    Google Scholar 

  • Metcalf JS, Codd GA (2014) Cyanobacterial toxins (cyanotoxins) in water. In: Foundation for Water Research, Marlow, Bucks, UK

    Google Scholar 

  • Metcalf JS, Bell SG, Codd GA (2000a) Production of novel polyclonal antibodies against the cyanobacterial toxin microcystin-LR and their application for the detection and quantification of microcystins and nodularin. Water Res 34:2761–2769

    Article  Google Scholar 

  • Metcalf JS, Hyenstrand P, Beattie KA, Codd GA (2000b) Effects of physicochemical variables and cyanobacterial extracts on the immunoassay of microcystin-LR by two ELISA kits. J Appl Microbiol 89:532–538

    Article  Google Scholar 

  • Molica RJR, Oliveira EJA, Carvalho PVVC, Costa ANSF, Cunha MCC, Melo GL, Azevedo SMFO (2005) Occurrence of saxitoxins and an anatoxin-a(s)-like anticholinesterase in a Brazilian drinking water supply. Harmful Algae 4:743–753

    Article  Google Scholar 

  • Moura AN, Dantas EW, Oliveira HSB, Bittencourt-Oliveira MC (2011) Vertical and temporal dynamics of cyanobacteria in the Carpina potable water reservoir in Northeastern Brazilian. J Biol 71:451–459

    Google Scholar 

  • Negri AP, Jones GJ, Hindmarsh M (1995) Sheep mortality associated with paralytic shellfish poisons from the cyanobacterium Anabaena circinalis. Toxicon 33:1321–1329

    Article  Google Scholar 

  • Neilan BA, Pearson LA, Muenchhoff L, Moffitt MC, Dittmann E (2013) Environmental conditions that influence toxin biosynthesis in cyanobacteria. Environ Microbiol 15:1239–1253

    Article  Google Scholar 

  • O’Neil J, Davis T, Burford M, Gobler C (2012) The rise of harmful cyanobacteria blooms: the potential roles of eutrophication and climate change. Harmful Algae 14:312–334

    Article  Google Scholar 

  • Ohtani I, Moore RE, Runnegar MTC (1992) Cylindrospermopsin, a potent hepatotoxin from the blue-green-alga Cylindrospermopsis raciborskii. J Am Chem Soc 114:7941–7942

    Article  Google Scholar 

  • Paerl HW, Hall NS, Calandrino ES (2011) Controlling harmful cyanobacterial blooms in a world experiencing anthropogenic and climatic-induced change. Sci Total Environ 409:1739–1745

    Article  Google Scholar 

  • Pearson LA, Dittmann E, Mazmouz R, Ongley SE, D’Agostino PM, Neilan BA (2016) The genetics, biosynthesis and regulation of toxic specialized metabolites of cyanobacteria. Harmful Algae 54:98–111

    Article  Google Scholar 

  • Piccin-Santos V, Bittencourt-Oliveira MC (2012) Toxic cyanobacteria in four Brazilian water supply reservoirs. J Environ Prot 3:68–73

    Article  Google Scholar 

  • Rastogi RP, Sinha RP, Incharoensakdi A (2014) The cyanotoxin microcystins: current overview. Rev Environ Sci Bio/Technol 13:215–249

    Article  Google Scholar 

  • Ren Y, Yang M, Chen M, Zhu Q, Zhou L, Qin W, Wang T (2017) Microcystin-LR promotes epithelial-mesenchymal transition in colorectal cancer cells through PI3-K/AKT and SMAD2. Toxicol Lett 265:53–60

    Article  Google Scholar 

  • Runnegar M, Berndt N, Kong SM, Lee EYC, Zhang LF (1995) In-vivo and in-vitro binding of microcystin to protein phosphatase-1 and phosphatase-2A. Biochem Biophys Res Commun 216:162–169

    Article  Google Scholar 

  • Shimizu Y (1986) Toxigenesis and biosynthesis of saxitoxin analogs. Pure Appl Chem 58:257–262

    Article  Google Scholar 

  • Silva-Stenico ME, Cantúsio Neto R, Alves IR, Moraes LAB, Shishido TK, Fiore MF (2009) Hepatotoxin microcystin-LR extraction optimization. J Braz Chem Soc 20:535–542

