Skip to main content
SpringerLink
Log in

Haemolytic activity of live Phaeocystis pouchetii during mesocosm blooms

  • Original Paper
  • Chapter
  • First Online:
Phaeocystis, major link in the biogeochemical cycling of climate-relevant elements

Abstract

Chemical defence is a potential mechanism contributing to the success of Phaeocystis species that repeatedly dominate the phytoplankton in coastal areas. Species within the genus Phaeocystis have long been suspected of imposing negative effects on co-occurring organisms. Recently a number of toxins have been extracted and identified from Phaeocystis samples, but it is not clear if they do enhance the competitive advantage of Phaeocystis species.

In the present study the cytotoxic impact of live Phaeocystis pouchetii to human blood cells in close proximity, regardless of the nature of the responsible mechanism, was quantified using a bioassay. Haemolytic activity was measured during blooms of P. pouchetii in mesocosms. These environments were chosen to mimic natural conditions including chemically mediated interactions that could trigger defensive and/or allelopathic responses of Phaeocystis.

Haemolytic activity correlated with P. pouchetii numbers and was absent during the preceding diatom bloom. Samples containing live P. pouchetii cells showed the highest activity, while filtered sea water and cell extracts were less haemolytic or without effect. Dose-response curves were linear up to 70% lysis, and haemolysis in samples containing live P. pouchetii cells reached EC50 values comparable to known toxic prymnesiophytes (1.9 * 107 cells l−1). Haemolytic activity was enhanced by increased temperature and light. The results indicate that unprotected and thus presumably vulnerable cells present in a P. pouchetii bloom may lyse within days.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Aanesen RT, Eilertsen HC, Stabell OB (1998) Light-induced toxic properties of the marine alga Phaeocystis pouchetii towards cod larvae. Aquat Toxicol 40:109–121

    Article  Google Scholar 

  • Admiraal W, Werner D (1983) Utilisation of limiting concentrations of ortho-phosphate and production of extracellular organic phosphate in culture of marine diatoms. J Plankton Res 5:495–513

    Article  Google Scholar 

  • Arrigo KR, Robinson DH, Worthen DL, Dunbar RB, DiTullio GR, VanWoert M and, Lizotte MP (1999) Phytoplankton community structure and the drawdown of nutrients and CO2 in the Southern Ocean. Science 283:365–367

    Article  Google Scholar 

  • Arzul G, Gentien P, Bodennec G (1998) Potential toxicity of microalgal polyunsaturated fatty acids (PUFAs). In: Baudimant G, Guezennec JH, Roy P, Samain JF (eds) Marine lipids. IFREMIER, Nantes, pp 53–62

    Google Scholar 

  • Brussaard CPD, Kuipers B, Veldhuis MJW (2005) A mesocosm study of Phaeocystis globosa population dynamics - 1. Regulatory role of viruses in bloom. Harmful Algae 4:859–874

    Article  Google Scholar 

  • Brussaard CPD (2006) Phaeocystis and its interaction with viruses. Biogeochemistry (this issue)

    Google Scholar 

  • Cadée GC, Hegeman J (2002) Phytoplankton in the Marsdiep at the end of the 20th century; 30 years monitoring biomass, primary production and Phaeocystis blooms. J Sea Res 48:97–110

    Article  Google Scholar 

  • de Boer MK, Tyl MR, Vrieling EG, van Rijssel M (2004) Effects of salinity and nutrient conditions on growth and haemolytic activity of Fibrocapsa japonica (Raphidophyceae). Aquat Microb Ecol 37:171–181

    Google Scholar 

  • DiTullio GR, Grebmeier JM, Arrigo KR, Lizotte MP, Robinson DH, Leventer A, Barry JB, VanWoert ML, Dunbar RB (2000) Rapid and early export of Phaeocystis antarctica blooms in the Ross Sea, Antarctica. Nature 404:595–598

    Article  Google Scholar 

  • Eilertsen HC, Raa J (1995) Toxins in seawater produced by a common phytoplankter: Phaeocystis pouchetii. J Mar Biotechnol 3:115–119

    Google Scholar 

  • Eschbach E, Scharsack JP, John U, Medlin LK (2001) Improved erythrocyte lysis assay in microtitre plates for sensitive detection and efficient measurement of haemolytic compounds from ichtyotoxic algae. J Appl Toxicol 21:513–519

