Microcystin producing cyanobacterial communities in Amvrakikos Gulf (Mediterranean Sea, NW Greece) and toxin accumulation in mussels (Mytilus galloprovincialis)

Harmful Algae

Volumn 15, Issue , 2012, Pages 109-118

  Vareli, Katerina ^a   Zarali, Ekaterini ^b   Zacharioudakis, Georgios S A ^c,d   Vagenas, Georgios ^e   Varelis, Vasileios ^b   Pilidis, George ^a   Briasoulis, Evangelos ^a,b   Sainis, Ioannis ^a  

^a UNIVERSITY OF IOANNINA   (Greece)

^b UNIVERSITY OF IOANNINA   (Greece)

^c UNIVERSITY OF ATHENS   (Greece)

^d NeoLab SA   (Greece)

^e General Chemical State Laboratory   (Greece)

Author keywords

Amvrakikos gulf; Cyanobacteria; Cyanobacterial toxins; Marine ecosystem; Mediterranean sea; Microcystin LR; Microcystin YR; Microcystins; Synechococcus sp.; Synechocystis sp.

Indexed keywords

CYANOBACTERIA; MYTILUS GALLOPROVINCIALIS; SYNECHOCOCCUS; SYNECHOCOCCUS SP.; SYNECHOCYSTIS; SYNECHOCYSTIS SP.;

EID: 84857361091     PISSN: 15689883     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.hal.2011.12.005     Document Type: Article

References (77)

