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Algologia 2018, 28(4): 409–427
https://doi.org/10.15407/alg28.04.409
Ecology, Cenology, Conservation of Algae and Their Role in Nature

Chemical and molecular evidences for the poisoning of a duck by anatoxin-a, nodularin and cryptophycin at the coast of lake Shoormast (Mazandaran province, Iran)

Bahareh Nowruzi1, Saúl Blanco2, Taher Nejadsattari1
Abstract

The toxic cyanobacteria in aquatic ecosystems are a big concern especially in warm summer months. Animals are incapable of avoiding toxic blooms near the shore and might get poisoned. In this study the aim was to find a cause of death of a domestic duck found near the coastal area of the ShoorMast Lake. Cyanotoxin poisoning was suspected as the cause of fatalities, as a result, the water samples were collected and examined with phenotypic and genotypic analyses in order to find if the duck is poisoned by the toxic cyanobacteria. Different molecular and chemical methods such as phylogenetic analysis based on 16S rRNA gene sequence, polymerase chain reaction, disc diffusion bioassays and liquid chromatography-mass spectrometry were used. Based on the results, three different cyanobacteria strains were found in duck´s stomach and three diverse groups of potentially bioactive compounds (anatoxin-a, nodularin and cryptophycin) might account for the death of this animal. The cyanobacteria strains were identified and registered under DDBJ as Anabaena sp. BN KY303913, Nodularia sp. BN KY303914 and Nostoc sp. BN KY303912. This case is the first documented incident of toxicity from fresh water cyanobacteria related intoxication in Iran.

Keywords: anatoxin-a, cryptophycin, duck, nodularin, poiyanoyanosoning, ShoorMast Lake, Iran