    Article  Google Scholar 

  • Estep KW, Nejstgaard JC, Skjoldal HR, Rey F (1990) Predation by copepods upon natural populations of Phaeocystis pouchetii as a function of the physiological state of the prey. Mar Ecol Prog Ser 67:235–249

    Google Scholar 

  • Fistarol GO, Legrand C, Granéli E (2003) Allelopathic effect of Prymnesium parvum on a natural plankton community. Mar Ecol Prog Ser 255:115–125

    Google Scholar 

  • Fu M, Koulman A, Van Rijssel M, Lützen A, De Boer MK, Tyl MR, Liebezeit G (2004) Chemical characterisation of three haemolytic compounds from the microalgal species Fibrocapsa japonica (Raphidophyceae). Toxicon 43:355–363

    Article  Google Scholar 

  • Guillard RRL, Helleburst JA (1971) Growth and production of extracellular substances by two strain of Phaeocystis pouchetii. J Phycol 7:330–338

    Article  Google Scholar 

  • Hansen E, Eilertsen HC, Ernstsen A, Geneviere AM (2003) Anti-mitotic activity towards sea urchin embryos in extracts from the marine haptophycean Phaeocystis pouchetii (Hariot) Lagerheim collected along the coast of northern Norway. Toxicon 41:803–812

    Article  Google Scholar 

  • Hansen E, Ernstsen A, Eilertsen HC (2004) Isolation and characterisation of a cytotoxic polyunsaturated aldehyde from the marine phytoplankter Phaeocystis pouchetii (Hariot) Lagerheim. Toxicology 199:207–217

    Article  Google Scholar 

  • Hamm CE, Rousseau V (2003) Composition, assimilation and degradation of Phaeocystis globosa-derived fatty acids in the North Sea. J Sea Res 50:271–283

    Article  Google Scholar 

  • Hay ME, Kubanek J (2002) Community and ecosystem level consequences of chemical cues in the phytoplankton. J Chem Ecol 28:2001–2016

    Article  Google Scholar 

  • He J, Shi Z, Zhang Y, Liu Y, Jiang T, Yin Y, Qi Y (1999) Morphological characteristics and toxins of Phaeocystis cf pouchetii (Prymnesiophyceae). Oceanol Limnol Sin 30:76–83

    Google Scholar 

  • Huang CJ, Dong QX, Zheng L (1999) Taxonomic and ecological studies on a large scale Phaeocystis pouchetii bloom in the Southeast Coast of China during late 1997. Oceanol Limnol Sin 30:581–590

    Google Scholar 

  • Huntley M, Tande K, Eilertsen HC (1987) On the trophic fate of Phaeocystis pouchetii (Hariot). II. Grazing rates of Calanus hyperboreus (Kroyer) on diatoms and different size categories of Phaeocystis pouchetii. J Exp Mar Biol Ecol 110:197–212

    Article  Google Scholar 

  • Kuroda A, Nakashima T, Yamaguchi K, Oda T (2005) Isolation and characterization of light-dependent haemolytic cytotoxin from harmful red tide phytoplankton Chattonella marina. Comp Biochem Physiol C 141:297–305

    Google Scholar 

  • Jacobsen A (2000) New aspects of bloom dynamics of Phaeocystis pouchetii (Haptophyta) in Norwegian waters. Ph. D. thesis, University of Bergen

    Google Scholar 

  • Jakobsen HH, Tang KW (2002) Effects of protozoan grazing on colony formation in Phaeocystis globosa (Prymnesiophyceae) and the potential costs and benefits. Aquat Microb Ecol 27:261–273

    Google Scholar 

  • Jebram D (1980) Prospection for a sufficient nutrition for the cosmopolitic marine bryozoan Electra pilosa (Linnaeus). Zoologische Jahrbücher Abteilung für Systematik, Ökologie und Geographie der Tiere 107:368–390

    Google Scholar 

  • Johansson N, Granéli E (1999) Influence of different nutrient conditions on cell density, chemical composition and toxicity of Prymnesium parvum (haptophyta) in semi-continuous cultures. J Exp Mar Biol Ecol 239:243–258

    Article  Google Scholar 

  • Jüttner F (2001) Liberation of 5,8,11,14,17-eicosapantaenoic acid and other polyunsaturated fatty acids from lipids as a grazer defence reaction in epilithic diatom biofilms. J Phycol 37:744–755