1. Ahern K.S., Ahern C.R., Udy J.W. In situ field experiment shows Lyngbya majuscula (cyanobacterium) growth stimulated by added iron, phosphorus and nitrogen. Harmful Algae 2007, 7:389-404.
2. Ahlgren N.A., Rocap G. Culture isolation and culture independent clone libraries reveal new marine Synechococcus ecotypes with distinctive light and N physiologies. Appl. Environ. Microbiol. 2006, 72:7193-7204.
3. Amorim A., Vasconcelos V. Dynamics of microcystins in the mussel Mytilus galloprovincialis. Toxicon 1999, 37:1041-1052.
4. Andersen R.J., Luu H.A., Chen D.Z.X., Holmes C.F.B., Kent M., LeBlanc M., Taylor F.J.R., Williams D.E. Chemical and biological evidence links microcystins to salmon netpen liver disease. Toxicon 1993, 31:1315L 1323.
5. APHA, AWWA, WPCF Standard Methods for the Examination of Water and Wastewater 2005, American Public Health Association, Washington, DC, USA. 21st ed.
6. Ballot A., Pflugmacher S., Weigand C., Kotut K., Krause E., Metcalf J.S., Morrison L.F., Codd G.A., Krienitz L. Cyanobacterial toxins, a further contributory cause of mass deaths of flamingos at Kenyan rift valley lakes. Proceedings of the Xth International Conference on Harmful Algae 2002.
7. Briand J.F., Jacquet S., Bernard C., Humbert J.F. Health hazards for terrestrial vertebrates from toxic cyanobacteria in surface water ecosystems. Vet. Res. 2003, 34:361-377.
8. Camargo J.A., Alonso A. Ecological and toxicological effects of inorganic nitrogen pollution in aquatic ecosystems: a global assessment. Environ. Int. 2006, 32:831-849.
9. Carmichael W.W., Falconer I.R. Diseases related to freshwater blue-green algal toxins, and control measures. Algal Toxins in Seafood and Drinking Water 1993, 187-209. Academic Press, San Diego, CA. I.R. Falconer (Ed.).
10. Carmichael W.W. The toxins of cyanobacteria. Sci. Am. 1994, 270:78-86.
11. Carmichael W.W., Azevedo S.M., An J.S., Molica R.J., Jochimsen E.M., Lau S., Rinehart K.L., Shaw G.R., Eaglesham G.K. Human fatalities from cyanobacteria: chemical and biological evidence for cyanotoxins. Environ. Health Perspect. 2001, 109:663-668.
12. Carmichael W.W., Li R.-H. Cyanobacteria toxins in the Salton Sea. Saline Syst. 2006, 2:5. 10.1186/1746-1448-2-5.
13. Chen Z.X.D., Boland P.M., Smillie A.M., Klix H., Ptak C., Andersen J.R., Holmes B.F.C. Identification of protein phosphatase inhibitors of the microcystin class in the marine environment. Toxicon 1993, 31(11):1407-1414.
14. Choi D.H., Noh J.H. Phylogenetic diversity of Synechococcus strains isolated from the East China Sea and the East Sea. FEMS Microbiol. Ecol. 2009, 69:439-448.
15. Christiansen G., Fastner J., Erhard M., Borner T., Dittmann E. Microcystin biosynthesis in Planktothrix: genes, evolution, and manipulation. J. Bacteriol. 2003, 185:564-572.
16. Codd G.A., Morrison L.F., Metcalf J.S. Cyanobacterial toxin: risk management for health protection. Toxicol. Appl. Pharmacol. 2005, 203(3):264-272.
17. Dahl E., Aune T., Aase B. Reddish water due to mass occurrences of Dinophysis sp. Harmful and Toxic Algae Blooms 1996, 101-104. Intergovernmental Oceanographic Commission of UNESCO. T. Yasumoto, Y. Oshima, Y. Fukayo (Eds.).
18. Dawson R.M. The toxicology of microcystins. Toxicon 1998, 36:953-962.
19. Driscoll C.P., McGowan P.C., Miller E.A., Carmichael W.W. Case Report: great blue heron (Ardea herodias) morbidity and mortality investigation in Maryland's Chesapeake Bay. Proceedings of the Southeast Fish and Wildlife Conference Baltimore 2002.
20. Economou V., Papadopoulou C., Brett M., Kansouzidou A., Charalabopoulos K., Filioussis G., Seferiadis K. Diarrheic shellfish poisoning due to toxic mussel consumption: the first recorded outbreak in Greece. Food Addit. Contam. A 2007, 24(3):297-305.
21. Falconer I.R., Humpage A.R. Health risk assessment of cyanobacterial (blue-green algal) toxins in drinking water. Int. J. Environ. Res. Public Health. 2005, 2:43-50.
