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Haemolytic activity in different species of the genus Prymnesium (Haptophyta)

Published online by Cambridge University Press:  30 August 2016

S. Seoane ,
P. Riobó  and
J. Franco
S. Seoane*
Affiliation:
Department of Plant Biology and Ecology, University of the Basque Country (UPV/EHU), Leioa, 48940, Spain
P. Riobó
Affiliation:
Institute of Marine Research (IIM-CSIC), Eduardo Cabello 6, 36208 Vigo, Spain
J. Franco
Affiliation:
Institute of Marine Research (IIM-CSIC), Eduardo Cabello 6, 36208 Vigo, Spain
*
Correspondence should be addressed to: S. Seoane, Department of Plant Biology and Ecology, University of the Basque Country (UPV/EHU), Leioa, 48940, Spain email: [email protected]
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Abstract

The genus Prymnesium includes several species that produce toxins with cytotoxic, ichthyotoxic, neurotoxic and haemolytic activity. Bloom episodes of Prymnesium species have been reported from several parts of the world (North America, Europe, Africa, Asia and Australia), especially from temperate and subtropical regions and most of them from brackish waters. Blooms cause great economic losses to aquaculture and fisheries around the world. The ichthyotoxic and allelopathic effects of Prymnesium have been linked to the presence of Haemolysin 1, Prymnesins 1 and 2 and, more recently, fatty acids and fatty acid amides. The toxicology of this genus with regard to different growth conditions such as light, nutrients and other parameters has been well documented. It is unknown, however, whether different species and strains from the Prymnesium genus all produce the same types and level of toxins. In this study, we have determined the haemolytic activity of eight different strains from the genus Prymnesium in both exponential and stationary phases of growth. We have also evaluated the efficiency of the extraction solvent.

Keywords

harmful algaehaemolyticPrymnesiumtoxicity
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 97 , Special Issue 3: European Marine Biology Symposium , May 2017 , pp. 491 - 496
Copyright
Copyright © Marine Biological Association of the United Kingdom 2016 