    Article  Google Scholar 

  • Lancelot C, Billen G, Sournia A, Weisse T, Colijn F, Veldhuis MJW, Davies A, Wassmann P (1987) Phaeocystis blooms and nutrient enrichment in the continental coastal zones of the North Sea. Ambio 16:38–46

    Google Scholar 

  • Legrand C, Rengefors K, Fistarol GO, Granéli E (2003) Allelopathy in phytoplankton – biochemical, ecological and evolutionary aspects. Phycologia 42:406–419

    Article  Google Scholar 

  • Marshall JA, Ross T, Pyecroft S, Hallegraeff G (2005) Superoxide production by marine microalgae. II. Towards understanding ecological consequences and possible functions. Mar Biol 147:541–549

    Article  Google Scholar 

  • Menden-Deuer S, Lessard EJ (2000) Carbon to volume relationships for dinoflagellates, diatoms, and other protist plankton. Limnol Oceanogr 45:569–579

    Article  Google Scholar 

  • Nejstgaard JC, Frischer ME, Verity PG, Anderson JT, Jacobsen A, Zirbel MJ, Larsen A, Martínez-Martínez J, Sazhin AF, Walters T, Bronk DA, Whipple SJ, Borrett SR, Patten BC, Long JD (2006) Plankton development and trophic transfer in sea water enclosures with nutrients and Phaeocystis pouchetii added. Mar Ecol Prog Ser 321:99–121

    Google Scholar 

  • Nejstgaard JC, Tang KW, Steinke M, Dutz J, Koski M, Antajan E, Long JD (2006) Zooplankton grazing on Phaeocystis: a critical review and future challenges. Biogeochemistry. This volume

    Google Scholar 

  • Noordkamp DJB, Schotten M, Gieskes WWC, Forney LJ, Gottschal JC, van Rijssel M (1998) High acrylate concentrations in the mucus of Phaeocystis globosa colonies. Aquat Microb Ecol.16:45–52

    Google Scholar 

  • Noordkamp DJB, Gieskes WWC, Gottschal JC, Forney LJ, van Rijssel M (2000) Acrylate in Phaeocystis colonies does not affect the surrounding bacteria. J Sea Res 43:287–296

    Article  Google Scholar 

  • Paffenhöfer GA, Ianora A, Miralto A, Turner JT, Kleppel GS, d’Alcala MR, Casotti R, Caldwell GS, Pohnert G, Fontana A, Muller-Navarra D, Jonasdottir S, Armbrust V, Bamstedt U, Ban S, Bentley MG, Boersma M, Bundy M, Buttino I, Calbet A, Carlotti F, Carotenuto Y, d’Ippolito G, Frost B, Guisande C, Lampert W, Lee RF, Mazza S, Mazzocchi MG, Nejstgaard JC, Poulet SA, Romano G, Smetacek V, Uye S, Wakeham S, Watson S, Wichard T (2005) Colloquium on diatom-copepod interactions. Mar Ecol Prog Ser 286:293–305

    Google Scholar 

  • Parsons T, Maita Y, Lalli C (1984) A manual of chemical and biological methods for seawater analysis. Pergamon Press, Oxford, UK, 173 pp

    Google Scholar 

  • Peng XC, Yang WD, Liu JS, Peng ZY, Lu SH, Ding WZ (2005) Characterization of the hemolytic properties of an extract from Phaeocystis globosa Scherffel. J Integrative plant biol Y47:165–171

    Article  Google Scholar 

  • Pohnert G, Boland W (2002) The oxylipin chemistry of attraction and defence in brown algae and diatoms. Nat Prod Rep 19:108–122

    Article  Google Scholar 

  • Savage RE (1930) The influence of Phaeocystis on the migration of the herring. Fish Invest Lond (Ser II) 12:1–14

    Google Scholar 

  • Schoemann V, Becquevort S, Stefels J, Rousseau V, Lancelot C (2005) Phaeocystis blooms in the global ocean and their controlling mechanisms: a review. J Sea Res 53:43–66

    Article  Google Scholar 

  • Sieburth JM (1960) Acrylic acid an “antibiotic” principle in Phaeocystis blooms in Antarctic waters. Science 132:676–677

    Article  Google Scholar 

  • Sieburth JM (1961) Antibiotic properties of acrylic acid, a factor in gastrointestinal antibiosis of polar marine animals. J Bacteriol 82:72–79