22. Frazao B., Martins R., Vasconcelos V. Are known cyanotoxins involved in the toxicity of picoplanktonic and filamentous North Atlantic marine cyanobacteria?. Mar. Drugs 2010, 8:1906-1919.
23. Garcia C.A., Bargu S., Dash P., Rabalais N.N., Sutor M., Morrison W., Walker D.N. Evaluating the potential risk of microcystins to blue crab (Callinectes sapidus) fisheries and human health in a eutrophic estuary. Harmful Algae 2010, 9:134-143.
24. Glas S.M., Motti A.C., Negri P.A., Sato Y., Froscio S., Humpage R.A., Krock B., Cembella A., Bourne G.D. Cyanotoxins are not implicated in the etiology of coral black band disease outbreaks on Pelorus Island, Great Barrier Reef. FEMS Microbiol. Ecol. 2010, 73:43-54.
25. Gobler J.C., Davis W.T., Coyne J.K., Boyer G.L. Interacting influences of nutrient loading, zooplankton grazing, and microcystin synthetase gene expression on cyanobacterial bloom dynamics in a eutrophic New York lake. Harmful Algae 2007, 6:119-133.
26. Hawkins P.R., Runnegar M.T., Jackson A.B., Falconer I.R. Severe hepatotoxicity caused by the tropical cyanobacterium (blue-green algae) Cylindrospermopsis raciborskii (Woloszynska) Seenaya and Subba Raju isolated from a domestic water supply reservoir. Appl. Environ. Microbiol. 1985, 50:1292-1295.
27. Hisbergues M., Christiansen G., Rouhiainen L., Sivonen K., Borner T. PCR-based identification of microcystin producing genotypes of different cyanobacterial genera. Arch. Microbiol. 2003, 180:402-410.
28. Ignatiades L., Gotsis-Skretas O. A review on toxic and harmful algae in Greek Coastal Waters (E. Mediterranean Sea). Toxins 2010, 2:1019-1037.
29. Jacquet C., Thermes V., de Luze A., Puiseux-Dao S., Bernard C., Joly J.S., Bourrat F., Edery M. Effects of microcystin-LR on development of medaka fish embryos (Oryzias latipes). Toxicon 2004, 43:141-147.
30. Janse I., Meima M., Kardinaal W.E., Zwart G. High-resolution differentiation of Cyanobacteria by using rRNA-internal transcribed spacer denaturing gradient gel electrophoresis. Appl. Environ. Microbiol. 2003, 69:6634-6643.
31. Jochimsen E.M., Carmichael W.W., An J.S., Cardo D.M., Cookson S.T., Holmes C.E., Antunes M.B., De Melo Filho D.A., Lyra T.M., Barreto V.S., Azevedo S.M., Jarvis W.R. Liver failure and death after exposure to microcystins at a hemodialysis center in Brazil. N. Engl. J. Med. 1998, 338:873-878.
32. Kaebernick M., Neilan B.A., Borner T., Dittmann E. Light and the transcriptional response of the microcystin biosynthesis gene cluster. Appl. Environ. Microbiol. 2000, 66(8):3387-3392.
33. Kankaanpaa H.T., Sjovall O., Huttunen M., Olin M., Karlsson K., Hyvarinen K., Sneitz L., Harkonen J., Sipia V.O., Meriluoto J.A.O. Production and sedimentation of peptide toxins nodularin-R and microcystin-LR in the northern Baltic Sea. Environ. Pollut. 2009, 157:1301-1309.
34. Karlsson K., Kankaanpää H., Huttunen M., Meriluoto J. First observation of microcystin-LR in pelagic cyanobacterial blooms in the northern Baltic Sea. Harmful Algae 2005, 4:163-166.
35. Karlsson K.M., Spoof L.E., Meriluoto J.A. Quantitative LC-ESI-MS analyses of microcystins and nodularin-R in animal tissue-matrix effects and method validation. Environ. Toxicol. 2005, 20:381-389.
36. Korelusova J., Kastovsky J., Komarek J. Heterogeneity of the cyanobacterial genus Synechocystis and description of a new genus, Geminocystis. J. Phycol. 2009, 45:928-937.
37. Kurmayer R., Christiansen G. The genetic basis of toxin production in Cyanobacteria. Freshwater Rev. 2009, 2:31-50.
38. Langston W.J., Spence S.K. Biological factors involved in metal concentrations observed in aquatic organisms. Metal Speciation and Bioavailability in Aquatic Systems 1995, Wiley & Sons, N.Y. A. Tessier, D.R. Turner (Eds.).
39. Long B.M., Jones G.J., Orr P.T. Cellular microcystin content in N-limited Microcystis aeruginosa can be predicted from growth rate. Appl. Environ. Microbiol. 2001, 67(1):278-283.