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References
  1. Becker J.E., Moore R.F., Moore B.S. Cloning, sequencing, and biochemical characterization of the nosto-cyclopeptide biosynthetic gene cluster: molecular basis for imine macrocyclization. Gene. 2004. 325: 35–42. https://doi.org/10.1016/j.gene.2003.09.034 https://www.ncbi.nlm.nih.gov/pubmed/14697508
  2. Cadel-Six C., Peyraud-Thomas C., Brient L., Tandeau de Marsac N., Rippka R., Mejean A. Different genotypes of anatoxin producing cyanobacteria co-exist in the Tarn River, France. Appl. and Environ. Microbiol. 2007. 73: 7605–7614. https://doi.org/10.1128/AEM.01225-07 https://www.ncbi.nlm.nih.gov/pubmed/17933923 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2168053
  3. Carmichael W.W., Biggs D.F., Gorham P.R. Toxicology and pharmacological action of Anabaena flos-aquae toxin. Science. 1975. 187: 542–544. https://doi.org/10.1126/science.803708 https://www.ncbi.nlm.nih.gov/pubmed/803708
  4. Edwards C., Beattie K.A., Scrimgeour C.M., Codd G.A. Identification of anatoxin-a in benthic cyanobacteria (blue-green algae) and in associated dog poisonings at Loch Insh, Scotland. Toxicon. 1992. 30: 1165–1175. https://doi.org/10.1016/0041-0101(92)90432-5
  5. Fewer D., Jokela J., Rouhiainen L., Wahlsten M., Koskenniemi K., Stal L.J., Sivonen K. The non-ribosomal assembly and frequent occurrence of the protease inhibitors spumigins in the bloom-forming cyanobacterium Nodularia spumigena. Mol. Microbiol. 2009. 73(5): 924–937. https://doi.org/10.1111/j.1365-2958.2009.06816.x https://www.ncbi.nlm.nih.gov/pubmed/19691450
  6. Francis G. Poisonous Australian lake. Nature. 1878. 18: 11–12. https://doi.org/10.1038/018011d0
  7. Fujii K., Sivonen K., Kashiwagi T., Hirayama K., Harada K.I. Nostophycin, a novel cyclic peptide from the toxic cyanobacterium, Nostoc sp. 152. J. Org. Chem. 1999. 64: 5777–5782. https://doi.org/10.1021/jo982306i
  8. Golakoti T., Ogino J., Heltzel C.E., Husebo T.L., Jensen C.M., Larsen L.K., Patterson G.M.L., Moore R.E., Mooberry S.L., Corbett T.H., Valeriote F.A. Structure determination, conformational analysis, chemical stability studies and antitumor evaluation of the cryptophycins. Isolation of eighteen new analogs from Nostoc sp. strain GSV 224. J. Amer. Chem. Soc. 1994. 117(49): 12030–12049. https://doi.org/10.1021/ja00154a002
  9. Golakoti T., Ohtani I., Patterson D.J., Moore R.E., Corbett T.H., Valerlote F.A., Demchik L. Total structures of cryptophycins, potent antitumor depsipeptides from the blue green alga Nostoc sp. strain GSV 224. J. Amer. Chem. Soc. 1994. 116: 4729–4737. https://doi.org/10.1021/ja00090a020
  10. Gugger M., Lenoir S., Berger C., Ledreux A., Druart J.C., Humbert J.F., Guette C., Bernard C. First report in a river in France of the benthic cyanobacterium Phormidium favosum producing anatoxin-a associated with dog neurotoxicosis. Toxicon. 2005. 45: 919–928. https://doi.org/10.1016/j.toxicon.2005.02.031 https://www.ncbi.nlm.nih.gov/pubmed/15904687
  11. Gunn G.J., Rafferty A.G., Rafferty G.C. Fatal canine neurotoxicosis attributed to blue-green algae (cyanobacteria). Vet. Record. 1992. 130: 301–302. https://doi.org/10.1136/vr.130.14.301 https://www.ncbi.nlm.nih.gov/pubmed/1595148
  12. Halinen K., Fewer D.P., Sihvonen L.M., Lyra C., Eronen E., Sivonen K. Genetic diversity in strains of the genus Anabaena isolated from planktonic and benthic habitats of the Gulf of Finland (Baltic Sea). FEMS Microbiol. Ecol. 2008. 64: 99–108. https://doi.org/10.1111/j.1574-6941.2008.00461.x https://www.ncbi.nlm.nih.gov/pubmed/18336556
  13. Komárek J., Sant´Anna C.L., Bohunická M., Mareš J., Hentschke G.S., Rigonato J., Fioreet M.F. Phenotype diversity and phylogeny of selected Scytonema-species (Cyanoprokaryota) from SE Brazil. Fottea. 2013. 13(2): 173–200. https://doi.org/10.5507/fot.2013.015
  14. Koskenniemi K., Lyra C., Rajaniemi-Wacklin P., Jokela J., Sivonen K. Quantitative real-time PCR detection of toxic Nodularia cyanobacteria in the Baltic Sea. Appl. and Environ. Microbiol. 2007. 73: 2173–2179. https://doi.org/10.1128/AEM.02746-06 https://www.ncbi.nlm.nih.gov/pubmed/17277219 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1855639
  15. Leikoski N., Fewer D.P., Jokela J., Wahlsten M., Rouhiainen L., Sivonen K. Highly diverse cyanobactins in strains of the genus Anabaena. Appl. and Environ. Microbiol. 2010. 76: 701–709. https://doi.org/10.1128/AEM.01061-09 https://www.ncbi.nlm.nih.gov/pubmed/20008171 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2813007
  16. Liang J., Moore R.E., Moher E.D., Munroe J.E., Al-awar R.S., Hay D.A., Varie D.L., Zhang T.Y., Aikins J.A., Martinelli M.J., Shih C., Ray J.E., Gibson L.L., Vasudevan V., Polin L., White K., Kushner J., Simpson C., Pugh S., Corbett T.H. Cryptophycins 309, 249 and other cryptophycin analogs: Preclinical efficay studies with mouse and human tumors. Invest New Drugs. 2005. 23(3): 213–224. https://doi.org/10.1007/s10637-005-6729-9 https://www.ncbi.nlm.nih.gov/pubmed/15868377
  17. Liu L., Jokela J., Fewer D., Wahlsten M., Permi P., Sivonen K. Nostoginosins: trypsin inhibitors from Nostoc sp. strain FSN. J. Nat. Prod. 2015. 77(8): 1784–1790. https://doi.org/10.1021/np500106w https://www.ncbi.nlm.nih.gov/pubmed/25069058