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References

REFERENCES

Abida, H., Ruchaud, S., Rios, L., Humeau, A., Probert, I., De Vargas, C., Bach, S. and Bowler, C. (2013) Bioprospecting marine plankton. Marine Drugs 11, 4594–4611.Google Scholar
Baden, D.G., Rein, K.S. and Gawley, R.E. (1998) Marine toxins: how they are studied and what they can tell us. In Cooksey, K.E. (ed.) Molecular approaches to the study of the ocean. London: Chapman & Hall, pp. 487–514.Google Scholar
Bertin, M.J., Zimba, P.V., Beauchesne, K.B., Huncik, K.M. and Moeller, P.D.R. (2012a) Identification of toxic fatty acid amides isolated from the harmful alga Prymnesium parvum . Harmful Algae 20, 111–116.CrossRefGoogle Scholar
Bertin, M.J., Zimba, P.V., Beauchesne, K.B., Huncik, K.M. and Moeller, P.D.R. (2012b) The contribution of fatty acid amides to Prymnesium parvum Carter toxicity. Harmful Algae 20, 117–125.CrossRefGoogle Scholar
Billard, C. (1983) Prymnesiun zebrinum sp. nov. et P. annuliferum sp. nov., deux nouvelles espèces apparentées à P. parvum Carter (Prymnesiophyceae). Phycologia 22, 141–151.Google Scholar
Blossom, H.E., Andersen, N.G., Rasmussen, S.A. and Hansen, P.J. (2014) Stability of the intra- and extracellular toxins of Prymnesium parvum using a microalgal bioassay. Harmful Algae 32, 11–21.Google Scholar
Fistarol, G.O., Legrand, C. and Granéli, E. (2003) Allelopathic effect of Prymnesium parvum on a natural plankton community. Marine Ecology Progress Series 255, 115–125.Google Scholar
Freitag, M., Beszteri, S., Vogel, H. and John, U. (2011) Effects of physiological shock treatments on toxicity and polyketide synthase gene expression in Prymnesium parvum (Prymnesiophyceae). European Journal of Phycology 46, 193–201.CrossRefGoogle Scholar
Fresnel, J., Probert, I. and Billard, C. (2001) Prymnesium faveolatum sp. nov. (Prymnesiophyceae), a new toxic species from the Mediterranean Sea. Vie et Milieu 51, 89–97.Google Scholar
Gieskes, W.W.C. and Kraay, G.W. (1983) Dominance of Cryptophyceae during the phytoplankton spring bloom in the central North Sea detected by HPLC analysis of pigments. Marine Biology 75, 179–185.CrossRefGoogle Scholar
Granéli, E., Edvardsen, B., Roelke, D.L. and Hagström, J.A. (2012) The ecophysiology and bloom dynamics of Prymnesium spp. Harmful Algae 14, 260–270.Google Scholar
Granéli, E. and Hansen, P.J. (2006) Allelopathy in harmful algae: a mechanism to compete for resources? In Granéli, E. and Turner, J.T. (eds) Ecology of harmful algae. Berlin: Springer Verlag, pp. 189–201.Google Scholar
Granéli, E. and Johansson, N. (2003) Increase in the production of allelopathic sub-stances by Prymnesium parvum cells grown under N- or P-deficient conditions. Harmful Algae 2, 135–145.CrossRefGoogle Scholar
Grant, B., Waller, R.F. and Wetherbee, R. (2011) Platychrysis moestrupii sp. nov. (Prymnesiophyceae): a new dimorphic, sand-dwelling haptophyte species from southeastern Australia. Phycologia 50, 608–615.Google Scholar
Guillard, R.R.L. and Ryther, J.H. (1962) Studies of marine planktonic diatoms. I. Cyclotella nana Hutedt and Detonula confervacea Cleve. Canadian Journal of Microbiology 8, 229–239.Google Scholar
Henrikson, J.C., Gharfeh, M.S., Easton, A.C., Easton, J.D., Glenn, K.L., Shadfan, M., Mooberry, S.L., Hambright, K.D. and Cichewicz, R.H. (2010) Reassessing the ichthyotoxin profile of cultured Prymnesium parvum (golden algae) and comparing it to samples collected from recent freshwater bloom and fish kill events in North America. Toxicon 55, 1396–1404.Google Scholar
Igarashi, T., Satake, M. and Yasumoto, T. (1996) Prymnesin-2: a potent ichthyotoxic and hemolytic glycoside isolated from the red tide alga Prymnesium parvum . Journal of the American Chemical Society 118, 479–480.Google Scholar
Kozakai, H., Oshima, Y. and Yasumoto, T. (1982) Isolation and structural elucidation of hemolysin from the phytoflagellate Prymnesium parvum . Agricultural and Biological Chemistry 47, 233–236.Google Scholar
Larsen, A. and Bryant, S. (1998) Growth rate and toxicity of Prymnesium parvum and Prymnesium patelliferum (Haptophyta) in response to changes in salinity, light and temperature. Sarsia 83, 409–418.CrossRefGoogle Scholar
Liebert, F. and Deerns, W.M. (1920) Onderzoek naar de oorzak van een Vischsterfte in den Polder Workumer Nieuwland, nabij Workum. Verhandlungen en Rapporten uitgegeven door Rijksinstituten voor Visscherijonderzoek 1, 81–93.Google Scholar
Manning, S.R. and La Claire, J.W. (2010) Prymnesins: toxic metabolites of the golden alga, Prymnesium parvum Carter (Haptophyta). Marine Drugs 8, 678–704.Google Scholar
Manning, S.R. and La Claire, J.W. (2013) Isolation of polyketides from Prymnesium parvum (Haptophyta) and their detection by liquid chromatography/mass spectrometry metabolic fingerprint analysis. Analytical Biochemistry 442, 189–195.Google Scholar
Martin, D.F. and Padilla, G.M. (1971) Hemolysis induced by Prymnesium parvum toxin: kinetics and hiding. Biochimica et Biophysica Acta 241, 213–225.Google Scholar