40. Lukac M., Aegerter R. Influence of trace metals on growth and toxin production of Microcystis aeruginosa. Toxicon 1993, 31(3):293-305.
41. Madenwald N.D. Effect of water temperature on the loss of PSP from the butter clam Saxidomus giganteus. Toxic Dinoflagellates 1985, 479-484. Elsevier Science Publishing, New York. D.M. Andersen, A.W. White, D.G. Baden (Eds.).
42. Martins R., Fernandez N., Beiras R., Vasconcelos V. Toxicity assessment of crude and partially purified extracts of marine Synechocystis and Synechococcus cyanobacterial strains in marine invertebrates. Toxicon 2007, 50:791-799.
43. Martins R., Pereira P., Welker M., Fastner J., Vasconcelos V.M. Toxicity of culturable cyanobacteria strains isolated from the Portuguese coast. Toxicon 2005, 46:454-464.
44. McElhiney J., Lawton L.A. Detection of the cyanobacterial hepatotoxins microcystins. Toxicol. Appl. Pharmacol. 2005, 203:219-230.
45. Miller M.A., Kudela R.M., Mekebri A., Crane D., Oates S.C., Tinker M.T., Staedler M., Miller W.A., Toy-Choutka S., Dominik C., Hardin D., Langlois G., Murray M., Ward K., Jessup D.A. Evidence for a novel marine harmful algal bloom: cyanotoxin (microcystin) transfer from land to sea otters. PLoS ONE 2010, 5(9):e12576. 10.1371/journal.pone.0012576.
46. Muyzer G., de Waal E.C., Uitterlinden A.G. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl. Environ. Microbiol. 1993, 59:695-700.
47. Nishiwaki R., Ohta T., Sueoka E., Suganuma M., Harada K., Watanabe M.F., Fujiki H. Two significant aspects of microcystin-LR: specific binding and liver specificity. Cancer Lett. 1994, 83:283-289.
48. Novaczek I., Madhyastha M.S., Ablett R.F., Donald A., Johnson G., Nijar M.S., Sims D.E. Depuration of domoic acid from live blue mussels (Mytilus edulis). Can. J. Fish. Aquat. Sci. 1992, 49:312-318.
49. Panayotidis P., Pancucci M.A., Balopoulos E., Gotsis-Skretas O. Plankton distribution patterns in a Mediterranean dilution basin: Amvrakikos (Ionian Sea, Greece). Mar. Ecol. 1994, 15(2):93-104.
50. Pearson L.A., Moffitt M.C., Ginn H.P., Neilan B.A. The molecular genetics and regulation of cyanobacterial peptide hepatotoxin biosynthesis. Crit. Rev. Toxicol. 2008, 38:847-856.
51. Plinski M., Mazur-Marzec H., Jozwiak T., Kobos J. The potential causes of cyanobacterial blooms in Baltic Sea estuaries. Oceanol. Hydrobiol. Stud. 2007, 36:125-137.
52. Rantala A., Rajaniemi-Wacklin P., Lyra C., Lepisto L., Rintala J., Mankiewicz-Boczek J., Sivonen K. Detection of microcystin-producing cyanobacteria in Finnish lakes with genus-specific microcystin synthetase gene E (mcyE) PCR and associations with environmental factors. Appl. Environ. Microbiol. 2006, 72:6101-6110.
53. Repavich W.M., Sonzogni W.C., Standridge J.H., Wedepohl R.E., Meisner L.F. Cyanobacteria (blue-green algae) in Wisconsin waters: acute and chronic toxicity. Water Res. 1990, 24:225-231.
54. Repka S., Meyerhofer M., von Brockel K., Sivonen K. Associations of cyanobacterial toxin, nodularin, with environmental factors and zooplankton in the Baltic Sea. Microb. Ecol. 2004, 47:350-358.
55. Richardson L.L., Sekar R., Myers J.L., Gantar M., Voss J.D., Kaczmarsky L., Remily E.R., Boyer G.L., Zimba P.V. The presence of the cyanobacterial toxin microcystin in black band disease of corals. FEMS Microbiol. Lett. 2007, 272:182-187.
56. Rouhiainen L., Vakkilainen T., Siemer B.L., Buikema W., Haselkorn R., Sivonen K. Genes coding for hepatotoxic heptapeptides (microcystins) in the cyanobacterium Anabaena strain 90. Appl. Environ. Microbiol. 2004, 70:686-692.
57. Scanlan J.D., Ostrowski M., Mazard S., Dufresne A., Garczarek L., Hess R.W., Post F.A., Hagemann M., Paulsen I., Partensky F. Ecological genomics of marine picocyanobacteria. Microbiol. Mol. Biol. Rev. 2009, 73(2):249-299.
58. Schembri M.A., Neilan B.A., Saint C.P. Identification of genes implicated in toxin production in the cyanobacterium Cylindrospermopsis raciborskii. Environ. Toxicol. 2001, 16:413-421. 10.1002/tox.1051.