    Article  Google Scholar 

  • Silva-Stenico ME, Silva CSP, Lorenzi AS, Shishido TK, Etchegaray A, Lira SP, Moraes LAB, Fiore MF (2011) Non-ribosomal peptides produced by Brazilian cyanobacterial isolates with antimicrobial activity. Microbiol Res 166:161–175

    Article  Google Scholar 

  • Sivonen K, Börner T (2008) Bioactive compounds produced by cyanobacteria. In: Herrero A, Flores E (eds) The cyanobacteria: molecular biology, genomics and evolution. Caister Academic Press, Norfolk, pp 159–197

    Google Scholar 

  • Sivonen K, Jones GJ (1999) Cyanobacterial toxins. In: Chorus I, Bartram J (eds) Toxic cyanobacteria in water. WHO, Spon Press, London, pp 41–111

    Google Scholar 

  • SRH—Secretaria de Recursos Hídricos de Pernambuco (2000) Plano Estadual de Recursos Hídricos do Estado de Pernambuco—Documento Síntese, Recife

  • Su Z, Sheets M, Ishida H, Li F, Barry WH (2004) Saxitoxin blocks L-type ICa. J Pharmacol Exp Ther 308:324–329

    Article  Google Scholar 

  • Terao K, Ohmori S, Igarashi K, Ohtani I, Watanabe MF, Harada KI et al (1994) Electron-microscopic studies on experimental poisoning in mice induced by cylindrospermopsin isolated from blue-green-alga, Umezakia natans. Toxicon 32:833–843

    Article  Google Scholar 

  • Trout-Haney JV, Wood ZT, Cottingham KL (2016) Presence of the cyanotoxin microcystin in Arctic Lakes of southwestern Greenland. Toxins (Basel) 8:256

    Article  Google Scholar 

  • Ueno Y, Nagata S, Tsutsumi T, Hasegawa A, Watanabe MF, Park HD, Chen G-C, Chen G, Yu S-Z (1996) 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. Carcinogenesis 17:1317–1321

    Article  Google Scholar 

  • Wang J, Salata JJ, Bennett PB (2003) Saxitoxin is a gating modifier of HERG K+ channels. J Gen Physiol 121:583–598

    Article  Google Scholar 

  • Wiese M, D’agostino PM, Mihali TK, Moffitt MC, Neilan BA (2010) Neurotoxic alkaloids: saxitoxin and its analogs. Mar Drugs 8:2185–2211

    Article  Google Scholar 

  • Wood SA, Mountfort D, Selwood AI, Holland PT, Puddick J, Cary SC (2008) Widespread distribution and identification of eight novel microcystins in antarctic cyanobacterial mats. Appl Environ Microbiol 74:7243–7251

    Article  Google Scholar 

  • Zhou L, Yu H, Chen K (2002) Relationship between microcystin in drinking water and colorectal cancer. Biomed Environ Sci 15:166–171

    Google Scholar 

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Acknowledgements

This study was sponsored by grant from the Brazilian National Council for Scientific and Technological Development—CNPq (Proc. 576890/2008-1). A.S.L., M.K.C.A and M.A.C were supported by FAPESP post-doctoral fellowships (Grant 2014/01913-2, 15/17397-6 and 2013/11306-3, respectively).

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Authors and Affiliations

  1. Department of Biological Sciences, Luiz de Queiroz College of Agriculture, University of São Paulo (USP), Piracicaba, SP, Brazil

    Adriana Sturion Lorenzi, Micheline Kézia Cordeiro-Araújo & Maria do Carmo Bittencourt-Oliveira

  2. Department of Botany, Ahmadu Bello University, Zaria, Nigeria

    Mathias Ahii Chia

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  1. Adriana Sturion Lorenzi
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  2. Micheline Kézia Cordeiro-Araújo
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  3. Mathias Ahii Chia
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  4. Maria do Carmo Bittencourt-Oliveira
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Contributions

MKCA and MCBO conceived and designed the study. ASL, MKCA and MAC analyzed the data. ASL, MKCA, MAC and MCBO wrote the manuscript.

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Correspondence to Maria do Carmo Bittencourt-Oliveira.

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Lorenzi, A.S., Cordeiro-Araújo, M.K., Chia, M.A. et al. Cyanotoxin contamination of semiarid drinking water supply reservoirs. Environ Earth Sci 77, 595 (2018). https://doi.org/10.1007/s12665-018-7774-y

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