Martins, C.A., Kulis, D., Franca, S. and Anderson, D.M. (2004) The loss of PSP toxin production in a formerly toxic Alexandrium lusitanicum clone. Toxicon 43, 195–205.Google Scholar
Moestrup, Ø. (1994) Economic aspects: blooms, nuisance species and toxins. In Green, J.C. and Leadbeater, B.S.C. (eds) The haptophyte algae. New York, NY: Oxford University Press, pp. 265–285.CrossRefGoogle Scholar
Olenina, I., Hajdu, S., Edler, L., Andersson, A., Wasmund, N., Busch, S., Göbel, J., Gromisz, S., Huseby, S., Huttunen, M., Jaanus, A., Kokkonen, P., Ledaine, I. and Niemkiewicz, E. (2006) Biovolumes and size-classes of phytoplankton in the Baltic Sea. HELCOM Baltic Sea Environment Proceedings No. 106, pp. 144.Google Scholar
Padilla, G.M. (1970) Growth and toxigenesis of the chrysomonad Prymnesium as a function of salinity. Journal of Protozoology 17, 456–462.CrossRefGoogle Scholar
Parnas, I., Reich, K. and Bergmann, F. (1962) Photoinactivation of ichthyotoxin from axenic cultures of Prymnesium parvum Carter. Journal of Applied Microbiology 10, 237–239.Google Scholar
Prince, E.K., Poulson, K.L., Myers, T.L., Sieg, R.D. and Kubanek, J. (2010) Characterization of allelopathic compounds from the red tide dinoflagellate Karenia brevis . Harmful Algae 10, 39–48.Google Scholar
Schmidt, L.E. and Hansen, P.J. (2001) Allelopathy in the prymnesiophyte Chrysochromulina polylepis: effect of cell concentration, growth phase and pH. Marine Ecology Progress Series 216, 67–81.CrossRefGoogle Scholar
Schug, K.A., Skingel, T.R., Spencer, S.E., Serrano, C.A., Le, C.Q., Schug, C.A., Valenti, T.W., Brooks, B.W., Mydlarz, L.D. and Grover, J.P. (2010) Hemolysis, fish mortality, and LC-ESI-MS of cultured and fractionated golden alga (Prymnesium parvum). Journal of the American Water Resources Association 46, 33–44.Google Scholar
Seoane, S., Elkrem, W., Pienaar, R. and Edvardsen, B. (2009) Chrysochromulina palpebralis sp. nov. (Prymnesiophyceae): a haptophyte, possessing two alternative morphologies. Phycologia 48, 165–176.Google Scholar
Shilo, M. (1967) Formation and mode of action of algal toxins. Bacteriological Reviews 31, 180–193.CrossRefGoogle ScholarPubMed
Shilo, M. and Rosenberger, R.F. (1960) Studies on the toxic principles formed by the chrysomonad Prymnesium parvum Carter. Annals of the New York Academy of Sciences 90, 866–876.Google Scholar
Simonsen, S. and Moestrup, Ø. (1997) Toxicity tests in eight species of Chrysochromulina (Haptophyta). Canadian Journal of Botany 75, 129–136.Google Scholar
Stolte, W., Panosso, R., Gisselson, L.A. and Granéli, E. (2002) Utilization efficiency of nitrogen associated with riverine dissolved organic carbon (>1 kDa) by two toxin-producing phytoplankton species. Aquatic Microbial Ecology 29, 97–105.CrossRefGoogle Scholar
Sugg, L.M. and Van Dolah, F.M. (1999) No evidence for an allelopathic role of okadaic acid among ciguatera-associated dinoflagellates. Journal of Phycology 35, 93–103.Google Scholar
Suikkanen, S., Fistarl, G. and Granéli, E. (2004) Allelopathic effects of the Baltic cyanobacteria Nodularia spumigena, Aphanizomenon flos-aquae and Anabaena lemmermannii on algal monocultures. Journal of Experimental Marine Biology and Ecology 308, 85–101.Google Scholar
Sym, S.D., Pienaar, R.N., Edvardsen, B. and Egge, E.S. (2011) Fine structure and systematics of Prymnesium radiatum sp. nov (Prymnesiophyceae) from False Bay and Franskraal, South Africa. European Journal of Phycology 46, 229–248.Google Scholar
Tillman, U., Alpermann, T., John, U. and Cembella, A. (2008) Allelochemical interactions and short-term effects of the dinoflagellate Alexandrium on selected photoautotrophic and heterotrophic protists. Harmful Algae 7, 52–64.Google Scholar
Ulitzer, S. and Shilo, M. (1966) Mode of action of Prymnesium parvum ichthyotoxin. Journal of Protozoology 13, 332–336.Google Scholar
Uronen, P., Lehtinen, S., Legrand, C., Kuuppo, P. and Tamminen, T. (2005) Haemolytic activity and allelopathy of the haptophyte Prymnesium parvum in nutrient-limited and balanced growth conditions. Marine Ecology Progress Series 299, 137–148.CrossRefGoogle Scholar
White, A.W. (1986) High toxin content in the dinoflagellate Gonyaulax excavata in nature. Toxicon 24, 605–610.Google Scholar
Yariv, J. and Hestrin, S. (1961) Toxicity of the extracellular phase of Prymnesium parvum cultures. Journal of General Microbiology 24, 165–175.Google Scholar
Yasumoto, T., Underdal, B., Aune, T., Hormazabal, V., Skulberg, O.M. and Oshima, Y. (1990) Screening for hemolytic and ichthyotoxic components of Chrysochromulina polylepis and Gyrodinium aureolum from Norwegian coastal waters. In Graneli, E., Sundström, B., Edler, L. and Anderson, D.M. (eds) Toxic marine phytoplankton. New York, NY: Elsevier, pp. 436–440.Google Scholar
Zapata, M., Rodríguez, F. and Garrido, J.L. (2000) Separation of chlorophylls and carotenoids from marine phytoplankton: a new HPLC method using a reversed phase C-8 column and pyridine-containing mobile phases. Marine Ecology Progress Series 195, 29–45.Google Scholar