59. Schwimmer M., Schwimmer D. Medical aspects of phycology. Algae, Man and the Environment 1968, 279-358. Syracuse University Press, Syracuse, New York. D.F. Jackson (Ed.).
60. Sivonen K., Kononen K., Carmichael W.W., Dahlem A.M., Rinehart K., Kiviranta J., Niemela S.I. Occurrence of the hepatotoxic cyanobacterium Nodularia spumigena in the Baltic Sea and the structure of the toxin. Appl. Environ. Microbiol. 1989, 55(8):1990-1995.
61. Sivonen K. Effects of light, temperature, nitrate, orthophosphate, and bacteria on growth of and hepatotoxin production by Oscillatoria agardhii strains. Appl. Environ. Microbiol. 1990, 56:2658-2666.
62. Soares R.M., Yuan M., Servaites J.C., Delgado A., Magalhaes V.F., Hilborn E.D., Carmichael W.W., Azevedo S.M. Sublethal exposure from microcystins to renal insufficiency patients in Rio de Janeiro, Brazil. Environ. Toxicol. 2006, 21:95-103.
63. Song L., Sano T., Li R., Watanabe M., Liu Y., Kaya K. Microcystin production of Microcystis viridis (cyanobacteria) under different culture conditions. Phycol. Res. 1998, 42:19.
64. Spoof L., Vesterkvist P., Lindholm T., Meriluoto J. Screening for cyanobacterial hepatotoxins, microcystins and nodularin in environmental water samples by reversed-phase liquid chromatography-electrospray ionisation mass spectrometry. J. Chromatogr. A 2003, 1020(1):105-119.
65. Tamura K., Dudley J., Nei M., Kumar S. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 2007, 24:1596-1599.
66. Tillett D., Dittmann E., Erhard M., von Dohren H., Borner T., Neilan B.A. Structural organization of microcystin biosynthesis in Microcystis aeruginosa PCC7806: an integrated peptide-polyketide synthetase system. Chem. Biol. 2000, 7:753-764.
67. Tillett D., Parker D.L., Neilan B.A. Detection of toxigenicity by a probe for the microcystin synthetase A gene (mcyA) of the cyanobacterial genus Microcystis: comparison of toxicities with 16S rRNA and phycocyanin operon (phycocyanin intergenic spacer) phylogenies. Appl. Environ. Microbiol. 2001, 67:2810-2818.
68. 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.
69. van derWesthuizen A.J., Eloff J.N. Effect of temperature and light on the toxicity and growth of the blue-green alga Microcystis aeruginosa (UV-006). Planta 1985, 163:55-59.
70. Vareli K., Briasoulis E., Pilidis G., Sainis I. Molecular confirmation of Planktothrix rubescens as the cause of intense, microcystin-synthesizing cyanobacterial bloom in Lake Ziros, Greece. Harmful Algae 2009, 8:447-453.
71. Vareli K., Pilidis G., Mavrogiorgou M-Ch.Briasoulis E., Sainis I. Molecular characterization of cyanobacterial diversity and yearly fluctuations of Microcystin loads in a suburban Mediterranean Lake (Lake Pamvotis, Greece). J. Environ. Monit. 2009, 11:1506-1512.
72. Vassilopoulou, V., Papaconstantinou, C., Caragitsou, E., 2002. Life history adaptations of a demersal fish species in a nutrient rich embayment of the Ionian Sea (Greece). U.S. Environmental Protection Agency Report, 600/R02/097, pp. 107-119.
73. Wang P.J., Chien M.S., Wu F.J., Chou H.N., Lee S.J. Inhibition of embryonic development by microcystin-LR in zebrafish, Danio rerio. Toxicon 2005, 45:303-308.
74. Watanabe M.F., Oishi S. Toxic substance from natural blooms of some lakes. Reservoirs, Ponds and moat in Tokyo and adjacent regions. Jpn. J. Limnol. 1982, 41:5-9.
75. WHO Guidelines for Drinking-Water Quality. Addendum to vol. 2. Health Criteria and Other Supporting Information 1998, World Health Organization, Geneva. 2nd ed.
76. Xie L., Xie P., Guo L., Li L., Miyabara Y., Park H.D. Organ distribution and bioaccumulation of microcystins in freshwater fish at different trophic levels from the eutrophic Lake Chaohu, China. Environ. Toxicol. 2005, 20:293-300.
77. Yuan M., Carmichael W.W., Hilborn E.D. Microcystin analysis in human sera and liver from human fatalities in Caruaru, Brazil 1996. Toxicon 2006, 48:627-640.