  18. Liu L., Jokela J., Herfindal L., Wahlsten M., Sinkkonen J., Permi P., Sivonen K. 4-methylproline guided natural product discovery: Co-occurrence of 4-hydroxy- and 4-methylprolines in nostoweipeptins and nostopeptolides. ACS Chem. Biol. 2014. 9(11): 2646–2655. https://doi.org/10.1021/cb500436p https://www.ncbi.nlm.nih.gov/pubmed/25203327
  19. Luesch H., Hoffmann D., Hevel J.M., Becker J.E., Golakoti T., Moore R.E. Biosynthesis of 4-Methylproline in Cyanobacteria: Cloning of nosE and nosF Genes and Biochemical Characterization of the Encoded Dehydrogenase and Reductase Activities. J. Org. Chem. 2003. 68: 83–91. https://doi.org/10.1021/jo026479q https://www.ncbi.nlm.nih.gov/pubmed/12515465
  20. Msagati T.A.M., Siame B.A., Shushu D.D. Evaluation of methods for the isolation, detection and quantification of cyanobacterial hepatotoxins. Aquat. Toxicol. 2006. 78: 382–397. https://doi.org/10.1016/j.aquatox.2006.03.011 https://www.ncbi.nlm.nih.gov/pubmed/16757036
  21. Nowruzi B., Khavari-Nejad R.-A., Sivonen K., Kazemi B., Najafi F., Nejadsattari T. Identification and toxigenic potential of a Nostoc sp. Algae. 2012. 27(4): 303–313. https://doi.org/10.4490/algae.2012.27.4.303
  22. Nowruzi B., Khavari-Nejad R.A., Sivonen K., Kazemi B., Najafi F., Nejadsattari T. Identification and toxigenic potential of a cyanobacterial strain (Stigomena sp.). Prog. Biol. Sci. 2013. 3(1): 79–85.
  23. Nübel U., Garcia Pichel F., Muyzer G. PCR primers to amplify 16S rRNA genes from cyanobacteria. Appl. and Environ. Microbiol. 1997. 63: 3327–3332. https://www.ncbi.nlm.nih.gov/pubmed/9251225 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC168636
  24. Oksanen I., Jokela J., Fewer D.P., Wahlsten M., Rikkinen J., Sivonen K. Discovery of Rare and Highly Toxic Microcystins from Lichen-Associated Cyanobacterium Nostoc sp. Strain IO-102-I. Appl. and Environ. Microbiol. 2004. 70(10): 5756–5763. https://doi.org/10.1128/AEM.70.10.5756-5763.2004 https://www.ncbi.nlm.nih.gov/pubmed/15466511 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC522101
  25. Onodera H., Oshima Y., Henriksen P., Yasumoto T. Confirmation of anatoxin-A(S), in the cyanobacterium Anabaena lemmermannii, as the cause of bird kills in Danish lakes. Toxicon. 1997. 35: 1645–1648. https://doi.org/10.1016/S0041-0101(97)00038-X
  26. Puschner B., Hoff B., Tor E.R. Diagnosis of anatoxin-a poisoning in dogs from North America. J. Vet. Diag. Invest. 2008. 20(1): 89–92. https://doi.org/10.1177/104063870802000119 https://www.ncbi.nlm.nih.gov/pubmed/18182518
  27. Rajaniemi P., Hrouzek P., Kastovska K., Willame R., Rantala A., Hoffmann L., Komarek J., Sivonen K. Phylogenetic and morphological evaluation of the genera Anabaena, Aphanizomenon, Trichormus and Nostoc (Nostocales, Cyanobacteria). Int. J. Syst. and Evol. Microbiol. 2005. 55: 11–26. https://doi.org/10.1099/ijs.0.63276-0 https://www.ncbi.nlm.nih.gov/pubmed/15653847
  28. Sivonen K. Cyanobacterial toxins. Encycl. Microbiol. 2009: 290–307. https://doi.org/10.1016/B978-012373944-5.00005-5
  29. Sivonen K., Börner T. Bioactive compounds produced by cyanobacteria. In: The cyanobacteria: molecular biology, genomics and evolution. Norfolk: Caister Acad. Press, 2008. Pp. 159–197.
  30. Sivonen K., Jones G.J. Cyanobacterial toxins. In: Toxic Cyanobacteria in Water. A Guide to their Public Health Consequences, Monitoring and Management. London: E.F.N. Spon, 1999. Pp. 41–111.
  31. Sivonen K., Leikoski N., Fewer D.P., Jokela J. Cyanobactins – ribosomal cyclic peptides produced by cyanobacteria. Appl. and Environ. Microbiol. 2010. 86: 1213–1225.
  32. Sivonen K., Namikoshi M., Evans W.R., Carmichael W.W., Sun F. Isolation and characterization of a variety of microcystins from seven strains of the cyanobacterial genus Anabaena. Appl. and Environ. Microbiol. 1992. 58: 2495–2500. https://www.ncbi.nlm.nih.gov/pubmed/1514796 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC195810
  33. Sivonen K., Carmichael W.W., Namikoshi M., Rinehart K.L., Dahlem A.M., Niemelä S.I. Isolation and characterisation of hepatotoxic microcystin homologues from the filamentous freshwaters cyanobacterium Nostoc sp. 152. Appl. and Environ. Microbiol. 1990. 56: 2650–2657. https://www.ncbi.nlm.nih.gov/pubmed/2125813 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC184822
  34. Sivonen K., Himberg K., Luukkainen R., Niemelä S.I., Poon G.K., Codd G.A. Preliminary characterization of neurotoxic cyanobacteria blooms and strains from Finland. Toxic. Assess. 1989. 4: 339–352. https://doi.org/10.1002/tox.2540040310
  35. Van Apeldoorn M.E., van Egmond H.P., Speijers G.J., Bakker G.J. Toxins of cyanobacteria. Mol. Nutr. & Food Res. 2007. 51: 7–60. https://doi.org/10.1002/mnfr.200600185 https://www.ncbi.nlm.nih.gov/pubmed/17195276
  36. Wood S.A., Selwood A.I., Rueckert A. First report of homoanatoxin-a and associated dog neurotoxicosis in New Zealand. Toxicon. 2007. 50: 292–301. https://doi.org/10.1016/j.toxicon.2007.03.025 https://www.ncbi.nlm.nih.gov/pubmed/17517427
  37. Ylinen-Rantala A., Känä S., Wang H., Rouhiainen L., Wahlsten M., Rizzi E., Berg K., Gugger M., Sivonen K. Anatoxin-a synthetase gene cluster of the cyanobacterium Anabaena sp. strain 37 and molecular methods to detect potential producers. Appl. and Environ. Microbiol. 2011. 77: 7271–7278. https://doi.org/10.1128/AEM.06022-11 https://www.ncbi.nlm.nih.gov/pubmed/21873484 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3194866