    Google Scholar 

  • Simonsen S, Moestrup Ø (1997) Toxicity tests in eight species of Chrysochromulina (Haptophyta). Can J Bot 75:129–136

    Article  Google Scholar 

  • Stabell OB, Aanesen RT, Eilertsen HC (1999) Toxic peculiarities of the marine alga Phaeocystis pouchetii detected by in vivo and in vitro bioassay methods. Aquat Toxicol 44:279–288

    Article  Google Scholar 

  • Stefels J, Dijkhuizen L (1996) Characteristics of DMSP-lyase in Phaeocystis sp. (Prymnesiophyceae). Mar Ecol Prog Ser 131:307–313

    Google Scholar 

  • Stolte W, Panosso R, Gisselson LA, Granéli E (2002) Utilization efficiency of nitrogen associated with riverine dissolved organic carbon (>1 kDa) by two toxin-producing phytoplankton species. Aquat Microb Ecol 29:97–105

    Google Scholar 

  • Svensen C, Egge JK, Stiansen JE (2001) Can silicate and turbulence regulate the vertical flux of biogenic matter? A mesocosm study. Mar Ecol Prog Ser 217:67–80

    Google Scholar 

  • Sverdrup LE, Källqvist T, Kelley AE, Fürst CS, Hagen SB (2001) Comparative toxicity of acrylic acid to marine and freshwater microalgae and the significance for environmental effects assessments. Chemosphere 45:653–658

    Article  Google Scholar 

  • Tang KW (2003) Grazing and colony size development in Phaeocystis globosa (Prymnesiophyceae): the role of a chemical signal. J of Plankton Res 25:831–842

    Article  Google Scholar 

  • Wolfe GV, Steinke M, Kirst GO (1997) Grazing-activated chemical defence in a unicellular marine alga. Nature 387:894–897

    Article  Google Scholar 

  • Yasumoto T, Underdal B, Aune T, Hormazabal V, Skulberg OM, Oshima Y (1990) Screening for hemolytic and ichthyotoxic components of Chrysochromulina polylepis and Gyrodinium aurolum from Norwegian coastal waters. In: Granèli E., Sundström B, Edler L, Anderson DM (eds) Toxic marine phytoplankton. Elsevier, New York, pp 436–440

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Marine Biology, Centre for Ecological and Evolutionary Studies, University of Groningen, P.O. Box 14, 9750AA, Haren, The Netherlands

    Marion van Rijssel & Anne-Carlijn Alderkamp

  2. Department of Fisheries and Marine Biology, University of Bergen, P.O. Box 7800, 5020, Bergen, Norway

    Jens C. Nejstgaard

  3. P. P. Shirshov Institute of Oceanology, Russian Academy of Science, 36 Nakhimovski Prospekt, 117997, Moscow, Russia

    Andrey F. Sazhin

  4. Skidaway Institute of Oceanography, 10 Oceans Science Circle, Savannah, GA, 31411, USA

    Peter G. Verity

Authors
  1. Marion van Rijssel
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Anne-Carlijn Alderkamp
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jens C. Nejstgaard
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Andrey F. Sazhin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Peter G. Verity
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Marion van Rijssel .

Editor information

Editors and Affiliations

  1. University of Groningen, Haren, The Netherlands

    M. A. van Leeuwe , J. Stefels  & W. W. C. Gieskes ,  & 

  2. Laboratoire des Sciences du Climat et de l'Environnment, Gif sur Yvette, France

    S. Belviso

  3. Université Libre de Bruxelles, Bruxelles, Belgium

    C. Lancelot

  4. Skidaway Institute of Oceanography, Savannah, GA, USA

    P. G. Verity

Rights and permissions

Reprints and permissions

Copyright information

© 2007 Springer Science+Business Media B.V.

About this chapter

Cite this chapter

van Rijssel, M., Alderkamp, AC., Nejstgaard, J.C., Sazhin, A.F., Verity, P.G. (2007). Haemolytic activity of live Phaeocystis pouchetii during mesocosm blooms. In: van Leeuwe, M.A., Stefels, J., Belviso, S., Lancelot, C., Verity, P.G., Gieskes, W.W.C. (eds) Phaeocystis, major link in the biogeochemical cycling of climate-relevant elements. Springer, Dordrecht. https://doi.org/10.1007/978-1-4020-6214-8_14

Download citation

Publish with us

Policies and ethics

Search

Navigation